Chapter 4 : DNA-Binding Proteins and Chromatin

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Procaryotic genomic DNA and associated proteins together form an irregularly shaped structure, designated as the nucleoid. In contrast to the range of different chromatin proteins identified in bacteria, almost all eucaryal genomes are compacted into nucleosomes, chromatin, and chromosomes by essentially the same four proteins, histones H2A, H2B, H3, and H4. This chapter describes several different families of archaeal chromatin proteins with unrelated structures, but with the common properties of abundance, small size, positive charge, and ability to bind to DNA with little or no sequence specificity. Alba does bind to both DNA and RNA in species, but chromatin immunoprecipitation experiments argue convincingly that Alba is bound to genomic DNA and functions as a chromatin protein in . Sul10a is the generic name of an abundant ~11 kDa DNA-binding protein investigated from (Sac10a) and (Sso10a). An NMR solution structure has been established for methanogen chromosomal protein 1 (MC1) from sp. CHTI55. It is apparent that many different chromatin proteins have evolved, all of which must bind and compact DNA into complexes that are readily disassembled, or that are inherently compatible with DNA replication and transcription machineries. Gene expression requires transcription activators, for example, histone acetylases that help disassemble chromatin and so allow transcription factor access to the DNA. With the accumulation of genome sequences, it is now apparent that most archaea have the capacity to synthesize several different chromatin proteins.

Citation: Samson R, Reeve J. 2007. DNA-Binding Proteins and Chromatin, p 110-119. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch4
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Image of Figure 1.
Figure 1.

Phylogenetic tree based on rDNA sequence alignments of selected organisms. Branch lengths do not reflect evolutionary distances, but the branching orders are correctly represented. The numbers of histones (H), Sul7d (S), Alba (A), MC1 (M), 7kMk and HU-family members encoded in the genomes of representative archaea are denoted in parentheses. The NRC-1 histone has two HFs in one polypeptide (*). has two members of the HMfB family of archaeal histones with one HF (^), and also HMk, an archaeal histone with two HFs.

Citation: Samson R, Reeve J. 2007. DNA-Binding Proteins and Chromatin, p 110-119. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch4
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Image of Figure 2.
Figure 2.

Sequences and structures of representative archaeal chromatin proteins. Primary sequences of HMfB from (A), Sul7d (Sac7d) from (B), Alba (Sso10b1) from (C), and MC1 from sp. CHTI55 (D) are shown below the corresponding protein structure. The figure was constructed using structures available from the Protein Data Bank ( ). Regions with α-helical and β-strand structures are colored identically in the sequence and in the corresponding structure.

Citation: Samson R, Reeve J. 2007. DNA-Binding Proteins and Chromatin, p 110-119. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch4
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1. Agback, P.,, H. Baumann,, S. Knapp,, R. Ladenstein, and, T. Hard. 1998. Architecture of nonspecific protein-DNA interactions in the Sso7d-DNA complex. Nat. Struct. Biol. 5 : 579584.
2. Aravind, L.,, L. M. Iyer, and, V. Anantharaman. 2003. The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism. Genome Biol. 4 : R64.
3. Azam, T. A.,, A. Iwata,, A. Nishimura,, S. Ueda, and, A. Ishihama. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181 : 63616370.
4. Azam, T. A.,, S. Hiraga, and, A. Ishihama. 2000. Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5 : 613626.
5. Bailey, K. A.,, C. S. Chow, and, J. N. Reeve. 1999. Histone stoi-chiometry and DNA circularization in archaeal nucleosomes. Nucleic Acids Res. 27 : 532536.
6. Bailey, K. A.,, S. L. Pereira,, J. Widom, and, J. N. Reeve. 2000. Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. J. Mol. Biol. 303 : 2534.
7. Bartlett, M. S. 2005. Determinants of transcription initiation by archaeal RNA polymerase. Curr. Opin. Microbiol. 8 : 677684.
8. Bedell, J. L.,, S. P. Edmondson, and, J. W. Shriver. 2005 Role of a surface tryptophan in defining the structure, stability, and DNA binding of the hyperthermophile protein Sac7d. Biochemistry 44 : 915925.
9. Bell, S. D. 2005. Archaeal transcriptional regulation—variation on a bacterial theme? Trends Microbiol. 13 : 262265.
10. Bell, S. D.,, C. H. Botting,, B. N. Wardleworth,, S. P. Jackson, and, M. F. White. 2002. The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science 296 : 148151.
11. Berman, H. M.,, J. Westbrook,, Z. Feng,, G. Gilliland,, T. N. Bhat,, H. Weissig,, I. N. Shindyalov, and, P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28 : 235242.
12. Briggs, S. D.,, T. Xiao,, Z.-W. Sun,, J. A. Caldwell,, J. Shabanowitz,, D. F. Hunt,, C. D. Allis, and, B. D. Strahl. 2002. Trans-histone regulatory pathway in chromatin. Nature 418 : 498.
13. Brochier, C.,, S. Gribaldo,, Y. Zivanovic,, F. Confalonieri, and, P. Forterre. 2005. Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol. 6 : R42.
14. Cam, E. L.,, F. Culard,, E. Larquet,, E. Delain, and, J. A. Cognet. 1999. DNA bending induced by the archaebacterial histone-like protein MC1. J Mol Biol 285 : 101121.
15. Chen, C. Y.,, T. P. Ko,, T. W. Lin,, C. C. Chou,, C. J. Chen, and, A. H. Wang. 2005 Probing the DNA kink structure induced by the hyperthermophilic chromosomal protein Sac7d. Nucleic Acids Res. 33 : 430438.
16. Chen, L.,, L. R. Chen,, X. E. Zhou,, Y. Wang,, M. A. Kahsai,, A. T. Clark,, S. P. Edmondson,, Z. J. Liu,, J. P. Rose,, B. C. Wang,, E. J. Meehan, and, J. W. Shriver. 2004. The hyperthermophile protein Sso10a is a dimer of winged helix DNA-binding domains linked by an antiparallel coiled coil rod. J. Mol. Biol. 341 : 7391.
17. Chou, C-C.,, T-W. Lin,, C-Y. Chen, and, A.H-J. Wang. 2003. Crystal structure of the hyperthermophilic archaeal DNA-binding protein Sso10b2 at a resolution of 1.85 angstroms. J. Bacteriol. 185 : 40664073.
18. Cosgrove, M. S.,, J. D. Boeke, and, C. Wolberger. 2004. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11 : 10371043.
19. Cubonova, L.,, K. Sandman,, S. J. Hallam,, E. F. Delong, and, J. N. Reeve. 2005. Histones in Crenarchaea. J. Bacteriol. 187 : 54825485.
20. Cui, Q.,, Y. Tong,, H. Xue,, L. Huang,, Y. Feng,, Y., and, J. Wang. 2003. Two conformations of archaeal Ssh10b. J. Biol. Chem. 278 : 5101551022.
21. Decanniere, K.,, A. M. Babu,, K. Sandman,, J. N. Reeve, and, U. Heinemann. 2000. Crystal structures of recombinant his-tones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. J. Mol. Biol. 303 : 3547.
22. DeLange, R. J.,, G. R. Green, and, D. G. Searcy. 1981. A histone-like protein (HTa) from Thermoplasma acidophilum. I. Purification and properties. J. Biol. Chem. 256 : 900904.
23. De Vuyst, G.,, S. Aci,, D. Genest, and, F. Culard. 2005. Atypical recognition of particular DNA sequences by the archaeal chromosomal MC1 protein. Biochemistry 44 : 1036910377.
24. Dinger, M. E.,, G. J. Baillie, and, D. R. Musgrave. 2000. Growth phase-dependent expression and degradation of his-tones in the thermophilic archaeon Thermococcus zilligii. Mol. Microbiol. 36 : 876885.
25. Drlica, K., and, J. Rouviere-Yaniv. 1987. Histone-like proteins of bacteria. Microbiol. Rev. 51 : 301319.
26. Edmondson, S. P.,, M. A. Kahsai,, R. Gupta, and, J. W. Shriver. 2004. Characterization of Sac10a, a hyperthermophile DNA-binding protein from Sulfolobus acidocaldarius. Biochemistry 43 : 1302613036.
27. Fahrner, R. L.,, D. Cascio,, J. A. Lake, and, A. Slesarev. 2001. An ancestral nuclear protein assembly: crystal structure of the Methanopyrus kandleri histone. Protein Sci. 10 : 20022007.
28. Forbes, A. J.,, S. M. Patrie,, G. K. Taylor,, Y. B. Kim,, L. Jiang, and, N. L. Kelleher. 2004. Targeted analysis and discovery of posttranslational modifications in proteins from methanogenic archaea by top-down MS. Proc. Natl. Acad. Sci. USA 101 : 26782683.
29. Gao, Y. G.,, S. Y. Su,, H. Robinson,, S. Padmanabhan,, L. Lim,, B. S. McCrary,, S. P. Edmondson,, J. W. Shriver, and, A. H. Wang. 1998. The crystal structure of the hyperthermophile chromosomal protein Sso7d bound to DNA. Nat. Struct. Biol. 5 : 782786.
30. Guagliardi, A.,, L. Cerchia, and, M. Rossi. 2002. The Sso7d protein of Sulfolobus solfataricus: in vitro relationship among different activities. Archaea 1 : 8793.
31. Guagliardi, A.,, L. Mancusi, and, M. Rossi. 2004. Reversion of protein aggregation mediated by Sso7d in cell extracts of Sulfolobus solfataricus. Biochem. J. 381 : 249255.
32. Guo, R.,, H. Xue, and, L. Huang. 2003. Ssh10b, a conserved thermophilic archaeal protein, binds RNA in vivo. Mol. Microbiol. 50 : 16051615.
33. Hayat, M. A., and, D. A. Mancarella. 1995. Nucleoid proteins. Micron 26 : 461480.
34. Heinicke, I.,, J. Muller,, M. Pittelkow, and, A. Klein. 2004. Mutational analysis of genes encoding chromatin proteins in the archaeon Methanococcus voltae indicates their involvement in the regulation of gene expression. Mol. Genet. Genomics 272 : 7687.
35. Jelinska, C.,, M. J. Conroy,, C. J. Craven,, A. M. Hounslow,, P. A. Bullough,, J. P. Waltho,, G. L. Taylor, and, M. F. White. 2005. Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging. Structure 13 : 963971.
36. Kahsai, M. A.,, B. Vogler,, A. T. Clark,, S. P. Edmondson, and, J. W. Shriver. 2005. Solution structure, stability, and flexibility of Sso10a: a hyperthermophile coiled-coil DNA-binding protein. Biochemistry 44 : 28222832.
37. Kamau, E.,, N. D. Tsihlis,, L. A. Simmons, and, A. Grove. 2005. Surface salt bridges modulate the DNA site size of bacterial histone-like HU proteins. Biochem. J. 390 : 4955.
38. Kasinsky, H. E.,, J. D. Lewis,, J. B. Dacks and, J. Ausió. 2001. Origin of H1 linker histones. FASEB J. 15 : 3442
39. Kelman, Z., and, M. F. White. 2005. Archaeal DNA replication and repair. Curr. Opin. Microbiol. 8 : 669676.
40. Ko, T. P.,, H. M. Chu,, C. Y Chen,, C. C. Chou, and, A. H. Wang. 2004. Structures of the hyperthermophilic chromosomal protein Sac7d in complex with DNA decamers. Acta Crystallogr. D Biol. Crystallogr. 60 : 13811387.
41. Kvaratskhelia, M.,, B. N. Wardleworth,, C. S. Bond,, J. M. Fogg,, D. M. Lilley, and, M. F. White. 2002. Holliday junction resolution is modulated by archaeal chromatin components in vitro . J. Biol. Chem. 277 : 29922996.
42. Le Cam, E.,, F. Culard,, E. Larquet,, E. Delain, and, J. A. H. Cognet. 1999. DNA bending induced by the archaebacterial histone-like protein MC1. J. Mol. Biol. 285 : 10111021.
43. Li, W. T.,, K. Sandman,, S. L. Pereira, and, J. N. Reeve. 2000. MJ1647, an open reading frame in the genome of the hyper-thermophile Methanococcus jannaschii, encodes a very thermostable archaeal histone with a C-terminal extension. Extre-mophiles 4 : 4351.
44. Lopez-Garcia, P.,, S. Knapp,, R. Ladenstein, and, P. Forterre. 1998. In vitro DNA binding of the archaeal protein Sso7d induces negative supercoiling at temperatures typical for thermophilic growth. Nucleic Acids Res. 26 : 23222328.
45. Lou, H.,, Z. Duan,, X. Huo, and, L. Huang. 2004. Modulation of hyperthermophilic DNA polymerase activity by archaeal chromatin proteins. J Biol Chem 279 : 12732.
46. Luger, K.,, A. W. Mader,, R. K. Richmond,, D. F. Sargent, and, T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 : 251260.
47. Marc, F.,, K. Sandman,, R. Lurz, and, J. N. Reeve. 2002. Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J. Biol. Chem. 277 : 3087930886.
48. Marsh, V. L.,, A. T. McGeoch, and, S. D. Bell. 2006. Influence of chromatin and single strand binding proteins of the activity of an archaeal MCM. J. Mol. Biol. 357 : 13451350.
49. Marsh, V. L.,, S. Y. Peak-Chew, and, S. D. Bell. 2005. Sir2 and the acetyltransferase, Pat, regulate the archaeal chromatin protein, Alba. J. Biol. Chem. 280 : 2112221128.
50. Martin, W. 2005. Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. Curr. Opin. Microbiol. 8 : 630637.
51. McAfee, J. G.,, S. P. Edmondson,, I. Zegar, and, J. W. Shriver. 1996. Equilibrium DNA binding of Sac7d protein from the hyperthermophile Sulfolobus acidocaldarius: fluorescence and circular dichroism studies. Biochemistry 35 : 40344045.
52. Mellor, J. 2005. The dynamics of chromatin remodeling at promoters. Mol. Cell 19 : 147157.
53. Minsky, A. 2004. Information content and complexity in the high-order organization of DNA. Annu. Rev. Biophys. Biomol. Struct. 33 : 317342.
54. Napoli, A.,, Y. Zivanovic,, C. Bocs,, C. Buhler,, M. Rossi,, P. Forterre, and, M. Ciaramella. 2002. DNA bending, compaction and negative supercoiling by the architectural protein Sso7d of Sulfolobus solfataricus. Nucleic Acids Res. 30 : 26562662.
55. Narliker, G. J.,, H.-Y. Fan, and, R. E. Kingston. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108 : 475487.
56. Paquet, F.,, F. Culard,, F. Barbault,, J. C. Maurizot, and, G. Lancelot. 2004. NMR solution structure of the archaebacterial chromosomal protein MC1 reveals a new protein fold. Biochemistry 43 : 1497114978.
57. Paradinas, C.,, A. Gervais,, J. C. Maurizot, and, F. Culard. 1998. Structure-specific binding recognition of a methanogen chromosomal protein. Eur. J. Biochem. 257 : 372379.
58. Pavlov, N. A.,, D. I. Cherny,, T. M. Jovin, and, A. I. Slesarev. 2002. Nucleosome-like complex of the histone from the hyperthermophile Methanopyrus kandleri (MkaH) with linear DNA. J. Biomol. Struct. Dyn. 20 : 207214.
59. Pavlov, N. A.,, D. I. Cherny,, I. V. Nazimov,, A. I. Slesarev, and, V. Subramaniam. 2002. Identification, cloning and characterization of a new DNA-binding protein from the hyperthermophilic methanogen Methanopyrus kandleri. Nucleic Acids Res. 30 : 685694.
60. Pedersen, L. B.,, S. Birkelund, and, G. Christiansen. 1996. Purification of recombinant Chlamydia trachomatis histone H1-like protein Hc2, and comparative functional analysis of Hc2 and Hc1. Mol. Microbiol. 20 : 295311.
61. Pereira, S. L.,, R. A. Grayling,, R. Lurz, and, J. N. Reeve. 1997. Archaeal nucleosomes. Proc. Natl. Acad. Sci. USA 94 : 1263312637.
62. Pereira, S. L., and, J. N. Reeve. 1999 Archaeal nucleosome positioning sequence from Methanothermus fervidus. J. Mol. Biol. 289 : 675681.
63. Peters, W. B.,, S. P. Edmondson, and, J. W. Shriver. 2005. Effect of mutation of the Sac7d intercalating residues on the temperature dependence of DNA distortion and binding thermodynamics. Biochemistry 44 : 47944804.
64. Reeve, J. N. 2003. Archaeal chromatin and transcription. Mol. Microbiol. 48 : 587598.
65. Ruepp, A.,, W. Graml,, M. L. Santos-Martinez,, K. K. Koretke,, C. Volker,, H. W. Mewes,, D. Frishman,, S. Stocker,, A. N. Lupas, and, W. Baumeister. 2000. The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407 : 508513.
66. Sandman, K.,, R. A. Grayling,, B. Dobrinski,, R. Lurz, and, J. N. Reeve. 1994. Growth-phase-dependent synthesis of histones in the archaeon Methanothermus fervidus. Proc. Natl. Acad. Sci. USA 91 : 1262412628.
67. Sandman, K.,, J. A. Krzycki,, B. Dobrinski,, R. Lurz, and, J. N. Reeve. 1990. DNA binding protein HMf, from the hyperthermophilic archaebacterium Methanothermus fervidus, is most closely related to histones. Proc. Natl. Acad. Sci. USA 87 : 57885791.
68. Sandman, K., and, J. N. Reeve. 2000. Structure and functional relationships of archaeal and eucaryal histones and nucleo-somes. Arch. Microbiol. 173 : 165169.
69. Sato, N.,, K. Terasawa,, K. Miyajima, and, Y. Kabeya. 2003. Organization, developmental dynamics, and evolution of plastid nucleoids. Int. Rev. Cytol. 232 : 217262.
70. Schieg, P., and, H. Herzel, H. 2004. Periodicities of 10-11 bp as indicators of the supercoiled state of genomic DNA. J. Mol. Biol. 343 : 891901.
71. Setlow, P. 1995. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49 : 2954.
72. Shehi, E.,, S. Serina,, G. Fumagalli,, M. Vanoni,, R. Consonni, and, L. Zetta. 2001. The Sso7d DNA-binding protein from Sulfolobus solfataricus has ribonuclease activity. FEBS Lett. 497 : 131136.
73. Shin, J. H.,, T. J. Santangelo,, Y. Xie,, J. N. Reeve, and, Z. Kelman. Archaeal MCM helicase can unwind DNA bound by archaeal histones and transcription factors. J. Biol. Chem., in press.
74. Strahl, B. D., and, C. D. Allis. 2000. The language of covalent histone modifications. Nature 403 : 4145.
75. Struhl, K. 1999. Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell 98 : 14.
76. Su, S.,, Y.-G. Gao,, H. Robinson,, Y-C. Liaw,, S. P. Edmondson,, J. W. Shriver, and, A. H.-J. Wang. 2000. Crystal structures of the chromosomal proteins Sso7d/Sac7d bound to DNA containing T-G mismatched base pairs. J. Mol. Biol. 303 : 395403.
77. Swinger, K. K.,, K. M. Lemberg,, Y. Zhang, and, P. A. Rice. 2003. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J. 22 : 37493760.
78. Teyssier, C.,, B. Laine,, A. Gervais,, J. C. Maurizot, and, F. Culard. 1994. Archaebacterial histone-like protein MC1 can exhibit a sequence-specific binding to DNA. Biochem. J. 303 : 567573.
79. Teyssier, C.,, F. Toulme,, J. P. Touzel,, A. Gervais,, J. C. Maurizot, and, F. Culard. 1996. Preferential binding of the archaebacter-ial histone-like MC1 protein to negatively supercoiled DNA minicircles. Biochemistry 35:7954–7958.
80. Tomschik, M.,, M. A. Karymov,, J. Zlatanova, and, S. H. Leuba,, S.H. 2001. The archaeal histone-fold protein HMf organizes DNA in bona fide chromatin fibres. Structure 9 : 12011211.
81. Triana, O.,, N. Galanti,, N. Olea,, U. Hellman,, C. Wernstedt,, H. Lujan,, C. Medina, and, G. C. Toro. 2001. Chromatin and histones from Giardia lamblia: a new puzzle in primitive eukaryotes. J. Cell. Biochem. 82 : 573582.
82. Tsukiyama, T. 2002. The in vivo functions of ATP-dependent chromatin-remodelling factors. Nat. Rev. Mol. Cell. Biol. 3 : 422429.
83. Wang, G.,, R. Guo,, M. Bartlam,, H. Yang,, H. Xue,, Y. Liu,, L. Huang, and, Z. Rao. 2003. Crystal structure of a DNA binding protein from the hyperthermophilic euryarchaeon Methanococcus jannaschii. Protein Sci. 12 : 28152822.
84. Wardleworth, B. N.,, R. J. Russell,, S. D. Bell,, G. L. Taylor, and, M. F. White. 2002. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J. 21 : 46544662.
85. White, M. F., and, S. D. Bell. 2002. Holding it together: chromatin in the Archaea. Trends Genet. 18 : 621626.
86. Wong, J. T.,, D. C. New,, J. C. Wong, and, V. K. Hung. 2003. Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Eukaryot. Cell 2 : 646650.
87. Xie, Y., and, J. N. Reeve. 2004. Transcription by an archaeal RNA polymerase is slowed but not blocked by an archaeal nucleosome. J. Bacteriol. 186 : 34923498.
88. Xue, H.,, R. Guo,, Y. Wen,, D. Liu, and, L. Huang. 2000. An abundant DNA binding protein from the hyperthermophilic archaeon Sulfolobus shibatae affects DNA supercoiling in a temperature-dependent fashion. J. Bacteriol. 182 : 39293933.
89. Zhao, K.,, X. Chai, and, R. Marmorstein. 2003. Structure of a Sir2 substrate, Alba, reveals a mechanism for deacetylation-induced enhancement of DNA binding. J. Biol. Chem. 278 : 2607126077.

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