Intrinsic properties of the two replicative DNA polymerases of pyrococcus abyssi in replicating abasic sites: Possible role in DNA damage tolerance?

Molecular Microbiology

Volumn 70, Issue 3, 2008, Pages 746-761

  Palud, Adeline ^a,b   Villani, Giuseppe ^c   L'Haridon, Stéphane ^b   Querellou, Joël ^a,b   Raffin, Jean Paul ^a,b   Henneke, Ghislaine ^a,b  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; NUCLEOTIDE; OLIGONUCLEOTIDE;

ARTICLE; DNA DAMAGE; DNA SYNTHESIS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PYROCOCCUS ABYSSI; STEADY STATE;

ESCHERICHIA COLI; PYROCOCCUS ABYSSI;

EID: 53849113965     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06446.x     Document Type: Article

References (70)

1. Barry, E.R. Bell, S.D. (2006) DNA replication in the archaea. Microbiol Mol Biol Rev 70 : 876 887.
2. Baynton, K. Fuchs, R.P. (2000) Lesions in DNA: hurdles for polymerases. Trends Biochem Sci 25 : 74 79.
3. Bebenek, K. Kunkel, T.A. (2004) Functions of DNA polymerases. Adv Protein Chem 69 : 137 165.
4. Bernander, R. Poplawski, A. (1997) Cell cycle characteristics of thermophilic archaea. J Bacteriol 179 : 4963 4969.
5. Blanca, G., Delagoutte, E., Tanguy le Gac, N., Johnson, N.P., Baldacci, G. Villani, G. (2007) Accessory proteins assist exonuclease-deficient bacteriophage T4 DNA polymerase in replicating past an abasic site. Biochem J 402 : 321 329.
6. Bloom, L.B., Chen, X., Fygenson, D.K., Turner, J., O'Donnell, M. Goodman, M.F. (1997) Fidelity of Escherichia coli DNA polymerase III holoenzyme. The effects of beta, gamma complex processivity proteins and epsilon proofreading exonuclease on nucleotide misincorporation efficiencies. J Biol Chem 272 : 27919 27930.
7. Boudsocq, F., Iwai, S., Hanaoka, F. Woodgate, R. (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta. Nucleic Acids Res 29 : 4607 4616.
8. Breen, A.P. Murphy, J.A. (1995) Reactions of oxyl radicals with DNA. Free Radic Biol Med 18 : 1033 1077.
9. Breuert, S., Allers, T., Spohn, G. Soppa, J. (2006) Regulated polyploidy in halophilic archaea. PLoS ONE 1 : e92.
10. Cadet, J., Delatour, T., Douki, T., Gasparutto, D., Pouget, J.P., Ravanat, J.L. Sauvaigo, S. (1999) Hydroxyl radicals and DNA base damage. Mutat Res 424 : 9 21.
11. Charbonnier, F., Forterre, P., Erauso, G. Prieur, D. (1995) Purification of plasmids from thermophilic and hyperthermophilic archaea. In Archaea: A Laboratory Manual. Robb, F.T. Place, A.R. (eds). Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press, pp. 87 90.
12. Chen, X., Zuo, S., Kelman, Z., O'Donnell, M., Hurwitz, J. Goodman, M.F. (2000) Fidelity of eucaryotic DNA polymerase delta holoenzyme from Schizosaccharomyces pombe. J Biol Chem 275 : 17677 17682.
13. Cohen, G.N., Barbe, V., Flament, D., Galperin, M., Heilig, R., Lecompte, O., et al. (2003) An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol Microbiol 47 : 1495 1512.
14. Courcelle, J., Donaldson, J.R., Chow, K.H. Courcelle, C.T. (2003) DNA damage-induced replication fork regression and processing in Escherichia coli. Science 299 : 1064 1067.
15. Erauso, G., Reysenbach, A.L., Godfroy, A., Meunier, J.R., Crump, B., Partensky, F., et al. (1993) Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Arch Microbiology 160 : 338 349.
16. Freisinger, E., Grollman, A.P., Miller, H. Kisker, C. (2004) Lesion (in)tolerance reveals insights into DNA replication fidelity. EMBO J 23 : 1494 1505.
17. Friedberg, E.C. (2005) Suffering in silence: the tolerance of DNA damage. Nat Rev Mol Cell Biol 6 : 943 953.
18. Friedberg, E.C., Feaver, W.J. Gerlach, V.L. (2000) The many faces of DNA polymerases: strategies for mutagenesis and for mutational avoidance. Proc Natl Acad Sci USA 97 : 5681 5683.
19. Friedberg, E.C., Lehmann, A.R. Fuchs, R.P. (2005) Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol Cell 18 : 499 505.
20. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A. Ellenberger, T. (2006) Biological responses to DNA damage. In DNA Repair and Mutagenesis. Washington, D.C. : ASM Press, pp. 3 7.
21. Grogan, D.W. (1998) Hyperthermophiles and the problem of DNA instability. Mol Microbiol 28 : 1043 1049.
22. Grogan, D.W. (2000) The question of DNA repair in hyperthermophilic archaea. Trends Microbiol 8 : 180 185.
23. Grogan, D.W. (2004) Stability and repair of DNA in hyperthermophilic archaea. Curr Issues Mol Biol 6 : 137 144.
24. Grogan, D.W., Carver, G.T. Drake, J.W. (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci USA 98 : 7928 7933.
25. Gruz, P., Shimizu, M., Pisani, F.M., De Felice, M., Kanke, Y. Nohmi, T. (2003) Processing of DNA lesions by archaeal DNA polymerases from Sulfolobus solfataricus. Nucleic Acids Res 31 : 4024 4030.
26. Gueguen, Y., Rolland, J.L., Lecompte, O., Azam, P., Le Romancer, G., Flament, D., et al. (2001) Characterization of two DNA polymerases from the hyperthermophilic euryarchaeon Pyrococcus abyssi. Eur J Biochem 268 : 5961 5969.
27. Haracska, L., Unk, I., Johnson, R.E., Johansson, E., Burgers, P.M., Prakash, S. Prakash, L. (2001) Roles of yeast DNA polymerases delta and zeta and of Rev1 in the bypass of abasic sites. Genes Dev 15 : 945 954.
28. Henneke, G., Flament, D., Hubscher, U., Querellou, J. Raffin, J.P. (2005) The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J Mol Biol 350 : 53 64.
29. Hoeijmakers, J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature 411 : 366 374.
30. Hogg, M., Wallace, S.S. Doublie, S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site. EMBO J 23 : 1483 1493.
31. Hubscher, U., Maga, G. Spadari, S. (2002) Eukaryotic DNA polymerases. Annu Rev Biochem 71 : 133 163.
32. Jacobs, K.L. Grogan, D.W. (1997) Rates of spontaneous mutation in an archaeon from geothermal environments. J Bacteriol 179 : 3298 3303.
33. Jin, Y.H., Ayyagari, R., Resnick, M.A., Gordenin, D.A. Burgers, P.M. (2003) Okazaki fragment maturation in yeast. II. Cooperation between the polymerase and 3′-5′-exonuclease activities of Pol delta in the creation of a ligatable nick. J Biol Chem 278 : 1626 1633.
34. Jin, Y.H., Garg, P., Stith, C.M., Al-Refai, H., Sterling, J.F., Murray, L.J., et al. (2005) The multiple biological roles of the 3′ ->5′ exonuclease of Saccharomyces cerevisiae DNA polymerase delta require switching between the polymerase and exonuclease domains. Mol Cell Biol 25 : 461 471.
35. Jolivet, E., Matsunaga, F., Ishino, Y., Forterre, P., Prieur, D. Myllykallio, H. (2003) Physiological responses of the hyperthermophilic archaeon 'Pyrococcus abyssi' to DNA damage caused by ionizing radiation. J Bacteriol 185 : 3958 3961.
36. Khare, V. Eckert, K.A. (2002) The proofreading 3′->5′ exonuclease activity of DNA polymerases: a kinetic barrier to translesion DNA synthesis. Mutat Res 510 : 45 54.
37. Kool, E.T. (2002) Active site tightness and substrate fit in DNA replication. Annu Rev Biochem 71 : 191 219.
38. Kow, Y.W. Dare, A. (2000) Detection of abasic sites and oxidative DNA base damage using an ELISA-like assay. Methods 22 : 164 169.
39. Kroeger, K.M., Kim, J., Goodman, M.F. Greenberg, M.M. (2006) Replication of an oxidized abasic site in Escherichia coli by a dNTP-stabilized misalignment mechanism that reads upstream and downstream nucleotides. Biochemistry 45 : 5048 5056.
40. Kubo, K., Ide, H., Wallace, S.S. Kow, Y.W. (1992) A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry 31 : 3703 3708.
41. Kuroita, T., Matsumura, H., Yokota, N., Kitabayashi, M., Hashimoto, H., Inoue, T., et al. (2005) Structural mechanism for coordination of proofreading and polymerase activities in archaeal DNA polymerases. J Mol Biol 351 : 291 298.
42. Lawrence, C.W., Borden, A., Banerjee, S.K. LeClerc, J.E. (1990) Mutation frequency and spectrum resulting from a single abasic site in a single-stranded vector. Nucleic Acids Res 18 : 2153 2157.
43. Le Breton, M., Henneke, G., Norais, C., Flament, D., Myllykallio, H., Querellou, J. Raffin, J.P. (2007) The heterodimeric primase from the euryarchaeon Pyrococcus abyssi: a multifunctional enzyme for initiation and repair? J Mol Biol 374 : 1172 1185.
44. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature 362 : 709 715.
45. Lindahl, T. Nyberg, B. (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11 : 3610 3618.
46. Loeb, L.A., Preston, B.D., Snow, E.T. Schaaper, R.M. (1986) Apurinic sites as common intermediates in mutagenesis. Basic Life Sci 38 : 341 347.
47. McCulloch, S.D. Kunkel, T.A. (2006) Multiple solutions to inefficient lesion bypass by T7 DNA polymerase. DNA Repair (Amst) 5 : 1373 1383.
48. McGlynn, P. Lloyd, R.G. (2002) Recombinational repair and restart of damaged replication forks. Nat Rev Mol Cell Biol 3 : 859 870.
49. Myllykallio, H., Lopez, P., Lopez Garcia, P., Heilig, R., Saurin, W., Zivanovic, Y., et al. (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288 : 2212 2215.
50. Nohmi, T. (2006) Environmental stress and lesion-bypass DNA polymerases. Annu Rev Microbiol 60 : 231 253.
51. Pages, V. Fuchs, R.P. (2002) How DNA lesions are turned into mutations within cells? Oncogene 21 : 8957 8966.
52. Pages, V., Janel-Bintz, R. Fuchs, R.P. (2005) Pol III proofreading activity prevents lesion bypass as evidenced by its molecular signature within E. coli cells. J Mol Biol 352 : 501 509.
53. Park, D. (2007) Genomic DNA isolation from different biological materials. Methods Mol Biol 353 : 3 13.
54. Rothwell, P.J. Waksman, G. (2005) Structure and mechanism of DNA polymerases. Adv Protein Chem 71 : 401 440.
55. Rouillon, C., Henneke, G., Flament, D., Querellou, J. Raffin, J.P. (2007) DNA polymerase switching on homotrimeric PCNA at the replication fork of the euryarchaea Pyrococcus abyssi. J Mol Biol 369 : 343 355.
56. Schaaper, R.M. Loeb, L.A. (1981) Depurination causes mutations in SOS-induced cells. Proc Natl Acad Sci USA 78 : 1773 1777.
57. Schaaper, R.M., Kunkel, T.A. Loeb, L.A. (1983) Infidelity of DNA synthesis associated with bypass of apurinic sites. Proc Natl Acad Sci USA 80 : 487 491.
58. Scharer, O.D. Jiricny, J. (2001) Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23 : 270 281.
59. Shibutani, S., Takeshita, M. Grollman, A.P. (1997) Translesional synthesis on DNA templates containing a single abasic site. A mechanistic study of the 'A rule'. J Biol Chem 272 : 13916 13922.
60. Shimizu, K., Hashimoto, K., Kirchner, J.M., Nakai, W., Nishikawa, H., Resnick, M.A. Sugino, A. (2002) Fidelity of DNA polymerase epsilon holoenzyme from budding yeast Saccharomyces cerevisiae. J Biol Chem 277 : 37422 37429.
61. Shimizu, M., Gruz, P., Kamiya, H., Kim, S.R., Pisani, F.M., Masutani, C., et al. (2003) Erroneous incorporation of oxidized DNA precursors by Y-family DNA polymerases. EMBO Rep 4 : 269 273.
62. Strauss, B.S. (1991) The 'A rule' of mutagen specificity: a consequence of DNA polymerase bypass of non-instructional lesions? Bioessays 13 : 79 84.
63. Tanguy Le Gac, N., Delagoutte, E., Germain, M. Villani, G. (2004) Inactivation of the 3′-5′ exonuclease of the replicative T4 DNA polymerase allows translesion DNA synthesis at an abasic site. J Mol Biol 336 : 1023 1034.
64. Taylor, J.S. (2002) New structural and mechanistic insight into the A-rule and the instructional and non-instructional behavior of DNA photoproducts and other lesions. Mutat Res 510 : 55 70.
65. Villani, G., Boiteux, S. Radman, M. (1978) Mechanism of ultraviolet-induced mutagenesis: extent and fidelity of in vitro DNA synthesis on irradiated templates. Proc Natl Acad Sci USA 75 : 3037 3041.
66. Yang, W. (2005) Portraits of a Y-family DNA polymerase. FEBS Lett 579 : 868 872.
67. Yang, W. Woodgate, R. (2007) What a difference a decade makes: insights into translesion DNA synthesis. Proc Natl Acad Sci USA 104 : 15591 15598.
68. Zahn, K.E., Belrhali, H., Wallace, S.S. Doublie, S. (2007) Caught bending the A-rule: crystal structures of translesion DNA synthesis with a non-natural nucleotide. Biochemistry 46 : 10551 10561.
69. Zhao, B., Xie, Z., Shen, H. Wang, Z. (2004) Role of DNA polymerase eta in the bypass of abasic sites in yeast cells. Nucleic Acids Res 32 : 3984 3994.
70. Zhao, H., Shen, J., Deininger, P. Hunt, J.D. (2006) Abasic sites and survival in resected patients with non-small cell lung cancer. Cancer Lett 246 : 47 53.