Overview of Homologous Recombination and Repair Machines

Andrei Kuzminov; Franklin W. Stahl

doi:10.1128/9781555817640.ch19

Chapter 19 : Overview of Homologous Recombination and Repair Machines

Authors: Andrei Kuzminov¹, Franklin W. Stahl²

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Affiliations: 1: Department of Microbiology, University of Illinois, Urbana-Champaign, B103 C&LSL, 601 S. Goodwin Ave., Urbana, IL 61801-3709; 2: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403-1229

Content Type: Monograph

Publication Year: 2005

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

Book DOI: 10.1128/9781555817640

Chapter DOI: 10.1128/9781555817640.ch19

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Abstract:

The study of homologous recombination between plasmids, or between a plasmid and the chromosome, revealed that the RecFOR pathway is less of a poor cousin than first thought. When the exquisite sensitivity to DNA damage of the first recombination-deficient mutants was found, it became clear that homologous recombination might be the only way to repair certain DNA lesions. Generally, the stronger the defect in homologous recombination, the higher the sensitivity to DNA damage. In Escherichia coli, chromosomal lesions are repaired by homology-guided strand exchange between sister chromatids. The evidence in support of this notion comes in three forms. First, physical connections between parental and daughter strands, associated with lesion repair, can be detected. Second, repair of chromosomal lesions is not observed in recA mutants. Third, DNA damage stimulates homologous recombination although the structure of chromosomal lesions in this case is unspecified. Single-stranded DNA-binding protein (SSB) complexes single-stranded DNA (ssDNA), facilitating its subsequent use in replication and in degradation and repair pathways of DNA metabolism. Chromosomal dimerization in E. coli creates a chromosomal lesion, because it prevents segregation of the replicated chromosomes into daughter cells. The understanding of the formation of replication-dependent chromosomal lesions is still primitive. There is one in vivo study on the structure of stalled replication forks, a report documenting replication fork reversal in vivo, as well as a few reports of replication fork reversal in vitro, likely to be an artifact of DNA isolation.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19

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Overview of Homologous Recombination and Repair Machines

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Figure 1

Basic types of merozygotes to detect homologous recombination in bacteria. See text for explanation.

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Figure 1

Basic types of merozygotes to detect homologous recombination in bacteria. See text for explanation.

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Figure 2

Genetic pathways for homologous recombination in E. coli. See text for explanation.

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Figure 2

Genetic pathways for homologous recombination in E. coli. See text for explanation.

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Figure 3

The idea of recombinational repair. (A) Two homologous chromosomes: the top one has a two-strand DNA lesion, and the bottom one is intact. (B) Homologous pairing and strand exchange between the two homologues, leading to conversion of the two-strand DNA lesion into a pair of one-strand DNA lesions in the hybrid DNA segments, bracketed by the double Holliday junction. One of two possible directions of the junction resolution is indicated by small arrows. (C) Holliday junction resolution breaks the joint molecule apart. (D) Excision repair removes the one-strand lesions. Open double line, the intact duplex; filled double line, the duplex with DNA lesions; lollipops in the filled strands, one-strand DNA lesions.

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Figure 3

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Figure 4

Configuration of chromosomal lesions.

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Figure 4

Configuration of chromosomal lesions.

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Figure 5

Formation of a daughter-strand gap during replication fork passage over a noncoding lesion. (A) A replication fork approaching a pyrimidine dimer. (B) The replication fork is traversing the pyrimidine dimer. (C) The stalled replisome is released, while the fork recruits a new replisome to reinitiate downstream from the lesion. (D) The replication fork moves away, leaving behind a daughter-strand gap. T=T, pyrimidine dimer (a noncoding lesion).

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Figure 5

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Figure 6

Replication fork collapse at a single-strand interruption in template DNA. (A) A replication fork. (B) The replication fork is approaching a single-strand interruption. (C) The replication fork has reached the interruption and come apart (collapsed). (D) The single-strand interruption in the full-length chromosome is repaired, while the detached double-strand end awaits its fate.

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Figure 6

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Figure 7

Replication fork collapse as a chromosomal lesion. (A) A theta-replicating chromosome. (B) As a result of collapse of the right replication fork, the chromosome starts replicating as a sigmastructure. (C) Collapse of the second replication fork terminates sigma-replication. (D) Collapse of the second replication fork linearizes the chromosome.

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Figure 7

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Figure 8

Regression of a stalled replication fork with subsequent resetting or breakage. The shaded circle indicates a protein tightly bound to the template DNA. (A) A replication fork approaches a block in the downstream template. (B) The replication fork stalls at the block. (C) The replication fork regresses from the block, forming a Holliday junction and extruding the newly replicated strands in a duplex of their own. (D) The regressed replication fork is reset and the block is removed. (E) A nuclease degrades the extruded fourth arm, recreating the replication fork structure. (F) Resolution of the Holliday junction leads to replication fork breakage. (G) Closure of the nicks completes the formation of a chromosomal lesion, in this case a double-strand end.

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Figure 8

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Figure 9

Locking and unlocking of a replication fork stalled at a small palindrome: a hypothesis. (A) A replication fork approaches a block in the downstream template, which happens to be near a small palindrome. (B) The replication fork is stalled at the block; one strand of the palindrome is replicated, while the opposite strand is complexed with SSB and remains single stranded. (C) The replication fork regresses from the block, extruding the newly replicated strand. The possibility of homologous pairing between the single-strand regions is shown by arrows. (D) Template switching due to the annealing of the complementary strands. (E) DNA synthesis, primed by the switched end, locks the replication fork. (F) Further regression of the locked replication fork extrudes the palindrome into a hairpin. (G) Hairpin degradation by SbcCD regenerates a replication fork structure. Shaded circle, a protein tightly bound to the template DNA; black and white arrows, palindrome (a black arrow forms a duplex with a codirectional white arrow).

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Figure 9

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Figure 10

The two hypothetical pathways of recombinational repair. A scheme for daughter-strand gap repair, catalyzed by RecFOR and RecA, is shown on the left; a scheme for double-strand-end repair, catalyzed by RecBCD and RecA, is shown on the right. T=T, pyrimidine dimer (a noncoding lesion).

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Figure 10

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Figure 11

Holliday junction processing by the RuvABC resolvasome. (A) A Holliday junction in the folded conformation (difficult to process but preferred in physiological conditions). The arrow indicates the 1808 rotation required to convert the folded conformation into the square planar one. (B) A Holliday junction in the square planar conformation (easy to process, observed in the absence of Mg2þ ions). (C) RuvA tetramers bind Holliday junctions under physiological conditions and isomerize them into the square planar conformation. (D) RuvB hexamers are shown as washers on opposite arms of the Holliday junction; they interact with RuvA and “pump” DNA through their central openings (the direction of DNA movement is shown by arrows). At this stage of the Holliday junction processing, two RuvA tetramers assemble around the junction in a turtle-shell configuration (not shown). (E) One of the RuvA tetramers is replaced with a RuvC dimer (two circles), while the RuvC consensus resolution sequences (diamonds) are drawn into the junction by RuvB pumping. (F) RuvC symmetrically cuts at the resolution consensus sequences, resolving the joint molecule (RuvABC proteins are not shown). The two original duplexes, forming a joint molecule, are shown as either open or filled double lines.

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Figure 11

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Figure 12

The two ways of restoring theta-replication to a circular chromosome that suffered replication fork collapse. (A) A theta-replicating chromosome. (B) The right fork of the replication bubble has collapsed, shifting chromosome replication into sigma-mode. (C) RecBCD- and RecA-catalyzed strand exchange restores replication fork structure, returning the chromosome to theta-replication. (D) RecBCD-catalyzed degradation of the linear tail makes theta-replication possible again without repairing the collapsed replication fork.

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Figure 12

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Figure 13

A hypothetical, RecG-dependent way of Holliday junction processing. (A) An end-invasion intermediate, with the 3′ end being extended by DNA pol I. (B) DNA pol I cleaves the displaced strand and starts nick-translating. (C) DNA ligase seals the nick, while RecG helicase binds to the side of the Holliday junction opposite the side bound by the RecA filament. (D) RecG translocates the Holliday junction toward the DNA end, dispersing the RecA filament and restoring replication fork structure. Rectangle with rounded corners, RecA filament; gray oval, RecG; open circles, RecA monomers; small arrow, the position of DNA strand cleavage; one-sided arrow, the 3′end used by DNA pol I.

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Figure 13

References

/content/book/10.1128/9781555817640.chap19

1. Arthur, H. M.,, and R. G. Lloyd. 1980. Hyper-recombination in uvrD mutants of Escherichia coli K-12. Mol. Gen. Genet. 180: 185– 191.

2. Avery, O. T.,, C. M. Macleod,, and M. McCarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. I. Induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus type III. J. Exp. Med. 79: 137– 158.

3. Bazemore, L. R.,, E. Folta-Stogniew,, M. Takahashi,, and C. M. Radding. 1997. RecA tests homology at both pairing and strand exchange. Proc. Natl. Acad. Sci. USA 94: 11863– 11868.

4. Bazemore, L. R.,, M. Takahashi,, and C. M. Radding. 1997. Kinetic analysis of pairing and strand exchange catalyzed by RecA. Detection by fluorescence energy transfer. J. Biol. Chem. 272: 14672– 14682.

5. Bi, X.,, and L. F. Liu. 1996. DNA rearrangements mediated by inverted repeats. Proc. Natl. Acad. Sci. USA 93: 819– 823.

6. Bianco, P. R.,, and S. C. Kowalczykowski. 2000. Translocation step size and mechanism of the RecBC DNA helicase. Nature 405: 368– 372.

7. Billen, D.,, and R. Hewitt. 1967. Concerning the dynamics of chromosome replication and degradation in a bacterial population exposed to X-rays. Biochim. Biophys. Acta 138: 587– 595.

8. Blinkowa, A. 1976. The role of polymerase III in conjugation between E. coli K12 donor and recipient strains carrying dnaEts mutation. Acta Microbiol. Pol. 25: 95– 108.

9. Bradshaw, J. S.,, and A. Kuzminov. 2003. RdgB acts to avoid chromosome fragmentation in Escherichia coli. Mol. Microbiol. 48: 1711– 1725.

10. Bresler, S. E.,, V. A. Lanzov,, and A. A. Lukjaniec-Blinkova. 1968. On the mechanism of conjugation in Escherichia coli K12. Mol. Gen. Genet. 102: 269– 284.

11. Chalker, A. F.,, D. R. F. Leach,, and R. G. Lloyd. 1988. Escherichia coli sbcC mutants permit stable propagation of DNA replicons containing a long palindrome. Gene 71: 201– 205.

12. Clark, A. J. 1971. Toward a metabolic interpretation of genetic recombination of E. coli and its phages. Annu. Rev. Microbiol. 25: 437– 464.

13. Clark, A. J.,, and K. B. Low,. 1988. Pathways and systems of homologous recombination in Escherichia coli, p. 155– 215. In K. B. Low (ed.), The Recombination of Genetic Material. Academic Press, Inc., San Diego, Calif.

14. Clark, A. J.,, and A. D. Margulies. 1965. Isolation and characterization of recombination-deficient mutants of Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 53: 451– 459.

15. Clark, A. J.,, and S. J. Sandler. 1994. Homologous recombination: the pieces begin to fall into place. Crit. Rev. Microbiol. 20: 125– 142.

16. Clark, J. B.,, F. Haas,, W. S. Stone,, and O. Wyss. 1950. The stimulation of gene recombination in Escherichia coli. J. Bacteriol. 59: 375– 379.

17. Cole, R. S. 1971. Inactivation of Escherichia coli, F′ episomes at transfer, and bacteriophage lambda by psoralen plus 360- nm light: significance of deoxyribonucleic acid cross-links. J. Bacteriol. 107: 846– 852.

18. Cole, R. S. 1973. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination. Proc. Natl. Acad. Sci. USA 70: 1064– 1068.

19. Connelly, J. C.,, E. S. de Leau,, E. A. Okely,, and D. R. F. Leach. 1997. Overexpression, purification, and characterization of the SbcCD protein from Escherichia coli. J. Biol. Chem. 272: 19819– 19826.

20. Connelly, J. C.,, L. A. Kirkham,, and D. R. F. Leach. 1998. The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. USA 95: 7969– 7974.

21. Cordone, L.,, R. M. Sperandeo-Mineo,, and S. Mannino. 1975. UV-induced enhancement of recombination among lambda bacteriophages: relation with replication of irradiated DNA. Nucleic Acids Res. 2: 1129– 1142.

22. Courcelle, J.,, A. K. Ganesan,, and P. C. Hanawalt. 2001. Therefore, what are recombination proteins there for? Bioessays 23: 463– 470.

23. Courcelle, J.,, A. Khodursky,, B. Peter,, P. O. Brown,, and P. C. Hanawalt. 2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41– 64.

24. Cox, M. M. 1998. A broadening view of recombinational DNA repair in bacteria. Genes Cells 3: 65– 78.

25. Dillingham, M. S.,, M. Spies,, and S. C. Kowalczykowski. 2003. RecBCD enzyme is a bipolar DNA helicase. Nature 423: 893– 897.

26. Dri, A.-M.,, P. L. Moreau,, and J. Rouviere-Yaniv. 1992. Role of the histone-like proteins OsmZ and HU in homologous recombination. Gene 120: 11– 16.

27. Dzidic, S.,, E. Salaj-Smic,, and Z. Trgovcevic. 1986. The relationship between survival and mutagenesis in Escherichia coli after fractionated ultraviolet irradiation. Mutat. Res. 173: 89– 91.

28. Ennis, D. G.,, S. K. Amundsen,, and G. R. Smith. 1987. Genetic functions promoting homologous recombination in Escherichia coli: a study of inversion in phage λ. Genetics 115: 11– 24.

29. Fernández de Henestrosa, A. R.,, T. Ogi,, S. Aoyagi,, D. Chafin,, J. J. Hayes,, H. Ohmori,, and R. Woodgate. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35: 1560– 1572.

30. Fishel, R. A.,, and R. Kolodner. 1984. Escherichia coli strains containing mutations in the structural gene for topoisomerase I are recombination deficient. J. Bacteriol. 160: 1168– 1170.

31. Friedberg, E. C.,, G. C. Walker,, and W. Siede. 1995. DNA Repair and Mutagenesis. ASM Press, Washington, D.C.

32. Fujiwara, Y.,, and M. Tatsumi. 1976. Replicative bypass repair of ultraviolet damage to DNA of mammalian cells: caffeine sensitive and caffeine resistant mechanisms. Mutat. Res. 37: 91– 110.

33. Gibson, F. P.,, D. R. F. Leach,, and R. G. Lloyd. 1992. Identification of sbcD mutations as cosuppressors of recBC that allow propagation of DNA palindromes in Escherichia coli K-12. J. Bacteriol. 174: 1222– 1228.

34. Glassberg, J.,, R. R. Meyer,, and A. Kornberg. 1979. Mutant single-strand binding protein of Escherichia coli: genetic and physiological characterization. J. Bacteriol. 140: 14– 19.

35. Golub, E. I.,, and K. B. Low. 1983. Indirect stimulation of genetic recombination. Proc. Natl. Acad. Sci. USA 80: 1401– 1405.

36. Goodman, M. F. 2000. Coping with replication “train wrecks” in Escherichia coli using Pol V, Pol II and RecA proteins. Trends Biochem. Sci. 25: 189– 195.

37. Gray, W. J. H.,, M. H. L. Green,, and B. A. Bridges. 1972. DNA synthesis in gamma-irradiated recombination deficient strains of Escherichia coli. J. Gen. Microb. 71: 359– 366.

38. Gregg, A. V.,, P. McGlynn,, R. P. Jaktaji,, and R. G. Lloyd. 2002. Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. Mol. Cell 9: 241– 251.

39. Gruber, M.,, R. E. Wellinger,, and J. M. Sogo. 2000. Architecture of the replication fork stalled at the 3′end of yeast ribosomal genes. Mol. Cell. Biol. 20: 5777– 5787.

40. Gupta, R. C.,, E. Folta-Stogniew,, S. O’Malley,, M. Takahashi,, and C. M. Radding. 1999. Rapid exchange of A:T base pairs is essential for recognition of DNA homology by human Rad51 recombination protein. Mol. Cell 4: 705– 714.

41. Gupta, R. C.,, E. Folta-Stogniew,, and C. M. Radding. 1999. Human Rad51 protein can form homologous joints in the absence of net strand exchange. J. Biol. Chem. 274: 1248– 1256.

42. Hanawalt, P. C. 1966. The U.V. sensitivity of bacteria: its relation to the DNA replication cycle. Photochem. Photobiol. 5: 1– 12.

43. Harm, W. 1964. On the control of UV-sensitivity of phage T4 by the gene x. Mutat. Res. 1: 344– 354.

44. Hays, J. B.,, and S. Boehmer. 1978. Antagonists of DNA gyrase inhibit repair and recombination of UV-irradiated phage λ. Proc. Natl. Acad. Sci. USA 75: 4125– 4129.

45. Hays, J. B.,, B. K. Duncan,, and S. Boehmer. 1981. Recombination of uracil-containing lambda bacteriophages. J. Bacteriol. 145: 306– 320.

46. Higgins, N. P.,, K. Kato,, and B. Strauss. 1976. A model for replication repair in mammalian cells. J. Mol. Biol. 101: 417– 425.

47. Horiuchi, T.,, and Y. Fujimura. 1995. Recombinational rescue of the stalled DNA replication fork: a model based on analysis of an Escherichia coli strain with a chromosomal region difficult to replicate. J. Bacteriol. 177: 783– 791.

48. Horiuchi, T.,, Y. Fujimura,, H. Nishitani,, T. Kobayashi,, and M. Hidaka. 1994. The DNA replication fork blocked at the Ter site may be an entrance for the RecBCD enzyme into duplex DNA. J. Bacteriol. 176: 4656– 4663.

49. Howard-Flanders, P. 1973. DNA repair and recombination. Br. Med. Bull. 29: 226– 235.

50. Iyer, V. N.,, and W. D. Rupp. 1971. Usefulness of benzoylated naphthoylated DEAE-cellulose to distinguish and fractionate double-stranded DNA bearing different extents of single-stranded regions. Biochim. Biophys. Acta 228: 117– 126.

51. Jacob, F.,, and E. L. Wollman. 1955. Étude génétique d’un bactériophage tempéré d’ Escherichia coli. III. Effet du rayonnement ultraviolet sur la recombinaison génétique. Ann. Inst. Pasteur 88: 724– 749.

52. King, S. R.,, and J. P. Richardson. 1986. Role of homology and pathway specificity for recombination between plasmids and bacteriophage λ. Mol. Gen. Genet. 204: 141– 147.

53. Kogoma, T.,, G. W. Cadwell,, K. G. Barnard,, and T. Asai. 1996. The DNA replication priming protein, PriA, is required for homologous recombination and double-strand break repair. J. Bacteriol. 178: 1258– 1264.

54. Konrad, E. B. 1977. Method for the isolation of Escherichia coli mutants with enhanced recombination between chromosomal duplications. J. Bacteriol. 130: 167– 172.

55. Kouzminova, E. A.,, and A. Kuzminov. 2004. Chromosomal fragmentation in dUTPase-deficient mutants of Escherichia coli and its recombinational repair. Mol. Microbiol. 51: 1279– 1295.

56. Kowalczykowski, S. C.,, D. A. Dixon,, A. K. Eggleston,, S. D. Lauder,, and W. M. Rehrauer. 1994. Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 58: 401– 465.

57. Krasin, F.,, and F. Hutchinson. 1977. Repair of DNA double-strand breaks in Escherichia coli, which requires recA function and the presence of a duplicate genome. J. Mol. Biol. 116: 81– 98.

58. Kuzminov, A. 1995. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16: 373– 384.

59. Kuzminov, A. 2001. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. USA 98: 8461– 8468.

60. Kuzminov, A. 1995. Instability of inhibited replication forks in E. coli. Bioessays 17: 733– 741.

61. Kuzminov, A. 1995. A mechanism for induction of the SOS response in E. coli: insights into the regulation of reversible protein polymerization in vivo. J. Theor. Biol. 177: 29– 43.

62. Kuzminov, A. 1999. Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol. Mol. Biol. Rev. 63: 751– 813.

63. Kuzminov, A. 2001. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl. Acad. Sci. USA 98: 8241– 8246.

64. Kuzminov, A.,, E. Schabtach,, and F. W. Stahl. 1994. X-sites in combination with RecA protein increase the survival of linear DNA in E. coli by inactivating ExoV activity of RecBCD nuclease. EMBO J. 13: 2764– 2776.

65. Kuzminov, A.,, and F. W. Stahl. 1997. Stability of linear DNA in recA mutant Escherichia coli cells reflects ongoing chromosomal DNA degradation. J. Bacteriol. 179: 880– 888.

66. Lederberg, J. 1947. Gene recombination and linked segregations in Escherichia coli. Genetics 32: 505– 525.

67. Lin, C.-T.,, Y. L. Lyu,, and L. F. Liu. 1997. A cruciformdumbbell model for inverted dimer formation mediated by inverted repeats. Nucleic Acids Res. 25: 3009– 3016.

68. Lin, P.-F.,, and P. Howard-Flanders. 1976. Genetic exchanges caused by ultraviolet photoproducts in phage λ DNA molecules: the role of DNA replication. Mol. Gen. Genet. 146: 107– 115.

69. Lloyd, R. G. 1991. Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG. J. Bacteriol. 173: 5414– 5418.

70. Lloyd, R. G. 1983. lexA dependent recombination in uvrD strains of Escherichia coli. Mol. Gen. Genet. 189: 157– 161.

71. Lloyd, R. G.,, and C. Buckman. 1995. Conjugational recombination in Escherichia coli: genetic analysis of recombinant formation in Hfr x F − crosses. Genetics 139: 1123– 1148.

72. Lloyd, R. G.,, and C. Buckman. 1991. Genetic analysis of the recG locus of Escherichia coli K-12 and of its role in recombination and DNA repair. J. Bacteriol. 173: 1004– 1011.

73. Lloyd, R. G.,, and C. Buckman. 1985. Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12. J. Bacteriol. 164: 836– 844.

74. Lloyd, R. G.,, and C. Buckman. 1991. Overlapping functions of recD, recJ and recN provide evidence of three epistatic groups of genes in Escherichia coli recombination and DNA repair. Biochimie 73: 313– 320.

75. Lloyd, R. G.,, C. Buckman,, and F. E. Benson. 1987. Genetic analysis of conjugational recombination in Escherichia coli K12 strains deficient in RecBCD enzyme. J. Gen. Microbiol. 133: 2531– 2538.

76. Lloyd, R. G.,, N. P. Evans,, and C. Buckman. 1987. Formation of recombinant lacZþ DNA in conjugational crosses with a recB mutant of Escherichia coli K12 depends on recF, recJ and recO. Mol. Gen. Genet. 209: 135– 141.

77. Lloyd, R. G.,, M. C. Porton,, and C. Buckman. 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.

78. Lorenz, M. G.,, and W. Wackernagel. 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563– 602.

79. Louarn, J.-M.,, J. Louarn,, V. Franc¸ois,, and J. Patte. 1991. Analysis and possible role of hyperrecombination in the termination region of the Escherichia coli chromosome. J. Bacteriol. 173: 5097– 5104.

80. Lundquist, R. C.,, and B. M. Olivera. 1982. Transient generation of displaced single-stranded DNA during nick translation. Cell 31: 53– 60.

81. Luria, S. E. 1947. Reactivation of irradiated bacteriophage by transfer of self-reproducing units. Proc. Natl. Acad. Sci. USA 33: 253– 264.

82. Mahajan, S. K., 1988. Pathways of homologous recombination in Escherichia coli, p. 87– 140. In R. Kucherlapati, and G. R. Smith (ed.), Genetic Recombination. American Society for Microbiology, Washington, D.C.

83. Mahdi, A. A.,, and R. G. Lloyd. 1989. Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair. Mol. Gen. Genet. 216: 503– 510.

84. Malagón, F.,, and A. Aguilera. 1998. Genetic stability and DNA rearrangements associated with a 2 x 1.1-Kb perfect palindrome in Escherichia coli. Mol. Gen. Genet. 259: 639– 644.

85. Marians, K. J. 2000. PriA-directed replication fork restart in Escherichia coli. Trends Biochem. Sci. 25: 185– 189.

86. Martignoni, K. D. 1978. Inhibition of x-ray-induced protection of Escherichia coli K-12 cells against the lethal effects of ultra-violet light by nitrofurantoin. Int. J. Radiat. Biol. 33: 577– 585.

87. Masters, M., 1996. Generalized transduction, p. 2421– 2441. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella:Cellular and Molecular Biology, 2nd ed., vol. 2. ASM Press, Washington, D.C.

88. McDaniel, L. S.,, L. H. Rogers,, and W. E. Hill. 1978. Survival of recombination-deficient mutants of Escherichia coli during incubation with nalidixic acid. J. Bacteriol. 134: 1195– 1198.

89. McGlynn, P.,, and R. G. Lloyd. 2002. Genome stability and the processing of damaged replication forks by RecG. Trends Genet. 18: 413– 419.

90. McPartland, A.,, L. Green,, and H. Echols. 1980. Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20: 731– 737.

91. Meyer, R. R.,, and P. S. Laine. 1990. The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Rev. 54: 342– 380.

92. Michel, B. 2000. Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25: 173– 178.

93. Michel, B.,, G. D. Recchia,, M. Penel-Colin,, S. D. Ehrlich,, and D. J. Sherratt. 2000. Resolution of Holliday junctions by RuvABC prevents dimer formation in rep mutants and UV-irradiated cells. Mol. Microbiol. 37: 180– 191.

94. Miranda, A.,, and A. Kuzminov. 2003. Chromosomal lesion suppression and removal in Escherichia coli via linear DNA degradation. Genetics 163: 1255– 1271.

95. Morgan, T. H.,, and E. Cattell. 1912. Data for the study of sex-linked inheritance in Drosophila. J. Exp. Zool. 13: 79– 101.

96. Morimatsu, K.,, and S. C. Kowalczykowski. 2003. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 11: 1337– 1347.

97. Mudgett, J. S.,, M. Buckholt,, and W. D. Taylor. 1991. Ultraviolet light-induced plasmid-chromosome recombination in Escherichia coli: the role of recB and recF. Gene 97: 131– 136.

98. Myers, R. S.,, and F. W. Stahl. 1994. X and the RecBCD enzyme of Escherichia coli. Annu. Rev. Genet. 28: 49– 70.

99. Otsuji, N.,, H. Iyehara,, and Y. Hideshima. 1974. Isolation and characterization of Escherichia coli ruv mutant which forms nonseptate filaments after low doses of ultraviolet light irradiation. J. Bacteriol. 117: 337– 344.

100. Picksley, S. M.,, P. V. Attfield,, and R. G. Lloyd. 1984. Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product. Mol. Gen. Genet. 195: 267– 274.

101. Pinder, D. J.,, C. E. Blake,, J. C. Lindsey,, and D. R. F. Leach. 1998. Replication strand preference for deletions associated with DNA palindromes. Mol. Microbiol. 28: 719– 727.

102. Pollard, E. C.,, and J. K. J. Fugate. 1978. Relative rates of repair of single-strand breaks and postirradiation DNA degradation in normal and induced cells of Escherichia coli. Biophys. J. 24: 429– 437.

103. Radman, M., 1975. SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis, p. 355– 367. In P. C. Hanawalt, and R. B. Setlow (ed.), Molecular Mechanisms for Repair of DNA, vol. A. Plenum Press, New York, N.Y.

104. Roberts, J. J. 1978. The repair of DNA modified by cytotoxic, mutagenic, and carcinogenic chemicals. Adv. Radiat. Biol. 7: 211– 436.

105. Roca, A. I.,, and M. M. Cox. 1997. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucleic Acid Res. Mol. Biol. 56: 129– 223.

106. Ross, P.,, and P. Howard-Flanders. 1977. Initiation of recAþdependent recombination in Escherichia coli (λ). II. Specificity in the induction of recombination and strand cutting in undamaged covalent circular bacteriophage 186 and lambda DNA molecules in phage-infected cells. J. Mol. Biol. 117: 159– 174.

107. Rothman, R. H.,, T. Kato,, and A. J. Clark,. 1975. The beginning of an investigation of the role of recF in the pathways of metabolism of ultraviolet-irradiated DNA in Escherichia coli, p. 283– 291. In P. C. Hanawalt, and R. B. Setlow (ed.), Molecular Mechanisms for Repair of DNA, vol. A. Plenum Press, New York, N.Y.

108. Rupp, W. D.,, and P. Howard-Flanders. 1968. Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J. Mol. Biol. 31: 291– 304.

109. Rupp, W. D.,, C. E. Wilde III,, D. L. Reno,, and P. Howard- Flanders. 1971. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J. Mol. Biol. 61: 25– 44.

110. Salaj-Smic, E.,, S. Dzidic,, and Z. Trgovcevic. 1985. The effect of a split UV dose on survival, division delay and mutagenesis in Escherichia coli. Mutat. Res. 144: 127– 130.

111. Sandler, S. J.,, and K. J. Marians. 2000. Role of PriA in replication fork reactivation in Escherichia coli. J. Bacteriol. 182: 9– 13.

112. Sandler, S. J.,, H. S. Samra,, and A. J. Clark. 1996. Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. Genetics 143: 5– 13.

113. Sargentini, N. J.,, and K. C. Smith. 1986. Quantitation of the involvement of the recA, recB, recC, recF, recJ, recN, lexA, radA, radB, uvrD, and umuC genes in the repair of X-rayinduced DNA double-strand breaks in Escherichia coli. Radiat. Res. 107: 58– 72.

114. Seigneur, M.,, V. Bidnenko,, S. D. Ehrlich,, and B. Michel. 1998. RuvAB acts at arrested replication forks. Cell 95: 419– 430.

115. Shen, P.,, and H. V. Huang. 1986. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112: 441– 457.

116. Sherratt, D. J.,, L. K. Arciszewska,, G. Blakely,, S. Colloms,, K. Grant,, N. Leslie,, and R. McCulloch. 1995. Site-specific recombination and circular chromosome segregation. Phil. Trans. R. Soc. Lond. 347: 37– 42.

117. Singer, B. S.,, L. Gold,, P. Gauss,, and D. H. Doherty. 1982. Determination of the amount of homology required for recombination in bacteriophage T4. Cell 31: 25– 33.

118. Smith, K. C.,, and D. H. C. Meun. 1970. Repair of radiationinduced damage in Escherichia coli. I. Effect of rec mutations on post-replication repair of damage due to ultraviolet radiation. J. Mol. Biol. 51: 459– 472.

119. Sogo, J. M.,, M. Lopes,, and M. Foiani. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599– 602.

120. Spies, M.,, P. R. Bianco,, M. S. Dillingham,, N. Handa,, R. J. Baskin,, and S. C. Kowalczykowski. 2003. A molecular throttle: the recombination hotspot x controls DNA translocation by the RecBCD helicase. Cell 114: 647– 654.

121. Stahl, F. W.,, and M. M. Stahl. 1977. Recombination pathway specificity of Chi. Genetics 86: 715– 725.

122. Stallions, D. R.,, and R. Curtiss III. 1971. Chromosome transfer and recombinant formation with deoxyribonucleic acid temperature-sensitive strains of Escherichia coli. J. Bacteriol. 105: 886– 895.

123. Steiner, W. W.,, and P. L. Kuempel. 1998. Cell division is required for resolution of dimer chromosomes at the dif locus of Escherichia coli. Mol. Microbiol. 27: 257– 268.

124. Steiner, W. W.,, and P. L. Kuempel. 1998. Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J. Bacteriol. 180: 6269– 6275.

125. Stewart, G. J.,, and C. A. Carlson. 1986. The biology of natural transformation. Annu. Rev. Microbiol. 40: 211– 235.

126. Strauss, B. S., 1972. The relationship of repair mechanisms to the induction of chromosome aberrations in eukaryotic cells, p. 151– 171. In H. Altmann (ed.), DNA-Repair Mechanisms. F.K. Schattauer, Stuttgart, Germany.

127. Strumberg, D.,, A. A. Pilon,, M. Smith,, R. Hickey,, L. Malkas,, and Y. Pommier. 2000. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff. Mol. Cell. Biol. 20: 3977– 3987.

128. Taylor, A. F., 1988. RecBCD enzyme of Escherichia coli, p. 231– 263. In R. Kucherlapati, and G. R. Smith (ed.), Genetic Recombination. American Society for Microbiology, Washington, D.C.

129. Taylor, A. F.,, and G. R. Smith. 2003. RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423: 889– 893.

130. Templin, A.,, S. R. Kushner,, and A. J. Clark. 1972. Genetic analysis of mutations indirectly suppressing recB and recC mutations. Genetics 72: 205– 215.

131. Tseng, Y.-C.,, J.-L. Hung,, and T.-C. V. Wang. 1994. Involvement of the RecF pathway recombination genes in postreplication repair in UV-irradiated Escherichia coli cells. Mutat. Res. 315: 1– 9.

132. Uzest, M.,, S. D. Ehrlich,, and B. Michel. 1995. Lethality of rep recB and rep recC double mutants of Escherichia coli. Mol. Microbiol. 17: 1177– 1188.

133. West, S. C. 1997. Processing of recombination intermediates by the RuvABC proteins. Annu. Rev. Genet. 31: 213– 244.

134. Willetts, N. S.,, and A. J. Clark. 1969. Characteristics of some multiply recombination-deficient strains of Escherichia coli. J. Bacteriol. 100: 231– 239.

135. Xu, L.,, and K. J. Marians. 2003. PriA mediates DNA replication pathway choice at recombination intermediates. Mol. Cell 11: 817– 826.

136. Yarmolinsky, M. B.,, and E. Stevens. 1983. Replicationcontrol functions block the induction of an SOS response by a damaged P1 bacteriophage. Mol. Gen. Genet. 192: 140– 148.

137. Zieg, J.,, V. F. Maples,, and S. R. Kushner. 1978. Recombination levels of Escherichia coli K-12 mutants deficient in various replication, recombination, or repair genes. J. Bacteriol. 134: 958– 966.

138. Zinder, N. D.,, and J. Lederberg. 1952. Genetic exchange in Salmonella. J. Bacteriol. 64: 679– 699.

Tables

Overview of Homologous Recombination and Repair Machines

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Table 1

Viability of homologous recombination mutants and their sensitivity to different kinds of DNA-damaging treatments

Table 1

Viability of homologous recombination mutants and their sensitivity to different kinds of DNA-damaging treatments

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Table 2

The pageant of homologous recombination enzymes of E. coli

Table 2

The pageant of homologous recombination enzymes of E. coli