Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2010 (2010), Article ID 179594, 32 pages
http://dx.doi.org/10.4061/2010/179594
Review Article

Molecular Mechanisms of the Whole DNA Repair System: A Comparison of Bacterial and Eukaryotic Systems

1Department of Biological Sciences, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka, Osaka 560-0043, Japan
2RIKEN SPring-8 Center, Harima Institute, 1-1-1 Kouto, Sayo-cho, Sayo-gun, Hyogo 679-5148, Japan
3Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka 565-0871, Japan

Received 15 June 2010; Accepted 27 July 2010

Academic Editor: Shigenori Iwai

Copyright © 2010 Rihito Morita et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. O. D. Schärer, “Chemistry and biology of DNA repair,” Angewandte Chemie, vol. 42, no. 26, pp. 2946–2974, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. F. Altieri, C. Grillo, M. Maceroni, and S. Chichiarelli, “DNA damage and repair: from molecular mechanisms to health implications,” Antioxidants and Redox Signaling, vol. 10, no. 5, pp. 891–937, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. E. C. Friedberg, G. C. Walker, and W. Siede, DNA Repair and Mutagenesis, ASM Press, Washington, DC, USA, 2006.
  4. T. Oshima and K. Imahori, “Description of Thermus thermophilus (Yoshida and Oshima) comb. nov., a nonsporulating thermophilic bacterium from a Japanese thermal spa,” International Journal of Systematic Bacteriology, vol. 24, no. 1, pp. 102–112, 1974. View at Google Scholar · View at Scopus
  5. H. Iino, H. Naitow, Y. Nakamura et al., “Crystallization screening test for the whole-cell project on Thermus thermophilus HB8,” Acta Crystallographica Section F, vol. 64, no. 6, pp. 487–491, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Yokoyama, H. Hirota, T. Kigawa et al., “Structural genomics projects in Japan,” Nature Structural Biology, vol. 7, supplement, pp. 943–945, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Payne, P. F. Heelis, B. R. Rohrs, and A. Sancar, “The active form of Escherichia coli DNA photolyase contains a fully reduced flavin and not a flavin radical, both in vivo and in vitro,” Biochemistry, vol. 26, no. 22, pp. 7121–7127, 1987. View at Google Scholar · View at Scopus
  8. A. Sancar and G. B. Sancar, “DNA repair enzymes,” Annual Review of Biochemistry, vol. 57, pp. 29–67, 1988. View at Google Scholar · View at Scopus
  9. C. Aubert, M. H. Vos, P. Mathis, A. P. M. Eker, and K. Brettel, “Intraprotein radical transfer during photoactivation of DNA photolyase,” Nature, vol. 405, no. 6786, pp. 586–590, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Kato, K. Hasegawa, Y. Hidaka, S. Kuramitsu, and T. Hoshino, “Characterization of a thermostable DNA photolyase from an extremely thermophilic bacterium, Thermus thermophilus HB27,” Journal of Bacteriology, vol. 179, no. 20, pp. 6499–6503, 1997. View at Google Scholar · View at Scopus
  11. H.-W. Park, S.-T. Kim, A. Sancar, and J. Deisenhofer, “Crystal structure of DNA photolyase from Escherichia coli,” Science, vol. 268, no. 5219, pp. 1866–1872, 1995. View at Google Scholar · View at Scopus
  12. T. Tamada, K. Kitadokoro, Y. Higuchi et al., “Crystal structure of DNA photolyase from Anacystis nidulans,” Nature Structural Biology, vol. 4, no. 11, pp. 887–891, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Komori, R. Masui, S. Kuramitsu et al., “Crystal structure of thermostable DNA photolyase: pyrimidine-dimer recognition mechanism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 24, pp. 13560–13565, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Torizawa, T. Ueda, S. Kuramitsu et al., “Investigation of the cyclobutane pyrimidine dimer (CPD) photolyase DNA recognition mechanism by NMR analyses,” Journal of Biological Chemistry, vol. 279, no. 31, pp. 32950–32956, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Mees, T. Klar, P. Gnau et al., “Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair,” Science, vol. 306, no. 5702, pp. 1789–1793, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Ueda, A. Kato, Y. Ogawa et al., “NMR study of repair mechanism of DNA photolyase by FAD-induced paramagnetic relaxation enhancement,” Journal of Biological Chemistry, vol. 279, no. 50, pp. 52574–52579, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Ueda, A. Kato, S. Kuramitsu, H. Terasawa, and I. Shimada, “Identification and characterization of a second chromophore of DNA photolyase from Thermus thermophilus HB27,” Journal of Biological Chemistry, vol. 280, no. 43, pp. 36237–36243, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Klar, G. Kaiser, U. Hennecke, T. Carell, A. Batschauer, and L.-O. Essen, “Natural and non-natural antenna chromophores in the DNA photolyase from Thermus thermophilus,” ChemBioChem, vol. 7, no. 11, pp. 1798–1806, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Kiefer, K. Arnold, M. Künzli, L. Bordoli, and T. Schwede, “The SWISS-MODEL repository and associated resources,” Nucleic Acids Research, vol. 37, supplement 1, pp. D387–D392, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Schwede, J. Kopp, N. Guex, and M. C. Peitsch, “SWISS-MODEL: an automated protein homology-modeling server,” Nucleic Acids Research, vol. 31, no. 13, pp. 3381–3385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. G. T. J. Van Der Horst, M. Muijtjens, K. Kobayashi et al., “Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms,” Nature, vol. 398, no. 6728, pp. 627–630, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Müller and T. Carell, “Structural biology of DNA photolyases and cryptochromes,” Current Opinion in Structural Biology, vol. 19, no. 3, pp. 277–285, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. E. L. Loechler, C. L. Green, and J. M. Essigmann, “In vivo mutagenesis by O6-methylguanine built into a unique site in a viral genome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 20, pp. 6271–6275, 1984. View at Google Scholar · View at Scopus
  24. A. Loveless, “Possible relevance of O-6 alkylation of deoxyguanosine to the mutagenicity and carcinogenicity of nitrosamines and nitrosamides,” Nature, vol. 223, no. 5202, pp. 206–207, 1969. View at Publisher · View at Google Scholar · View at Scopus
  25. E. T. Snow, R. S. Foote, and S. Mitra, “Base-pairing properties of O6-methylguanine in template DNA during in vitro DNA replication,” Journal of Biological Chemistry, vol. 259, no. 13, pp. 8095–8100, 1984. View at Google Scholar · View at Scopus
  26. T. Lindahl, B. Demple, and P. Robins, “Suicide inactivation of the E. coliO6-methylguanine-DNA methyltransferase,” EMBO Journal, vol. 1, no. 11, pp. 1359–1363, 1982. View at Google Scholar · View at Scopus
  27. M. Olsson and T. Lindahl, “Repair of alkylated DNA in Escherichia coli. Methyl group transfer from O6-methylguanine to a protein cysteine residue,” Journal of Biological Chemistry, vol. 255, no. 22, pp. 10569–10571, 1980. View at Google Scholar · View at Scopus
  28. O. Wiestler, P. Kleihues, and A. E. Pegg, “O6-alkylguanine-DNA alkyltransferase activity in human brain and brain tumors,” Carcinogenesis, vol. 5, no. 1, pp. 121–124, 1984. View at Google Scholar · View at Scopus
  29. D. Bhattacharyya, R. S. Foote, A. M. Boulden, and S. Mitra, “Physicochemical studies of human O6-methylguanine-DNA methyltransferase,” European Journal of Biochemistry, vol. 193, no. 2, pp. 337–343, 1990. View at Google Scholar · View at Scopus
  30. A. M. Boulden, R. S. Foote, G. S. Fleming, and S. Mitra, “Purification and some properties of human DNA-O6-methylguanine methyltransferase,” Journal of Biosciences, vol. 11, no. 1–4, pp. 215–224, 1987. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Demple, A. Jacobsson, and M. Olsson, “Repair of alkylated DNA in Escherichia coli. Physical properties of O6-methylguanine-DNA methyltransferase,” Journal of Biological Chemistry, vol. 257, no. 22, pp. 13776–13780, 1982. View at Google Scholar · View at Scopus
  32. D. S. Daniels and J. A. Tainer, “Conserved structural motifs governing the stoichiometric repair of alkylated DNA by O6-alkylguanine-DNA alkyltransferase,” Mutation Research, vol. 460, no. 3-4, pp. 151–163, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. D. S. Daniels, T. T. Woo, K. X. Luu et al., “DNA binding and nucleotide flipping by the human DNA repair protein AGT,” Nature Structural and Molecular Biology, vol. 11, no. 8, pp. 714–720, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Aramini, J. L. Tubbs, S. Kanugula et al., “Structural basis of O6-alkylguanine recognition by a bacterial alkyltransferase-like DNA repair protein,” Journal of Biological Chemistry, vol. 285, no. 18, pp. 13736–13741, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. G. P. Margison, A. Butt, S. J. Pearson et al., “Alkyltransferase-like proteins,” DNA Repair, vol. 6, no. 8, pp. 1222–1228, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Mazon, G. Philippin, J. Cadet, D. Gasparutto, and R. P. Fuchs, “The alkyltransferase-like ybaZ gene product enhances nucleotide excision repair of O6-alkylguanine adducts in E. coli,” DNA Repair, vol. 8, no. 6, pp. 697–703, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Morita, N. Nakagawa, S. Kuramitsu, and R. Masui, “An O6-methylguanine-DNA methyltransferase-like protein from Thermus thermophilus interacts with a nucleotide excision repair protein,” Journal of Biochemistry, vol. 144, no. 2, pp. 267–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. S. J. Pearson, J. Ferguson, M. Santibanez-Koref, and G. P. Margison, “Inhibition of O6-methylguanine-DNA methyltransferase by an alkyltransferase-like protein from Escherichia coli,” Nucleic Acids Research, vol. 33, no. 12, pp. 3837–3844, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. J. Pearson, S. Wharton, A. J. Watson et al., “A novel DNA damage recognition protein in Schizosaccharomyces pombe,” Nucleic Acids Research, vol. 34, no. 8, pp. 2347–2354, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. J. L. Tubbs, V. Latypov, S. Kanugula et al., “Flipping of alkylated DNA damage bridges base and nucleotide excision repair,” Nature, vol. 459, no. 7248, pp. 808–813, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. L. H. Breimer and T. Lindahl, “DNA glycosylase activities for thymine residues damaged by ring saturation, fragmentation, or ring contraction are functions of endonuclease III in Escherichia coli,” Journal of Biological Chemistry, vol. 259, no. 9, pp. 5543–5548, 1984. View at Google Scholar · View at Scopus
  42. B. Demple, A. Johnson, and D. Fung, “Exonuclease III and endonuclease IV remove 3 blocks from DNA synthesis primers in H2O2-damaged Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 20, pp. 7731–7735, 1986. View at Google Scholar · View at Scopus
  43. J. D. Levin, A. W. Johnson, and B. Demple, “Homogeneous Escherichia coli endonuclease IV. Characterization of an enzyme that recognizes oxidative damage in DNA,” Journal of Biological Chemistry, vol. 263, no. 17, pp. 8066–8071, 1988. View at Google Scholar · View at Scopus
  44. T. V. McCarthy and T. Lindahl, “Methyl phosphotriesters in alkylated DNA are repaired by the Ada regulatory protein of E. coli,” Nucleic Acids Research, vol. 13, no. 8, pp. 2683–2698, 1985. View at Google Scholar · View at Scopus
  45. P. Landini and M. R. Volkert, “Regulatory responses of the adaptive response to alkylation damage: a simple regulon with complex regulatory features,” Journal of Bacteriology, vol. 182, no. 23, pp. 6543–6549, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Sedgwick and T. Lindahl, “Recent progress on the Ada response for inducible repair of DNA alkylation damage,” Oncogene, vol. 21, no. 58, pp. 8886–8894, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. S. C. Trewick, T. F. Henshaw, R. P. Hausinger, T. Lindahl, and B. Sedgwick, “Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage,” Nature, vol. 419, no. 6903, pp. 174–178, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. A. Kurowski, A. S. Bhagwat, G. Papaj, and J. M. Bujnicki, “Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB,” BMC Genomics, vol. 4, no. 1, article no. 48, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Duncan, S. C. Trewick, P. Koivisto, P. A. Bates, T. Lindahl, and B. Sedgwick, “Reversal of DNA alkylation damage by two human dioxygenases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 26, pp. 16660–16665, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. Y.-F. Wei, K. C. Carter, R.-P. Wang, and B. K. Shell, “Molecular cloning functional analysis of a human cDNA encoding an Escherichia coli AlkB homolog, a protein involved in DNA alkylation damage repair,” Nucleic Acids Research, vol. 24, no. 5, pp. 931–937, 1996. View at Google Scholar · View at Scopus
  51. P. A. Aas, M. Otterlei, P. Ø. Falnes et al., “Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA,” Nature, vol. 421, no. 6925, pp. 859–863, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. K. S. Gates, “An overview of chemical processes that damage cellular DNA: spontaneous hydrolysis, alkylation, and reactions with radicals,” Chemical Research in Toxicology, vol. 22, no. 11, pp. 1747–1760, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. M. D. Gibbs, R. A. Reeves, D. Mandelman, Q. Mi, J. Lee, and P. L. Bergquist, “Molecular diversity and catalytic activity of Thermus DNA polymerases.,” Extremophiles, vol. 13, no. 5, pp. 817–826, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Makiela-Dzbenska, M. Jaszczur, M. Banach-Orlowska, P. Jonczyk, R. M. Schaaper, and I. J. Fijalkowska, “Role of Escherichia coli DNA polymerase I in chromosomal DNA replication fidelity,” Molecular Microbiology, vol. 74, no. 5, pp. 1114–1127, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Yoshiyama, K. Higuchi, H. Matsumura, and H. Maki, “Directionality of DNA replication fork movement strongly affects the generation of spontaneous mutations in Escherichia coli,” Journal of Molecular Biology, vol. 307, no. 5, pp. 1195–1206, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. B. Dalhus, J. K. Laerdahl, P. H. Backe, and M. Bjørås, “DNA base repair—recognition and initiation of catalysis,” FEMS Microbiology Reviews, vol. 33, no. 6, pp. 1044–1078, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. D. O. Zharkov, “Base excision DNA repair,” Cellular and Molecular Life Sciences, vol. 65, no. 10, pp. 1544–1565, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Visnes, B. Doseth, H. S. Pettersen et al., “Uracil in DNA and its processing by different DNA glycosylases,” Philosophical Transactions of the Royal Society B, vol. 364, no. 1517, pp. 563–568, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. J. C. Fromme, A. Banerjee, and G. L. Verdine, “DNA glycosylase recognition and catalysis,” Current Opinion in Structural Biology, vol. 14, no. 1, pp. 43–49, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. A. A. Ischenko and M. K. Saparbaev, “Alternative nucleotide incision repair pathway for oxidative DNA damage,” Nature, vol. 415, no. 6868, pp. 183–187, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. E. S. Motta, P. T. Souza-Santos, T. R. Cassiano, F. J. S. Dantas, A. Caldeira-De-Araujo, and J. C. P. De Mattos, “Endonuclease IV is the main base excision repair enzyme involved in DNA damage induced by UVA radiation and stannous chloride,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 376218, 9 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. S. T. Mundle, J. C. Delaney, J. M. Essigmann, and P. R. Strauss, “Enzymatic mechanism of human apurinic/apyrimidinic endonuclease against a THF AP site model substrate,” Biochemistry, vol. 48, no. 1, pp. 19–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. G. Dianov, B. Sedgwick, G. Daly, M. Olsson, S. Lovett, and T. Lindahl, “Release of 5-terminal deoxyribose-phosphate residues from incised abasic sites in DNA by the Escherichia coli RecJ protein,” Nucleic Acids Research, vol. 22, no. 6, pp. 993–998, 1994. View at Google Scholar · View at Scopus
  64. C. E. Piersen, A. K. McCullough, and R. S. Lloyd, “AP lyases and dRPases: commonality of mechanism,” Mutation Research, vol. 459, no. 1, pp. 43–53, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Prasad, V. K. Batra, X.-P. Yang et al., “Structural insight into the DNA polymerase β deoxyribose phosphate lyase mechanism,” DNA Repair, vol. 4, no. 12, pp. 1347–1357, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. A. K. McCullough, A. Sanchez, M. L. Dodson, P. Marapaka, J.-S. Taylor, and R. Stephen Lloyd, “The reaction mechanism of DNA glycosylase/AP lyases at abasic sites,” Biochemistry, vol. 40, no. 2, pp. 561–568, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. A. B. Robertson, A. Klungland, T. Rognes, and I. Leiros, “DNA repair in mammalian cells,” Cellular and Molecular Life Sciences, vol. 66, no. 6, pp. 981–993, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Hoseki, A. Okamoto, R. Masui et al., “Crystal structure of a family 4 uracil-DNA glycosylase from Thermus thermophilus HB8,” Journal of Molecular Biology, vol. 333, no. 3, pp. 515–526, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Kosaka, J. Hoseki, N. Nakagawa, S. Kuramitsu, and R. Masui, “Crystal structure of family 5 uracil-DNA glycosylase bound to DNA,” Journal of Molecular Biology, vol. 373, no. 4, pp. 839–850, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Sugahara, T. Mikawa, R. Kato et al., “Crystallization and preliminary X-ray crystallographic studies of Thermus thermophilus HB8 MutM protein involved in repairs of oxidative DNA damage,” Journal of Biochemistry, vol. 127, no. 1, pp. 9–11, 2000. View at Google Scholar · View at Scopus
  71. L. H. Pearl, “Structure and function in the uracil-DNA glycosylase superfamily,” Mutation Research, vol. 460, no. 3-4, pp. 165–181, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. O. D. Schärer and J. Jiricny, “Recent progress in the biology, chemistry and structural biology of DNA glycosylases,” BioEssays, vol. 23, no. 3, pp. 270–281, 2001. View at Google Scholar · View at Scopus
  73. T. Mikawa, R. Kato, M. Sugahara, and S. Kuramitsu, “Thermostable repair enzyme for oxidative DNA damage from extremely thermophilic bacterium, Thermus thermophilus HB8,” Nucleic Acids Research, vol. 26, no. 4, pp. 903–910, 1998. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Fortini, B. Pascucci, E. Parlanti, R. W. Sobol, S. H. Wilson, and E. Dogliotti, “Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells,” Biochemistry, vol. 37, no. 11, pp. 3575–3580, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. A. J. Podlutsky, I. I. Dianova, S. H. Wilson, V. A. Bohr, and G. L. Dianov, “DNA synthesis and dRPase activities of polymerase β are both essential for single-nucleotide patch base excision repair in mammalian cell extracts,” Biochemistry, vol. 40, no. 3, pp. 809–813, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. U. Sattler, P. Frit, B. Salles, and P. Calsou, “Long-patch DNA repair synthesis during base excision repair in mammalian cells,” EMBO Reports, vol. 4, no. 4, pp. 363–367, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. R. Gary, K. Kim, H. L. Cornelius, M. S. Park, and Y. Matsumoto, “Proliferating cell nuclear antigen facilitates excision in long-patch base excision repair,” Journal of Biological Chemistry, vol. 274, no. 7, pp. 4354–4363, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. A. S. Jaiswal, R. Balusu, M. L. Armas, C. N. Kundu, and S. Narayan, “Mechanism of adenomatous polyposis coli (APC)-mediated blockage of long-patch base excision repair,” Biochemistry, vol. 45, no. 51, pp. 15903–15914, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. N. A. Lebedeva, N. I. Rechkunova, S. V. Dezhurov et al., “Comparison of functional properties of mammalian DNA polymerase λ and DNA polymerase β in reactions of DNA synthesis related to DNA repair,” Biochimica et Biophysica Acta, vol. 1751, no. 2, pp. 150–158, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Lin, W. A. Beard, D. D. Shock, R. Prasad, E. W. Hou, and S. H. Wilson, “DNA polymerase β and flap endonuclease 1 enzymatic specificities sustain DNA synthesis for long patch base excision repair,” Journal of Biological Chemistry, vol. 280, no. 5, pp. 3665–3674, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. R. Prasad, M. J. Longley, F. S. Sharief, E. W. Hou, W. C. Copeland, and S. H. Wilson, “Human DNA polymerase θ possesses 5-dRP lyase activity and functions in single-nucleotide base excision repair in vitro,” Nucleic Acids Research, vol. 37, no. 6, pp. 1868–1877, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Stucki, B. Pascucci, E. Parlanti et al., “Mammalian base excision repair by DNA polymerases δ and ε,” Oncogene, vol. 17, no. 7, pp. 835–843, 1998. View at Google Scholar · View at Scopus
  83. J.-S. Sung and D. W. Mosbaugh, “Escherichia coli uracil- and ethenocytosine-initiated base excision DNA repair: rate-limiting step and patch size distribution,” Biochemistry, vol. 42, no. 16, pp. 4613–4625, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Singh, A. Srivastava, S. S. Patel, and M. J. Modak, “Participation of the fingers subdomain of Escherichia coli DNA polymerase I in the strand displacement synthesis of DNA,” Journal of Biological Chemistry, vol. 282, no. 14, pp. 10594–10604, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. D. L. Ho, W. M. Byrnes, W.-P. Ma, Y. Shi, D. J. E. Callaway, and Z. Bu, “Structure-specific DNA-induced conformational changes in Taq polymerase revealed by small angle neutron scattering,” Journal of Biological Chemistry, vol. 279, no. 37, pp. 39146–39154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. M. W. Kaiser, N. Lyamicheva, W. Ma et al., “A comparison of eubacterial and archaeal structure-specific 5- exonucleases,” Journal of Biological Chemistry, vol. 274, no. 30, pp. 21387–21394, 1999. View at Publisher · View at Google Scholar · View at Scopus
  87. V. Lyamichev, M. A. D. Brow, and J. E. Dahlberg, “Structure-specific endonucleolytic cleavage of nucleic acids by eubacterial DNA polymerases,” Science, vol. 260, no. 5109, pp. 778–783, 1993. View at Google Scholar · View at Scopus
  88. W.-P. Ma, M. W. Kaiser, N. Lyamicheva et al., “RNA template-dependent 5 nuclease activity of Thermus aquaticus and Thermus thermophilus DNA polymerases,” Journal of Biological Chemistry, vol. 275, no. 32, pp. 24693–24700, 2000. View at Publisher · View at Google Scholar · View at Scopus
  89. Y. Xu, N. D. F. Grindley, and C. M. Joyce, “Coordination between the polymerase and 5-nuclease components of DNA polymerase I of Escherichia coli,” Journal of Biological Chemistry, vol. 275, no. 27, pp. 20949–20955, 2000. View at Publisher · View at Google Scholar · View at Scopus
  90. F. J. López de Saro and M. O'Donnell, “Interaction of the β sliding clamp with MutS, ligase, and DNA polymerase I,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8376–8380, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Yamtich and J. B. Sweasy, “DNA polymerase Family X: function, structure, and cellular roles,” Biochimica et Biophysica Acta, vol. 1804, no. 5, pp. 1136–1150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. W. W. Duym, K. A. Fiala, N. Bhatt, and Z. Suo, “Kinetic effect of a downstream strand and its 5-terminal moieties on single nucleotide gap-filling synthesis catalyzed by human DNA polymerase λ,” Journal of Biological Chemistry, vol. 281, no. 47, pp. 35649–35655, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. B. Baños, J. M. Lázaro, L. Villar, M. Salas, and M. de Vega, “Characterization of a Bacillus subtilis 64-kDa DNA Polymerase X Potentially Involved in DNA Repair,” Journal of Molecular Biology, vol. 384, no. 5, pp. 1019–1028, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. N. P. Khairnar and H. S. Misra, “DNA polymerase X from Deinococcus radiodurans implicated in bacterial tolerance to DNA damage is characterized as a short patch base excision repair polymerase,” Microbiology, vol. 155, no. 9, pp. 3005–3014, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. B. Baños, J. M. Lázaro, L. Villar, M. Salas, and M. de Vega, “Editing of misaligned 3-termini by an intrinsic 35 exonuclease activity residing in the PHP domain of a family X DNA polymerase,” Nucleic Acids Research, vol. 36, no. 18, pp. 5736–5749, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Blasius, I. Shevelev, E. Jolivet, S. Sommer, and U. Hübscher, “DNA polymerase X from Deinococcus radiodurans possesses a structure-modulated 3>5 exonuclease activity involved in radioresistance,” Molecular Microbiology, vol. 60, no. 1, pp. 165–176, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Nakane, N. Nakagawa, S. Kuramitsu, and R. Masui, “Characterization of DNA polymerase X from Thermus thermophilus HB8 reveals the POLXc and PHP domains are both required for 35 exonuclease activity,” Nucleic Acids Research, vol. 37, no. 6, pp. 2037–2052, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Sukhanova, S. Khodyreva, and O. Lavrik, “Poly(ADP-ribose) polymerase 1 regulates activity of DNA polymerase β in long patch base excision repair,” Mutation Research, vol. 685, no. 1-2, pp. 80–89, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. M. J. Cuneo and R. E. London, “Oxidation state of the XRCC1 N-terminal domain regulates DNA polymerase β binding affinity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 15, pp. 6805–6810, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. ZH. K. Nazarkina, S. N. Khodyreva, S. Marsin, J. P. Radicella, and O. I. Lavrik, “Study of interaction of XRCC1 with DNA and proteins of base excision repair by photoaffinity labeling technique,” Biochemistry, vol. 72, no. 8, pp. 878–886, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Sancar, “DNA excision repair,” Annual Review of Biochemistry, vol. 65, pp. 43–81, 1996. View at Google Scholar · View at Scopus
  102. B. Van Houten, “Nucleotide excision repair in Escherichia coli,” Microbiological Reviews, vol. 54, no. 1, pp. 18–51, 1990. View at Google Scholar · View at Scopus
  103. J. J. Truglio, D. L. Croteau, B. van Houten, and C. Kisker, “Prokaryotic nucleotide excision repair: the UvrABC system,” Chemical Reviews, vol. 106, no. 2, pp. 233–252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. C. P. Selby and A. Sancar, “Mechanisms of transcription-repair coupling and mutation frequency decline,” Microbiological Reviews, vol. 58, no. 3, pp. 317–329, 1994. View at Google Scholar · View at Scopus
  105. J. Q. Svejstrup, “Mechanisms of transcription-coupled DNA repair,” Nature Reviews Molecular Cell Biology, vol. 3, no. 1, pp. 21–29, 2002. View at Publisher · View at Google Scholar · View at Scopus
  106. C. P. Selby and A. Sancar, “Molecular mechanism of transcription-repair coupling,” Science, vol. 259, no. 5104, pp. 53–58, 1993. View at Google Scholar · View at Scopus
  107. L. C. J. Gillet and O. D. Schärer, “Molecular mechanisms of mammalian global genome nucleotide excision repair,” Chemical Reviews, vol. 106, no. 2, pp. 253–276, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. D. K. Orren and A. Sancar, “The (A)BC excinuclease of Escherichia coli has only the UvrB and UvrC subunits in the incision complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 14, pp. 5237–5241, 1989. View at Google Scholar · View at Scopus
  109. E. E. A. Verhoeven, C. Wyman, G. F. Moolenaar, and N. Goosen, “The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands,” EMBO Journal, vol. 21, no. 15, pp. 4196–4205, 2002. View at Publisher · View at Google Scholar · View at Scopus
  110. G. F. Moolenaar, M. F. Herron, V. Monaco et al., “The role of ATP binding and hydrolysis by UvrB during nucleotide excision repair,” Journal of Biological Chemistry, vol. 275, no. 11, pp. 8044–8050, 2000. View at Publisher · View at Google Scholar · View at Scopus
  111. P. R. Caron and L. Grossman, “Involvement of a cryptic ATPase activity of UvrB and its proteolysis product, UvrB* in DNA repair,” Nucleic Acids Research, vol. 16, no. 20, pp. 9651–9662, 1988. View at Google Scholar · View at Scopus
  112. R. Kato, N. Yamamoto, K. Kito, and S. Kuramitsu, “ATPase activity of UvrB protein from Thermus thermophilus HB8 and its interaction with DNA,” Journal of Biological Chemistry, vol. 271, no. 16, pp. 9612–9618, 1996. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Yamagata, R. Masui, R. Kato et al., “Interaction of UvrA and UvrB proteins with a fluorescent single-stranded DNA. Implication for slow conformational change upon interaction of UvrB with DNA,” Journal of Biological Chemistry, vol. 275, no. 18, pp. 13235–13242, 2000. View at Publisher · View at Google Scholar · View at Scopus
  114. J.-J. Lin and A. Sancar, “Active site of (A)BC excinuclease. I. Evidence for 5 incision by UvrC through a catalytic site involving Asp399, Asp438, Asp466, and His538 residues,” Journal of Biological Chemistry, vol. 267, no. 25, pp. 17688–17692, 1992. View at Google Scholar · View at Scopus
  115. E. E. A. Verhoeven, M. Van Kesteren, G. F. Moolenaar, R. Visse, and N. Goosen, “Catalytic sites for 3 and 5 incision of Escherichia coli nucleotide excision repair are both located in UvrC,” Journal of Biological Chemistry, vol. 275, no. 7, pp. 5120–5123, 2000. View at Publisher · View at Google Scholar · View at Scopus
  116. T. Ohta, S.-I. Tokishita, R. Imazuka, I. Mori, J. Okamura, and H. Yamagata, “β-Glucosidase as a reporter for the gene expression studies in Thermus thermophilus and constitutive expression of DNA repair genes,” Mutagenesis, vol. 21, no. 4, pp. 255–260, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. R. Collins and T. V. McCarthy, “Purification and characterization of Thermus thermophilus UvrD,” Extremophiles, vol. 7, no. 1, pp. 35–41, 2003. View at Publisher · View at Google Scholar · View at Scopus
  118. V. A. Bohr, C. A. Smith, D. S. Okumoto, and P. C. Hanawalt, “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, vol. 40, no. 2, pp. 359–369, 1985. View at Google Scholar · View at Scopus
  119. C. P. Selby and A. Sancar, “Transcription preferentially inhibits nucleotide excision repair of the template DNA strand in vitro,” Journal of Biological Chemistry, vol. 265, no. 34, pp. 21330–21336, 1990. View at Google Scholar · View at Scopus
  120. C. P. Selby, E. M. Witkin, and A. Sancar, “Escherichia coli mfd mutant deficient in “mutation frequency decline” lacks strand-specific repair: in vitro complementation with purified coupling factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 24, pp. 11574–11578, 1991. View at Google Scholar · View at Scopus
  121. C. P. Selby and A. Sancar, “Structure and function of transcription-repair coupling factor. I. Structural domains and binding properties,” Journal of Biological Chemistry, vol. 270, no. 9, pp. 4882–4889, 1995. View at Publisher · View at Google Scholar · View at Scopus
  122. A. M. Deaconescu, A. L. Chambers, A. J. Smith et al., “Structural basis for bacterial transcription-coupled DNA repair,” Cell, vol. 124, no. 3, pp. 507–520, 2006. View at Publisher · View at Google Scholar · View at Scopus
  123. E. Karakas, J. J. Truglio, D. Croteau et al., “Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad,” EMBO Journal, vol. 26, no. 2, pp. 613–622, 2007. View at Publisher · View at Google Scholar · View at Scopus
  124. M. Machius, L. Henry, M. Palnitkar, and J. Deisenhofer, “Crystal structure of the DNA nucleotide excision repair enzyme UvrB from Thermus thermophilus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 21, pp. 11717–11722, 1999. View at Publisher · View at Google Scholar · View at Scopus
  125. N. Nakagawa, M. Sugahara, R. Masui, R. Kato, K. Fukuyama, and S. Kuramitsu, “Crystal structure of Thermus thermophilus HB8 UvrB protein, a key enzyme of nucleotide excision repair,” Journal of Biochemistry, vol. 126, no. 6, pp. 986–990, 1999. View at Google Scholar · View at Scopus
  126. D. Pakotiprapha, Y. Inuzuka, B. R. Bowman et al., “Crystal Structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding,” Molecular Cell, vol. 29, no. 1, pp. 122–133, 2008. View at Publisher · View at Google Scholar · View at Scopus
  127. K. Theis, P. J. Chen, M. Skorvaga, B. Van Houten, and C. Kisker, “Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair,” EMBO Journal, vol. 18, no. 24, pp. 6899–6907, 1999. View at Google Scholar · View at Scopus
  128. J. J. Truglio, B. Rhau, D. L. Croteau et al., “Structural insights into the first incision reaction during nucleotide excision repair,” EMBO Journal, vol. 24, no. 5, pp. 885–894, 2005. View at Publisher · View at Google Scholar · View at Scopus
  129. J. J. Truglio, E. Karakas, B. Rhau et al., “Structural basis for DNA recognition and processing by UvrB,” Nature Structural and Molecular Biology, vol. 13, no. 4, pp. 360–364, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. N. Nakagawa, R. Masui, R. Kato, and S. Kuramitsu, “Domain structure of Thermus thermophilus UvrB protein. Similarity in domain structure to a helicase,” Journal of Biological Chemistry, vol. 272, no. 36, pp. 22703–22713, 1997. View at Publisher · View at Google Scholar · View at Scopus
  131. M. Hori, C. Ishiguro, T. Suzuki et al., “UvrA and UvrB enhance mutations induced by oxidized deoxyribonucleotides,” DNA Repair, vol. 6, no. 12, pp. 1786–1793, 2007. View at Publisher · View at Google Scholar · View at Scopus
  132. R. M. Schaaper, “Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli,” Journal of Biological Chemistry, vol. 268, no. 32, pp. 23762–23765, 1993. View at Google Scholar · View at Scopus
  133. R. Fishel and R. D. Kolodner, “Identification of mismatch repair genes and their role in the development of cancer,” Current Opinion in Genetics and Development, vol. 5, no. 3, pp. 382–395, 1995. View at Publisher · View at Google Scholar · View at Scopus
  134. R. R. Lyer, A. Pluciennik, V. Burdett, and P. L. Modrich, “DNA mismatch repair: functions and mechanisms,” Chemical Reviews, vol. 106, no. 2, pp. 302–323, 2006. View at Publisher · View at Google Scholar · View at Scopus
  135. P. Modrich, “Methyl-directed DNA mismatch correction,” Journal of Biological Chemistry, vol. 264, no. 12, pp. 6597–6600, 1989. View at Google Scholar · View at Scopus
  136. M. H. Lamers, A. Perrakis, J. H. Enzlin, H. H. K. Winterwerp, N. De Wind, and T. K. Sixma, “The crystal structure of DNA mismatch repair protein MutS binding to a G·T mismatch,” Nature, vol. 407, no. 6805, pp. 711–717, 2000. View at Publisher · View at Google Scholar · View at Scopus
  137. G. Obmolova, C. Ban, P. Hsieh, and W. Yang, “Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA,” Nature, vol. 407, no. 6805, pp. 703–710, 2000. View at Publisher · View at Google Scholar · View at Scopus
  138. S. Takamatsu, R. Kato, and S. Kuramitsu, “Mismatch DNA recognition protein from an extremely thermophilic bacterium, Thermus thermophilus HB8,” Nucleic Acids Research, vol. 24, no. 4, pp. 640–647, 1996. View at Publisher · View at Google Scholar · View at Scopus
  139. C. Ban and W. Yang, “Structural basis for MutH activation in E. coli mismatch repair and relationship of MutH to restriction endonucleases,” EMBO Journal, vol. 17, no. 5, pp. 1526–1534, 1998. View at Publisher · View at Google Scholar · View at Scopus
  140. L. E. Mechanic, B. A. Frankel, and S. W. Matson, “Escherichia coli MutL loads DNA helicase II onto DNA,” Journal of Biological Chemistry, vol. 275, no. 49, pp. 38337–38346, 2000. View at Publisher · View at Google Scholar · View at Scopus
  141. V. Burdett, C. Baitinger, M. Viswanathan, S. T. Lovett, and P. Modrich, “In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 12, pp. 6765–6770, 2001. View at Publisher · View at Google Scholar · View at Scopus
  142. A. Yamagata, Y. Kakuta, R. Masui, and K. Fukuyama, “The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 5908–5912, 2002. View at Publisher · View at Google Scholar · View at Scopus
  143. A. Yamagata, R. Masui, Y. Kakuta, S. Kuramitsu, and K. Fukuyama, “Overexpression, purification and characterization of RecJ protein from Thermus thermophilus HB8 and its core domain,” Nucleic Acids Research, vol. 29, no. 22, pp. 4617–4624, 2001. View at Google Scholar · View at Scopus
  144. W.-H. Fang and P. Modrich, “Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction,” Journal of Biological Chemistry, vol. 268, no. 16, pp. 11838–11844, 1993. View at Google Scholar · View at Scopus
  145. L. Dzantiev, N. Constantin, J. Genschel, R. R. Iyer, P. M. Burgers, and P. Modrich, “A defined human system that supports bidirectional mismatch-provoked excision,” Molecular Cell, vol. 15, no. 1, pp. 31–41, 2004. View at Publisher · View at Google Scholar · View at Scopus
  146. N. Constantin, L. Dzantiev, F. A. Kadyrov, and P. Modrich, “Human mismatch repair: reconstitution of a nick-directed bidirectional reaction,” Journal of Biological Chemistry, vol. 280, no. 48, pp. 39752–39761, 2005. View at Publisher · View at Google Scholar · View at Scopus
  147. P. Modrich, “Mechanisms in eukaryotic mismatch repair,” Journal of Biological Chemistry, vol. 281, no. 41, pp. 30305–30309, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. J. Genschel, L. R. Bazemore, and P. Modrich, “Human exonuclease I is required for 5 and 3 mismatch repair,” Journal of Biological Chemistry, vol. 277, no. 15, pp. 13302–13311, 2002. View at Publisher · View at Google Scholar · View at Scopus
  149. K. Wei, A. B. Clark, E. Wong et al., “Inactivation of exonuclease I in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility,” Genes and Development, vol. 17, no. 5, pp. 603–614, 2003. View at Publisher · View at Google Scholar · View at Scopus
  150. F. A. Kadyrov, L. Dzantiev, N. Constantin, and P. Modrich, “Endonucleolytic function of MutLα in human mismatch repair,” Cell, vol. 126, no. 2, pp. 297–308, 2006. View at Google Scholar
  151. F. A. Kadyrov, S. F. Holmes, M. E. Arana et al., “Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease,” Journal of Biological Chemistry, vol. 282, no. 51, pp. 37181–37190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. K. Fukui, M. Nishida, N. Nakagawa, R. Masui, and S. Kuramitsu, “Bound nucleotide controls the endonuclease activity of mismatch repair enzyme MutL,” Journal of Biological Chemistry, vol. 283, no. 18, pp. 12136–12145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  153. V. Duppatla, C. Bodda, C. Urbanke, P. Friedhoff, and D. N. Rao, “The C-terminal domain is sufficient for endonuclease activity of Neisseria gonorrhoeae MutL,” Biochemical Journal, vol. 423, no. 2, pp. 265–277, 2009. View at Publisher · View at Google Scholar · View at Scopus
  154. J. Mauris and T. C. Evans Jr., “Adenosine triphosphate stimulates Aquifex aeolicus MutL endonuclease activity,” PLoS ONE, vol. 4, no. 9, article no. e7175, 2009. View at Publisher · View at Google Scholar · View at Scopus
  155. H. Tachiki, R. Kato, and S. Kuramitsu, “DNA binding and protein-protein interaction sites in MutS, a mismatched DNA recognition protein from Thermus thermophilus HB8,” Journal of Biological Chemistry, vol. 275, no. 52, pp. 40703–40709, 2000. View at Publisher · View at Google Scholar · View at Scopus
  156. R. Kato, M. Kataoka, H. Kamikubo, and S. Kuramitsu, “Direct observation of three conformations of MutS protein regulated by adenine nucleotides,” Journal of Molecular Biology, vol. 309, no. 1, pp. 227–238, 2001. View at Publisher · View at Google Scholar · View at Scopus
  157. S. Acharya, P. L. Foster, P. Brooks, and R. Fishel, “The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair,” Molecular Cell, vol. 12, no. 1, pp. 233–246, 2003. View at Publisher · View at Google Scholar · View at Scopus
  158. M. L. Mendillo, C. D. Putnam, A. O. Mo et al., “Probing DNA- and ATP-mediated conformational changes in the MutS family of mispair recognition proteins using deuterium exchange mass spectrometry,” Journal of Biological Chemistry, vol. 285, no. 17, pp. 13170–13182, 2010. View at Publisher · View at Google Scholar · View at Scopus
  159. L. J. Blackwell, D. Martik, K. P. Bjornson, E. S. Bjornson, and P. Modrich, “Nucleotide-promoted release of hMutSa from heteroduplex DNA is consistent with an ATP-dependent translocation mechanism,” The Journal of Biological Chemistry, vol. 273, no. 48, pp. 32055–32062, 1998. View at Google Scholar
  160. L. J. Blackwell, K. P. Bjornson, D. J. Allen, and P. Modrich, “Distinct MutS DNA-binding modes that are differentially modulated by ATP binding and hydrolysis,” Journal of Biological Chemistry, vol. 276, no. 36, pp. 34339–34347, 2001. View at Publisher · View at Google Scholar · View at Scopus
  161. G. Natrajan, M. H. Lamers, J. H. Enzlin, H. H. K. Winterwerp, A. Perrakis, and T. K. Sixma, “Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates,” Nucleic Acids Research, vol. 31, no. 16, pp. 4814–4821, 2003. View at Publisher · View at Google Scholar · View at Scopus
  162. J. J. Warren, T. J. Pohlhaus, A. Changela et al., “Structure of the human MutSa DNA lesion recognition complex,” Molecular Cell, vol. 26, no. 4, pp. 579–592, 2007. View at Google Scholar
  163. R. Dutta and M. Inouye, “GHKL, an emergent ATPase/kinase superfamily,” Trends in Biochemical Sciences, vol. 25, no. 1, pp. 24–28, 2000. View at Publisher · View at Google Scholar · View at Scopus
  164. C. Ban, M. Junop, and W. Yang, “Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair,” Cell, vol. 97, no. 1, pp. 85–97, 1999. View at Google Scholar · View at Scopus
  165. E. J. Sacho, F. A. Kadyrov, P. Modrich, T. A. Kunkel, and D. A. Erie, “Direct visualization of asymmetric adenine nucleotide-induced conformational changes in MutLα,” Molecular Cell, vol. 29, no. 1, pp. 112–121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  166. G.-L. Moldovan, B. Pfander, and S. Jentsch, “PCNA, the maestro of the replication fork,” Cell, vol. 129, no. 4, pp. 665–679, 2007. View at Publisher · View at Google Scholar · View at Scopus
  167. S. S. Shell, C. D. Putnam, and R. D. Kolodner, “The N terminus of Saccharomyces cerevisiae Msh6 is an unstructured tether to PCNA,” Molecular Cell, vol. 26, no. 4, pp. 565–578, 2007. View at Publisher · View at Google Scholar · View at Scopus
  168. T. A. Kunkel and D. A. Erie, “DNA mismatch repair,” Annual Review of Biochemistry, vol. 74, pp. 681–710, 2005. View at Publisher · View at Google Scholar · View at Scopus
  169. P. J. Masih, D. Kunnev, and T. Melendy, “Mismatch repair proteins are recruited to replicating DNA through interaction with Proliferating Cell Nuclear Antigen (PCNA),” Nucleic Acids Research, vol. 36, no. 1, pp. 67–75, 2008. View at Publisher · View at Google Scholar · View at Scopus
  170. R. R. Iyer, T. J. Pohlhaus, S. Chen et al., “The MutSα-proliferating cell nuclear antigen interaction in human DNA mismatch repair,” Journal of Biological Chemistry, vol. 283, no. 19, pp. 13310–13319, 2008. View at Publisher · View at Google Scholar · View at Scopus
  171. L. A. Simmons, B. W. Davies, A. D. Grossman, and G. C. Walker, “β clamp directs localization of mismatch repair in Bacillus subtilis,” Molecular Cell, vol. 29, no. 3, pp. 291–301, 2008. View at Publisher · View at Google Scholar · View at Scopus
  172. J. Genschel and P. Modrich, “Analysis of the excision step in human DNA mismatch repair,” Methods in Enzymology, vol. 408, pp. 273–284, 2006. View at Publisher · View at Google Scholar · View at Scopus
  173. J. Genschel and P. Modrich, “Mechanism of 5-directed excision in human mismatch repair,” Molecular Cell, vol. 12, no. 5, pp. 1077–1086, 2003. View at Publisher · View at Google Scholar · View at Scopus
  174. J. Mauris and T. C. Evans Jr., “A human PMS2 homologue from Aquifex aeolicus stimulates an ATP-dependent DNA helicase,” Journal of Biological Chemistry, vol. 285, no. 15, pp. 11087–11092, 2010. View at Publisher · View at Google Scholar · View at Scopus
  175. A. Shimada, R. Masui, N. Nakagawa et al., “A novel single-stranded DNA-specific 35 exonuclease, Thermus thermophilus exonuclease I, is involved in several DNA repair pathways,” Nucleic Acids Research, vol. 38, no. 17, pp. 5792–5705, 2010. View at Google Scholar
  176. T. Wakamatsu, Y. Kitamura, Y. Kotera, N. Nakagawa, S. Kuramitsu, and R. Masui, “Structure of RecJ exonuclease defines its specificity for single-stranded DNA,” Journal of Biological Chemistry, vol. 285, no. 13, pp. 9762–9769, 2010. View at Publisher · View at Google Scholar · View at Scopus
  177. W. Yang, “An equivalent metal ion in one- and two-metal-ion catalysis,” Nature Structural and Molecular Biology, vol. 15, no. 11, pp. 1228–1231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  178. M. Shrivastav, L. P. De Haro, and J. A. Nickoloff, “Regulation of DNA double-strand break repair pathway choice,” Cell Research, vol. 18, no. 1, pp. 134–147, 2008. View at Publisher · View at Google Scholar · View at Scopus
  179. M. E. Moynahan and M. Jasin, “Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis,” Nature Reviews Molecular Cell Biology, vol. 11, no. 3, pp. 196–207, 2010. View at Publisher · View at Google Scholar · View at Scopus
  180. T. Helleday, J. Lo, D. C. van Gent, and B. P. Engelward, “DNA double-strand break repair: from mechanistic understanding to cancer treatment,” DNA Repair, vol. 6, no. 7, pp. 923–935, 2007. View at Publisher · View at Google Scholar · View at Scopus
  181. L. H. Thompson and D. Schild, “Recombinational DNA repair and human disease,” Mutation Research, vol. 509, no. 1-2, pp. 49–78, 2002. View at Publisher · View at Google Scholar · View at Scopus
  182. A. Nowosielska, “Bacterial DNA repair genes and their eukaryotic homologues: 5. The role of recombination in DNA repair and genome stability,” Acta Biochimica Polonica, vol. 54, no. 3, pp. 483–494, 2007. View at Google Scholar · View at Scopus
  183. E. P. C. Rocha, E. Cornet, and B. Michel, “Comparative and evolutionary analysis of the bacterial homologous recombination systems,” PLoS Genetics, vol. 1, no. 2, article no. e15, pp. 0247–0259, 2005. View at Publisher · View at Google Scholar · View at Scopus
  184. G. A. Cromie, J. C. Connelly, and D. R. F. Leach, “Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans,” Molecular Cell, vol. 8, no. 6, pp. 1163–1174, 2001. View at Publisher · View at Google Scholar · View at Scopus
  185. M. Sasaki, J. Lange, and S. Keeney, “Genome destabilization by homologous recombination in the germ line,” Nature Reviews Molecular Cell Biology, vol. 11, no. 3, pp. 182–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  186. C. M. Thomas and K. M. Nielsen, “Mechanisms of, and barriers to, horizontal gene transfer between bacteria,” Nature Reviews Microbiology, vol. 3, no. 9, pp. 711–721, 2005. View at Publisher · View at Google Scholar · View at Scopus
  187. G.-M. Li, “Mechanisms and functions of DNA mismatch repair,” Cell Research, vol. 18, no. 1, pp. 85–98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  188. P. Sung and H. Klein, “Mechanism of homologous recombination: mediators and helicases take on regulatory functions,” Nature Reviews Molecular Cell Biology, vol. 7, no. 10, pp. 739–750, 2006. View at Publisher · View at Google Scholar · View at Scopus
  189. P. Huertas, “DNA resection in eukaryotes: deciding how to fix the break,” Nature Structural and Molecular Biology, vol. 17, no. 1, pp. 11–16, 2010. View at Publisher · View at Google Scholar · View at Scopus
  190. N. Handa, K. Morimatsu, S. T. Lovett, and S. C. Kowalczykowski, “Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli,” Genes and Development, vol. 23, no. 10, pp. 1234–1245, 2009. View at Publisher · View at Google Scholar · View at Scopus
  191. J. T.P. Yeeles and M. S. Dillingham, “The processing of double-stranded DNA breaks for recombinational repair by helicase-nuclease complexes,” DNA Repair, vol. 9, no. 3, pp. 276–285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  192. R. D. Shereda, D. A. Bernstein, and J. L. Keck, “A central role for SSB in Escherichia coli RecQ DNA helicase function,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 19247–19258, 2007. View at Publisher · View at Google Scholar · View at Scopus
  193. H. Brüggemann and C. Chen, “Comparative genomics of Thermus thermophilus: plasticity of the megaplasmid and its contribution to a thermophilic lifestyle,” Journal of Biotechnology, vol. 124, no. 4, pp. 654–661, 2006. View at Publisher · View at Google Scholar · View at Scopus
  194. R. Sharma and D. N. Rao, “Orchestration of Haemophilus influenzae RecJ exonuclease by interaction with single-stranded DNA-binding protein,” Journal of Molecular Biology, vol. 385, no. 5, pp. 1375–1396, 2009. View at Publisher · View at Google Scholar · View at Scopus
  195. K. Morimatsu and S. C. Kowalczykowski, “RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair,” Molecular Cell, vol. 11, no. 5, pp. 1337–1347, 2003. View at Publisher · View at Google Scholar · View at Scopus
  196. M. Honda, T. Fujisawa, T. Shibata, and T. Mikawa, “RecR forms a ring-like tetramer that encircles dsDNA by forming a complex with RecF,” Nucleic Acids Research, vol. 36, no. 15, pp. 5013–5020, 2008. View at Publisher · View at Google Scholar · View at Scopus
  197. M. Honda, J. Inoue, M. Yoshimasu, Y. Ito, T. Shibata, and T. Mikawa, “Identification of the RecR Toprim domain as the binding site for both recF and recO: A role of recR in recFOR assembly at double-stranded DNA-single-stranded DNA junctions,” Journal of Biological Chemistry, vol. 281, no. 27, pp. 18549–18559, 2006. View at Publisher · View at Google Scholar · View at Scopus
  198. J. Inoue, M. Honda, S. Ikawa, T. Shibata, and T. Mikawa, “The process of displacing the single-stranded DNA-binding protein from single-stranded DNA by RecO and RecR proteins,” Nucleic Acids Research, vol. 36, no. 1, pp. 94–109, 2008. View at Publisher · View at Google Scholar · View at Scopus
  199. A. Carreira and S. C. Kowalczykowski, “BRCA2: shining light on the regulation of DNA-binding selectivity by RAD51,” Cell Cycle, vol. 8, no. 21, pp. 3445–3447, 2009. View at Google Scholar · View at Scopus
  200. S. L. Gasior, H. Olivares, U. Ear, D. M. Hari, R. Weichselbaum, and D. K. Bishop, “Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8411–8418, 2001. View at Publisher · View at Google Scholar · View at Scopus
  201. A. V. Mazin, O. M. Mazina, D. V. Bugreev, and M. J. Rossi, “Rad54, the motor of homologous recombination,” DNA Repair, vol. 9, no. 3, pp. 286–302, 2010. View at Publisher · View at Google Scholar · View at Scopus
  202. M. J. McIlwraith, E. Van Dyck, J.-Y. Masson, A. Z. Stasiak, A. Stasiak, and S. C. West, “Reconstitution of the strand invasion step of double-strand break repair using human Rad51 Rad52 and RPA proteins,” Journal of Molecular Biology, vol. 304, no. 2, pp. 151–164, 2000. View at Publisher · View at Google Scholar · View at Scopus
  203. Z. Lin, H. Kong, M. Nei, and H. Ma, “Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 27, pp. 10328–10333, 2006. View at Publisher · View at Google Scholar · View at Scopus
  204. D. A. McGrew and K. L. Knight, “Molecular design and functional organization of the RecA protein,” Critical Reviews in Biochemistry and Molecular Biology, vol. 38, no. 5, pp. 385–432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  205. M. M. Cox, “Motoring along with the bacterial RecA protein,” Nature Reviews Molecular Cell Biology, vol. 8, no. 2, pp. 127–138, 2007. View at Publisher · View at Google Scholar · View at Scopus
  206. J. San Filippo, P. Sung, and H. Klein, “Mechanism of eukaryotic homologous recombination,” Annual Review of Biochemistry, vol. 77, pp. 229–257, 2008. View at Publisher · View at Google Scholar · View at Scopus
  207. R. M. Story, I. T. Weber, and T. A. Steitz, “The structure of the E. coli recA protein monomer and polymer,” Nature, vol. 355, no. 6358, pp. 318–325, 1992. View at Publisher · View at Google Scholar · View at Scopus
  208. Z. Chen, H. Yang, and N. P. Pavletich, “Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures,” Nature, vol. 453, no. 7194, pp. 489–494, 2008. View at Publisher · View at Google Scholar · View at Scopus
  209. T. Nishinaka, Y. Ito, S. Yokoyama, and T. Shibata, “An extended DNA structure through deoxyribose-base stacking induced by RecA protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 13, pp. 6623–6628, 1997. View at Publisher · View at Google Scholar · View at Scopus
  210. M. D. Sutton and G. C. Walker, “Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8342–8349, 2001. View at Publisher · View at Google Scholar · View at Scopus
  211. T. Kawamoto, K. Araki, E. Sonoda et al., “Dual roles for DNA polymerase η in homologous DNA recombination and translesion DNA synthesis,” Molecular Cell, vol. 20, no. 5, pp. 793–799, 2005. View at Publisher · View at Google Scholar · View at Scopus
  212. X. Li, C. M. Stith, P. M. Burgers, and W.-D. Heyer, “PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase δ,” Molecular Cell, vol. 36, no. 4, pp. 704–713, 2009. View at Publisher · View at Google Scholar · View at Scopus
  213. M. J. McIlwraith and S. C. West, “DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair,” Molecular Cell, vol. 29, no. 4, pp. 510–516, 2008. View at Publisher · View at Google Scholar · View at Scopus
  214. M. J. McIlwraith, A. Vaisman, Y. Liu et al., “Human DNA polymerase η promotes DNA synthesis from strand invasion intermediates of homologous recombination,” Molecular Cell, vol. 20, no. 5, pp. 783–792, 2005. View at Google Scholar
  215. G.-L. Moldovan, M. V. Madhavan, K. D. Mirchandani, R. M. McCaffrey, P. Vinciguerra, and A. D. D'Andrea, “DNA polymerase POLN participates in cross-link repair and homologous recombination,” Molecular and Cellular Biology, vol. 30, no. 4, pp. 1088–1096, 2010. View at Publisher · View at Google Scholar · View at Scopus
  216. S. Delmas and I. Matic, “Interplay between replication and recombination in Escherichia coli: impact of the alternative DNA polymerases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 12, pp. 4564–4569, 2006. View at Publisher · View at Google Scholar · View at Scopus
  217. A. Henne, H. Brüggemann, C. Raasch et al., “The genome sequence of the extreme thermophile Thermus thermophilus,” Nature Biotechnology, vol. 22, no. 5, pp. 547–553, 2004. View at Publisher · View at Google Scholar · View at Scopus
  218. O. White, J. A. Eisen, J. F. Heidelberg et al., “Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1,” Science, vol. 286, no. 5444, pp. 1571–1577, 1999. View at Publisher · View at Google Scholar · View at Scopus
  219. D. Slade, A. B. Lindner, G. Paul, and M. Radman, “Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans,” Cell, vol. 136, no. 6, pp. 1044–1055, 2009. View at Publisher · View at Google Scholar · View at Scopus
  220. N. Kantake, M. V. V. M. Madiraju, T. Sugiyama, and S. C. Kowalczykowski, “Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15327–15332, 2002. View at Publisher · View at Google Scholar · View at Scopus
  221. T. Sugiyama, N. Kantake, Y. Wu, and S. C. Kowalczykowski, “Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture,” EMBO Journal, vol. 25, no. 23, pp. 5539–5548, 2006. View at Publisher · View at Google Scholar · View at Scopus
  222. A. V. Nimonkar, R. A. Sica, and S. C. Kowalczykowski, “Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 9, pp. 3077–3082, 2009. View at Publisher · View at Google Scholar · View at Scopus
  223. J. M. Martínez-Salazar, J. Zuñiga-Castillo, and D. Romero, “Differential roles of proteins involved in migration of Holliday junctions on recombination and tolerance to DNA damaging agents in Rhizobium etli,” Gene, vol. 432, no. 1-2, pp. 26–32, 2009. View at Publisher · View at Google Scholar · View at Scopus
  224. K. Yamada, M. Ariyoshi, and K. Morikawa, “Three-dimensional structural views of branch migration and resolution in DNA homologous recombination,” Current Opinion in Structural Biology, vol. 14, no. 2, pp. 130–137, 2004. View at Publisher · View at Google Scholar · View at Scopus
  225. C. J. Rudolph, A. L. Upton, G. S. Briggs, and R. G. Lloyd, “Is RecG a general guardian of the bacterial genome?” DNA Repair, vol. 9, no. 3, pp. 210–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  226. C. E. Beam, C. J. Saveson, and S. T. Lovett, “Role for radA/sms in recombination intermediate processing in Escherichia coli,” Journal of Bacteriology, vol. 184, no. 24, pp. 6836–6844, 2002. View at Publisher · View at Google Scholar · View at Scopus
  227. M. Ariyoshi, T. Nishino, H. Iwasaki, H. Shinagawa, and K. Morikawa, “Crystal structure of the holliday junction DNA in complex with a single RuvA tetramer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 15, pp. 8257–8262, 2000. View at Publisher · View at Google Scholar · View at Scopus
  228. Y. Fujiwara, K. Mayanagi, and K. Morikawa, “Functional significance of octameric RuvA for a branch migration complex from Thermus thermophilus,” Biochemical and Biophysical Research Communications, vol. 366, no. 2, pp. 426–431, 2008. View at Publisher · View at Google Scholar · View at Scopus
  229. K. Yamada, T. Miyata, D. Tsuchiya et al., “Crystal structure of the RuvA-RuvB complex: a structural basis for the holliday junction migrating motor machinery,” Molecular Cell, vol. 10, no. 3, pp. 671–681, 2002. View at Publisher · View at Google Scholar · View at Scopus
  230. K. Yamada, N. Kunishima, K. Mayanagi et al., “Crystal structure of the Holliday junction migration motor protein RuvB from Thermus thermophilus HB8,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 4, pp. 1442–1447, 2001. View at Publisher · View at Google Scholar · View at Scopus
  231. T. Ohnishi, T. Hishida, Y. Harada, H. Iwasaki, and H. Shinagawa, “Structure-function analysis of the three domains of RuvB DNA motor protein,” Journal of Biological Chemistry, vol. 280, no. 34, pp. 30504–30510, 2005. View at Publisher · View at Google Scholar · View at Scopus
  232. T. Ohnishi, H. Iwasaki, Y. Ishino, S. Kuramitsu, A. Nakata, and H. Shinagawa, “Identification and characterization of Thermus thermophilus HB8 RuvA protein, the subunit of the RuvAB protein complex that promotes branch migration of Holliday junctions,” Genes and Genetic Systems, vol. 75, no. 5, pp. 233–243, 2000. View at Publisher · View at Google Scholar · View at Scopus
  233. K. Mayanagi, Y. Fujiwara, T. Miyata, and K. Morikawa, “Electron microscopic single particle analysis of a tetrameric RuvA/RuvB/Holliday junction DNA complex,” Biochemical and Biophysical Research Communications, vol. 365, no. 2, pp. 273–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  234. M. Ariyoshi, D. G. Vassylyev, H. Iwasaki, H. Nakamura, H. Shinagawa, and K. Morikawa, “Atomic structure of the RuvC resolvase: a Holliday junction-specific endonuclease from E. coli,” Cell, vol. 78, no. 6, pp. 1063–1072, 1994. View at Publisher · View at Google Scholar · View at Scopus
  235. A. K. Eggleston and S. C. West, “Cleavage of holliday junctions by the Escherichia coli RuvABC complex,” Journal of Biological Chemistry, vol. 275, no. 34, pp. 26467–26476, 2000. View at Publisher · View at Google Scholar · View at Scopus
  236. A. J. Van Gool, N. M. A. Hajibagheri, A. Stasiak, and S. C. West, “Assembly of the Escherichia coli RuvABC resolvasome directs the orientation of Holliday junction resolution,” Genes and Development, vol. 13, no. 14, pp. 1861–1870, 1999. View at Google Scholar · View at Scopus
  237. D. Zerbib, C. Mézard, H. George, and S. C. West, “Coordinated actions of RuvABC in Holliday junction processing,” Journal of Molecular Biology, vol. 281, no. 4, pp. 621–630, 1998. View at Publisher · View at Google Scholar · View at Scopus
  238. J. M. Svendsen and J. W. Harper, “GEN1/Yen1 and the SLX4 complex: solutions to the problem of Holliday junction resolution,” Genes and Development, vol. 24, no. 6, pp. 521–536, 2010. View at Publisher · View at Google Scholar · View at Scopus
  239. S. L. Andersen, D. T. Bergstralh, K. P. Kohl, J. R. LaRocque, C. B. Moore, and J. Sekelsky, “Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination,” Molecular Cell, vol. 35, no. 1, pp. 128–135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  240. S. Fekairi, S. Scaglione, C. Chahwan et al., “Human SLX4 is a holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases,” Cell, vol. 138, no. 1, pp. 78–89, 2009. View at Publisher · View at Google Scholar · View at Scopus
  241. I. M. Muñoz, K. Hain, A.-C. Déclais et al., “Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair,” Molecular Cell, vol. 35, no. 1, pp. 116–127, 2009. View at Publisher · View at Google Scholar · View at Scopus
  242. T. T. Saito, J. L. Youds, S. J. Boulton, and M. P. Colaiácovo, “Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates,” PLoS Genetics, vol. 5, no. 11, article no. e1000735, 2009. View at Google Scholar
  243. J. M. Svendsen, A. Smogorzewska, M. E. Sowa et al., “Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair,” Cell, vol. 138, no. 1, pp. 63–77, 2009. View at Publisher · View at Google Scholar · View at Scopus
  244. H. Iwasaki, M. Takahagi, T. Shiba, A. Nakata, and H. Shinagawa, “Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure,” EMBO Journal, vol. 10, no. 13, pp. 4381–4389, 1991. View at Google Scholar · View at Scopus
  245. E. L. Bolt and R. G. Lloyd, “Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo,” Molecular Cell, vol. 10, no. 1, pp. 187–198, 2002. View at Publisher · View at Google Scholar · View at Scopus
  246. S. N. Chan, L. Harris, E. L. Bolt, M. C. Whitby, and R. G. Lloyd, “Sequence specificity and biochemical characterization of the RusA Holliday junction resolvase of Escherichia coli,” Journal of Biological Chemistry, vol. 272, no. 23, pp. 14873–14882, 1997. View at Publisher · View at Google Scholar · View at Scopus
  247. C. R. Lopez, S. Yang, R. W. Deibler et al., “A role for topoisomerase III in a recombination pathway alternative to RuvABC,” Molecular Microbiology, vol. 58, no. 1, pp. 80–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  248. D. Sheng, R. Liu, Z. Xu, P. Singh, B. Shen, and Y. Hua, “Dual negative regulatory mechanisms of RecX on RecA functions in radiation resistance, DNA recombination and consequent genome instability in Deinococcus radiodurans,” DNA Repair, vol. 4, no. 6, pp. 671–678, 2005. View at Publisher · View at Google Scholar · View at Scopus
  249. K. Jimbo, J. Inoue, T. Masuda, T. Shibata, and T. Mikawa, “Purification and characterization of the Thermus thermophilus HB8 RecX protein,” Protein Expression and Purification, vol. 51, no. 2, pp. 320–323, 2007. View at Publisher · View at Google Scholar · View at Scopus
  250. S. Ragone, J. D. Maman, N. Furnham, and L. Pellegrini, “Structural basis for inhibition of homologous recombination by the RecX protein,” EMBO Journal, vol. 27, no. 16, pp. 2259–2269, 2008. View at Publisher · View at Google Scholar · View at Scopus
  251. R. Lestini and B. Michel, “UvrD controls the access of recombination proteins to blocked replication forks,” EMBO Journal, vol. 26, no. 16, pp. 3804–3814, 2007. View at Publisher · View at Google Scholar · View at Scopus
  252. X. Veaute, S. Delmas, M. Selva et al., “UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli,” EMBO Journal, vol. 24, no. 1, pp. 180–189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  253. K. Fukui, N. Nakagawa, Y. Kitamura, Y. Nishida, R. Masui, and S. Kuramitsu, “Crystal structure of Muts2 endonuclease domain and the mechanism of homologous recombination suppression,” Journal of Biological Chemistry, vol. 283, no. 48, pp. 33417–33427, 2008. View at Publisher · View at Google Scholar · View at Scopus
  254. A. V. Pinto, A. Mathieu, S. Marsin et al., “Suppression of homologous and homeologous recombination by the bacterial MutS2 protein,” Molecular Cell, vol. 17, no. 1, pp. 113–120, 2005. View at Publisher · View at Google Scholar · View at Scopus
  255. K. Fukui, Y. Takahata, N. Nakagawa, S. Kuramitsu, and R. Masui, “Analysis of a nuclease activity of catalytic domain of Thermus thermophilus MutS2 by high-accuracy mass spectrometry,” Nucleic Acids Research, vol. 35, no. 15, article no. e100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  256. K. Fukui, H. Kosaka, S. Kuramitsu, and R. Masui, “Nuclease activity of the MutS homologue MutS2 from Thermus thermophilus is confined to the Smr domain,” Nucleic Acids Research, vol. 35, no. 3, pp. 850–860, 2007. View at Publisher · View at Google Scholar · View at Scopus
  257. K. Fukui, R. Masui, and S. Kuramitsu, “Thermus thermophilus MutS2, a MutS paralogue, possesses an endonuclease activity promoted by MutL,” Journal of Biochemistry, vol. 135, no. 3, pp. 375–384, 2004. View at Publisher · View at Google Scholar · View at Scopus