The RAD51 gene family, genetic instability and cancer

Cancer Letters

Volumn 219, Issue 2, 2005, Pages 125-135

  Thacker, John ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Breast cancer; Genetic instability; Homologous recombination; RAD51; RAD51L1 (RAD51B); RAD51L2 (RAD51C); RAD51L3 (RAD51D); XRCC2; XRCC3

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA BINDING PROTEIN; RAD51 PROTEIN; RAD54 PROTEIN;

CANCER; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CHROMOSOME REARRANGEMENT; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; GENE ACTIVITY; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE MUTATION; GENE SEQUENCE; GENETIC DISORDER; GENETIC POLYMORPHISM; GENETIC STABILITY; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SHORT SURVEY;

EID: 13944268723     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2004.08.018     Document Type: Review

References (104)

1. J.H. Hoeijmakers Genome maintenance mechanisms for preventing cancer Nature 411 2001 366 374
2. C.J. Sherr Principles of tumor suppression Cell 116 2004 235 246
3. L.A. Loeb, K.R. Loeb, and J.P. Anderson Multiple mutations and cancer Proc. Natl Acad. Sci. USA 100 2003 776 781
4. O.M. Sieber, K. Heinimann, and I.P. Tomlinson Genomic instability - the engine of tumorigenesis? Nat. Rev. Cancer 3 2003 701 708
5. P. Duesberg, A. Fabarius, and R. Hehlmann Aneuploidy, the primary cause of the multilateral genomic instability of neoplastic and preneoplastic cells, IUBMB Life 56 2004 65 81
6. D.L. Stoler, N. Chen, M. Basik, M.S. Kahlenberg, M.A. Rodriguez-Bigas, N.J. Petrelli, and G.R. Anderson The onset and extent of genomic instability in sporadic colorectal tumor progression Proc. Natl Acad. Sci. USA 96 1999 15121 15126
7. B. Vogelstein, and K.W. Kinzler The multistep nature of cancer Trends Genet. 9 1993 138 141
8. S.C. West Molecular views of recombination proteins and their control Nat. Rev. Mol. Cell Biol. 4 2003 435 445
9. J. Thacker A surfeit of RAD51-like genes? Trends Genet. 15 1999 166 168
10. J. Thacker The role of homologous recombination processes in the repair of severe forms of DNA damage in mammalian cells Biochimie 81 1999 77 85
11. L.H. Thompson, and D. Schild The contribution of homologous recombination in preserving genome integrity in mammalian cells Biochimie 81 1999 87 105
12. C. Webber, and C.P. Ponting Genes and homology Curr. Biol. 14 2004 R332 R333
13. M. Jasin Homologous repair of DNA damage and tumorigenesis: the BRCA connection Oncogene 21 2002 8981 8993
14. L. Pellegrini, D.S. Yu, T. Lo, S. Anand, M. Lee, T.L. Blundell, and A.R. Venkitaraman Insights into DNA recombination from the structure of a RAD51-BRCA2 complex Nature 420 2002 287 293
15. T. Lo, L. Pellegrini, A.R. Venkitaraman, and T.L. Blundell Sequence fingerprints in BRCA2 and RAD51: implications for DNA repair and cancer DNA Repair (Amst.) 2 2003 1015 1028
16. D. Schild, Y. Lio, D.W. Collins, T. Tsomondo, and D.J. Chen Evidence for simultaneous protein interactions between human Rad51 paralogs J. Biol. Chem. 275 2000 16443 16449
17. J.P. Braybrooke, K.G. Spink, J. Thacker, and I.D. Hickson The RAD51 family member, RAD51L3, is a DNA-stimulated ATPase that forms a complex with XRCC2 J. Biol. Chem. 275 2000 29100 29106
18. S. Sigurdsson, S. Van Komen, W. Bussen, D. Schild, J.S. Albala, and P. Sung Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange Genes Dev. 15 2001 3308 3318
19. K.A. Miller, D.M. Yoshikawa, I.R. McConnell, R. Clark, D. Schild, and J.S. Albala RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51 J. Biol. Chem. 277 2002 8406 8411
20. J.Y. Masson, A.Z. Stasiak, A. Stasiak, F.E. Benson, and S.C. West Complex formation by the human RAD51C and XRCC3 recombination repair proteins Proc. Natl Acad. Sci. USA 98 2001 8440 8446
21. H. Kurumizaka, S. Ikawa, M. Nakada, K. Eda, W. Kagawa, and M. Takata Homologous-pairing activity of the human DNA-repair proteins Xrcc3.Rad51C Proc. Natl Acad. Sci. USA 98 2001 5538 5543
22. C. Wiese, D.W. Collins, J.S. Albala, L.H. Thompson, A. Kronenberg, and D. Schild Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells Nucleic Acids Res. 30 2002 1001 1008
23. J.Y. Masson, M.C. Tarsounas, A.Z. Stasiak, A. Stasiak, R. Shah, and M.J. McIlwraith Identification and purification of two distinct complexes containing the five RAD51 paralogs Genes Dev. 15 2001 3296 3307
24. N. Liu, D. Schild, M.P. Thelen, and L.H. Thompson Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells Nucleic Acids Res. 30 2002 1009 1015
25. Y.C. Lio, A.V. Mazin, S.C. Kowalczykowski, and D.J. Chen Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro J. Biol. Chem. 278 2003 2469 2478
26. P. O'Regan, C. Wilson, S. Townsend, and J. Thacker XRCC2 is a nuclear RAD51-like protein required for damage-dependent RAD51 focus formation without the need for ATP binding J. Biol. Chem. 276 2001 22148 22153
27. C.A. French, C.E. Tambini, and J. Thacker Identification of functional domains in the RAD51L2 (RAD51C) protein and its requirement for gene conversion J. Biol. Chem. 278 2003 45445 45450
28. D.K. Bishop, U. Ear, A. Bhattacharyya, C. Calderone, M. Beckett, R.R. Weichselbaum, and A. Shinohara Xrcc3 is required for assembly of Rad51 complexes in vivo J. Biol. Chem. 273 1998 21482 21488
29. C.A. French, J.Y. Masson, C.S. Griffin, P. O'Regan, S.C. West, and J. Thacker Role of mammalian RAD51L2 (RAD51C) in recombination and genetic stability J. Biol. Chem. 277 2002 19322 19330
30. B.C. Godthelp, W.W. Wiegant, A. van Duijn-Goedhart, O.D. Scharer, P.P. van Buul, R. Kanaar, and M.Z. Zdzienicka Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability Nucleic Acids Res. 30 2002 2172 2182
31. H. Kurumizaka, S. Ikawa, M. Nakada, R. Enomoto, W. Kagawa, and T. Kinebuchi Homologous pairing and ring and filament structure formation activities of the human Xrcc2*Rad51D complex J. Biol. Chem. 277 2002 14315 14320
32. Y. Liu, J.Y. Masson, R. Shah, P. O'Regan, and S.C. West RAD51C is required for Holliday junction processing in mammalian cells Science 303 2004 243 246
33. M.A. Brenneman, B.M. Wagener, C.A. Miller, C. Allen, and J.A. Nickoloff XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination Mol. Cell 10 2002 387 395
34. D.S. Lim, and P. Hasty A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53 Mol. Cell. Biol. 16 1996 7133 7143
35. T. Tsuzuki, Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, and M. Sekiguchi Targeted disruption of the Rad51 gene leads to lethality in embryonic mice Proc. Natl Acad. Sci. USA 93 1996 6236 6240
36. B. Deans, C.S. Griffin, M. Maconochie, and J. Thacker Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice Eur. Mol. Biol. Org. J. 19 2000 6675 6685
37. Z. Shu, S. Smith, L. Wang, M.C. Rice, and E.B. Kmiec Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p53(-/-) background Mol. Cell. Biol. 19 1999 8686 8693
38. D.L. Pittman, and J.C. Schimenti Midgestation lethality in mice deficient for the RecA-related gene, Rad51d/Rad51l3 Genesis 26 2000 167 173
39. E. Sonoda, M.S. Sasaki, J.M. Buerstedde, O. Bezzubova, A. Shinohara, and H. Ogawa Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death Eur. Mol. Biol. Org. J. 17 1998 598 608
40. S.J. Xia, M.A. Shammas, and R.J. Shmookler Reis Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase Mol. Cell. Biol. 17 1997 7151 7158
41. S. Vispe, C. Cazaux, C. Lesca, and M. Defais Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation Nucleic Acids Res. 26 1998 2859 2864
42. C. Arnaudeau, T. Helleday, and D. Jenssen The RAD51 protein supports homologous recombination by an exchange mechanism in mammalian cells J. Mol. Biol. 289 1999 1231 1238
43. S. Lambert, and B.S. Lopez Characterization of mammalian RAD51 double strand break repair using non-lethal dominant-negative forms Eur. Mol. Biol. Org. J. 19 2000 3090 3099
44. P.M. Kim, C. Allen, B.M. Wagener, Z. Shen, and J.A. Nickoloff Overexpression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells Nucleic Acids Res. 29 2001 4352 4360
45. C. Richardson, J.M. Stark, M. Ommundsen, and M. Jasin Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability Oncogene 23 2004 546 553
46. P. Bertrand, S. Lambert, C. Joubert, and B.S. Lopez Overexpression of mammalian Rad51 does not stimulate tumorigenesis while a dominant-negative Rad51 affects centrosome fragmentation, ploidy and stimulates tumorigenesis, in p53-defective CHO cells Oncogene 22 2003 7587 7592
47. B. Deans, C.S. Griffin, P. O'Regan, M. Jasin, and J. Thacker Homologous recombination deficiency leads to profound genetic instability in cells derived from Xrcc2-knockout mice Cancer Res. 63 2003 8181 8187
48. C.S. Griffin, P.J. Simpson, C.R. Wilson, and J. Thacker Mammalian recombination-repair genes XRCC2 and XRCC3 promote correct chromosome segregation Nat. Cell Biol. 2 2000 757 761
49. H.M. Hut, W. Lemstra, E.H. Blaauw, G.W. Van Cappellen, H.H. Kampinga, and O.C. Sibon Centrosomes split in the presence of impaired DNA integrity during mitosis Mol. Biol. Cell 14 2003 1993 2004
50. M. Tarsounas, P. Munoz, A. Claas, P.G. Smiraldo, D.L. Pittman, M.A. Blasco, and S.C. West Telomere maintenance requires the RAD51D recombination/repair protein Cell 117 2004 337 347
51. A.R. Venkitaraman Chromosome stability, DNA recombination and the BRCA2 tumour suppressor Curr. Opin. Cell Biol. 13 2001 338 343
52. M. Kraakman-van der Zwet, W.J. Overkamp, R.E. van Lange, J. Essers, A. van Duijn-Goedhart, and I. Wiggers Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions Mol. Cell. Biol. 22 2002 669 679
53. A. Tutt, A. Gabriel, D. Bertwistle, F. Connor, H. Paterson, and J. Peacock Absence of Brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification Curr. Biol. 9 1999 1107 1110
54. X. Xu, Z. Weaver, S.P. Linke, C. Li, J. Gotay, and X.W. Wang Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells Mol. Cell. 3 1999 389 395
55. M.J. Difilippantonio, J. Zhu, H.T. Chen, E. Meffre, M.C. Nussenzweig, and E.E. Max DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation Nature 404 2000 510 514
56. H.W. Mohrenweiser, D.M. Wilson 3rd, and I.M. Jones Challenges and complexities in estimating both the functional impact and the disease risk associated with the extensive genetic variation in human DNA repair genes Mutat. Res. 526 2003 93 125
57. T. Xi, I.M. Jones, and H.W. Mohrenweiser Many amino acid substitution variants identified in DNA repair genes during human population screenings are predicted to impact protein function Genomics 83 2004 970 979
58. S. Rafii, P. O'Regan, G. Xinarianos, I. Azmy, T. Stephenson, and M. Reed A potential role for the XRCC2 R188H polymorphic site in DNA-damage repair and breast cancer Hum. Mol. Genet. 11 2002 1433 1438
59. F.D. Araujo, A.J. Pierce, J.M. Stark, and M. Jasin Variant XRCC3 implicated in cancer is functional in homology-directed repair of double-strand breaks Oncogene 21 2002 4176 4180
60. S. Rafii, A. Lindblom, M. Reed, M. Meuth, and A. Cox A naturally occurring mutation in an ATP-binding domain of the recombination repair gene XRCC3 ablates its function without causing cancer susceptibility Hum. Mol. Genet. 12 2003 915 923
61. R. Rodriguez-Lopez, A. Osorio, G. Ribas, M. Pollan, L. Sanchez-Pulido, and M. de la Hoya The variant E233G of the RAD51D gene could be a low-penetrance allele in high-risk breast cancer families without BRCA1/2 mutations Int. J. Cancer 110 2004 845 849
62. M. Kato, K. Yano, F. Matsuo, H. Saito, T. Katagiri, and H. Kurumizaka Identification of Rad51 alteration in patients with bilateral breast cancer J. Hum. Genet. 45 2000 133 137
63. W. Wick, I. Petersen, R.K. Schmutzler, B. Wolfarth, D. Lenartz, and E. Bierhoff Evidence for a novel tumor suppressor gene on chromosome 15 associated with progression to a metastatic stage in breast cancer Oncogene 12 1996 973 978
64. R. Gonzalez, J.M. Silva, G. Dominguez, J.M. Garcia, G. Martinez, and J. Vargas Detection of loss of heterozygosity at RAD51, RAD52, RAD54 and BRCA1 and BRCA2 loci in breast cancer: pathological correlations Br. J. Cancer 81 1999 503 509
65. C.Y. Shen, J.C. Yu, Y.L. Lo, C.H. Kuo, C.T. Yue, and Y.S. Jou Genome-wide search for loss of heterozygosity using laser capture microdissected tissue of breast carcinoma: an implication for mutator phenotype and breast cancer pathogenesis Cancer Res. 60 2000 3884 3892
66. C. Schmutte, G. Tombline, K. Rhiem, M.M. Sadoff, R. Schmutzler, A. von Deimling, and R. Fishel Characterization of the human Rad51 genomic locus and examination of tumors with 15q14-15 loss of heterozygosity (LOH) Cancer Res. 59 1999 4564 4569
67. K. Yoshikawa, T. Ogawa, R. Baer, H. Hemmi, K. Honda, and A. Yamauchi Abnormal expression of BRCA1 and BRCA1-interactive DNA-repair proteins in breast carcinomas Int. J. Cancer 88 2000 28 36
68. H. Maacke, S. Opitz, K. Jost, W. Hamdorf, W. Henning, and S. Kruger Over-expression of wild-type Rad51 correlates with histological grading of invasive ductal breast cancer Int. J. Cancer 88 2000 907 913
69. H. Maacke, K. Jost, S. Opitz, S. Miska, Y. Yuan, and L. Hasselbach DNA repair recombination factor Rad51 is over-expressed in human pancreatic adenocarcinoma Oncogene 19 2000 2791 2795
70. H. Han, D.J. Bearss, L.W. Browne, R. Calaluce, R.B. Nagle, and D.D. Von Hoff Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray Cancer Res. 62 2002 2890 2896
71. N.C. Munshi, T. Hideshima, D. Carrasco, M. Shammas, D. Auclair, and F. Davies Identification of genes modulated in multiple myeloma using genetically identical twin samples Blood 103 2004 1799 1806
72. E.F. Schoenmakers, C. Huysmans, and W.J. Van de Ven Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas Cancer Res. 59 1999 19 23
73. S.E. Ingraham, R.A. Lynch, S. Kathiresan, A.J. Buckler, and A.G. Menon hREC2, a RAD51-like gene, is disrupted by t(12;14) (q15;q24.1) in a uterine leiomyoma Cancer Genet. Cytogenet. 115 1999 56 61
74. T. Takahashi, N. Nagai, H. Oda, K. Ohama, N. Kamada, and K. Miyagawa Evidence for RAD51L1/HMGIC fusion in the pathogenesis of uterine leiomyoma Genes Chromosomes Cancer 30 2001 196 201
75. B.J. Quade, S. Weremowicz, D.M. Neskey, R. Vanni, C. Ladd, P. Dal Cin, and C.C. Morton Fusion transcripts involving HMGA2 are not a common molecular mechanism in uterine leiomyomata with rearrangements in 12q15 Cancer Res. 63 2003 1351 1358
76. F. Amant, M. Debiec-Rychter, E.F. Schoenmakers, A. Hagemeijer-Hausman, and I. Vergote Cumulative dosage effect of a RAD51L1/HMGA2 fusion and RAD51L1 loss in a case of pseudo-Meigs' syndrome Genes Chromosomes Cancer 32 2001 324 329
77. C. Blank, E.F. Schoenmakers, P. Rogalla, E.H. Huys, A.A. van Rijk, N. Drieschner, and J. Bullerdiek Intragenic breakpoint within RAD51L1 in a t(6;14)(p21.3;q24) of a pulmonary chondroid hamartoma Cytogenet. Cell Genet. 95 2001 17 19
78. G.J. Wu, C.S. Sinclair, J. Paape, J.N. Ingle, P.C. Roche, C.D. James, and F.J. Couch 17q23 amplifications in breast cancer involve the PAT1, RAD51C, PS6K, and SIGma1B genes Cancer Res. 60 2000 5371 5375
79. M. Barlund, O. Monni, J. Kononen, R. Cornelison, J. Torhorst, and G. Sauter Multiple genes at 17q23 undergo amplification and overexpression in breast cancer Cancer Res. 60 2000 5340 5344
80. A. Mohindra, L.E. Hays, E.N. Phillips, B.D. Preston, T. Helleday, and M. Meuth Defects in homologous recombination repair in mismatch-repair-deficient tumour cell lines Hum. Mol. Genet. 11 2002 2189 2200
81. A. Mohindra, E. Bolderson, J. Stone, M. Wells, T. Helleday, and M. Meuth A tumour-derived mutant allele of XRCC2 preferentially suppresses homologous recombination at DNA replication forks Hum. Mol. Genet. 13 2004 203 212
82. R. Rodriguez-Lopez, A. Osorio, L. Sanchez-Pulido, M. De La Hoya, A. Barroso, T. Caldes, and J. Benitez No mutations in the XRCC2 gene in BRCA1/2-negative high-risk breast cancer families Int. J. Cancer 103 2003 136 137
83. S.N. Agoff, J.E. Mendelin, V.S. Grieco, and R.L. Garcia Unexpected gynecologic neoplasms in patients with proven or suspected BRCA-1 or -2 mutations: implications for gross examination, cytology, and clinical follow-up Am. J. Surg. Pathol. 26 2002 171 178
84. O. Lavie, G. Hornreich, A. Ben-Arie, G. Rennert, Y. Cohen, and R. Keidar BRCA germline mutations in Jewish women with uterine serous papillary carcinoma Gynecol. Oncol. 92 2004 521 524
85. M.E. Moynahan The cancer connection: BRCA1 and BRCA2 tumor suppression in mice and humans Oncogene 21 2002 8994 9007
86. W.W. Wang, A.B. Spurdle, P. Kolachana, B. Bove, B. Modan, and S.M. Ebbers A single nucleotide polymorphism in the 5′ untranslated region of RAD51 and risk of cancer among BRCA1/2 mutation carriers Cancer Epidemiol. Biomarkers Prev. 10 2001 955 960
87. E. Levy-Lahad, A. Lahad, S. Eisenberg, E. Dagan, T. Paperna, and L. Kasinetz A single nucleotide polymorphism in the RAD51 gene modifies cancer risk in BRCA2 but not BRCA1 carriers Proc. Natl Acad. Sci. USA 98 2001 3232 3236
88. L. Kadouri, Z. Kote-Jarai, A. Hubert, F. Durocher, D. Abeliovich, and B. Glaser A single-nucleotide polymorphism in the RAD51 gene modifies breast cancer risk in BRCA2 carriers, but not in BRCA1 carriers or noncarriers Br. J. Cancer 90 2004 2002 2005
89. A. Jakubowska, S.A. Narod, D.E. Goldgar, M. Mierzejewski, B. Masojc, and K. Nej Breast cancer risk reduction associated with the RAD51 polymorphism among carriers of the BRCA1 5382insC mutation in Poland Cancer Epidemiol. Biomarkers Prev. 12 2003 457 459
90. B. Kuschel, A. Auranen, S. McBride, K.L. Novik, A. Antoniou, and J.M. Lipscombe Variants in DNA double-strand break repair genes and breast cancer susceptibility Hum. Mol. Genet. 11 2002 1399 1407
91. J. Han, S.E. Hankinson, S.M. Zhang, I. De Vivo, and D.J. Hunter Interaction between genetic variations in DNA repair genes and plasma folate on breast cancer risk Cancer Epidemiol. Biomarkers Prev. 13 2004 520 524
92. J. Han, S.E. Hankinson, H. Ranu, I. De Vivo, and D.J. Hunter Polymorphisms in DNA double-strand break repair genes and breast cancer risk in the Nurses' Health Study Carcinogenesis 25 2004 189 195
93. J. Han, G.A. Colditz, L.D. Samson, and D.J. Hunter Polymorphisms in DNA double-strand break repair genes and skin cancer risk Cancer Res. 64 2004 3009 3013
94. S.L. Winsey, N.A. Haldar, H.P. Marsh, M. Bunce, S.E. Marshall, and A.L. Harris A variant within the DNA repair gene XRCC3 is associated with the development of melanoma skin cancer Cancer Res. 60 2000 5612 5616
95. G. Matullo, S. Guarrera, S. Carturan, M. Peluso, C. Malaveille, and L. Davico DNA repair gene polymorphisms, bulky DNA adducts in white blood cells and bladder cancer in a case-control study Int. J. Cancer 92 2001 562 567
96. G.L. David-Beabes, R.M. Lunn, and S.J. London No association between the XPD (Lys751G1n) polymorphism or the XRCC3 (Thr241Met) polymorphism and lung cancer risk Cancer Epidemiol. Biomarkers Prev. 10 2001 911 912
97. Z. Duan, H. Shen, J.E. Lee, J.E. Gershenwald, M.I. Ross, and P.F. Mansfield DNA repair gene XRCC3 241Met variant is not associated with risk of cutaneous malignant melanoma Cancer Epidemiol. Biomarkers Prev. 11 2002 1142 1143
98. M.C. Stern, D.M. Umbach, R.M. Lunn, and J.A. Taylor DNA repair gene XRCC3 codon 241 polymorphism, its interaction with smoking and XRCC1 polymorphisms, and bladder cancer risk Cancer Epidemiol. Biomarkers Prev. 11 2002 939 943
99. H. Shen, E.M. Sturgis, K.R. Dahlstrom, Y. Zheng, M.R. Spitz, and Q. Wei A variant of the DNA repair gene XRCC3 and risk of squamous cell carcinoma of the head and neck: a case-control analysis Int. J. Cancer 99 2002 869 872
100. T.R. Smith, M.S. Miller, K. Lohman, E.M. Lange, L.D. Case, H.W. Mohrenweiser, and J.J. Hu Polymorphisms of XRCC1 and XRCC3 genes and susceptibility to breast cancer Cancer Lett. 190 2003 183 190
101. Y. Wang, D. Liang, M.R. Spitz, K. Zhang, Q. Dong, C.I. Amos, and X. Wu XRCC3 genetic polymorphism, smoking, and lung carcinoma risk in minority populations Cancer 98 2003 1701 1706
102. N.R. Jacobsen, B.A. Nexo, A. Olsen, K. Overvad, H. Wallin, A. Tjonneland, and U. Vogel No association between the DNA repair gene XRCC3 T241M polymorphism and risk of skin cancer and breast cancer Cancer Epidemiol. Biomarkers Prev. 12 2003 584 585
103. C.G. Bertram, R.M. Gaut, J.H. Barrett, J. Randerson-Moor, L. Whitaker, and F. Turner An assessment of a variant of the DNA repair gene XRCC3 as a possible nevus or melanoma susceptibility genotype J. Invest. Dermatol. 122 2004 429 432
104. J.C. Figueiredo, J.A. Knight, L. Briollais, I.L. Andrulis, and H. Ozcelik Polymorphisms XRCC1-R399Q and XRCC3-T241M and the risk of breast cancer at the Ontario site of the Breast Cancer Family Registry Cancer Epidemiol. Biomarkers Prev. 13 2004 583 591