Replication of damaged genomes

Critical Reviews in Eukaryotic Gene Expression

Volumn 21, Issue 4, 2011, Pages 323-336

  Klarer, Alden C ^a   Glenn McGregor, W ^a,b  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

Benzo a pyrene; DNA damage; Mutagenesis; UV radiation; Y family DNA polymerases

Indexed keywords

BRCA1 PROTEIN; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE ETA; DNA DIRECTED DNA POLYMERASE IOTA; DNA DIRECTED DNA POLYMERASE ZETA; DNA POLYMERASE; DNA POLYMERASE REV1; PYRIMIDINE DIMER; UNCLASSIFIED DRUG;

ARTICLE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CHROMOSOME REARRANGEMENT; DNA DAMAGE; DNA RECOMBINATION; DNA REPLICATION; DNA STRAND BREAKAGE; EXCISION REPAIR; GENE EXPRESSION; GENE SWITCHING; GENETIC LINKAGE; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MUTAGENESIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 83455163803     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v21.i4.30     Document Type: Article

References (92)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74.
2. Baynton K, Bresson-Roy A, Fuchs R P. Analysis of damage tolerance pathways in Saccharomyces cerevisiae: a requirement for Rev3 DNA polymerase in translesion synthesis. Mol Cell Biol. 1998;18(2):960-6.
3. Adar S, Izhar L, Hendel A, Geacintov N, Livneh Z. Repair of gaps opposite lesions by homologous recombination in mammalian cells. Nucleic Acids Res. 2009;37:5737-48.
4. Vasquez KM, Marburger K, Intody Z, Wilson JH. Manipulating the mammalian genome by homologous recombination. Proc Natl Acad Sci U S A. 2001;98:8403-10.
5. Shulman MJ, Collins C, Connor A, Read LR, Baker MD. Interchromosomal recombination is suppressed in mammalian somatic cells. EMBO J. 1995;14(16):4102-7.
6. Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R. The Y-family of DNA polymerases. Mol Cell. 2001;8:7.
7. Gibbs P E, McGregor W G, Maher V M, Nisson P, Lawrence C W. A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase zeta. Proc Natl Acad Sci U S A. 1998;95:6876.
8. Lin W, Wu X, Wang Z. A full-length cDNA of hREV3 is predicted to encode DNA polymerase zeta for damage-induced mutagenesis in humans. Mutat Res. 1999;89433.
9. McCulloch SD, Kunkel TA, The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 2008;18, 148.
10. Cann KL, Dellaire G, Heterochromatin and the DNA damage response: the need to relax. Biochem Cell Biol. 2011;89, 45.
11. Larimer FW, Perry JR, Hardigree AA. The REV1 gene of Saccharomyces cerevisiae: isolation, sequence, and functional analysis, J Bacteriol. 1989;171, 230.
12. Nelson JR, Lawrence CW, Hinkle DC. Deoxycytidyl transferase activity of yeast REV1 protein. Nature. 1996;382, 729.
13. Swan MK, Johnson RE, Prakash L, Prakash S, Aggarwal AK. Structure of the human Rev1-DNA-dNTP ternary complex. J. Mol. Biol. 2009;390, 699.
14. Gibbs PE, Wang XD, Li Z, McManus TP, McGregor WG, Lawrence CW, Maher VM. The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by UV light. Proc Natl Acad Sci U S A. 2000;97, 4186.
15. Mukhopadhyay S, Clark DR, Watson NB, Zacharias W, McGregor WG. REV1 accumulates in DNA damage-induced nuclear foci in human cells and is implicated in mutagenesis by benzo[a]pyrenediolepoxide. Nucleic Acids Res. 2004;32, 5820.
16. Clark DR, Zacharias W, Panaitescu L, McGregor WG, Ribozyme-mediated REV1 inhibition reduces the frequency of UV-induced mutations in the human HPRT gene. Nucleic Acids Res. 2003;31, 4981.
17. Lawrence CW, Gibbs PE, Murante RS, Wang XD, Li Z, McManus TP, McGregor WG, Nelson JR, Hinkle DC, Maher VM. Roles of DNA polymerase zeta and Rev1 protein in eukaryotic mutagenesis and translesion replication. Cold Spring Harb Symp Quant Biol. 2000;65, 61.
18. Ross AL, Simpson LJ, Sale JE. Vertebrate DNA damage tolerance requires the C-terminus but not BRCT or transferase domains of REV1. Nucleic Acids Res. 2005;33, 1280.
19. Jansen JG, Tsaalbi-Shtylik A, Langerak P, Calleja F, Meijers CM, Jacobs H, de, WN. The BRCT domain of mammalian Rev1 is involved in regulating DNA translesion synthesis. Nucleic Acids Res. 2005;33, 356.
20. Tsaalbi-Shtylik A, Verspuy JW, Jansen JG, Rebel H, Carlee LM, van d, V, Jonkers J, de Gruijl FR, de, WN. Error-prone translesion replication of damaged DNA suppresses skin carcinogenesis by controlling inflammatory hyperplasia. Proc Natl Acad Sci U S A. 2009;106, 21836.
21. Zhao B, Wang J, Geacintov NE, Wang Z. Poleta, Polzeta, and Rev1 together are required for G to T transversion mutations induced by the (+)- and (-)-trans-anti-BPDE-N2-dG DNA adducts in yeast cells. Nucleic Acids Res. 2006;34, 417.
22. Dumstorf CA, Mukhopadhyay S, Krishnan E, Haribabu B, McGregor WG. REV1 is implicated in the development of carcinogen-induced lung cancer. Mol. Cancer Res. 2009;7, 247.
23. Sakiyama T, Kohno T, Mimaki S, Ohta T, Yanagitani N, Sobue T, Kunitoh H, Saito R, Shimizu K, Hirama C, Kimura J, Maeno G, Hirose H, Eguchi T, Saito D, Ohki M, Yokota J. Association of amino acid substitution polymorphisms in DNA repair genes TP53, POLI, REV1 and LIG4 with lung cancer risk. Int J Cancer. 2005;114, 730.
24. Young RP, Hopkins RJ, Hay BA, Epton MJ, Mills GD, Black PN, Gardner HD, Sullivan R, Gamble GD. A gene-based risk score for lung cancer susceptibility in smokers and ex-smokers. Postgrad. Med. J. 2009;85 515.
25. Waters LS, Walker GC. The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G(2)/M phase rather than S phase. Proc Natl Acad Sci U S A. 2006;103, 8971.
26. Johnson RE, Kondratick CM, Prakash S, Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science. 1999;285, 263.
27. Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, Yuasa M, Araki M, Iwai S, Takio K, Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature. 1999;399, 700.
28. Cleaver JE. Xeroderma pigmentosum: variants with normal DNA repair and normal sensitivity to ultraviolet light. J Invest Dermatol. 1972;58, 124.
29. Tung BS, McGregor WG, Wang YC, Maher VM, McCormick JJ. Comparison of the rate of excision of major UV photoproducts in the strands of the human HPRT gene of normal and xeroderma pigmentosum variant cells. Mutat Res. 1996;362, 65.
30. Boyer JC, Kaufmann WK, Brylawski BP, Cordeiro-Stone M. Defective postreplication repair in xeroderma pigmentosum variant fibroblasts. Cancer Res. 1990;50, 2593.
31. Maher VM, Ouellette LM, Curren RD, McCormick JJ. Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells. Nature. 1976;261, 593.
32. Masutani C, Araki M, Yamada A, Kusumoto R, Nogimori T, Maekawa T, Iwai S, Hanaoka F. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 1999;18, 3491.
33. Johnson RE, Prakash S, Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta. Science. 1999;283, 1001.
34. Guo C, Kosarek-Stancel JN, Tang TS, Friedberg EC. Y-family DNA polymerases in mammalian cells. Cell Mol Life Sci. 2009;66, 2363.
35. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol Biol Rev. 2009;73, 134.
36. Lin Q, Clark AB, McCulloch SD, Yuan T, Bronson RT, Kunkel TA, Kucherlapati R. Increased susceptibility to UV-induced skin carcinogenesis in polymerase {eta}-deficient mice. Cancer Res. 2006;66, 87.
37. Kuwamoto K, Miyauchi-Hashimoto H, Isei T, Horio T. Xeroderma pigmentosum variant associated with multiple cancers. Photodermatol Photoimmunol Photomed. 1999;15, 127.
38. Kraemer KH, Lee MM, Scotto J. DNA repair protects against cutaneous and internal neoplasia: evidence from xeroderma pigmentosum. Carcinogenesis. 1984;5, 511.
39. Di LJ, Guedj M, Lacapere JJ, Fargnoli MC, Bourillon A, Dieude P, Dupin N, Wolkenstein P, Aegerter P, Saiag P, Descamps V, Lebbe C, Basset-Seguin N, Peris K, Grandchamp B, Soufir N. Variants of the xeroderma pigmentosum variant gene (POLH) are associated with melanoma risk. Eur J Cancer. 2009;45, 3228.
40. Glick E, White LM, Elliott NA, Berg D, Kiviat NB, Loeb LA. Mutations in DNA polymerase eta are not detected in squamous cell carcinoma of the skin. Int J Cancer. 2006;119, 2225.
41. Flanagan AM, Rafferty G, O'Neill A, Rynne L, Kelly J, McCann J, Carty MP. The human POLH gene is not mutated, and is expressed in a cohort of patients with basal or squamous cell carcinoma of the skin. Int J Mol Med. 2007;19, 589.
42. McDonald JP, Rapic-Otrin V, Epstein JA, Broughton BC, Wang X, Lehmann AR, Wolgemuth DJ, Woodgate R. Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase eta. Genomics. 1999;60, 20.
43. Nair DT, Johnson RE, Prakash L, Prakash S, Aggarwal AK. Human DNA polymerase iota incorporates dCTP opposite template G via a G.C + Hoogsteen base pair. Structure. 13, 1569, 2005.
44. Wang J. DNA polymerases: Hoogsteen base-pairing in DNA replication? Nature. 2005;437:E6-E7.
45. Lee GH, Nishimori H, Sasaki Y, Matsushita H, Kitagawa T, Tokino T. Analysis of lung tumorigenesis in chimeric mice indicates the Pulmonary adenoma resistance 2 (Par2) locus to operate in the tumor-initiation stage in a cell-autonomous manner: detection of polymorphisms in the Poli gene as a candidate for Par2. Oncogene. 22, 2374, 2003.
46. Wang M, Devereux TR, Vikis HG, McCulloch SD, Holliday W, Anna C, Wang Y, Bebenek K, Kunkel TA, Guan K, You M. Pol iota is a candidate for the mouse pulmonary adenoma resistance 2 locus, a major modifier of chemically induced lung neoplasia. Cancer Res. 64, 1924, 2004.
47. Lee GH, Matsushita H. Genetic linkage between Pol iota deficiency and increased susceptibility to lung tumors in mice. Cancer Sci. 96, 256, 2005.
48. Obata M, Nishimori H, Ogawa K, Lee GH. Identification of the Par2 (Pulmonary adenoma resistance) locus on mouse chromosome 18, a major genetic determinant for lung carcinogen resistance in BALB/cByJ mice. Oncogene. 13, 1599, 1996.
49. Bonner AE, Lemon WJ, Devereux TR, Lubet RA, You M. Molecular profiling of mouse lung tumors: association with tumor progression, lung development, and human lung adenocarcinomas. Oncogene. 23, 1166, 2003.
50. Choudhury S, Adhikari S, Cheema A, Roy R. Evidence of complete cellular repair of 1,N6-ethenoadenine, a mutagenic and potential damage for human cancer, revealed by a novel method. Mol Cell Biochem. 313, 19, 2008.
51. McDonald JP, Frank EG, Plosky BS, Rogozin IB, Masutani C, Hanaoka F, Woodgate R, Gearhart PJ. 129-derived strains of mice are deficient in DNA polymerase iota and have normal immunoglobulin hypermutation. J Exp Med. 198, 635, 2003.
52. Gening LV, Makarova AV, Malashenko AM, Tarantul VZ. A false note of DNA polymerase iota in the choir of genome caretakers in mammals. Biochemistry (Mosc.). 71, 155, 2006.
53. Makarova AV, Grabow C, Gening LV, Tarantul VZ, Tahirov TH, Bessho T, Pavlov YI. Inaccurate DNA synthesis in cell extracts of yeast producing active human DNA polymerase iota. PLoS. ONE. 6, e16612, 2011.
54. Dumstorf CA, Clark AB, Lin Q, Kissling GE, Yuan T., Kucherlapati R., McGregor WG, Kunkel TA. Participation of mouse DNA polymerase iota in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc Natl Acad Sci U S A. 103, 18083, 2006.
55. Wang Y, Woodgate R, McManus TP, Mead S, McCormick JJ, Maher VM. Evidence that in xeroderma pigmentosum variant cells, which lack DNA polymerase eta, DNA polymerase iota causes the very high frequency and unique spectrum of UV-induced mutations. Cancer Res. 67, 3018, 2007.
56. Ohkumo T, Kondo Y, Yokoi M, Tsukamoto T, Yamada A, Sugimoto T, Kanao R, Higashi Y, Kondoh H, Tatematsu M, Masutani C, Hanaoka F. UV-B radiation induces epithelial tumors in mice lacking DNA polymerase eta and mesenchymal tumors in mice deficient for DNA polymerase iota. Mol Cell Biol. 26, 7696, 2006.
57. Newcomb EW, Diamond LE, Sloan SR, Corominas M, Guerrerro I, Pellicer A. Radiation and chemical activation of ras oncogenes in different mouse strains. Environ Health Perspect. 81, 33, 1989.
58. Petta TB, Nakajima S, Zlatanou A, Despras E, Couve-Privat S, Ishchenko A, Sarasin A, Yasui A, Kannouche P. Human DNA polymerase iota protects cells against oxidative stress. EMBO J. 27, 2883, 2008.
59. Poltoratsky V, Horton JK, Prasad R, Beard WA, Woodgate R, Wilson SH. Negligible impact of pol iota expression on the alkylation sensitivity of pol beta-deficient mouse fibroblast cells. DNA Repair (Amst). 7, 830, 2008.
60. Wang H, Wu W, Wang HW, Wang S, Chen Y, Zhang X, Yang J, Zhao S, Ding HF, Lu D. Analysis of specialized DNA polymerases expression in human gliomas: association with prognostic significance. Neuro. Oncol. 2010.
61. Zienolddiny S, Campa D, Lind H, Ryberg D, Skaug V, Stangeland L, Phillips DH, Canzian F, Haugen A. Polymorphisms of DNA repair genes and risk of non-small cell lung cancer. Carcinogenesis. 27, 560, 2006.
62. Manuguerra M, Saletta F, Karagas MR, Berwick M, Veglia F, Vineis P, Matullo G. XRCC3 and XPD/ERCC2 single nucleotide polymorphisms and the risk of cancer: a HuGE review. Am J Epidemiol. 164, 297, 2006.
63. Luedeke M, Linnert CM, Hofer MD, Surowy HM, Rinckleb AE, Hoegel J, Kuefer R, Rubin MA, Vogel W, Maier C. Predisposition for TMPRSS2-ERG fusion in prostate cancer by variants in DNA repair genes. Cancer Epidemiol Biomarkers Prev. 18, 3030, 2009.
64. Petrovics G, Liu A, Shaheduzzaman S, Furusato B, Sun C, Chen Y, Nau M, Ravindranath L, Chen Y, Dobi A, Srikantan V, Sesterhenn IA, McLeod DG, Vahey M, Moul JW, Srivastava S. Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene. 24, 3847, 2005.
65. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 310, 644, 2005.
66. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, Coull B, Kannouche P, Wider G, Peter M, Lehmann AR, Hofmann K, Dikic I. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science. 310, 1821, 2005.
67. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 310, 644, 2005.
68. Suzuki N, Ohashi E, Kolbanovskiy A, Geacintov NE, Grollman AP, Ohmori H, Shibutani S. Translesion synthesis by human DNA polymerase kappa on a DNA template containing a single stereoisomer of dG-(+)- or dG-(-)-anti-N(2)-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene). Biochemistry. 41, 6100, 2002.
69. Rechkoblit O, Zhang Y, Guo D, Wang Z, Amin S, Krzeminsky, J, Louneva N, Geacintov NE. Trans-Lesion synthesis past bulky benzo[a]pyrene diol epoxide N2-dG and N6-dA lesions catalyzed by DNA bypass polymerases. J Biol Chem. 277, 30488, 2002.
70. Zhang Y, Wu X, Guo D, Rechkoblit O, Wang Z. Activities of human DNA polymerase [kappa] in response to the major benzo[a]pyrene DNA adduct: error-free lesion bypass and extension synthesis from opposite the lesion. DNA Repair. 1, 559, 2002.
71. Guo N, Faller DV, Vaziri C. Carcinogen-induced S-phase arrest is Chk1 mediated and caffeine sensitive. Cell Growth Differ. 13, 77, 2002.
72. Bi X, Slater DM, Ohmori H, Vaziri C. DNA polymerase kappa is specifically required for recovery from the benzo[a]pyrene-dihydrodiol epoxide (BPDE)-induced S-phase checkpoint. J Biol Chem. 280, 22343, 2005.
73. Avkin S, Goldsmith M, Velasco-Miguel S, Geacintov N, Friedberg EC, Livneh Z. Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: the role of DNA polymerase kappa2. J Biol Chem. 279, 53298, 2004.
74. Shachar S, Ziv, O, Avkin, S, Adar, S, Wittschieben, J, Reissner, T, Chaney, S, Friedberg, EC, Wang, Z, Carell, T, Geacintov, N, Livneh, Z. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J. 28, 383, 2009.
75. Ogi T, Lehmann AR. The Y-family DNA polymerase kappa (pol kappa) functions in mammalian nucleotide-excision repair. Nat Cell Biol. 8, 640, 2006.
76. Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K, Cloney R, Nakazawa Y, Niimi A, Miki Y, Jaspers NG, Mullenders LH, Yamashita S, Fousteri MI, Lehmann AR. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell. 37, 714, 2010.
77. Schenten D, Gerlach VL, Guo C, Velasco-Miguel S, Hladik CL, White CL, Friedberg EC, Rajewsky K, Esposito G. DNA polymerase kappa deficiency does not affect somatic hypermutation in mice. Eur J Immunol. 32, 3152, 2002.
78. Shimizu T, Shinkai Y, Ogi T, Ohmori H, Azuma T. The absence of DNA polymerase kappa does not affect somatic hypermutation of the mouse immunoglobulin heavy chain gene2. Immunol Lett. 86, 265, 2003.
79. Stancel JN, McDaniel LD, Velasco S, Richardson J, Guo C, Friedberg EC. Polk mutant mice have a spontaneous mutator phenotype. DNA Repair (Amst). 8, 1355, 2009.
80. Wang J, Kawamura K, Tada Y, Ohmori H, Kimura H, Sakiyama S, Tagawa M. DNA polymerase kappa, implicated in spontaneous and DNA damage-induced mutagenesis, is overexpressed in lung cancer. Cancer Res. 61, 5366, 2001.
81. Wang Y, Seimiya M, Kawamura K, Yu L, Ogi T, Takenaga K, Shishikura T, Nakagawara A, Sakiyama S, Tagawa M, Wang J. Elevated expression of DNA polymerase kappa in human lung cancer is associated with p53 inactivation: Negative regulation of POLK promoter activity by p53. Int J Oncol. 25, 161, 2004.
82. Skaug V, Ryberg D, Kure EH, Arab MO, Stangeland L, Myking AO, Haugen A. p53 mutations in defined structural and functional domains are related to poor clinical outcome in non-small cell lung cancer patients. Clin Cancer Res. 6, 1031, 2000.
83. Diaz M, Watson NB, Turkington G, Verkoczy LK, Klinman NR, McGregor WG, Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in the hprt gene of mouse fibroblasts expressing antisense RNA to DNA polymerase zeta. Mol Cancer Res. 1, 836, 2003.
84. Li Z, Zhang H, McManus TP, McCormick JJ, Lawrence CW, Maher VM. 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, 71, 2002.
85. Murakumo Y, Roth T, Ishii H, Rasio D, Numata S, Croce CM, Fishel R. A human REV7 homolog that interacts with the polymerase zeta catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2. J Biol Chem. 275, 4391, 2000.
86. Quah SK, von Borstel RC, Hastings PJ. The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics. 96, 819, 1980.
87. Van Sloun PP, Varlet I, Sonneveld E, Boei JJ, Romeijn RJ, Eeken JC, De Wind N. Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol Cell Biol. 22, 2159, 2002.
88. Wittschieben JP, Reshmi SC, Gollin SM, Wood RD. Loss of DNA polymerase zeta causes chromosomal instability in mammalian cells. Cancer Res. 66, 134, 2006.
89. Wittschieben J, Shivji MK, Lalani E, Jacobs MA, Marini F, Gearhart PJ, Rosewell I, Stamp G, Wood RD. Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr Biol. 10, 1217, 2000.
90. Bemark M, Khamlichi AA, Davies SL, Neuberger MS. Disruption of mouse polymerase zeta (Rev3) leads to embryonic lethality and impairs blastocyst development in vitro. Curr Biol. 10, 1213, 2000.
91. Brondello JM, Pillaire MJ, Rodriguez C, Gourraud PA, Selves J, Cazaux C, Piette J. Novel evidences for a tumor suppressor role of Rev3, the catalytic subunit of Pol zeta. Oncogene. 27, 6093, 2008.
92. Kawamura K, Wang J, Bahar R, Koshikawa N, Shishikura T, Nakagawara A, Sakiyama S, Kajiwara K, Kimura M, Tagawa M. The error-prone DNA polymerase zeta catalytic subunit (Rev3) gene is ubiquitously expressed in normal and malignant human tissues. Int J Oncol. 18, 97, 2001.