No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Direct DNA Lesion Reversal and Excision Repair in

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Sophie Couvé1, Alexander A. Ishchenko2, Olga S. Fedorova3, Erlan M. Ramanculov4, Jacques Laval5, and Murat Saparbaev6
  • Editor: Susan T. Lovett7
    Affiliations: 1: Groupe «Réparation de l’ADN», Université Paris-Sud, CNRS UMR8200 and Génétique Oncologique EPHE, INSERM U753; 2: Groupe «Réparation de l’ADN», Université Paris-Sud, CNRS UMR8200; 3: Institut de Cancérologie Gustave Roussy, F-94805 Villejuif Cedex, France; Laboratory of Biopolymer Modification, Institute of Chemical Biology and Fundamental Medicine, University of Novosibirsk, 630090 Novosibirsk, Russian Federation; 4: National Center for Biotechnology of the Republic of Kazakhstan, Astana, Kazakhstan; 5: Groupe «Réparation de l’ADN», Université Paris-Sud, CNRS UMR8200; 6: Groupe «Réparation de l’ADN», Université Paris-Sud, CNRS UMR8200; 7: Brandeis University, Waltham, MA
  • Received 01 January 2012 Accepted 27 March 2012 Published 19 February 2013
  • Address correspondence to Murat Saparbaev [email protected]
image of Direct DNA Lesion Reversal and Excision Repair in <span class="jp-italic">Escherichia coli</span>
    Preview this reference work article:
    Zoom in

    Direct DNA Lesion Reversal and Excision Repair in , Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/5/2/7_2_4_module-1.gif /docserver/preview/fulltext/ecosalplus/5/2/7_2_4_module-2.gif
  • Abstract:

    Cellular DNA is constantly challenged by various endogenous and exogenous genotoxic factors that inevitably lead to DNA damage: structural and chemical modifications of primary DNA sequence. These DNA lesions are either cytotoxic, because they block DNA replication and transcription, or mutagenic due to the miscoding nature of the DNA modifications, or both, and are believed to contribute to cell lethality and mutagenesis. Studies on DNA repair in spearheaded formulation of principal strategies to counteract DNA damage and mutagenesis, such as: direct lesion reversal, DNA excision repair, mismatch and recombinational repair and genotoxic stress signalling pathways. These DNA repair pathways are universal among cellular organisms. Mechanistic principles used for each repair strategies are fundamentally different. Direct lesion reversal removes DNA damage without need for excision and de novo DNA synthesis, whereas DNA excision repair that includes pathways such as base excision, nucleotide excision, alternative excision and mismatch repair, proceeds through phosphodiester bond breakage, de novo DNA synthesis and ligation. Cell signalling systems, such as adaptive and oxidative stress responses, although not DNA repair pathways are nevertheless essential to counteract DNA damage and mutagenesis. The present review focuses on the nature of DNA damage, direct lesion reversal, DNA excision repair pathways and adaptive and oxidative stress responses in .

  • Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4


1. Setlow RB, Carrier WL. 1964. The disappearance of thymine dimers from DNA: an error-correcting mechanism. Proc Natl Acad Sci USA 51:226–231.
2. Boyce RP, Howard-Flanders P. 1964. Release of ultraviolet light-induced thymine dimers from DNA in E. coli K-12. Proc Natl Acad Sci USA 51:293–300.
3. Imlay JA, Linn S. 1988. DNA damage and oxygen radical toxicity. Science 240:1302–1309.
4. Lindahl T, Andersson A. 1972. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry 11:3618–3623.
5. Lindahl T, Nyberg B. 1974. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry 13:3405–3410.
6. Lindahl T, Nyberg B. 1972. Rate of depurination of native deoxyribonucleic acid. Biochemistry 11:3610–3618.
7. Hill-Perkins M, Jones MD, Karran P. 1986. Site-specific mutagenesis in vivo by single methylated or deaminated purine bases. Mutat Res 162:153–163.
8. Kamiya H, Miura H, Suzuki M, Murata N, Ishikawa H, Shimizu M, Komatsu Y, Murata T, Sasaki T, Inoue H, et al. 1992. Mutations induced by DNA lesions in hot spots of the c-Ha-ras gene. Nucleic Acids Symp Ser 179–180.
9. Lawley PD. 1966. Effects of some chemical mutagens and carcinogens on nucleic acids. Prog Nucleic Acids Res Mol Biol 5:89–131.
10. Singer B. 1976. All oxygens in nucleic acids react with carcinogenic ethylating agents. Nature 264:333–339.
11. Pegg AE. 1984. Methylation of the O 6 position of guanine in DNA is the most likely initiating event in carcinogenesis by methylating agents. Cancer Invest 2:223–231.
12. Singer B, Kusmierek JT. 1982. Chemical mutagenesis. Annu Rev Biochem 51:655–693.
13. Bodell WJ, Singer B. 1979. Influence of hydrogen bonding in DNA and polynucleotides on reaction of nitrogens and oxygens toward ethylnitrosourea. Biochemistry 18:2860–2863.
14. Boiteux S, Laval J. 1982. Mutagenesis by alkylating agents: coding properties for DNA polymerase of poly (dC) template containing 3-methylcytosine. Biochimie 64:637–641.
15. Larson K, Sahm J, Shenkar R, Strauss B. 1985. Methylation-induced blocks to in vitro DNA replication. Mutat Res 150:77–84.
16. Swann PF. 1990. Why do O 6-alkylguanine and O 4-alkylthymine miscode? The relationship between the structure of DNA containing O 6-alkylguanine and O 4-alkylthymine and the mutagenic properties of these bases. Mutat Res 233:81–94.
17. Taverna P, Sedgwick B. 1996. Generation of an endogenous DNA-methylating agent by nitrosation in Escherichia coli. J Bacteriol 178:5105–5111.
18. Posnick LM, Samson LD. 1999. Influence of S-adenosylmethionine pool size on spontaneous mutation, dammethylation, and cell growth of Escherichia coli. J Bacteriol 181:6756–6762.
19. Imlay JA, Chin SM, Linn S. 1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640–642.
20. Henle ES, Linn S. 1997. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J Biol Chem 272:19095–19098.
21. Bjelland S, Seeberg E. 2003. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 531:37–80.
22. Kasai H, Tanooka H, Nishimura S. 1984. Formation of 8-hydroxyguanine residues in DNA by X-irradiation. Gann 75:1037–1039.
23. Dizdaroglu M. 1986. Free-radical-induced formation of an 8,5′-cyclo-2′-deoxyguanosine moiety in deoxyribonucleic acid. Biochem J 238:247–254.
24. Schuchmann MN, Steenken S, Wroblewski J, von Sonntag C. 1984. Site of OH radical attack on dihydrouracil and some of its methyl derivatives. Int J Radiat Biol Relat Stud Phys Chem Med 46:225–232.
25. Teoule R, Bert C, Bonicel A. 1977. Thymine fragment damage retained in the DNA polynucleotide chain after gamma irradiation in aerated solutions. II. Radiat Res 72:190–200.
26. Ganguly T, Duker NJ. 1991. Stability of DNA thymine hydrates. Nucleic Acids Res 19:3319–3323.
27. Muller E, Gasparutto D, Jaquinod M, Romieu A, Cadet J. 2000. Chemical and biochemical properties of oligonucleotides that contain (5′S,6S)-cyclo-5,6-dihydro-2′-deoxyuridine and (5′S,6S)-cyclo-5,6-dihydrothymidine, two main radiation-induced degradation products of pyrimidine 2′-deoxyribonucleosides. Tetrahedron 56:8689–8701.
28. Dizdaroglu M, Schulte-Frohlinde D, von Sonntag C. 1977. Isolation of 2-deoxy-D-erythro-pentonic acid from an alkali-labile site in gamma-irradiated DNA. Int J Radiat Biol Relat Stud Phys Chem Med 32:481–483.
29. Giloni L, Takeshita M, Johnson F, Iden C, Grollman AP. 1981. Bleomycin-induced strand-scission of DNA. Mechanism of deoxyribose cleavage. J Biol Chem 256:8608–8615.
30. Henner WD, Rodriguez LO, Hecht SM, Haseltine WA. 1983. Gamma ray induced deoxyribonucleic acid strand breaks. 3′ Glycolate termini. J Biol Chem 258:711–713.
31. Akhlaq MS, Schuchmann HP, von Sonntag C. 1987. The reverse of the ‘repair’ reaction of thiols: H-abstraction at carbon by thiol radicals. Int J Radiat Biol Relat Stud Phys Chem Med 51:91–102.
32. Ward JF. 2000. Complexity of damage produced by ionizing radiation. Cold Spring Harb Symp Quant Biol 65:377–382.
33. Marnett LJ, Burcham PC. 1993. Endogenous DNA adducts: potential and paradox. Chem Res Toxicol 6:771–785.
34. Furlong EA, Jorgensen TJ, Henner WD. 1986. Production of dihydrothymidine stereoisomers in DNA by gamma-irradiation. Biochemistry 25:4344–4349.
35. Grollman AP, Moriya M. 1993. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet 9:246–249.
36. Kreutzer DA, Essigmann JM. 1998. Oxidized, deaminated cytosines are a source of C → Ttransitions in vivo. Proc Natl Acad Sci USA 95:3578–3582.
37. Kunkel TA, Bebenek K. 2000. DNA replication fidelity. Annu Rev Biochem 69:497–529.
38. Basu AK, Loechler EL, Leadon SA, Essigmann JM. 1989. Genetic effects of thymine glycol: site-specific mutagenesis and molecular modeling studies. Proc Natl Acad Sci USA 86:7677–7681.
39. Demple B, DeMott MS. 2002. Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 21:8926–8934.
40. Ide H, Petrullo LA, Hatahet Z, Wallace SS. 1991. Processing of DNA base damage by DNA polymerases. Dihydrothymine and beta-ureidoisobutyric acid as models for instructive and noninstructive lesions. J Biol Chem 266:1469–1477.
41. Laval J, Boiteux S. 1986. Repair of cyclic nucleic acid adducts and adverse effects of apurinic sites. IARC Sci Publ 381–385.
42. Kozmin S, Slezak G, Reynaud-Angelin A, Elie C, de Rycke Y, Boiteux S, Sage E. 2005. UVA radiation is highly mutagenic in cells that are unable to repair 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102:13538–13543.
43. Beukers R, Berends W. 1960. The effect of paramagnetic substances on the conversion of some pyrimidines by ultraviolet radiation. Biochim Biophys Acta 38:573–575.
44. Douki T, Court M, Sauvaigo S, Odin F, Cadet J. 2000. Formation of the main UV-induced thymine dimeric lesions within isolated and cellular DNA as measured by high performance liquid chromatography-tandem mass spectrometry. J Biol Chem 275:11678–11685.
45. Cole RS. 1971. Psoralen monoadducts and interstrand cross-links in DNA. Biochim Biophys Acta 254:30–39.
46. Johnston BH, Hearst JE. 1981. Low-level psoralen–deoxyribonucleic acid cross-links induced by single laser pulses. Biochemistry 20:739–745.
47. Cimino GD, Gamper HB, Isaacs ST, Hearst JE. 1985. Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry. Annu Rev Biochem 54:1151–1193.
48. Kohn KW, Spears CL, Doty P. 1966. Inter-strand crosslinking of DNA by nitrogen mustard. J Mol Biol 19:266–288.
49. Coste F, Malinge JM, Serre L, Shepard W, Roth M, Leng M, Zelwer C. 1999. Crystal structure of a double-stranded DNA containing a cisplatin interstrand cross-link at 1.63 A resolution: hydration at the platinated site. Nucleic Acids Res 27:1837–1846.
50. Tomasz M. 1995. Mitomycin C: small, fast and deadly (but very selective). Chem Biol 2:575–579.
51. Kozekov ID, Nechev LV, Moseley MS, Harris CM, Rizzo CJ, Stone MP, Harris TM. 2003. DNA interchain cross-links formed by acrolein and crotonaldehyde. J Am Chem Soc 125:50–61.
52. Barker S, Weinfeld M, Murray D. 2005. DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat Res 589:111–135.
53. Demple B, Sedgwick B, Robins P, Totty N, Waterfield MD, Lindahl T. 1985. Active site and complete sequence of the suicidal methyltransferase that counters alkylation mutagenesis. Proc Natl Acad Sci USA 82:2688–2692.
54. Jeggo P. 1979. Isolation and characterization of Escherichia coli K-12 mutants unable to induce the adaptive response to simple alkylating agents. J Bacteriol 139:783–791.
55. Sedgwick B, Lindahl T. 2002. Recent progress on the Ada response for inducible repair of DNA alkylation damage. Oncogene 21:8886–8894.
56. Falnes PO, Johansen RF, Seeberg E. 2002. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419:178–182.
57. Falnes PO. 2004. Repair of 3-methylthymine and 1-methylguanine lesions by bacterial and human AlkB proteins. Nucleic Acids Res 32:6260–6267.
58. Kataoka H, Yamamoto Y, Sekiguchi M. 1983. A new gene ( alkB) of Escherichia coli that controls sensitivity to methyl methane sulfonate. J Bacteriol 153:1301–1307.
59. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B. 2002. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419:174–178.
60. Margison GP, Cooper DP, Potter PM. 1990. The E. coliogt gene. Mutat Res 233:15–21.
61. Potter PM, Wilkinson MC, Fitton J, Carr FJ, Brennand J, Cooper DP, Margison GP. 1987. Characterisation and nucleotide sequence of ogt, the O 6-alkylguanine-DNA-alkyltransferase gene of E. coli. Nucleic Acids Res 15:9177–9193.
62. Rebeck GW, Samson L. 1991. Increased spontaneous mutation and alkylation sensitivity of Escherichia coli strains lacking the ogtO 6-methylguanine DNA repair methyltransferase. J Bacteriol 173:2068–2076.
63. Husain I, Sancar A. 1987. Photoreactivation in phr mutants of Escherichia coli K-12. J Bacteriol 169:2367–2372.
64. Rupert CS, Goodgal SH, Herriott RM. 1958. Photoreactivation in vitro of ultraviolet-inactivated Hemophilus influenzae transforming factor. J Gen Physiol 41:451–471.
65. Sancar A, Rupert CS. 1978. Cloning of the phr gene and amplification of photolyase in Escherichia coli. Gene 4:295–308.
66. Sancar A, Rupp WD. 1983. A novel repair enzyme: UVRABC excision nuclease of Escherichia coli cuts a DNA strand on both sides of the damaged region. Cell 33:249–260.
67. Dorrell N, Davies DJ, Moss SH. 1995. Evidence of photoenzymatic repair due to the phrA gene in a phrB mutant of Escherichia coli K-12. J Photochem Photobiol B 28:87–92.
68. Sutherland BM, Hausrath SG. 1979. Multiple loci affecting photoreactivation in Escherichia coli. J Bacteriol 138:333–338.
69. Evensen G, Seeberg E. 1982. Adaptation to alkylation resistance involves the induction of a DNA glycosylase. Nature 296:773–775.
70. O’Brien PJ, Ellenberger T. 2004. The Escherichia coli 3-methyladenine DNA glycosylase AlkA has a remarkably versatile active site. J Biol Chem 279:26876–26884.
71. Thomas L, Yang CH, Goldthwait DA. 1982. Two DNA glycosylases in Escherichia coli which release primarily 3-methyladenine. Biochemistry 21:1162–1169.
72. Yamamoto Y, Katsuki M, Sekiguchi M, Otsuji N. 1978. Escherichia coli gene that controls sensitivity to alkylating agents. J Bacteriol 135:144–152.
73. Boiteux S, Huisman O. 1989. Isolation of a formamidopyrimidine-DNA glycosylase ( fpg) mutant of Escherichia coli K12. Mol Gen Genet 215:300–305.
74. Boiteux S, Gajewski E, Laval J, Dizdaroglu M. 1992. Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 31:106–110.
75. Michaels ML, Pham L, Cruz C, Miller JH. 1991. MutM, a protein that prevents G.C—T.A transversions, is formamidopyrimidine-DNA glycosylase. Nucleic Acids Res 19:3629–3632.
76. Tchou J, Kasai H, Shibutani S, Chung MH, Laval J, Grollman AP, Nishimura S. 1991. 8-Oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc Natl Acad Sci USA 88:4690–4694.
77. Gallinari P, Jiricny J. 1996. A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature 383:735–738.
78. Mokkapati SK, Fernandez de Henestrosa AR, Bhagwat AS. 2001. Escherichia coli DNA glycosylase Mug: a growth-regulated enzyme required for mutation avoidance in stationary-phase cells. Mol Microbiol 41:1101–1111.
79. Saparbaev M, Laval J. 1998. 3, N 4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase. Proc Natl Acad Sci USA 95:8508–8513.
80. Saparbaev M, Langouet S, Privezentzev CV, Guengerich FP, Cai H, Elder RH, Laval J. 2002. 1, N(2)-ethenoguanine, a mutagenic DNA adduct, is a primary substrate of Escherichia coli mismatch-specific uracil-DNA glycosylase and human alkylpurine-DNA-N-glycosylase. J Biol Chem 277:26987–26993.
81. Michaels ML, Cruz C, Grollman AP, Miller JH. 1992. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc Natl Acad Sci USA 89:7022–7025.
82. Michaels ML, Pham L, Nghiem Y, Cruz C, Miller JH. 1990. MutY, an adenine glycosylase active on G-A mispairs, has homology to endonuclease III. Nucleic Acids Res 18:3841–3845.
83. Tsai-Wu JJ, Radicella JP, Lu AL. 1991. Nucleotide sequence of the Escherichia coli micA gene required for A/G-specific mismatch repair: identity of micA and mutY. J Bacteriol 173:1902–1910.
84. Jiang D, Hatahet Z, Melamede RJ, Kow YW, Wallace SS. 1997. Characterization of Escherichia coli endonuclease VIII. J Biol Chem 272:32230–32239.
85. Melamede RJ, Hatahet Z, Kow YW, Ide H, Wallace SS. 1994. Isolation and characterization of endonuclease VIII from Escherichia coli. Biochemistry 33:1255–1264.
86. Wallace SS, Bandaru V, Kathe SD, Bond JP. 2003. The enigma of endonuclease VIII. DNA Repair (Amst) 2:441–453.
87. Asahara H, Wistort PM, Bank JF, Bakerian RH, Cunningham RP. 1989. Purification and characterization of Escherichia coli endonuclease III from the cloned nth gene. Biochemistry 28:4444–4449.
88. Cunningham RP, Weiss B. 1985. Endonuclease III ( nth) mutants of Escherichia coli. Proc Natl Acad Sci USA 82:474–478.
89. Dizdaroglu M, Laval J, Boiteux S. 1993. Substrate specificity of the Escherichia coli endonuclease III: excision of thymine- and cytosine-derived lesions in DNA produced by radiation-generated free radicals. Biochemistry 32:12105–12111.
90. Bjelland S, Bjoras M, Seeberg E. 1993. Excision of 3-methylguanine from alkylated DNA by 3-methyladenine DNA glycosylase I of Escherichia coli. Nucleic Acids Res 21:2045–2049.
91. Riazuddin S, Lindahl T. 1978. Properties of 3-methyladenine-DNA glycosylase from Escherichia coli. Biochemistry 17:2110–2118.
92. Steinum AL, Seeberg E. 1986. Nucleotide sequence of the tag gene from Escherichia coli. Nucleic Acids Res 14:3763–3772.
93. Duncan BK, Rockstroh PA, Warner HR. 1978. Escherichia coli K-12 mutants deficient in uracil-DNA glycosylase. J Bacteriol 134:1039–1045.
94. Duncan BK, Weiss B. 1982. Specific mutator effects of ung (uracil-DNA glycosylase) mutations in Escherichia coli. J Bacteriol 151:750–755.
95. Krokan HE, Drablos F, Slupphaug G. 2002. Uracil in DNA—occurrence, consequences and repair. Oncogene 21:8935–8948.
96. Lindahl T. 1974. An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proc Natl Acad Sci USA 71:3649–3653.
97. Demple B, Halbrook J, Linn S. 1983. Escherichia colixth mutants are hypersensitive to hydrogen peroxide. J Bacteriol 153:1079–1082.
98. Rogers SG, Weiss B. 1980. Cloning of the exonuclease III gene of Escherichia coli. Gene 11:187–195.
99. Sancar A, Reardon JT. 2004. Nucleotide excision repair in E. coli and man. Adv Protein Chem 69:43–71.
100. Van Houten B. 1990. Nucleotide excision repair in Escherichia coli. Microbiol Rev 54:18–51.
101. Malta E, Moolenaar GF, Goosen N. 2007. Dynamics of the UvrABC nucleotide excision repair proteins analyzed by fluorescence resonance energy transfer. Biochemistry 46:9080–9088.
102. Truglio JJ, Rhau B, Croteau DL, Wang L, Skorvaga M, Karakas E, DellaVecchia MJ, Wang H, Van Houten B, Kisker C. 2005. Structural insights into the first incision reaction during nucleotide excision repair. EMBO J 24:885–894.
103. Verhoeven EE, van Kesteren M, Moolenaar GF, Visse R, Goosen N. 2000. Catalytic sites for 3′ and 5′ incision of Escherichia coli nucleotide excision repair are both located in UvrC. J Biol Chem 275:5120–5123.
104. Kumura K, Sekiguchi M, Steinum AL, Seeberg E. 1985. Stimulation of the UvrABC enzyme-catalyzed repair reactions by the UvrD protein (DNA helicase II). Nucleic Acids Res 13:1483–1492.
105. Orren DK, Selby CP, Hearst JE, Sancar A. 1992. Post-incision steps of nucleotide excision repair in Escherichia coli. Disassembly of the UvrBC-DNA complex by helicase II and DNA polymerase I. J Biol Chem 267:780–788.
106. Tang MS, Smith KC. 1981. The effects of lexA101, recB21, recF143 and uvrD3 mutations on liquid-holding recovery in ultraviolet-irradiated Escherichia coli K12 recA56. Mutat Res 80:15–25.
107. Washburn BK, Kushner SR. 1991. Construction and analysis of deletions in the structural gene ( uvrD) for DNA helicase II of Escherichia coli. J Bacteriol 173:2569–2575.
108. Moolenaar GF, van Rossum-Fikkert S, van Kesteren M, Goosen N. 2002. Cho, a second endonuclease involved in Escherichia coli nucleotide excision repair. Proc Natl Acad Sci USA 99:1467–1472.
109. Van Houten B, Eisen JA, Hanawalt PC. 2002. A cut above: discovery of an alternative excision repair pathway in bacteria. Proc Natl Acad Sci USA 99:2581–2583.
110. Selby CP, Sancar A. 1993. Molecular mechanism of transcription-repair coupling. Science 260:53–58.
111. Witkin EM. 1956. Time, temperature, and protein synthesis: a study of ultraviolet-induced mutation in bacteria. Cold Spring Harb Symp Quant Biol 21:123–140.
112. Kow YW. 2002. Repair of deaminated bases in DNA. Free Radic Biol Med 33:886–893.
113. Schouten KA, Weiss B. 1999. Endonuclease V protects Escherichia coli against specific mutations caused by nitrous acid. Mutat Res 435:245–254.
114. Cunningham RP, Saporito SM, Spitzer SG, Weiss B. 1986. Endonuclease IV ( nfo) mutant of Escherichia coli. J Bacteriol 168:1120–1127.
115. Ide H, Tedzuka K, Shimzu H, Kimura Y, Purmal AA, Wallace SS, Kow YW. 1994. Alpha-deoxyadenosine, a major anoxic radiolysis product of adenine in DNA, is a substrate for Escherichia coli endonuclease IV. Biochemistry 33:7842–7847.
116. Ischenko AA, Saparbaev MK. 2002. Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature 415:183–187.
117. Gellert M, Bullock ML. 1970. DNA ligase mutants of Escherichia coli. Proc Natl Acad Sci USA 67:1580–1587.
118. Gellert M. 1967. Formation of covalent circles of lambda DNA by E. coli extracts. Proc Natl Acad Sci USA 57:148–155.
119. Gottesman MM, Hicks ML, Gellert M. 1973. Genetics and function of DNA ligase in Escherichia coli. J Mol Biol 77:531–547.
120. Olivera BM, Lehman IR. 1967. Linkage of polynucleotides through phosphodiester bonds by an enzyme from Escherichia coli. Proc Natl Acad Sci USA 57:1426–1433.
121. Bambara RA, Uyemura D, Lehman IR. 1976. On the processive mechanism of Escherichia coli DNA polymerase I. Delayed initiation of polymerization. J Biol Chem 251:4090–4094.
122. Bebenek K, Joyce CM, Fitzgerald MP, Kunkel TA. 1990. The fidelity of DNA synthesis catalyzed by derivatives of Escherichia coli DNA polymerase I. J Biol Chem 265:13878–13887.
123. Kornberg A, Baker TA. 1992. DNA Replication, 2nd ed. W. H. Freeman, New York, NY.
124. Patel PH, Suzuki M, Adman E, Shinkai A, Loeb LA. 2001. Prokaryotic DNA polymerase I: evolution, structure, and “base flipping” mechanism for nucleotide selection. J Mol Biol 308:823–837.
125. Maki H, Sekiguchi M. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355:273–275.
126. Yanofsky C, Cox EC, Horn V. 1966. The unusual mutagenic specificity of an E. coli mutator gene. Proc Natl Acad Sci USA 55:274–281.
127. Bradshaw JS, Kuzminov A. 2003. RdgB acts to avoid chromosome fragmentation in Escherichia coli. Mol Microbiol 48:1711–1725.
128. Budke B, Kuzminov A. 2010. Production of clastogenic DNA precursors by the nucleotide metabolism in Escherichia coli. Mol Microbiol 75:230–245.
129. Chung JH, Park HY, Lee JH, Jang Y. 2002. Identification of the dITP- and XTP-hydrolyzing protein from Escherichia coli. J Biochem Mol Biol 35:403–408.
130. el-Hajj HH, Zhang H, Weiss B. 1988. Lethality of a dut (deoxyuridine triphosphatase) mutation in Escherichia coli. J Bacteriol 170:1069–1075.
131. Hochhauser SJ, Weiss B. 1978. Escherichia coli mutants deficient in deoxyuridine triphosphatase. J Bacteriol 134:157–166.
132. Kouzminova EA, Kuzminov A. 2006. Fragmentation of replicating chromosomes triggered by uracil in DNA. J Mol Biol 355:20–33.
133. Bowles T, Metz AH, O’Quin J, Wawrzak Z, Eichman BF. 2008. Structure and DNA binding of alkylation response protein AidB. Proc Natl Acad Sci USA 105:15299–15304.
134. Landini P, Hajec LI, Volkert MR. 1994. Structure and transcriptional regulation of the Escherichia coli adaptive response gene aidB. J Bacteriol 176:6583–6589.
135. Hidalgo E, Bollinger JM Jr, Bradley TM, Walsh CT, Demple B. 1995. Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription. J Biol Chem 270:20908–20914.
136. Pomposiello PJ, Bennik MH, Demple B. 2001. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183:3890–3902.
137. Tsaneva IR, Weiss B. 1990. soxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J Bacteriol 172:4197–4205.
138. Martin RG, Gillette WK, Rhee S, Rosner JL. 1999. Structural requirements for marbox function in transcriptional activation of mar/sox/rob regulon promoters in Escherichia coli: sequence, orientation and spatial relationship to the core promoter. Mol Microbiol 34:431–441.
139. Nunoshiba T, Hidalgo E, Amabile Cuevas CF, Demple B. 1992. Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene. J Bacteriol 174:6054–6060.
140. Wood TI, Griffith KL, Fawcett WP, Jair KW, Schneider TD, Wolf RE Jr. 1999. Interdependence of the position and orientation of SoxS binding sites in the transcriptional activation of the class I subset of Escherichia coli superoxide-inducible promoters. Mol Microbiol 34:414–430.
141. Christman MF, Storz G, Ames BN. 1989. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci USA 86:3484–3488.
142. Demple B, Halbrook J. 1983. Inducible repair of oxidative DNA damage in Escherichia coli. Nature 304:466–468.
143. Pomposiello PJ, Demple B. 2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–114.
144. Perna NT, Plunkett G III, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA, Posfai G, Hackett J, Klink S, Boutin A, Shao Y, Miller L, Grotbeck EJ, Davis NW, Lim A, Dimalanta ET, Potamousis KD, Apodaca J, Anantharaman TS, Lin J, Yen G, Schwartz DC, Welch RA, Blattner FR. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529–533.
145. Sriskanda V, Shuman S. 2001. A second NAD(+)-dependent DNA ligase (LigB) in Escherichia coli. Nucleic Acids Res 29:4930–4934.
146. Burdett V, Baitinger C, Viswanathan M, Lovett ST, Modrich P. 2001. In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair. Proc Natl Acad Sci USA 98:6765–6770.
147. Lehman IR, Nussbaum AL. 1964. The deoxyribonucleases of Escherichia coli. V. On the specificity of exonuclease I (phosphodiesterase). J Biol Chem 239:2628–2636.
148. Sandigursky M, Franklin WA. 1992. DNA deoxyribophosphodiesterase of Escherichia coli is associated with exonuclease I. Nucleic Acids Res 20:4699–4703.
149. Wang TC, Smith KC. 1985. Mechanism of sbcB-suppression of the recBC-deficiency in postreplication repair in UV-irradiated Escherichia coli K-12. Mol Gen Genet 201:186–191.
150. Courcelle CT, Chow KH, Casey A, Courcelle J. 2006. Nascent DNA processing by RecJ favors lesion repair over translesion synthesis at arrested replication forks in Escherichia coli. Proc Natl Acad Sci USA 103:9154–9159.
151. Dianov G, Lindahl T. 1994. Reconstitution of the DNA base excision-repair pathway. Curr Biol 4:1069–1076.
152. Lloyd RG, Porton MC, Buckman C. 1988. Effect of recF, recJ, recN, recO and ruv mutations on ultraviolet survival and genetic recombination in a recD strain of Escherichia coli K12. Mol Gen Genet 212:317–324.
153. Lovett ST, Kolodner RD. 1989. Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc Natl Acad Sci USA 86:2627–2631.
154. Kelner A. 1949. Effect of visible light on the recovery of Streptomyces Griseus conidia from ultra-violet irradiation injury. Proc Natl Acad Sci USA 35:73–79.
155. Harm W, Harm H, Rupert CS. 1968. Analysis of photoenzymatic repair of UV lesions in DNA by single light flashes. II. In vivo studies with Escherichia coli cells and bacteriophage. Mutat Res 6:371–385.
156. Ihara M, Yamamoto K, Ohnishi T. 1987. Induction of phr gene expression by irradiation of ultraviolet light in Escherichia coli. Mol Gen Genet 209:200–202.
157. Sancar A, Rupert CS. 1978. Correction of the map location for the phr gene in Escherichia coli K12. Mutat Res 51:139–143.
158. Youngs DA, Smith KC. 1978. Genetic location of the phr gene of Escherichia coli K-12. Mutat Res 51:133–137.
159. Bachmann BJ. 1983. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev 47:180–230.
160. Sancar GB, Smith FW, Heelis PF. 1987. Purification of the yeast PHR1 photolyase from an Escherichia coli overproducing strain and characterization of the intrinsic chromophores of the enzyme. J Biol Chem 262:15457–15465.
161. Yasui A, Eker AP, Yasuhira S, Yajima H, Kobayashi T, Takao M, Oikawa A. 1994. A new class of DNA photolyases present in various organisms including aplacental mammals. EMBO J 13:6143–6151.
162. Todo T. 1999. Functional diversity of the DNA photolyase/blue light receptor family. Mutat Res 434:89–97.
163. Sancar A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev 103:2203–2237.
164. Johnson JL, Hamm-Alvarez S, Payne G, Sancar GB, Rajagopalan KV, Sancar A. 1988. Identification of the second chromophore of Escherichia coli and yeast DNA photolyases as 5,10-methenyltetrahydrofolate. Proc Natl Acad Sci USA 85:2046–2050.
165. Li YF, Sancar A. 1991. Cloning, sequencing, expression and characterization of DNA photolyase from Salmonella typhimurium. Nucleic Acids Res 19:4885–4890.
166. Sancar GB. 1990. DNA photolyases: physical properties, action mechanism, and roles in dark repair. Mutat Res 236:147–160.
167. Srinivasan V, Schnitzlein WM, Tripathy DN. 2001. Fowlpox virus encodes a novel DNA repair enzyme, CPD-photolyase, that restores infectivity of UV light-damaged virus. J Virol 75:1681–1688.
168. Langeveld SA, Yasui A, Eker AP. 1985. Expression of an Escherichia coliphr gene in the yeast Saccharomyces cerevisiae. Mol Gen Genet 199:396–400.
169. Sancar GB. 1985. Expression of a Saccharomyces cerevisiae photolyase gene in Escherichia coli. J Bacteriol 161:769–771.
170. Park HW, Kim ST, Sancar A, Deisenhofer J. 1995. Crystal structure of DNA photolyase from Escherichia coli. Science 268:1866–1872.
171. Mees A, Klar T, Gnau P, Hennecke U, Eker AP, Carell T, Essen LO. 2004. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306:1789–1793.
172. Todo T, Takemori H, Ryo H, Ihara M, Matsunaga T, Nikaido O, Sato K, Nomura T. 1993. A new photoreactivating enzyme that specifically repairs ultraviolet light-induced (6–4)photoproducts. Nature 361:371–374.
173. Brash DE, Franklin WA, Sancar GB, Sancar A, Haseltine WA. 1985. Escherichia coli DNA photolyase reverses cyclobutane pyrimidine dimers but not pyrimidine-pyrimidone (6–4) photoproducts. J Biol Chem 260:11438–11441.
174. Daniels DS, Tainer JA. 2000. Conserved structural motifs governing the stoichiometric repair of alkylated DNA by O(6)-alkylguanine-DNA alkyltransferase. Mutat Res 460:151–163.
175. Hakura A, Morimoto K, Sofuni T, Nohmi T. 1991. Cloning and characterization of the Salmonella typhimuriumada gene, which encodes O 6-methylguanine-DNA methyltransferase. J Bacteriol 173:3663–3672.
176. Vaughan P, Sedgwick B. 1991. A weak adaptive response to alkylation damage in Salmonella typhimurium. J Bacteriol 173:3656–3662.
177. Margison GP, Butt A, Pearson SJ, Wharton S, Watson AJ, Marriott A, Caetano CM, Hollins JJ, Rukazenkova N, Begum G, Santibanez-Koref MF. 2007. Alkyltransferase-like proteins. DNA Repair (Amst) 6:1222–1228.
178. Pearson SJ, Ferguson J, Santibanez-Koref M, Margison GP. 2005. Inhibition of O 6-methylguanine-DNA methyltransferase by an alkyltransferase-like protein from Escherichia coli. Nucleic Acids Res 33:3837–3844.
179. Chen CS, Korobkova E, Chen H, Zhu J, Jian X, Tao SC, He C, Zhu H. 2008. A proteome chip approach reveals new DNA damage recognition activities in Escherichia coli. Nat Methods 5:69–74.
180. Tubbs JL, Latypov V, Kanugula S, Butt A, Melikishvili M, Kraehenbuehl R, Fleck O, Marriott A, Watson AJ, Verbeek B, McGown G, Thorncroft M, Santibanez-Koref MF, Millington C, Arvai AS, Kroeger MD, Peterson LA, Williams DM, Fried MG, Margison GP, Pegg AE, Tainer JA. 2009. Flipping of alkylated DNA damage bridges base and nucleotide excision repair. Nature 459:808–813.
181. Kataoka H, Sekiguchi M. 1985. Molecular cloning and characterization of the alkB gene of Escherichia coli. Mol Gen Genet 198:263–269.
182. Chen BJ, Carroll P, Samson L. 1994. The Escherichia coli AlkB protein protects human cells against alkylation-induced toxicity. J Bacteriol 176:6255–6261.
183. Wei YF, Carter KC, Wang RP, Shell BK. 1996. Molecular cloning and functional analysis of a human cDNA encoding an Escherichia coli AlkB homolog, a protein involved in DNA alkylation damage repair. Nucleic Acids Res 24:931–937.
184. Dinglay S, Trewick SC, Lindahl T, Sedgwick B. 2000. Defective processing of methylated single-stranded DNA by E. coli AlkB mutants. Genes Dev 14:2097–2105.
185. Aravind L, Koonin EV. 2001. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol 2:RESEARCH0007.
186. Delaney JC, Essigmann JM. 2004. Mutagenesis, genotoxicity, and repair of 1-methyladenine, 3-alkylcytosines, 1-methylguanine, and 3-methylthymine in alkBEscherichia coli. Proc Natl Acad Sci USA 101:14051–14056.
187. Koivisto P, Robins P, Lindahl T, Sedgwick B. 2004. Demethylation of 3-methylthymine in DNA by bacterial and human DNA dioxygenases. J Biol Chem 279:40470–40474.
188. Delaney JC, Smeester L, Wong C, Frick LE, Taghizadeh K, Wishnok JS, Drennan CL, Samson LD, Essigmann JM. 2005. AlkB reverses etheno DNA lesions caused by lipid oxidation in vitro and in vivo. Nat Struct Mol Biol 12:855–860.
189. Mishina Y, Yang CG, He C. 2005. Direct repair of the exocyclic DNA adduct 1, N 6-ethenoadenine by the DNA repair AlkB proteins. J Am Chem Soc 127:14594–14595.
190. Yu B, Edstrom WC, Benach J, Hamuro Y, Weber PC, Gibney BR, Hunt JF. 2006. Crystal structures of catalytic complexes of the oxidative DNA/RNA repair enzyme AlkB. Nature 439:879–884.
191. Yang CG, Yi C, Duguid EM, Sullivan CT, Jian X, Rice PA, He C. 2008. Crystal structures of DNA/RNA repair enzymes AlkB and ABH2 bound to dsDNA. Nature 452:961–965.
192. Verly WG, Paquette Y. 1972. An endonuclease for depurinated DNA in Escherichia coli B. Can. J Biochem 50:217–224.
193. Lindahl T. 1976. New class of enzymes acting on damaged DNA. Nature 259:64–66.
194. Laval J. 1977. Two enzymes are required from strand incision in repair of alkylated DNA. Nature 269:829–832.
195. Kirtikar DM, Dipple A, Goldthwait DA. 1975. Endonuclease II of Escherichia coli: DNA reacted with 7-bromomethyl-12-methylbenz[alpha]anthracene as a substrate. Biochemistry 14:5548–53.
196. Kirtikar DM, Goldthwait DA. 1974. The enzymatic release of O 6-methylguanine and 3-methyladenine from DNA reacted with the carcinogen N-methyl-N-nitrosourea. Proc Natl Acad Sci USA 71:2022–2026.
197. Krokan HE, Standal R, Slupphaug G. 1997. DNA glycosylases in the base excision repair of DNA. Biochem J 325(Pt 1) :1–16.
198. Sakumi K, Sekiguchi M. 1990. Structures and functions of DNA glycosylases. Mutat Res 236:161–172.
199. Brooks PJ, Wise DS, Berry DA, Kosmoski JV, Smerdon MJ, Somers RL, Mackie H, Spoonde AY, Ackerman EJ, Coleman K, Tarone RE, Robbins JH. 2000. The oxidative DNA lesion 8,5′-(S)-cyclo-2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem 275:22355–22362.
200. Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. 2000. Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci USA 97:3832–3837.
201. Johnson KA, Fink SP, Marnett LJ. 1997. Repair of propanodeoxyguanosine by nucleotide excision repair in vivo and in vitro. J Biol Chem 272:11434–11438.
202. Cunningham RP. 1997. DNA glycosylases. Mutat Res 383:189–196.
203. Dodson ML, Michaels ML, Lloyd RS. 1994. Unified catalytic mechanism for DNA glycosylases. J Biol Chem 269:32709–32712.
204. Demple B, Harrison L. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem 63:915–948.
205. Michaels ML, Miller JH. 1992. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J Bacteriol 174:6321–6325.
206. Saito Y, Uraki F, Nakajima S, Asaeda A, Ono K, Kubo K, Yamamoto K. 1997. Characterization of endonuclease III ( nth) and endonuclease VIII ( nei) mutants of Escherichia coli K-12. J Bacteriol 179:3783–3785.
207. Sung JS, Mosbaugh DW. 2003. Escherichia coli uracil- and ethenocytosine-initiated base excision DNA repair: rate-limiting step and patch size distribution. Biochemistry 42:4613–4625.
208. Scharer OD, Deng L, Verdine GL. 1997. Chemical approaches toward understanding base excision DNA repair. Curr Opin Chem Biol 1:526–531.
209. Weiss B, Grossman L. 1987. Phosphodiesterases involved in DNA repair. Adv Enzymol Relat Areas Mol Biol 60:1–34.
210. Mazumder A, Gerlt JA, Absalon MJ, Stubbe J, Cunningham RP, Withka J, Bolton PH. 1991. Stereochemical studies of the beta-elimination reactions at aldehydic abasic sites in DNA: endonuclease III from Escherichia coli, sodium hydroxide, and Lys-Trp-Lys. Biochemistry 30:1119–1126.
211. Bhagwat M, Gerlt JA. 1996. 3′- and 5′-strand cleavage reactions catalyzed by the Fpg protein from Escherichia coli occur via successive beta- and delta-elimination mechanisms, respectively. Biochemistry 35:659–665.
212. O’Connor TR, Laval J. 1989. Physical association of the 2,6-diamino-4-hydroxy-5N-formamidopyrimidine-DNA glycosylase of Escherichia coli and an activity nicking DNA at apurinic/apyrimidinic sites. Proc Natl Acad Sci USA 86:5222–5226.
213. Dodson ML, Schrock RD III, Lloyd RS. 1993. Evidence for an imino intermediate in the T4 endonuclease V reaction. Biochemistry 32:8284–8290.
214. Schrock RD III, Lloyd RS. 1991. Reductive methylation of the amino terminus of endonuclease V eradicates catalytic activities. Evidence for an essential role of the amino terminus in the chemical mechanisms of catalysis. J Biol Chem 266:17631–17639.
215. Boiteux S, O’Connor TR, Laval J. 1987. Formamidopyrimidine-DNA glycosylase of Escherichia coli: cloning and sequencing of the fpg structural gene and overproduction of the protein. EMBO J 6:3177–83.
216. Boiteux S, O’Connor TR, Lederer F, Gouyette A, Laval J. 1990. Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidinic sites. J Biol Chem 265:3916–3922.
217. Hatahet Z, Kow YW, Purmal AA, Cunningham RP, Wallace SS. 1994. New substrates for old enzymes. 5-Hydroxy-2′-deoxycytidine and 5-hydroxy-2′-deoxyuridine are substrates for Escherichia coli endonuclease III and formamidopyrimidine DNA N-glycosylase, while 5-hydroxy-2′-deoxyuridine is a substrate for uracil DNA N-glycosylase. J Biol Chem 269:18814–18820.
218. Jurado J, Saparbaev M, Matray TJ, Greenberg MM, Laval J. 1998. The ring fragmentation product of thymidine C5-hydrate when present in DNA is repaired by the Escherichia coli Fpg and Nth proteins. Biochemistry 37:7757–7763.
219. D’Ham C, Romieu A, Jaquinod M, Gasparutto D, Cadet J. 1999. Excision of 5,6-dihydroxy-5,6-dihydrothymine, 5,6-dihydrothymine, and 5-hydroxycytosine from defined sequence oligonucleotides by Escherichia coli endonuclease III and Fpg proteins: kinetic and mechanistic aspects. Biochemistry 38:3335–3344.
220. Bailly V, Verly WG, O’Connor T, Laval J. 1989. Mechanism of DNA strand nicking at apurinic/apyrimidinic sites by Escherichia coli [formamidopyrimidine]DNA glycosylase. Biochem J 262:581–589.
221. Graves RJ, Felzenszwalb I, Laval J, O’Connor TR. 1992. Excision of 5′-terminal deoxyribose phosphate from damaged DNA is catalyzed by the Fpg protein of Escherichia coli. J Biol Chem 267:14429–14435.
222. David SS, O’Shea VL, Kundu S. 2007. Base-excision repair of oxidative DNA damage. Nature 447:941–950.
223. Tajiri T, Maki H, Sekiguchi M. 1995. Functional cooperation of MutT, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat Res 336:257–267.
224. Duwat P, de Oliveira R, Ehrlich SD, Boiteux S. 1995. Repair of oxidative DNA damage in gram-positive bacteria: the Lactococcus lactis Fpg protein. Microbiology 141(Pt 2) :411–417.
225. Laval F. 1994. Expression of the E. colifpg gene in mammalian cells reduces the mutagenicity of gamma-rays. Nucleic Acids Res 22:4943–4946.
226. Ropolo M, Geroldi A, Degan P, Andreotti V, Zupo S, Poggi A, Reed A, Kelley MR, Frosina G. 2006. Accelerated repair and reduced mutagenicity of oxidative DNA damage in human bladder cells expressing the E. coli FPG protein. Int J Cancer 118:1628–1634.
227. O’Connor TR, Graves RJ, de Murcia G, Castaing B, Laval J. 1993. Fpg protein of Escherichia coli is a zinc finger protein whose cysteine residues have a structural and/or functional role. J Biol Chem 268:9063–9070.
228. Zharkov DO, Rieger RA, Iden CR, Grollman AP. 1997. NH 2-terminal proline acts as a nucleophile in the glycosylase/AP-lyase reaction catalyzed by Escherichia coli formamidopyrimidine-DNA glycosylase (Fpg) protein. J Biol Chem 272:5335–5341.
229. Sidorkina OM, Laval J. 2000. Role of the N-terminal proline residue in the catalytic activities of the Escherichia coli Fpg protein. J Biol Chem 275:9924–9929.
230. Sidorkina OM, Laval J. 1998. Role of lysine-57 in the catalytic activities of Escherichia coli formamidopyrimidine-DNA glycosylase (Fpg protein). Nucleic Acids Res 26:5351–5357.
231. Rabow LE, Kow YW. 1997. Mechanism of action of base release by Escherichia coli Fpg protein: role of lysine 155 in catalysis. Biochemistry 36:5084–5096.
232. Lavrukhin OV, Lloyd RS. 2000. Involvement of phylogenetically conserved acidic amino acid residues in catalysis by an oxidative DNA damage enzyme formamidopyrimidine glycosylase. Biochemistry 39:15266–15271.
233. Gilboa R, Zharkov DO, Golan G, Fernandes AS, Gerchman SE, Matz E, Kycia JH, Grollman AP, Shoham G. 2002. Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J Biol Chem 277:19811–19816.
234. Serre L, Pereira de Jesus K, Boiteux S, Zelwer C, Castaing B. 2002. Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analogue-containing DNA. EMBO J 21:2854–2865.
235. Coste F, Ober M, Carell T, Boiteux S, Zelwer C, Castaing B. 2004. Structural basis for the recognition of the FapydG lesion (2,6-diamino-4-hydroxy-5-formamidopyrimidine) by the Fpg DNA glycosylase. J Biol Chem 279:44074–44083.
236. Coste F, Ober M, Le Bihan YV, Izquierdo MA, Hervouet N, Mueller H, Carell T, Castaing B. 2008. Bacterial base excision repair enzyme Fpg recognizes bulky N7-substituted-FapydG lesion via unproductive binding mode. Chem Biol 15:706–717.
237. Vassylyev DG, Kashiwagi T, Mikami Y, Ariyoshi M, Iwai S, Ohtsuka E, Morikawa K. 1995. Atomic model of a pyrimidine dimer excision repair enzyme complexed with a DNA substrate: structural basis for damaged DNA recognition. Cell 83:773–782.
238. Hosfield DJ, Guan Y, Haas BJ, Cunningham RP, Tainer JA. 1999. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell 98:397–408.
239. Dalhus B, Arvai AS, Rosnes I, Olsen OE, Backe PH, Alseth I, Gao H, Cao W, Tainer JA, Bjoras M. 2009. Structures of endonuclease V with DNA reveal initiation of deaminated adenine repair. Nat Struct Mol Biol 16:138–143.
240. Demple B, Linn S. 1980. DNA N-glycosylases and UV repair. Nature 287:203–208.
241. Radman M. 1976. An endonuclease from Escherichia coli that introduces single polynucleotide chain scissions in ultraviolet-irradiated DNA. J Biol Chem 251:1438–1445.
242. Matsumoto Y, Zhang QM, Takao M, Yasui A, Yonei S. 2001. Escherichia coli Nth and human hNTH1 DNA glycosylases are involved in removal of 8-oxoguanine from 8-oxoguanine/guanine mispairs in DNA. Nucleic Acids Res 29:1975–1981.
243. Hazra TK, Hill JW, Izumi T, Mitra S. 2001. Multiple DNA glycosylases for repair of 8-oxoguanine and their potential in vivo functions. Prog Nucleic Acid Res Mol Biol 68:193–205.
244. Bailly V, Verly WG. 1989. AP endonucleases and AP lyases. Nucleic Acids Res 17:3617–3618.
245. Kim J, Linn S. 1988. The mechanisms of action of E. coli endonuclease III and T4 UV endonuclease (endonuclease V) at AP sites. Nucleic Acids Res 16:1135–1141.
246. Kuo CF, McRee DE, Cunningham RP, Tainer JA. 1992. Crystallization and crystallographic characterization of the iron-sulfur-containing DNA-repair enzyme endonuclease III from Escherichia coli. J Mol Biol 227:347–351.
247. Cunningham RP, Asahara H, Bank JF, Scholes CP, Salerno JC, Surerus K, Munck E, McCracken J, Peisach J, Emptage MH. 1989. Endonuclease III is an iron-sulfur protein. Biochemistry 28:4450–4455.
248. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA. 1995. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J 14:4108–4120.
249. Boal AK, Genereux JC, Sontz PA, Gralnick JA, Newman DK, Barton JK. 2009. Redox signaling between DNA repair proteins for efficient lesion detection. Proc Natl Acad Sci USA 106:15237–15242.
250. Boal AK, Yavin E, Lukianova OA, O’Shea VL, David SS, Barton JK. 2005. DNA-bound redox activity of DNA repair glycosylases containing [4Fe-4S] clusters. Biochemistry 44:8397–8407.
251. Romano CA, Sontz PA, Barton JK. 2011. Mutants of the base excision repair glycosylase, endonuclease III: DNA charge transport as a first step in lesion detection. Biochemistry 50:6133–6145.
252. Jiang D, Hatahet Z, Blaisdell JO, Melamede RJ, Wallace SS. 1997. Escherichia coli endonuclease VIII: cloning, sequencing, and overexpression of the nei structural gene and characterization of nei and nei nth mutants. J Bacteriol 179:3773–3782.
253. Burgess S, Jaruga P, Dodson ML, Dizdaroglu M, Lloyd RS. 2002. Determination of active site residues in Escherichia coli endonuclease VIII. J Biol Chem 277:2938–2944.
254. Blaisdell JO, Hatahet Z, Wallace SS. 1999. A novel role for Escherichia coli endonuclease VIII in prevention of spontaneous G→T transversions. J Bacteriol 181:6396–6402.
255. Hazra TK, Izumi T, Venkataraman R, Kow YW, Dizdaroglu M, Mitra S. 2000. Characterization of a novel 8-oxoguanine-DNA glycosylase activity in Escherichia coli and identification of the enzyme as endonuclease VIII. J Biol Chem 275:27762–27767.
256. Dizdaroglu M, Burgess SM, Jaruga P, Hazra TK, Rodriguez H, Lloyd RS. 2001. Substrate specificity and excision kinetics of Escherichia coli endonuclease VIII (Nei) for modified bases in DNA damaged by free radicals. Biochemistry 40:12150–12156.
257. Joffe A, Geacintov NE, Shafirovich V. 2003. DNA lesions derived from the site selective oxidation of Guanine by carbonate radical anions. Chem Res Toxicol 16:1528–1538.
258. Stover JS, Ciobanu M, Cliffel DE, Rizzo CJ. 2007. Chemical and electrochemical oxidation of C8-arylamine adducts of 2′-deoxyguanosine. J Am Chem Soc 129:2074–2081.
259. Hazra TK, Muller JG, Manuel RC, Burrows CJ, Lloyd RS, Mitra S. 2001. Repair of hydantoins, one electron oxidation product of 8-oxoguanine, by DNA glycosylases of Escherichia coli. Nucleic Acids Res 29:1967–1974.
260. Hailer MK, Slade PG, Martin BD, Sugden KD. 2005. Nei deficient Escherichia coli are sensitive to chromate and accumulate the oxidized guanine lesion spiroiminodihydantoin. Chem Res Toxicol 18:1378–1383.
261. Couve S, Mace-Aime G, Rosselli F, Saparbaev MK. 2009. The human oxidative DNA glycosylase NEIL1 excises psoralen-induced interstrand DNA cross-links in a three-stranded DNA structure. J Biol Chem 284:11963–11970.
262. Couve-Privat S, Mace G, Rosselli F, Saparbaev MK. 2007. Psoralen-induced DNA adducts are substrates for the base excision repair pathway in human cells. Nucleic Acids Res 35:5672–5682.
263. Zharkov DO, Grollman AP. 1998. MutY DNA glycosylase: base release and intermediate complex formation. Biochemistry 37:12384–12394.
264. Golan G, Zharkov DO, Feinberg H, Fernandes AS, Zaika EI, Kycia JH, Grollman AP, Shoham G. 2005. Structure of the uncomplexed DNA repair enzyme endonuclease VIII indicates significant interdomain flexibility. Nucleic Acids Res 33:5006–5016.
265. Saparbaev M, Laval J. 1994. Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases. Proc Natl Acad Sci USA 91:5873–5877.
266. Bjelland S, Birkeland NK, Benneche T, Volden G, Seeberg E. 1994. DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the AlkA enzyme in Escherichia coli. J Biol Chem 269:30489–30495.
267. Privezentzev CV, Saparbaev M, Sambandam A, Greenberg MM, Laval J. 2000. AlkA protein is the third Escherichia coli DNA repair protein excising a ring fragmentation product of thymine. Biochemistry 39:14263–14268.
268. Habraken Y, Carter CA, Sekiguchi M, Ludlum DB. 1991. Release of N 2,3-ethanoguanine from haloethylnitrosourea-treated DNA by Escherichia coli 3-methyladenine DNA glycosylase II. Carcinogenesis 12:1971–1973.
269. Matijasevic Z, Sekiguchi M, Ludlum DB. 1992. Release of N 2,3-ethenoguanine from chloroacetaldehyde-treated DNA by Escherichia coli 3-methyladenine DNA glycosylase II. Proc Natl Acad Sci USA 89:9331–9334.
270. Saparbaev M, Kleibl K, Laval J. 1995. Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1, N 6-ethenoadenine when present in DNA. Nucleic Acids Res 23:3750–3755.
271. Bramson J, O’Connor T, Panasci L. 1995. Effect of alkyl-N-purine DNA glycosylase overexpression on cellular resistance to bifunctional alkylating agents. Biochem Pharmacol 50:39–44.
272. Sidorkina O, Saparbaev M, Laval J. 1997. Effects of nitrous acid treatment on the survival and mutagenesis of Escherichia coli cells lacking base excision repair (hypoxanthine-DNA glycosylase-ALK A protein) and/or nucleotide excision repair. Mutagenesis 12:23–28.
273. Berdal KG, Johansen RF, Seeberg E. 1998. Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J 17:363–367.
274. Labahn J, Scharer OD, Long A, Ezaz-Nikpay K, Verdine GL, Ellenberger TE. 1996. Structural basis for the excision repair of alkylation-damaged DNA. Cell 86:321–329.
275. Yamagata Y, Kato M, Odawara K, Tokuno Y, Nakashima Y, Matsushima N, Yasumura K, Tomita K, Ihara K, Fujii Y, Nakabeppu Y, Sekiguchi M, Fujii S. 1996. Three-dimensional structure of a DNA repair enzyme, 3-methyladenine DNA glycosylase II, from Escherichia coli. Cell 86:311–319.
276. Bowman BR, Lee S, Wang S, Verdine GL. 2010. Structure of Escherichia coli AlkA in complex with undamaged DNA. J Biol Chem 285:35783–35791.
277. Metz AH, Hollis T, Eichman BF. 2007. DNA damage recognition and repair by 3-methyladenine DNA glycosylase I (TAG). EMBO J 26:2411–2420.
278. Mosbaugh DW, Bennett SE. 1994. Uracil-excision DNA repair. Prog Nucleic Acid Res Mol Biol 48:315–370.
279. Slupphaug G, Mol CD, Kavli B, Arvai AS, Krokan HE, Tainer JA. 1996. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 384:87–92.
280. Bennett SE, Jensen ON, Barofsky DF, Mosbaugh DW. 1994. UV-catalyzed cross-linking of Escherichia coli uracil-DNA glycosylase to DNA. Identification of amino acid residues in the single-stranded DNA binding site. J Biol Chem 269:21870–21879.
281. Varshney U, Hutcheon T, van de Sande JH. 1988. Sequence analysis, expression, and conservation of Escherichia coli uracil DNA glycosylase and its gene ( ung). J Biol Chem 263:7776–7784.
282. Pearl LH. 2000. Structure and function in the uracil-DNA glycosylase superfamily. Mutat Res 460:165–181.
283. Ingraham HA, Tseng BY, Goulian M. 1980. Mechanism for exclusion of 5-fluorouracil from DNA. Cancer Res 40:998–1001.
284. Zastawny TH, Doetsch PW, Dizdaroglu M. 1995. A novel activity of E. coli uracil DNA N-glycosylase excision of isodialuric acid (5,6-dihydroxyuracil), a major product of oxidative DNA damage, from DNA. FEBS Lett 364:255–258.
285. Bennett SE, Sanderson RJ, Mosbaugh DW. 1995. Processivity of Escherichia coli and rat liver mitochondrial uracil-DNA glycosylase is affected by NaCl concentration. Biochemistry 34:6109–6119.
286. Lindahl T, Ljungquist S, Siegert W, Nyberg B, Sperens B. 1977. DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli. J Biol Chem 252:3286–3294.
287. Cao C, Jiang YL, Krosky DJ, Stivers JT. 2006. The catalytic power of uracil DNA glycosylase in the opening of thymine base pairs. J Am Chem Soc 128:13034–13035.
288. Parker JB, Bianchet MA, Krosky DJ, Friedman JI, Amzel LM, Stivers JT. 2007. Enzymatic capture of an extrahelical thymine in the search for uracil in DNA. Nature 449:433–437.
289. Porecha RH, Stivers JT. 2008. Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils. Proc Natl Acad Sci USA 105:10791–10796.
290. Aravind L, Koonin EV. 2000. The alpha/beta fold uracil DNA glycosylases: a common origin with diverse fates. Genome Biol 1:RESEARCH0007.
291. Barrett TE, Scharer OD, Savva R, Brown T, Jiricny J, Verdine GL, Pearl LH. 1999. Crystal structure of a thwarted mismatch glycosylase DNA repair complex. EMBO J 18:6599–6609.
292. Sandigursky M, Franklin WA. 1999. Thermostable uracil-DNA glycosylase from Thermotoga maritima a member of a novel class of DNA repair enzymes. Curr Biol 9:531–534.
293. Sandigursky M, Franklin WA. 2000. Uracil-DNA glycosylase in the extreme thermophile Archaeoglobus fulgidus. J Biol Chem 275:19146–19149.
294. Haushalter KA, Todd Stukenberg MW, Kirschner MW, Verdine GL. 1999. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr Biol 9:174–185.
295. Sartori AA, Fitz-Gibbon S, Yang H, Miller JH, Jiricny J. 2002. A novel uracil-DNA glycosylase with broad substrate specificity and an unusual active site. EMBO J 21:3182–3191.
296. Hang B, Downing G, Guliaev AB, Singer B. 2002. Novel activity of Escherichia coli mismatch uracil-DNA glycosylase (Mug) excising 8-(hydroxymethyl)-3,N4-ethenocytosine, a potential product resulting from glycidaldehyde reaction. Biochemistry 41:2158–2165.
297. Borys-Brzywczy E, Arczewska KD, Saparbaev M, Hardeland U, Schar P, Kusmierek JT. 2005. Mismatch dependent uracil/thymine-DNA glycosylases excise exocyclic hydroxyethano and hydroxypropano cytosine adducts. Acta Biochim Pol 52:149–165.
298. Jurado J, Maciejewska A, Krwawicz J, Laval J, Saparbaev MK. 2004. Role of mismatch-specific uracil-DNA glycosylase in repair of 3, N(4)-ethenocytosine in vivo. DNA Repair (Amst) 3:1579–1590.
299. Lutsenko E, Bhagwat AS. 1999. The role of the Escherichia colimug protein in the removal of uracil and 3, N(4)-ethenocytosine from DNA. J Biol Chem 274:31034–31038.
300. O’Neill RJ, Vorob’eva OV, Shahbakhti H, Zmuda E, Bhagwat AS, Baldwin GS. 2003. Mismatch uracil glycosylase from Escherichia coli: a general mismatch or a specific DNA glycosylase? J Biol Chem 278:20526–20532.
301. Barrett TE, Savva R, Panayotou G, Barlow T, Brown T, Jiricny J, Pearl LH. 1998. Crystal structure of a G:T/U mismatch-specific DNA glycosylase: mismatch recognition by complementary-strand interactions. Cell 92:117–129.
302. Tsai-Wu JJ, Liu HF, Lu AL. 1992. Escherichia coli MutY protein has both N-glycosylase and apurinic/apyrimidinic endonuclease activities on A.C and A.G mispairs. Proc Natl Acad Sci USA 89:8779–8783.
303. David SS, Williams SD. 1998. Chemistry of glycosylases and endonucleases involved in base-excision repair. Chem Rev 98:1221–1262.
304. Manuel RC, Lloyd RS. 1997. Cloning, overexpression, and biochemical characterization of the catalytic domain of MutY. Biochemistry 36:11140–11152.
305. Manuel RC, Hitomi K, Arvai AS, House PG, Kurtz AJ, Dodson ML, McCullough AK, Tainer JA, Lloyd RS. 2004. Reaction intermediates in the catalytic mechanism of Escherichia coli MutY DNA glycosylase. J Biol Chem 279:46930–46939.
306. Chmiel NH, Golinelli MP, Francis AW, David SS. 2001. Efficient recognition of substrates and substrate analogs by the adenine glycosylase MutY requires the C-terminal domain. Nucleic Acids Res 29:553–564.
307. Pope MA, Porello SL, David SS. 2002. Escherichia coli apurinic-apyrimidinic endonucleases enhance the turnover of the adenine glycosylase MutY with G:A substrates. J Biol Chem 277:22605–22615.
308. Guan Y, Manuel RC, Arvai AS, Parikh SS, Mol CD, Miller JH, Lloyd S, Tainer JA. 1998. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat Struct Biol 5:1058–1064.
309. Fromme JC, Banerjee A, Huang SJ, Verdine GL. 2004. Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature 427:652–656.
310. Strauss BS. 1991. The ‘A rule’ of mutagen specificity: a consequence of DNA polymerase bypass of non-instructional lesions? Bioessays 13:79–84.
311. Barzilay G, Hickson ID. 1995. Structure and function of apurinic/apyrimidinic endonucleases. Bioessays 17:713–719.
312. Mol CD, Kuo CF, Thayer MM, Cunningham RP, Tainer JA. 1995. Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374:381–386.
313. Rogers SG, Weiss B. 1980. Exonuclease III of Escherichia coli K-12, an AP endonuclease. Methods Enzymol 65:201–211.
314. Shida T, Noda M, Sekiguchi J. 1996. Cleavage of single- and double-stranded DNAs containing an abasic residue by Escherichia coli exonuclease III (AP endonuclease VI). Nucleic Acids Res 24:4572–4576.
315. Kow YW, Wallace SS. 1985. Exonuclease III recognizes urea residues in oxidized DNA. Proc Natl Acad Sci USA 82:8354–8358.
316. Sammartano LJ, Tuveson RW. 1983. Escherichia colixthA mutants are sensitive to inactivation by broad-spectrum near-UV (300- to 400-nm) radiation. J Bacteriol 156:904–906.
317. Zieg J, Maples VF, Kushner SR. 1978. Recombinant levels of Escherichia coli K-12 mutants deficient in various replication, recombination, or repair genes. J Bacteriol 134:958–966.
318. Kuzminov A. 1999. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63:751–813.
319. Centore RC, Lestini R, Sandler SJ. 2008. XthA (Exonuclease III) regulates loading of RecA onto DNA substrates in log phase Escherichia coli cells. Mol Microbiol 67:88–101.
320. Ljungquist S. 1977. A new endonuclease from Escherichia coli acting at apurinic sites in DNA. J Biol Chem 252:2808–2814.
321. Levin JD, Shapiro R, Demple B. 1991. Metalloenzymes in DNA repair. Escherichia coli endonuclease IV and Saccharomycescerevisiae Apn1. J Biol Chem 266:22893–22898.
322. Nunoshiba T, deRojas-Walker T, Wishnok JS, Tannenbaum SR, Demple B. 1993. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc Natl Acad Sci USA 90:9993–9997.
323. Daviet S, Couve-Privat S, Gros L, Shinozuka K, Ide H, Saparbaev M, Ishchenko AA. 2007. Major oxidative products of cytosine are substrates for the nucleotide incision repair pathway. DNA Repair (Amst) 6:8–18.
324. Ishchenko AA, Sanz G, Privezentzev CV, Maksimenko AV, Saparbaev M. 2003. Characterisation of new substrate specificities of Escherichia coli and Saccharomyces cerevisiae AP endonucleases. Nucleic Acids Res 31:6344–6353.
325. Ishchenko AA, Ide H, Ramotar D, Nevinsky G, Saparbaev M. 2004. Alpha-anomeric deoxynucleotides, anoxic products of ionizing radiation, are substrates for the endonuclease IV-type AP endonucleases. Biochemistry 43:15210–15216.
326. Levin JD, Johnson AW, Demple B. 1988. Homogeneous Escherichia coli endonuclease IV. Characterization of an enzyme that recognizes oxidative damage in DNA. J Biol Chem 263:8066–8071.
327. Kerins SM, Collins R, McCarthy TV. 2003. Characterization of an endonuclease IV 3′-5′ exonuclease activity. J Biol Chem 278:3048–3054.
328. Ishchenko AA, Yang X, Ramotar D, Saparbaev M. 2005. The 3′→5′ exonuclease of apn1 provides an alternative pathway to repair 7,8-dihydro-8-oxodeoxyguanosine in Saccharomyces cerevisiae. Mol Cell Biol 25:6380–6390.
329. Garcin ED, Hosfield DJ, Desai SA, Haas BJ, Bjoras M, Cunningham RP, Tainer JA. 2008. DNA apurinic-apyrimidinic site binding and excision by endonuclease IV. Nat Struct Mol Biol 15:515–522.
330. Yang X, Tellier P, Masson JY, Vu T, Ramotar D. 1999. Characterization of amino acid substitutions that severely alter the DNA repair functions of Escherichia coli endonuclease IV. Biochemistry 38:3615–3623.
331. Hill RF. 1958. A radiation-sensitive mutant of Escherichia coli. Biochim Biophys Acta 30:636–637.
332. Hanawalt P, Setlow R. 1960. Effect of monochromatic ultraviolet light on macromolecular synthesis in Escherichia coli. Biochim Biophys Acta 41:283–294.
333. Howard-Flanders P, Boyce RP, Theriot L. 1966. Three loci in Escherichia coli K-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 53:1119–1136.
334. Setlow RB, Swenson PA, Carrier WL. 1963. Thymine dimers and inhibition of DNA synthesis by ultraviolet irradiation of cells. Science 142:1464–1466.
335. Pettijohn D, Hanawalt P. 1964. Evidence for repair-replication of ultraviolet damaged DNA in bacteria. J Mol Biol 9:395–410.
336. van de Putte P, van Sluis CA, van Dillewijn J, Rorsch A. 1965. The location of genes controlling radiation sensitivity in Escherichia coli. Mutat Res 2:97–110.
337. Howard-Flanders P, Theriot L. 1962. A method for selecting radiation-sensitive mutants of Escherichia coli. Genetics 47:1219–1224.
338. Seeberg E, Steinum AL. 1982. Purification and properties of the UvrA protein from Escherichia coli. Proc Natl Acad Sci USA 79:988–992.
339. Wang H, Lu M, Tang MS, Van Houten B, Ross JB, Weinfeld M, Le XC. 2009. DNA wrapping is required for DNA damage recognition in the Escherichia coli DNA nucleotide excision repair pathway. Proc Natl Acad Sci USA 106:12849–12854.
340. Lin JJ, Phillips AM, Hearst JE, Sancar A. 1992. Active site of (A)BC excinuclease. II. Binding, bending, and catalysis mutants of UvrB reveal a direct role in 3′ and an indirect role in 5′ incision. J Biol Chem 267:17693–17700.
341. Lin JJ, Sancar A. 1992. Active site of (A)BC excinuclease. I. Evidence for 5′ incision by UvrC through a catalytic site involving Asp399, Asp438, Asp466, and His538 residues. J Biol Chem 267:17688–17692.
342. Van Houten B, Croteau DL, DellaVecchia MJ, Wang H, Kisker C. 2005. ‘Close-fitting sleeves’: DNA damage recognition by the UvrABC nuclease system. Mutat Res 577:92–117.
343. Goosen N, Moolenaar GF, Visse R, van de Putte P. 1998. Functional domains of the E. coli UvrABC proteins in nucleotide excision repair, p 103–123. In Eckstein F and Eckstein DMJ (ed), Nucleic Acids and Molecular Biology: DNA Repair. Springer Verlag, Berlin, Germany.
344. Truglio JJ, Croteau DL, Van Houten B, Kisker C. 2006. Prokaryotic nucleotide excision repair: the UvrABC system. Chem Rev 106:233–252.
345. Seeberg E, Steinum AL, Nordenskjold M, Soderhall S, Jernstrom B. 1983. Strand-break formation in DNA modified by benzo[alpha]pyrene diolepoxide. Quantitative cleavage by Escherichia coli uvrABC endonuclease. Mutat Res 112:139–145.
346. Zou Y, Shell SM, Utzat CD, Luo C, Yang Z, Geacintov NE, Basu AK. 2003. Effects of DNA adduct structure and sequence context on strand opening of repair intermediates and incision by UvrABC nuclease. Biochemistry 42:12654–12661.
347. Minko IG, Kurtz AJ, Croteau DL, Van Houten B, Harris TM, Lloyd RS. 2005. Initiation of repair of DNA-polypeptide cross-links by the UvrABC nuclease. Biochemistry 44:3000–3009.
348. Minko IG, Zou Y, Lloyd RS. 2002. Incision of DNA-protein crosslinks by UvrABC nuclease suggests a potential repair pathway involving nucleotide excision repair. Proc Natl Acad Sci USA 99:1905–1909.
349. Koo HS, Claassen L, Grossman L, Liu LF. 1991. ATP-dependent partitioning of the DNA template into supercoiled domains by Escherichia coli UvrAB. Proc Natl Acad Sci U S A 88:1212–1216.
350. Oh EY, Grossman L. 1987. Helicase properties of the Escherichia coli UvrAB protein complex. Proc Natl Acad Sci USA 84:3638–3642.
351. Oh EY, Grossman L. 1989. Characterization of the helicase activity of the Escherichia coli UvrAB protein complex. J Biol Chem 264: 1336–1343.
352. Gordienko I, Rupp WD. 1997. The limited strand-separating activity of the UvrAB protein complex and its role in the recognition of DNA damage. EMBO J 16:889–895.
353. Theis K, Skorvaga M, Machius M, Nakagawa N, Van Houten B, Kisker C. 2000. The nucleotide excision repair protein UvrB, a helicase-like enzyme with a catch. Mutat Res 460:277–300.
354. Doolittle RF, Johnson MS, Husain I, Van Houten B, Thomas DC, Sancar A. 1986. Domainal evolution of a prokaryotic DNA repair protein and its relationship to active-transport proteins. Nature 323:451–453.
355. Van Houten B, Gamper H, Sancar A, Hearst JE. 1987. DNase I footprint of ABC excinuclease. J Biol Chem 262:13180–13187.
356. Myles GM, Sancar A. 1989. DNA repair. Chem Res Toxicol 2:197–226.
357. Navaratnam S, Myles GM, Strange RW, Sancar A. 1989. Evidence from extended X-ray absorption fine structure and site-specific mutagenesis for zinc fingers in UvrA protein of Escherichia coli. J Biol Chem 264:16067–16071.
358. Wang J, Mueller KL, Grossman L. 1994. A mutational study of the C-terminal zinc-finger motif of the Escherichia coli UvrA protein. J Biol Chem 269:10771–10775.
359. Visse R, de Ruijter M, Ubbink M, Brandsma JA, van de Putte P. 1993. The first zinc-binding domain of UvrA is not essential for UvrABC-mediated DNA excision repair. Mutat Res 294:263–274.
360. Ylihonko K, Tuikkanen J, Jussila S, Cong L, Mantsala P. 1996. A gene cluster involved in nogalamycin biosynthesis from Streptomyces nogalater: sequence analysis and complementation of early-block mutations in the anthracycline pathway. Mol Gen Genet 251:113–120.
361. Sancar A, Hearst JE. 1993. Molecular matchmakers. Science 259:1415–1420.
362. Lomovskaya N, Hong SK, Kim SU, Fonstein L, Furuya K, Hutchinson RC. 1996. The Streptomyces peucetius drrC gene encodes a UvrA-like protein involved in daunorubicin resistance and production. J Bacteriol 178:3238–3245.
363. Machius M, Henry L, Palnitkar M, Deisenhofer J. 1999. Crystal structure of the DNA nucleotide excision repair enzyme UvrB from Thermus thermophilus. Proc Natl Acad Sci USA 96:11717–11722.
364. Malta E, Moolenaar GF, Goosen N. 2006. Base flipping in nucleotide excision repair. J Biol Chem 281:2184–2194.
365. Skorvaga M, Theis K, Mandavilli BS, Kisker C, Van Houten B. 2002. The beta-hairpin motif of UvrB is essential for DNA binding, damage processing, and UvrC-mediated incisions. J Biol Chem 277:1553–1559.
366. Malta E, Verhagen CP, Moolenaar GF, Filippov DV, van der Marel GA, Goosen N. 2008. Functions of base flipping in E. coli nucleotide excision repair. DNA Repair (Amst) 7:1647–1658.
367. Aravind L, Walker DR, Koonin EV. 1999. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 27:1223–1242.
368. Karakas E, Truglio JJ, Croteau D, Rhau B, Wang L, Van Houten B, Kisker C. 2007. Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad. EMBO J 26:613–622.
369. Moolenaar GF, Uiterkamp RS, Zwijnenburg DA, Goosen N. 1998. The C-terminal region of the Escherichia coli UvrC protein, which is homologous to the C-terminal region of the human ERCC1 protein, is involved in DNA binding and 5′-incision. Nucleic Acids Res 26:462–468.
370. Moolenaar GF, Franken KL, Dijkstra DM, Thomas-Oates JE, Visse R, van de Putte P, Goosen N. 1995. The C-terminal region of the UvrB protein of Escherichia coli contains an important determinant for UvrC binding to the preincision complex but not the catalytic site for 3′-incision. J Biol Chem 270:30508–30515.
371. Moolenaar GF, Franken KL, van de Putte P, Goosen N. 1997. Function of the homologous regions of the Escherichia coli DNA excision repair proteins UvrB and UvrC in stabilization of the UvrBC-DNA complex and in 3′-incision. Mutat Res 385:195–203.
372. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35:1560–1572.
373. Cassuto E, Gross N, Bardwell E, Howard-Flanders P. 1977. Genetic effects of photoadducts and photocross-links in the DNA of phage lambda exposed to 360 nm light and tri-methylpsoralen or khellin. Biochim Biophys Acta 475:589–600.
374. Chanet R, Cassier C, Magana-Schwencke N, Moustacchi E. 1983. Fate of photo-induced 8-methoxypsoralen mono-adducts in yeast. Evidence for bypass of these lesions in the absence of excision repair. Mutat Res 112:201–214.
375. Cole RS. 1973. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination. Proc Natl Acad Sci USA 70:1064–1068.
376. Lin PF, Bardwell E, Howard-Flanders P. 1977. Initiation of genetic exchanges in lambda phage–prophage crosses. Proc Natl Acad Sci USA 74:291–295.
377. Sinden RR, Cole RS. 1978. Repair of cross-linked DNA and survival of Escherichia coli treated with psoralen and light: effects of mutations influencing genetic recombination and DNA metabolism. J Bacteriol 136:538–547.
378. Yoakum GH, Cole RS. 1977. Role of ATP in removal of psoralen cross-links from DNA of Escherichia coli permeabilized by treatment with toluene. J Biol Chem 252:7023–7030.
379. Yoakum GH, Cole RS. 1978. Cross-linking and relaxation of supercoiled DNA by psoralen and light. Biochim Biophys Acta 521:529–546.
380. Van Houten B, Gamper H, Holbrook SR, Hearst JE, Sancar A. 1986. Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defined position. Proc Natl Acad Sci USA 83:8077–8081.
381. Jones BK, Yeung AT. 1988. Repair of 4,5′,8-trimethylpsoralen monoadducts and cross-links by the Escherichia coli UvrABC endonuclease. Proc Natl Acad Sci USA 85:8410–8414.
382. Sladek FM, Munn MM, Rupp WD, Howard-Flanders P. 1989. In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 5′-exonuclease of DNA polymerase I. J Biol Chem 264:6755–6765.
383. Cheng S, Van Houten B, Gamper HB, Sancar A, Hearst JE. 1988. Use of psoralen-modified oligonucleotides to trap three-stranded RecA-DNA complexes and repair of these cross-linked complexes by ABC excinuclease. J Biol Chem 263:15110–15117.
384. Peng X, Ghosh AK, Van Houten B, Greenberg MM. 2010. Nucleotide excision repair of a DNA interstrand cross-link produces single- and double-strand breaks. Biochemistry 49:11–9.
385. Weng MW, Zheng Y, Jasti VP, Champeil E, Tomasz M, Wang Y, Basu AK, Tang MS. 2010. Repair of mitomycin C mono- and interstrand cross-linked DNA adducts by UvrABC: a new model. Nucleic Acids Res 38:6976–6984.
386. Berardini M, Mackay W, Loechler EL. 1997. Evidence for a recombination-independent pathway for the repair of DNA interstrand cross-links based on a site-specific study with nitrogen mustard. Biochemistry 36:3506–3513.
387. Piette J, Gamper HB, van de Vorst A, Hearst JE. 1988. Mutagenesis induced by site specifically placed 4′-hydroxymethyl-4,5′,8-trimethylpsoralen adducts. Nucleic Acids Res 16:9961–9977.
388. Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF, Lloyd RS. 2008. Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J Biol Chem 283:27433–27437.
389. Zdraveski ZZ, Mello JA, Marinus MG, Essigmann JM. 2000. Multiple pathways of recombination define cellular responses to cisplatin. Chem Biol 7:39–50.
390. Bridges BA, Stannard M. 1982. A new pathway for repair of cross-linkable 8-methoxypsoralen mono-adducts in Uvr strains of Escherichia coli. Mutat Res 92:9–14.
391. Zhen WP, Jeppesen C, Nielsen PE. 1986. Repair in Escherichia coli of a psoralen-DNA interstrand crosslink site specifically introduced into T410A411 of the plasmid pUC 19. Photochem Photobiol 44:47–51.
392. Michalke H, Bremer H. 1969. RNA synthesis in Escherichia coli after irradiation with ultraviolet light. J Mol Biol 41:1–23.
393. Sauerbier W, Millette RL, Hackett PB Jr. 1970. The effects of ultraviolet irradiation on the transcription of T4 DNA. Biochim Biophys Acta 209:368–386.
394. Witkin EM. 1966. Radiation-induced mutations and their repair. Science 152:1345–1353.
395. George DL, Witkin EM. 1974. Slow excision repair in an mfd mutant of Escherichia coli B/r. Mol Gen Genet 133:283–291.
396. Bockrath RC, Palmer JE. 1977. Differential repair of premutational UV-lesions at tRNA genes in E. coli. Mol Gen Genet 156:133–140.
397. Bohr VA, Smith CA, Okumoto DS, Hanawalt PC. 1985. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359–369.
398. Mellon I, Hanawalt PC. 1989. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature 342:95–98.
399. Selby CP, Witkin EM, Sancar A. 1991. Escherichia colimfd mutant deficient in “mutation frequency decline” lacks strand-specific repair: in vitro complementation with purified coupling factor. Proc Natl Acad Sci USA 88:11574–11578.
400. Park JS, Marr MT, Roberts JW. 2002. E. coli Transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109:757–767.
401. Selby CP, Sancar A. 1995. Structure and function of transcription-repair coupling factor. I. Structural domains and binding properties. J Biol Chem 270:4882–4889.
402. Selby CP, Sancar A. 1995. Structure and function of transcription-repair coupling factor. II. Catalytic properties. J Biol Chem 270:4890–4895.
403. Washburn RS, Wang Y, Gottesman ME. 2003. Role of E.coli transcription-repair coupling factor Mfd in Nun-mediated transcription termination. J Mol Biol 329:655–662.
404. Deaconescu AM, Chambers AL, Smith AJ, Nickels BE, Hochschild A, Savery NJ, Darst SA. 2006. Structural basis for bacterial transcription-coupled DNA repair. Cell 124:507–520.
405. Manelyte L, Kim YI, Smith AJ, Smith RM, Savery NJ. 2010. Regulation and rate enhancement during transcription-coupled DNA repair. Mol Cell 40:714–724.
406. Murphy MN, Gong P, Ralto K, Manelyte L, Savery NJ, Theis K. 2009. An N-terminal clamp restrains the motor domains of the bacterial transcription-repair coupling factor Mfd. Nucleic Acids Res 37:6042–6053.
407. Smith AJ, Szczelkun MD, Savery NJ. 2007. Controlling the motor activity of a transcription-repair coupling factor: autoinhibition and the role of RNA polymerase. Nucleic Acids Res 35:1802–1811.
408. Srivastava DB, Darst SA. 2011. Derepression of bacterial transcription-repair coupling factor is associated with a profound conformational change. J Mol Biol 406:275–284.
409. Blaisdell JO, Wallace SS. 2001. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc Natl Acad Sci USA 98:7426–7430.
410. Freyer GA, Davey S, Ferrer JV, Martin AM, Beach D, Doetsch PW. 1995. An alternative eukaryotic DNA excision repair pathway. Mol Cell Biol 15:4572–457.
411. Yajima H, Takao M, Yasuhira S, Zhao JH, Ishii C, Inoue H, Yasui A. 1995. A eukaryotic gene encoding an endonuclease that specifically repairs DNA damaged by ultraviolet light. EMBO J 14:2393–2399.
412. Gros L, Ishchenko AA, Ide H, Elder RH, Saparbaev MK. 2004. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res 32:73–81.
413. Redrejo-Rodriguez M, Saint-Pierre C, Couve S, Mazouzi A, Ishchenko AA, Gasparutto D, Saparbaev M. 2011. New insights in the removal of the hydantoins, oxidation product of pyrimidines, via the base excision and nucleotide incision repair pathways. PLoS One 6:e21039.
414. Souza LL, Eduardo IR, Padula M, Leitao AC. 2006. Endonuclease IV and exonuclease III are involved in the repair and mutagenesis of DNA lesions induced by UVB in Escherichia coli. Mutagenesis 21:125–130.
415. Georg J, Schomacher L, Chong JP, Majernik AI, Raabe M, Urlaub H, Muller S, Ciirdaeva E, Kramer W, Fritz HJ. 2006. The Methanothermobacter thermautotrophicus ExoIII homologue Mth212 is a DNA uridine endonuclease. Nucleic Acids Res 34:5325–5336.
416. Schomacher L, Chong JP, McDermott P, Kramer W, Fritz HJ. 2009. DNA uracil repair initiated by the archaeal ExoIII homologue Mth212 via direct strand incision. Nucleic Acids Res 37:2283–2293.
417. Ishchenko AA, Deprez E, Maksimenko A, Brochon JC, Tauc P, Saparbaev MK. 2006. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc Natl Acad Sci USA 103:2564–2569.
418. Izumi T, Ishizaki K, Ikenaga M, Yonei S. 1992. A mutant endonuclease IV of Escherichia coli loses the ability to repair lethal DNA damage induced by hydrogen peroxide but not that induced by methyl methanesulfonate. J Bacteriol 174:7711–7716.
419. Ivanov I, Tainer JA, McCammon JA. 2007. Unraveling the three-metal-ion catalytic mechanism of the DNA repair enzyme endonuclease IV. Proc Natl Acad Sci USA 104:1465–1470.
420. Golan G, Ishchenko AA, Khassenov B, Shoham G, Saparbaev MK. 2010. Coupling of the nucleotide incision and 3′–>5′ exonuclease activities in Escherichia coli endonuclease IV: structural and genetic evidences. Mutat Res 685:70–79.
421. Mol CD, Hosfield DJ, Tainer JA. 2000. Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: the 3′ ends justify the means. Mutat Res 460:211–229.
422. Hang B, Chenna A, Fraenkel-Conrat H, Singer B. 1996. An unusual mechanism for the major human apurinic/apyrimidinic (AP) endonuclease involving 5′ cleavage of DNA containing a benzene-derived exocyclic adduct in the absence of an AP site. Proc Natl Acad Sci USA 93:13737–13741.
423. Demple B, Linn S. 1982. On the recognition and cleavage mechanism of Escherichia coli endodeoxyribonuclease V, a possible DNA repair enzyme. J Biol Chem 257:2848–2855.
424. Gates FT III, Linn S. 1977. Endonuclease V of Escherichia coli. J Biol Chem 252:1647–1653.
425. Guo G, Weiss B. 1998. Endonuclease V ( nfi) mutant of Escherichia coli K-12. J Bacteriol 180:46–51.
426. Yao M, Kow YW. 1994. Strand-specific cleavage of mismatch-containing DNA by deoxyinosine 3′-endonuclease from Escherichia coli. J Biol Chem 269:31390–31396.
427. Yao M, Kow YW. 1996. Cleavage of insertion/deletion mismatches, flap and pseudo-Y DNA structures by deoxyinosine 3′-endonuclease from Escherichia coli. J Biol Chem 271:30672–30676.
428. Guo G, Ding Y, Weiss B. 1997. nfi, the gene for endonuclease V in Escherichia coli K-12. J Bacteriol 179:310–316.
429. Weiss B. 2001. Endonuclease V of Escherichia coli prevents mutations from nitrosative deamination during nitrate/nitrite respiration. Mutat Res 461:301–309.
430. Burgis NE, Brucker JJ, Cunningham RP. 2003. Repair system for noncanonical purines in Escherichia coli. J Bacteriol 185:3101–3110.
431. Lee CC, Yang YC, Goodman SD, Yu YH, Lin SB, Kao JT, Tsai KS, Fang WH. 2010. Endonuclease V-mediated deoxyinosine excision repair in vitro. DNA Repair (Amst) 9:1073–1079.
432. Weiss B. 2008. Removal of deoxyinosine from the Escherichia coli chromosome as studied by oligonucleotide transformation. DNA Repair (Amst) 7:205–212.
433. Huang J, Lu J, Barany F, Cao W. 2002. Mutational analysis of endonuclease V from Thermotoga maritima. Biochemistry 41:8342–8350.
434. Hitomi K, Iwai S, Tainer JA. 2007. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst) 6:410–428.
435. Feng H, Klutz AM, Cao W. 2005. Active site plasticity of endonuclease V from Salmonella typhimurium. Biochemistry 44:675–683.
436. Gros L, Saparbaev MK, Laval J. 2002. Enzymology of the repair of free radicals-induced DNA damage. Oncogene 21:8905–8925.
437. McCullough AK, Dodson ML, Lloyd RS. 1999. Initiation of base excision repair: glycosylase mechanisms and structures. Annu Rev Biochem 68:255–285.
438. Franklin WA, Lindahl T. 1988. DNA deoxyribophosphodiesterase. EMBO J 7:3617–3622.
439. Piersen CE, McCullough AK, Lloyd RS. 2000. AP lyases and dRPases: commonality of mechanism. Mutat Res 459:43–53.
440. Mosbaugh DW, Linn S. 1982. Characterization of the action of Escherichia coli DNA polymerase I at incisions produced by repair endodeoxyribonucleases. J Biol Chem 257:575–583.
441. Price A. 1992. Action of Escherichia coli and human 5′→3′ exonuclease functions at incised apurinic/apyrimidinic sites in DNA. FEBS Lett 300:101–104.
442. Matsumoto Y, Kim K. 1995. Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair. Science 269:699–702.
443. DeMott MS, Beyret E, Wong D, Bales BC, Hwang JT, Greenberg MM, Demple B. 2002. Covalent trapping of human DNA polymerase beta by the oxidative DNA lesion 2-deoxyribonolactone. J Biol Chem 277:7637–7640.
444. Jacobs AC, Kreller CR, Greenberg MM. 2011. Long patch base excision repair compensates for DNA polymerase beta Inactivation by the C4′-oxidized abasic site. Biochemistry 50:136–143.
445. Faure V, Saparbaev M, Dumy P, Constant JF. 2005. Action of multiple base excision repair enzymes on the 2′-deoxyribonolactone. Biochem Biophys Res Commun 328:1188–1195.
446. Hashimoto M, Greenberg MM, Kow YW, Hwang JT, Cunningham RP. 2001. The 2-deoxyribonolactone lesion produced in DNA by neocarzinostatin and other damaging agents forms cross-links with the base-excision repair enzyme endonuclease III. J Am Chem Soc 123:3161–3162.
447. Lundquist RC, Olivera BM. 1982. Transient generation of displaced single-stranded DNA during nick translation. Cell 31:53–60.
448. Hagensee ME, Moses RE. 1989. Multiple pathways for repair of hydrogen peroxide-induced DNA damage in Escherichia coli. J Bacteriol 171:991–995.
449. Nowosielska A, Smith SA, Engelward BP, Marinus MG. 2006. Homologous recombination prevents methylation-induced toxicity in Escherichia coli. Nucleic Acids Res 34:2258–2268.
450. Zhang QM, Yonei S, Kato M. 1992. Multiple pathways for repair of oxidative DNA damages caused by X rays and hydrogen peroxide in Escherichia coli. Radiat Res 132:334–338.
451. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. 2006. DNA Repair and Mutagenesis. ASM Press, Washington, DC.
452. Tait RC, Harris AL, Smith DW. 1974. DNA repair in Escherichia coli mutants deficient in DNA polymerases I, II and/or 3. Proc Natl Acad Sci USA 71:675–679.
453. Steitz TA. 1999. DNA polymerases: structural diversity and common mechanisms. J Biol Chem 274:17395–17398.
454. Joyce CM, Grindley ND. 1984. Method for determining whether a gene of Escherichia coli is essential: application to the polA gene. J Bacteriol 158:636–643.
455. Cao Y, Kogoma T. 1995. The mechanism of recApolA lethality: suppression by RecA-independent recombination repair activated by the lexA(Def) mutation in Escherichia coli. Genetics 139:1483–1494.
456. Dzidic S, Radman M. 1989. Genetic requirements for hyper-recombination by very short patch mismatch repair: involvement of Escherichia coli DNA polymerase I. Mol Gen Genet 217:254–256.
457. Kogoma T. 1996. Recombination by replication. Cell 85:625–627.
458. Stacey KA, Lloyd RG. 1976. Isolation of rec- mutants from an F-prime merodiploid strain of Escherichia coli K-12. Mol Gen Genet 143:223–232.
459. Konrad EB, Modrich P, Lehman IR. 1973. Genetic and enzymatic characterization of a conditional lethal mutant of Escherichia coli K12 with a temperature-sensitive DNA ligase. J Mol Biol 77:519–529.
460. Gumport RI, Lehman IR. 1971. Structure of the DNA ligase-adenylate intermediate: lysine (epsilon-amino)-linked adenosine monophosphoramidate. Proc Natl Acad Sci USA 68:2559–2563.
461. Sriskanda V, Shuman S. 2002. Conserved residues in domain Ia are required for the reaction of Escherichia coli DNA ligase with NAD+. J Biol Chem 277:9695–9700.
462. Olivera BM, Hall ZW, Lehman IR. 1968. Enzymatic joining of polynucleotides, V. A DNA-adenylate intermediate in the polynucleotide-joining reaction Proc Natl Acad Sci USA 61:237–244.
463. Lehman IR. 1974. DNA ligase: structure, mechanism, and function. Science 186:790–797.
464. Shuman S. 2009. DNA ligases: progress and prospects. J Biol Chem 284:17365–17369.
465. Nandakumar J, Nair PA, Shuman S. 2007. Last stop on the road to repair: structure of E. coli DNA ligase bound to nicked DNA-adenylate. Mol Cell 26:257–271.
466. Wilkinson A, Smith A, Bullard D, Lavesa-Curto M, Sayer H, Bonner A, Hemmings A, Bowater R. 2005. Analysis of ligation and DNA binding by Escherichia coli DNA ligase (LigA). Biochim Biophys Acta 1749:113–122.
467. Lindahl T, Sedgwick B, Sekiguchi M, Nakabeppu Y. 1988. Regulation and expression of the adaptive response to alkylating agents. Annu Rev Biochem 57:133–157.
468. Volkert MR, Gately FH, Hajec LI. 1989. Expression of DNA damage-inducible genes of Escherichia coli upon treatment with methylating, ethylating and propylating agents. Mutat Res 217:109–115.
469. Samson L, Cairns J. 1977. A new pathway for DNA repair in Escherichia coli. Nature 267:281–283.
470. Sedgwick B. 2004. Repairing DNA-methylation damage. Nat Rev Mol Cell Biol 5:148–157.
471. Myers LC, Wagner G, Verdine GL. 1995. Direct activation of the methyl chemosensor protein N-Ada by CH3I. J Am Chem Soc 117:10749–10750.
472. He C, Wei H, Verdine GL. 2003. Converting the sacrificial DNA repair protein N-ada into a catalytic methyl phosphotriester repair enzyme. J Am Chem Soc 125:1450–1451.
473. Takahashi K, Kawazoe Y. 1987. Methyl iodide, a potent inducer of the adaptive response without appreciable mutagenicity in E. coli. Biochem Biophys Res Commun 144:447–453.
474. Saget BM, Walker GC. 1994. The Ada protein acts as both a positive and a negative modulator of Escherichia coli’s response to methylating agents. Proc Natl Acad Sci USA 91:9730–9734.
475. Wyatt MD, Allan JM, Lau AY, Ellenberger TE, Samson LD. 1999. 3-methyladenine DNA glycosylases: structure, function, and biological importance. Bioessays 21:668–676.
476. Lawley PD. 1974. Some chemical aspects of dose-response relationships in alkylation mutagenesis. Mutat Res 23:283–295.
477. Volkert MR, Nguyen DC. 1984. Induction of specific Escherichia coli genes by sublethal treatments with alkylating agents. Proc Natl Acad Sci USA 81:4110–4114.
478. Volkert MR, Nguyen DC, Beard KC. 1986. Escherichia coli gene induction by alkylation treatment. Genetics 112:11–26.
479. Rohankhedkar MS, Mulrooney SB, Wedemeyer WJ, Hausinger RP. 2006. The AidB component of the Escherichia coli adaptive response to alkylating agents is a flavin-containing, DNA-binding protein. J Bacteriol 188:223–230.
480. Wulfing C, Pluckthun A. 1994. Protein folding in the periplasm of Escherichia coli. Mol Microbiol 12:685–692.
481. Green J, Paget MS. 2004. Bacterial redox sensors. Nat. Rev. Microbiol. 2: 954–966.
482. Demple B, Ding H, Jorgensen M. 2002. Escherichia coli SoxR protein: sensor/transducer of oxidative stress and nitric oxide. Methods Enzymol 348:355–364.
483. Wu J, Dunham WR, Weiss B. 1995. Overproduction and physical characterization of SoxR, a [2Fe-2S] protein that governs an oxidative response regulon in Escherichia coli. J Biol Chem 270:10323–10327.
484. Gaudu P, Weiss B. 1996. SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc Natl Acad Sci USA 93:10094–10098.
485. Koo MS, Lee JH, Rah SY, Yeo WS, Lee JW, Lee KL, Koh YS, Kang SO, Roe JH. 2003. A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J 22:2614–2622.
486. Ding H, Hidalgo E, Demple B. 1996. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J Biol Chem 271:33173–33175.
487. Ding H, Demple B. 1997. In vivo kinetics of a redox-regulated transcriptional switch. Proc Natl Acad Sci USA 94:8445–8449.
488. Nunoshiba T, DeRojas-Walker T, Tannenbaum SR, Demple B. 1995. Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages. Infect Immun 63:794–798.
489. Ding H, Demple B. 2000. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc Natl Acad Sci USA 97:5146–5150.
490. Martinez A, Kolter R. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179:5188–5194.
491. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. 1997. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90:43–53.
492. Gonzalez-Flecha B, Demple B. 1999. Role for the oxyS gene in regulation of intracellular hydrogen peroxide in Escherichia coli. J Bacteriol 181:3833–3836.
493. Altuvia S, Zhang A, Argaman L, Tiwari A, Storz G. 1998. The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 17:6069–6075.
494. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G. 1998. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17:6061–6068.
495. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603.
496. Sak BD, Eisenstark A, Touati D. 1989. Exonuclease III and the catalase hydroperoxidase II in Escherichia coli are both regulated by the katF gene product. Proc Natl Acad Sci USA 86:3271–3275.
497. Ivanova AB, Glinsky GV, Eisenstark A. 1997. Role of rpoS regulon in resistance to oxidative stress and near-UV radiation in delta oxyR suppressor mutants of Escherichia coli. Free Radic Biol Med 23:627–636.
498. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570.
499. Kullik I, Stevens J, Toledano MB, Storz G. 1995. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J Bacteriol 177:1285–1291.
500. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718–1721.
501. Aslund F, Zheng M, Beckwith J, Storz G. 1999. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96:6161–6165.
502. Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn WS, Yu MH, Storz G, Ryu SE. 2004. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11:1179–1185.
503. Choi H, Kim S, Mukhopadhyay P, Cho S, Woo J, Storz G, Ryu S. 2001. Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103–113.
504. Kim SO, Merchant K, Nudelman R, Beyer WF Jr, Keng T, DeAngelo J, Hausladen A, Stamler JS. 2002. OxyR: a molecular code for redox-related signaling. Cell 109:383–396.
505. Bailly V, Verly WG. 1987. Escherichia coli endonuclease III is not an endonuclease but a beta-elimination catalyst. Biochem J 242:565–572.
506. Boiteux S, Laval J. 1982. Coding properties of poly(deoxycytidylic acid) templates containing uracil or apyrimidinic sites: in vitro modulation of mutagenesis by deoxyribonucleic acid repair enzymes. Biochemistry 21:6746–6751.
507. Bulychev NV, Varaprasad CV, Dorman G, Miller JH, Eisenberg M, Grollman AP, Johnson F. 1996. Substrate specificity of Escherichia coli MutY protein. Biochemistry 35: 13147–13156.
508. Cole RS, Levitan D, Sinden RR. 1976. Removal of psoralen interstrand cross-links from DNA of Escherichia coli: mechanism and genetic control. J Mol Biol 103:39–59.
509. Demple B, Johnson A, Fung D. 1986. Exonuclease III and endonuclease IV remove 3′ blocks from DNA synthesis primers in H 2O 2-damaged Escherichia coli. Proc Natl Acad Sci USA 83:7731–7735.
510. Dizdaroglu M, Bergtold DS. 1986. Characterization of free radical-induced base damage in DNA at biologically relevant levels. Anal Biochem 156:182–188.
511. Landini P, Volkert MR. 2000. Regulatory responses of the adaptive response to alkylation damage: a simple regulon with complex regulatory features. J Bacteriol 182:6543–6549.
512. Levy MS, Pomposiello P, Nagel R. 1991. RecA-dependent increased precise excision of Tn10 in Salmonella typhimurium. Mutat Res 255:95–100.
513. Lindahl T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709–715.
514. Lindahl T, Karlstrom O. 1973. Heat-induced depyrimidination of deoxyribonucleic acid in neutral solution. Biochemistry 12:5151–5154.
515. Manuel RC, Czerwinski EW, Lloyd RS. 1996. Identification of the structural and functional domains of MutY, an Escherichia coli DNA mismatch repair enzyme. J Biol Chem 271:16218–16226.
516. Mol CD, Izumi T, Mitra S, Tainer JA. 2000. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected]. Nature 403:451–456.
517. O’Connor TR, Boiteux S, Laval J. 1989. Repair of imidazole ring-opened purines in DNA: overproduction of the formamidopyrimidine-DNA glycosylase of Escherichia coli using plasmids containing the fpg + gene. Ann Ist Super Sanita 25:27–31.
518. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39–85.
519. Zharkov DO, Golan G, Gilboa R, Fernandes AS, Gerchman SE, Kycia JH, Rieger RA, Grollman AP, Shoham G. 2002. Structural analysis of an Escherichia coli endonuclease VIII covalent reaction intermediate. EMBO J 21:789–800.
520. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A, Shales M, Lovett S, Winkler ME, Krogan NJ, Typas A, Gross CA. 2011. Phenotypic landscape of a bacterial cell. Cell 144:143–156.
521. Parkhomchuk D, Amstislavskiy V, Soldatov A, Ogryzko V. 2009. Use of high throughput sequencing to observe genome dynamics at a single cell level. Proc Natl Acad Sci USA 106:20830–20835.

Article metrics loading...



Cellular DNA is constantly challenged by various endogenous and exogenous genotoxic factors that inevitably lead to DNA damage: structural and chemical modifications of primary DNA sequence. These DNA lesions are either cytotoxic, because they block DNA replication and transcription, or mutagenic due to the miscoding nature of the DNA modifications, or both, and are believed to contribute to cell lethality and mutagenesis. Studies on DNA repair in spearheaded formulation of principal strategies to counteract DNA damage and mutagenesis, such as: direct lesion reversal, DNA excision repair, mismatch and recombinational repair and genotoxic stress signalling pathways. These DNA repair pathways are universal among cellular organisms. Mechanistic principles used for each repair strategies are fundamentally different. Direct lesion reversal removes DNA damage without need for excision and de novo DNA synthesis, whereas DNA excision repair that includes pathways such as base excision, nucleotide excision, alternative excision and mismatch repair, proceeds through phosphodiester bond breakage, de novo DNA synthesis and ligation. Cell signalling systems, such as adaptive and oxidative stress responses, although not DNA repair pathways are nevertheless essential to counteract DNA damage and mutagenesis. The present review focuses on the nature of DNA damage, direct lesion reversal, DNA excision repair pathways and adaptive and oxidative stress responses in .

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Comment has been disabled for this content
Submit comment
Comment moderation successfully completed


Image of Figure 1
Figure 1

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

(A) A monofunctional uracil-DNA glycosylase, UNG, generates the AP site, which is cleaved by exonuclease III (XthA), the major AP endonuclease, to generate a single-stranded nick with a 5′-deoxyribosephosphate group. This group is removed by DNA polymerase I through strand-displacement DNA synthesis coupled with a flap-structure endonuclease activity. (B) When bifunctional thymine glycol-DNA glycosylase Nth excises an oxidized base, it concomitantly performs β-elimination to generate a single-stranded nick with a 3′-α,β-unsaturated aldehyde. Xth removes the 3′-blocking group, generating a single nucleotide gap with a 3′-OH group that primes DNA repair synthesis by DNA polymerase I. Finally, the single-strand nick is sealed by DNA ligase to restore genetic integrity.

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

(A) Fpg–8oxoG-DNA interactions (adapted from reference 233 ). (B) T4 endonuclease V–thymine dimer-DNA interactions (adapted from reference 237 ). (C) Endonuclease IV–AP site-DNA interactions (adapted from reference 238 ). (D) Endonuclease V–hypoxanthine-DNA interactions (adapted from reference 239 ).

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

First, solution studies suggest that two monomers of UvrA (A) form a dimer in an ATP-dependent manner with four potential ATP-binding sites that may hydrolyze ATP and GTP. Then two UvrB (B) molecules bind to this UvrA dimer (for clarity, only one UvrB subunit is shown), and UvrAB interacts with DNA through the DNA-binding properties of UvrA. The cryptic ATP-binding site on UvrB becomes activated during the formation of the UvrAB complex responsible for damage search and recognition along DNA. Different models for the mechanism of damage recognition are proposed: the helicase-scanning model ( 349 , 350 , 351 ), the damage-processing model ( 352 ), and the padlock model ( 353 ). This complex binds to and wraps the DNA around one of the UvrB subunits and then waits for the arrival of the UvrC protein, responsible for both the 3′ and 5′ incision reactions of the damaged strand. After incision, UvrC dissociates, and UvrD (DNA helicase II), in concerted action with DNA polymerase I, releases the lesion-containing 12-base oligonucleotide, as well as the bound Uvr proteins. The resulting gap is filled in by DNA polymerase I, while the nick is sealed by DNA ligase.

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

(A) Schematic illustration of the nucleotide incision repair (NIR) pathway for oxidative DNA base damage in . Nfo cleaves the phosphodiester bond 5′ to the lesion (DHU, 5,6-dihydrouracil) generated from oxidation of cytosine. Following the incision of DHU-containing DNA, DNA polymerase I initiates DNA repair synthesis coupled to removal of the remaining dangling DHU base. Finally, DNA ligase seals the single-strand nick and restores duplex integrity. (B) Endonuclease V-dependent repair is initiated by cleavage at the second phosphodiester bond 3′ to the lesion (Hx, hypoxanthine) generated from deamination of adenine. After Nfi-catalyzed cleavage, DNA polymerase I removes deoxyinosine and deoxyadenosine residues by its 3′-5′ exonuclease activity and then it fills in the gap, while DNA ligase seals the phosphodiester backbone.

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

The Ada protein is represented in a dumbbell-shape structure to show N-terminal and C-terminal domains containing active cysteine residues (see the text for details). The Ada regulon contains the gene and also , , and genes shown as boxes. DNA is alkylated at the phosphate linkages (P-O-CH) and position of guanine (G-O-CH). The Ada protein demethylates Sp diastereoisomers of methylphosphotriesters in the sugar phosphate backbone by transferring the methyl groups to the N-terminal cysteine (Cys-38) and methylated bases by transferring the methyl groups to the C-terminal cysteine (Cys-321). The alkylation of Cys-38 converts Ada protein to a transcriptional activator that binds to the promoters of the Ada regulon, leading in enhanced transcription. The increased levels of Ada, AlkA, AlkB, and AidB proteins promote enhanced repair of alkylation damage in DNA (adapted from reference 470 ).

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4
Permissions and Reprints Request Permissions
Download as Powerpoint


Generic image for table
Table 1

genes involved in DNA repair

Citation: Couvé S, Ishchenko A, Fedorova O, Ramanculov E, Laval J, Saparbaev M. 2013. Direct DNA Lesion Reversal and Excision Repair in , EcoSal Plus 2013; doi:10.1128/ecosalplus.7.2.4

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error