Translesion synthesis: Y-family polymerases and the polymerase switch

DNA Repair

Volumn 6, Issue 7, 2007, Pages 891-899

  Lehmann, Alan R ^a   Niimi, Atsuko ^a   Ogi, Tomoo ^a   Brown, Stephanie ^a   Sabbioneda, Simone ^a   Wing, Jonathan F ^a   Kannouche, Patricia L ^b   Green, Catherine M ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

DNA polymerase; PCNA; Replication factories; Ubiquitination

Indexed keywords

DNA DIRECTED DNA POLYMERASE ETA; DNA DIRECTED DNA POLYMERASE IOTA; DNA DIRECTED DNA POLYMERASE KAPPA; DNA DIRECTED DNA POLYMERASE ZETA; DNA POLYMERASE; DNA POLYMERASE REV1; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; ENZYME REPLACEMENT; ENZYME SPECIFICITY; ENZYME SUBSTRATE; EUKARYOTE; GENE CONTROL; GENE SWITCHING; HUMAN; IMMUNE SYSTEM; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; UBIQUITINATION;

ANIMALS; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; HUMANS; MODELS, BIOLOGICAL; PROLIFERATING CELL NUCLEAR ANTIGEN; UBIQUITIN;

EUKARYOTA;

EID: 34249941966     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.02.003     Document Type: Article

References (97)

1. Friedberg E.C. Suffering in silence: the tolerance of DNA damage. Nat. Rev. Mol. Cell. Biol. 6 (2005) 943-953
2. Goodman M.F. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71 (2002) 17-50
3. Lehmann A.R. Replication of damaged DNA in mammalian cells: new solutions to an old problem. Mutat. Res. 509 (2002) 23-34
4. Lehmann A.R. Replication of damaged DNA by translesion synthesis in human cells. FEBS Lett. 579 (2005) 873-876
5. Lehmann A.R. Translesion synthesis in mammalian cells. Exp. Cell. Res. 312 (2006) 2673-2676
6. Rattray A.J., and Strathern J.N. Error-prone DNA polymerases: when making a mistake is the only way to get ahead. Annu. Rev. Genet. 37 (2003) 31-66
7. Vaisman A., Lehmann A.R., and Woodgate R. DNA polymerases eta and iota. Adv. Protein Chem. 69 (2004) 205-228
8. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005) 317-353
9. Jansen J.G., and de Wind N. Biological functions of translesion synthesis proteins in vertebrates. DNA Repair (Amst) 2 (2003) 1075-1085
10. McCulloch S.D., Kokoska R.J., Masutani C., Iwai S., Hanaoka F., and Kunkel T.A. Preferential cis-syn thymine dimer bypass by DNA polymerase η occurs with biased fidelity. Nature 428 (2004) 97-100
11. Masutani C., Kusumoto R., Iwai S., and Hanaoka F. Accurate translesion synthesis by human DNA polymerase η. EMBO J. 19 (2000) 3100-3109
12. Masutani C., Kusumoto R., Yamada A., Dohmae N., Yokoi M., Yuasa M., Araki M., Iwai S., Takio K., and Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399 (1999) 700-704
13. Johnson R.E., Kondratick C.M., Prakash S., and Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285 (1999) 263-265
14. Dumstorf C., Clark A.B., Lin Q., Kissling G.E., Yuan T., Kucherlapati R., McGregor W.G., and Kunkel T.A. Participation of mouse DNA polymerase ι in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 18083-18088
15. Lin Q., Clark A.B., McCulloch S.D., Yuan T., Bronson R.T., Kunkel T.A., and Kucherlapati R. Increased susceptibility to UV-induced skin carcinogenesis in polymerase eta-deficient mice. Cancer Res. 66 (2006) 87-94
16. Albertella M.R., Green C.M., Lehmann A.R., and O'Connor M.J. A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res. 65 (2005) 9799-9806
17. Chen Y.W., Cleaver J.E., Hanaoka F., Chang C.F., and Chou K.M. A novel role of DNA polymerase eta in modulating cellular sensitivity to chemotherapeutic agents. Mol. Cancer Res. 4 (2006) 257-265
18. Avkin S., and Livneh Z. Efficiency, specificity and DNA polymerase-dependence of translesion replication across the oxidative DNA lesion 8-oxoguanine in human cells. Mutat. Res. 510 (2002) 81-90
19. Avkin S., Adar S., Blander G., and Livneh Z. Quantitative measurement of translesion replication in human cells: evidence for bypass of abasic sites by a replicative DNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3764-3769
20. Kannouche P., Broughton B.C., Volker M., Hanaoka F., Mullenders L.H.F., and Lehmann A.R. Domain structure, localization and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells. Genes Dev. 15 (2001) 158-172
21. Kawamoto T., Araki K., Sonoda E., Yamashita Y.M., Harada K., Kikuchi K., Masutani C., Hanaoka F., Nozaki K., Hashimoto N., and Takeda S. Dual roles for DNA polymerase eta in homologous DNA recombination and translesion DNA synthesis. Mol. Cell 20 (2005) 793-799
22. McIlwraith M.J., Vaisman A., Liu Y., Fanning E., Woodgate R., and West S.C. Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol. Cell 20 (2005) 783-792
23. Cleaver J.E., Afzal V., Feeney L., McDowell M., Sadinski W., Volpe J.P., Busch D.B., Coleman D.M., Ziffer D.W., Yu Y., Nagasawa H., and Little J.B. Increased ultraviolet sensitivity and chromosomal instability related to p53 function in the xeroderma pigmentosum variant. Cancer Res. 59 (1999) 1102-1108
24. Tissier A., McDonald J.P., Frank E.G., and Woodgate R. Polι, a remarkably error-prone human DNA polymerase. Genes Dev. 14 (2000) 1642-1650
25. Kannouche P., Fernandez de Henestrosa A.R., Coull B., Vidal A.E., Gray C., Zicha D., Woodgate R., and Lehmann A.R. Localization of DNA polymerases η and ι to the replication machinery is tightly co-ordinated in human cells. EMBO J. 22 (2003) 1223-1233
26. Choi J.H., Besaratinia A., Lee D.H., Lee C.S., and Pfeifer G.P. The role of DNA polymerase iota in UV mutational spectra. Mutat. Res. 599 (2006) 58-65
27. McDonald J.P., Frank E.G., Plosky B.S., Rogozin I.B., Masutani C., Hanaoka F., Woodgate R., and Gearhart P.J. 129-derived strains of mice are deficient in DNA polymerase ι and have normal immunoglobulin hypermutation. J. Exp. Med. 198 (2003) 635-643
28. Ogi T., Shinkai Y., Tanaka K., and Ohmori H. Pol κ protects mammalian cells against the lethal and mutagenic effects of benzo[a]pyrene. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 15548-15553
29. Avkin S., Goldsmith M., Velasco-Miguel S., Geacintov N., Friedberg E.C., and Livneh Z. Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: the role of DNA polymerase kappa. J. Biol. Chem. 279 (2004) 53298-58305
30. Jarosz D.F., Godoy V.G., Delaney J.C., Essigmann J.M., and Walker G.C. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439 (2006) 225-228
31. Takenaka K., Ogi T., Okada T., Sonoda E., Guo C., Friedberg E.C., and Takeda S. Involvement of vertebrate Polkappa in translesion DNA synthesis across DNA monoalkylation damage. J. Biol. Chem. 281 (2006) 2000-2004
32. Ogi T., and Lehmann A.R. The Y-family DNA polymerase kappa (pol kappa) functions in mammalian nucleotide-excision repair. Nat. Cell. Biol. 8 (2006) 640-642
33. Schenten D., Gerlach V.L., Guo C., Velasco-Miguel S., Hladik C.L., White C.L., Friedberg E.C., Rajewsky K., and Esposito G. DNA polymerase κ deficiency does not affect somatic hypermutation in mice. Eur. J. Immunol. 32 (2002) 3152-3160
34. Shimizu T., Shinkai Y., Ogi T., Ohmori H., and Azuma T. The absence of DNA polymerase kappa does not affect somatic hypermutation of the mouse immunoglobulin heavy chain gene. Immunol. Lett. 86 (2003) 265-270
35. Ogi T., Kannouche P., and Lehmann A.R. Localization of human DNA polymerase κ (polκ), a Y-family DNA polymerase: relationship to PCNA foci. J. Cell Sci. 118 (2005) 129-136
36. Nelson J.R., Lawrence C.W., and Hinkle D.C. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382 (1996) 729-731
37. Gibbs P.E.M., Wang X.-D., Li Z., McManus T.P., McGregor G., Lawrence C.W., and Maher V.M. The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by ultraviolet light. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4186-4191
38. Gibbs P.E.M., McGregor W.G., Maher V.M., Nisson P., and Lawrence C.W. A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase ζ. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 6876-6880
39. Li Z., Zhang H., McManus T.P., McCormick J.J., Lawrence C.W., and Maher V.M. hREV3 is essential for error-prone translesion synthesis past UV or benzo[a]pyrene diol epoxide-induced DNA lesions in human fibroblasts. Mutat. Res. 510 (2002) 71-80
40. Otsuka C., Kunitomi N., Iwai S., Loakes D., and Negishi K. Roles of the polymerase and BRCT domains of Rev1 protein in translesion DNA synthesis in yeast in vivo. Mutat. Res. 578 (2005) 79-87
41. Guo C., Sonoda E., Tang T.S., Parker J.L., Bielen A.B., Takeda S., Ulrich H.D., and Friedberg E.C. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 23 (2006) 265-271
42. Nelson J.R., Gibbs P.E., Nowicka A.M., Hinkle D.C., and Lawrence C.W. Evidence for a second function for Saccharomyces cerevisiae Rev1p. Mol. Microbiol. 37 (2000) 549-554
43. Nakajima S., Lan L., Kanno S., Takao M., Yamamoto K., Eker A.P., and Yasui A. UV light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells. J. Biol. Chem. 279 (2004) 46674-46677
44. Gibbs P.E., McDonald J., Woodgate R., and Lawrence C.W. The relative roles in vivo of Saccharomyces cerevisiae Pol eta, Pol zeta, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169 (2005) 575-582
45. Simpson L.J., and Sale J.E. Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line. EMBO J. 22 (2003) 1654-1664
46. Jansen J.G., Tsaalbi-Shtylik A., Langerak P., Calleja F., Meijers C.M., Jacobs H., and de Wind N. The BRCT domain of mammalian Rev1 is involved in regulating DNA translesion synthesis. Nucleic Acids Res. 33 (2005) 356-365
47. Bemark M., Khamlichi A.A., Davies S.L., and Neuberger M.S. Disruption of mouse polymerase zeta (Rev3) leads to embryonic lethality and impairs blastocyst development in vitro. Curr. Biol. 10 (2000) 1213-1216
48. Esposito G., Godindagger I., Klein U., Yaspo M.L., Cumano A., and Rajewsky K. Disruption of the Rev3l-encoded catalytic subunit of polymerase zeta in mice results in early embryonic lethality. Curr. Biol. 10 (2000) 1221-1224
49. Van Sloun P.P., Varlet I., Sonneveld E., Boei J.J., Romeijn R.J., Eeken J.C., and De Wind N. Involvement of mouse rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell. Biol. 22 (2002) 2159-2169
50. Wittschieben J., Shivji M.K., Lalani E., Jacobs M.A., Marini F., Gearhart P.J., Rosewell I., Stamp G., and Wood R.D. Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr. Biol. 10 (2000) 1217-1220
51. Zander L., and Bemark M. Immortalized mouse cell lines that lack a functional Rev3 gene are hypersensitive to UV irradiation and cisplatin treatment. DNA Repair (Amst) 3 (2004) 743-752
52. Murakumo Y., Ogura Y., Ishii H., Numata S., Ichihara M., Croce C.M., Fishel R., and Takahashi M. Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J. Biol. Chem. 276 (2001) 35644-35651
53. Guo C., Fischhaber P.L., Luk-Paszyc M.J., Masuda Y., Zhou J., Kamiya K., Kisker C., and Friedberg E.C. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 22 (2003) 6621-6630
54. Ohashi E., Murakumo Y., Kanjo N., Akagi J., Masutani C., Hanaoka F., and Ohmori H. Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9 (2004) 523-531
55. Tissier A., Kannouche P., Reck M.-P., Lehmann A.R., Fuchs R.P.P., and Cordonnier A. Co-localization in replication foci and interaction of human Y-family members, DNA polymerase polη and Rev1 protein. DNA Repair 3 (2004) 1503-1514
56. Di Noia J., and Neuberger M.S. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419 (2002) 43-48
57. Martomo S.A., Yang W.W., Vaisman A., Maas A., Yokoi M., Hoeijmakers J.H., Hanaoka F., Woodgate R., and Gearhart P.J. Normal hypermutation in antibody genes from congenic mice defective for DNA polymerase iota. DNA Repair (Amst) 5 (2006) 392-398
58. Shimizu T., Azuma T., Ishiguro M., Kanjo N., Yamada S., and Ohmori H. Normal immunoglobulin gene somatic hypermutation in Pol kappa-Pol iota double-deficient mice. Immunol. Lett. 98 (2005) 259-264
59. Martomo S.A., Yang W.W., Wersto R.P., Ohkumo T., Kondo Y., Yokoi M., Masutani C., Hanaoka F., and Gearhart P.J. Different mutation signatures in DNA polymerase eta- and MSH6-deficient mice suggest separate roles in antibody diversification. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 8656-8661
60. Delbos F., De Smet A., Faili A., Aoufouchi S., Weill J.C., and Reynaud C.A. Contribution of DNA polymerase eta to immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 201 (2005) 1191-1196
61. Rogozin I.B., Pavlov Y.I., Bebenek K., Matsuda T., and Kunkel T.A. Somatic mutation hotspots correlate with DNA polymerase eta error spectrum. Nat. Immunol. 2 (2001) 530-536
62. Friedberg E.C., Lehmann A.R., and Fuchs R.P. Trading places: how do DNA polymerases switch during translesion DNA synthesis?. Mol. Cell 18 (2005) 499-505
63. Wagner J., Fujii S., Gruz P., Nohmi T., and Fuchs R.P. The beta clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep. 1 (2000) 484-488
64. Xiao W., Chow B.L., Broomfield S., and Hanna M. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways. Genetics 155 (2000) 1633-1641
65. Hoege C., Pfander B., Moldovan G.-L., Pyrolowakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
66. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
67. Kannouche P.L., Wing J., and Lehmann A.R. Interaction of human DNA polymerase η with monoubiquitinated PCNA; a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14 (2004) 491-500
68. Chiu R.K., Brun J., Ramaekers C., Theys J., Werng L., Lambin P., Gray D.A., and Wouters B.G. Lysine 63-polyubiquitination guards against translesion synthesis-induced mutations. PLOS Genet. 2 (2006) e116
69. Solomon D.A., Cardoso M.C., and Knudsen E.S. Dynamic targeting of the replication machinery to sites of DNA damage. J. Cell Biol. 166 (2004) 455-463
70. Soria G., Podhajcer O., Prives C., and Gottifredi V. P21(Cip1/WAF1) downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene 25 (2006) 2829-2838
71. Bi X., Barkley L.R., Slater D.M., Tateishi S., Yamaizumi M., Ohmori H., and Vaziri C. Rad18 regulates DNA polymerase kappa and is required for recovery from S-phase checkpoint-mediated arrest. Mol. Cell. Biol. 26 (2006) 3527-3540
72. Frampton J., Irmisch A., Green C.M., Neiss A., Trickey M., Ulrich H.D., Furuya K., Watts F.Z., Carr A.M., and Lehmann A.R. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell 17 (2006) 2976-2985
73. Leach C.A., and Michael W.M. Ubiquitin/SUMO modification of PCNA promotes replication fork progression in Xenopus laevis egg extracts. J. Cell Biol. 171 (2005) 947-954
74. Simpson L.J., Ross A.L., Szuts D., Alviani C.A., Oestergaard V.H., Patel K.J., and Sale J.E. RAD18-independent ubiquitination of proliferating-cell nuclear antigen in the avian cell line DT40. EMBO Rep. 7 (2006) 927-932
75. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., and Yamaizumi M. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 28 (2004) 3886-3896
76. Bailly V., Lauder S., Prakash S., and Prakash L. Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J. Biol. Chem. 272 (1997) 23360-23365
77. Bentley N.J., Holtzman D.A., Flaggs G., Keegan K.S., DeMaggio A., Ford J.C., Hoekstra M., and Carr A.M. The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J. 15 (1996) 6641-6651
78. Huang T.T., Nijman S.M., Mirchandani K.D., Galardy P.J., Cohn M.A., Haas W., Gygi S.P., Ploegh H.L., Bernards R., and D'Andrea A.D. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 8 (2006) 341-347
79. Sarkar S., Davies A.A., Ulrich H.D., and McHugh P.J. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J. 25 (2006) 1285-1294
80. Tateishi S., Niwa H., Miyazaki J., Fujimoto S., Inoue H., and Yamaizumi M. Enhanced genomic instability and defective postreplication repair in RAD 18 knockout mouse embryonic stem cells. Mol. Cell. Biol. 23 (2003) 474-481
81. Avkin S., Sevilya Z., Toube L., Geacintov N., Chaney S.G., Oren M., and Livneh Z. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol. Cell 22 (2006) 407-413
82. Bienko M., Green C.M., Crosetto N., Rudolf F., Zapart G., Coull B., Kannouche P., Wider G., Peter M., Lehmann A.R., Hofmann K., and Dikic I. Ubiquitin-binding domains in translesion synthesis polymerases. Science 310 (2005) 1821-1824
83. Guo C., Tang T.S., Bienko M., Parker J.L., Bielen A.B., Sonoda E., Takeda S., Ulrich H.D., Dikic I., and Friedberg E.C. Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell. Biol. (2006)
84. Garg P., and Burgers P.M. Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases eta and REV1. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 18361-18366
85. Plosky B.S., Vidal A.E., Fernandez de Henestrosa A.R., McLenigan M.P., McDonald J.P., Mead S., and Woodgate R. Controlling the subcellular localization of DNA polymerases iota and eta via interactions with ubiquitin. EMBO J. 25 (2006) 2847-2855
86. Ulrich H.D. Protein-protein interactions within an E2-RING finger complex. Implications for ubiquitin-dependent DNA damage repair. J. Biol. Chem. 278 (2003) 7051-7058
87. Zhang H., and Lawrence C.W. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 15954-15959
88. Li Z., Xiao W., McCormick J.J., and Maher V.M. Identification of a protein essential for a major pathway used by human cells to avoid UV-induced DNA damage. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 4459-4464
89. Motegi A., Sood R., Moinova H., Markowitz S.D., Liu P.P., and Myung K. Human SHPRH suppresses genomic instability through PCNA polyubiquitination. J. Cell Biol. 175 (2006) 703-708
90. Dionne I., Nookala R.K., Jackson S.P., Doherty A.J., and Bell S.D. A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol. Cell 11 (2003) 275-282
91. Lehmann A.R. Clubbing together on clamps: the key to translesion synthesis. DNA Repair (Amst) 5 (2006) 404-407
92. Solovjeva L., Svetlova M., Sasina L., Tanaka K., Saijo M., Nazarov I., Bradbury M., and Tomilin N. High mobility of flap endonuclease 1 and DNA polymerase eta associated with replication foci in mammalian S-phase nucleus. Mol. Biol. Cell 16 (2005) 2518-2528
93. Kannouche P., and Stary A. Xeroderma pigmentosum variant and error-prone DNA polymerases. Biochimie 85 (2003) 1123-1132
94. Rupp W.D., and Howard-Flanders P. Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J. Mol. Biol. 31 (1968) 291-304
95. Lopes M., Foiani M., and Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21 (2006) 15-27
96. Heller R.C., and Marians K.J. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439 (2006) 557-562
97. Waters L.S., and Walker G.C. The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G2/M phase rather than S phase. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 8971-8976