Archives of Toxicology

, Volume 90, Issue 10, pp 2369–2388 | Cite as

Single nucleotide polymorphisms in DNA repair genes and putative cancer risk

  • Beate Köberle
  • Barbara Koch
  • Bettina M. Fischer
  • Andrea Hartwig
Review Article


Single nucleotide polymorphisms (SNPs) are the most frequent type of genetic alterations between individuals. An SNP located within the coding sequence of a gene may lead to an amino acid substitution and in turn might alter protein function. Such a change in protein sequence could be functionally relevant and therefore might be associated with susceptibility to human diseases, such as cancer. DNA repair mechanisms are known to play an important role in cancer development, as shown in various human cancer syndromes, which arise due to mutations in DNA repair genes. This leads to the question whether subtle genetic changes such as SNPs in DNA repair genes may contribute to cancer susceptibility. In numerous epidemiological studies, efforts have been made to associate specific SNPs in DNA repair genes with altered DNA repair and cancer. The present review describes some of the common and most extensively studied SNPs in DNA repair genes and discusses whether they are functionally relevant and subsequently increase the likelihood that cancer will develop.


Single nucleotide polymorphism DNA repair mechanisms Repair genes Cancer susceptibility Cancer treatment 



The work was supported by Deutsche Forschungsgemeinschaft (DFG) and Exzellenzinitiative KIT.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abbasi R, Ramroth H, Becher H, Dietz A, Schmezer P, Popanda O (2009) Laryngeal cancer risk associated with smoking and alcohol consumption is modified by genetic polymorphisms in ERCC5, ERCC6 and RAD23B but not by polymorphisms in five other nucleotide excision repair genes. Int J Cancer 125:1431–1439PubMedCrossRefGoogle Scholar
  2. Aboussekhra A, Biggerstaff M, Shivji MK, Vilpo JA, Moncollin V, Podust VN, Protic M, Hubscher U, Egly JM, Wood RD (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80:859–868PubMedCrossRefGoogle Scholar
  3. Alanazi M, Pathan AA, Abduljaleel Z, Shaik JP, Alabdulkarim HA, Semlali A, Bazzi MD, Parine NR (2013) Association between PARP-1 V762A polymorphism and breast cancer susceptibility in Saudi population. PLoS ONE 8:e85541PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allan JM, Smith AG, Wheatley K, Hills RK, Travis LB, Hill DA, Swirsky DM, Morgan GJ, Wild CP (2004) Genetic variation in XPD predicts treatment outcome and risk of acute myeloid leukemia following chemotherapy. Blood 104:3872–3877PubMedCrossRefGoogle Scholar
  5. Almeida KH, Sobol RW (2007) A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair (Amst) 6:695–711CrossRefGoogle Scholar
  6. Batar B, Guven M, Baris S, Celkan T, Yildiz I (2009) DNA repair gene XPD and XRCC1 polymorphisms and the risk of childhood acute lymphoblastic leukemia. Leuk Res 33:759–763PubMedCrossRefGoogle Scholar
  7. Batty DP, Wood RD (2000) Damage recognition in nucleotide excision repair of DNA. Gene 241:193–204PubMedCrossRefGoogle Scholar
  8. Baynes C, Healey CS, Pooley KA, Scollen S, Luben RN, Thompson DJ, Pharoah PD, Easton DF, Ponder BA, Dunning AM (2007) Common variants in the ATM, BRCA1, BRCA2, CHEK2 and TP53 cancer susceptibility genes are unlikely to increase breast cancer risk. Breast Cancer Res 9:R27PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beck C, Robert I, Reina-San-Martin B, Schreiber V, Dantzer F (2014) Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp Cell Res 329:18–25PubMedCrossRefGoogle Scholar
  10. Benhamou S, Sarasin A (2002) ERCC2/XPD gene polymorphisms and cancer risk. Mutagenesis 17:463–469PubMedCrossRefGoogle Scholar
  11. Berhane N, Sobti RC, Mahdi SA (2012) DNA repair genes polymorphism (XPG and XRCC1) and association of prostate cancer in a north Indian population. Mol Biol Rep 39:2471–2479PubMedCrossRefGoogle Scholar
  12. Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, Goodarzi AA, Krempler A, Jeggo PA, Lobrich M (2009) ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J 28:3413–3427PubMedPubMedCentralCrossRefGoogle Scholar
  13. Biggerstaff M, Szymkowski DE, Wood RD (1993) Co-correction of the ERCC1, ERCC4 and xeroderma pigmentosum group F DNA repair defects in vitro. EMBO J 12:3685–3692PubMedPubMedCentralGoogle Scholar
  14. Broughton BC, Steingrimsdottir H, Lehmann AR (1996) 5 polymorphisms in the coding sequence of the xeroderma pigmentosum group D gene. Mutat Res DNA Repair 362:209–211PubMedCrossRefGoogle Scholar
  15. Butkiewicz D, Rusin M, Harris CC, Chorazy M (2000) Identification of four single nucleotide polymorphisms in DNA repair genes: XPA and XPB (ERCC3) in Polish population. Hum Mutat 15:577–578PubMedCrossRefGoogle Scholar
  16. Butkiewicz D, Rusin M, Enewold L, Shields PG, Chorazy M, Harris CC (2001) Genetic polymorphisms in DNA repair genes and risk of lung cancer. Carcinogenesis 22:593–597PubMedCrossRefGoogle Scholar
  17. Butkiewicz D, Popanda O, Risch A, Edler L, Dienemann H, Schulz V, Kayser K, Drings P, Bartsch H, Schmezer P (2004) Association between the risk for lung adenocarcinoma and a (−4) G-to-A polymorphism in the XPA gene. Cancer Epidemiol Biomark Prev 13:2242–2246Google Scholar
  18. Butkiewicz D, Krzesniak M, Vaitiekunaite R, Sikora B, Bowman ED, Harris CC, Rusin M (2010) A functional analysis of G23A polymorphism and the alternative splicing in the expression of the XPA gene. Cell Mol Biol Lett 15:611–629PubMedCrossRefGoogle Scholar
  19. Butkiewicz D, Rusin M, Sikora B, Lach A, Chorazy M (2011) An association between DNA repair gene polymorphisms and survival in patients with resected non-small cell lung cancer. Mol Biol Rep 38:5231–5241PubMedCrossRefGoogle Scholar
  20. Cao Y, Miao XP, Huang MY, Deng L, Hu LF, Ernberg I, Zeng YX, Lin DX, Shao JY (2006) Polymorphisms of XRCC1 genes and risk of nasopharyngeal carcinoma in the Cantonese population. BMC Cancer 6:167PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cavanagh H, Rogers KM (2015) The role of BRCA1 and BRCA2 mutations in prostate, pancreatic and stomach cancers. Hered Cancer Clin Pract 13:16PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chang CH, Chang CL, Tsai CW, Wu HC, Chiu CF, Wang RF, Liu CS, Lin CC, Bau DT (2009) Significant association of an XRCC4 single nucleotide polymorphism with bladder cancer susceptibility in Taiwan. Anticancer Res 29:1777–1782PubMedGoogle Scholar
  23. Clarkson SG, Wood RD (2005) Polymorphisms in the human XPD (ERCC2) gene, DNA repair capacity and cancer susceptibility: an appraisal. DNA Repair (Amst) 4:1068–1074CrossRefGoogle Scholar
  24. Cleaver JE (2005) Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat Rev Cancer 5:564–573PubMedCrossRefGoogle Scholar
  25. Coin F, Oksenych V, Egly JM (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell 26:245–256PubMedCrossRefGoogle Scholar
  26. Cottet F, Blanche H, Verasdonck P, Le Gall I, Schachter F, Burkle A, Muiras ML (2000) New polymorphisms in the human poly(ADP-ribose) polymerase-1 coding sequence: lack of association with longevity or with increased cellular poly(ADP-ribosyl)ation capacity. J Mol Med (Berl) 78:431–440CrossRefGoogle Scholar
  27. Cui Y, Morgenstern H, Greenland S, Tashkin DP, Mao J, Cao W, Cozen W, Mack TM, Zhang ZF (2006) Polymorphism of xeroderma pigmentosum group G and the risk of lung cancer and squamous cell carcinomas of the oropharynx, larynx and esophagus. Int J Cancer 118:714–720PubMedCrossRefGoogle Scholar
  28. Custodio AC, Almeida LO, Pinto GR, Santos MJ, Almeida JR, Clara CA, Rey JA, Casartelli C (2012) Variation in DNA repair gene XRCC3 affects susceptibility to astrocytomas and glioblastomas. Genet Mol Res 11:332–339PubMedCrossRefGoogle Scholar
  29. Danoy P, Sonoda E, Lathrop M, Takeda S, Matsuda F (2007) A naturally occurring genetic variant of human XRCC2 (R188H) confers increased resistance to cisplatin-induced DNA damage. Biochem Biophys Res Commun 352:763–768PubMedCrossRefGoogle Scholar
  30. David-Beabes GL, Lunn RM, London SJ (2001) No association between the XPD (Lys751G1n) polymorphism or the XRCC3 (Thr241 Met) polymorphism and lung cancer risk. Cancer Epidemiol Biomarkers Prev 10:911–912PubMedGoogle Scholar
  31. Davies AA, Masson JY, McIlwraith MJ, Stasiak AZ, Stasiak A, Venkitaraman AR, West SC (2001) Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol Cell 7:273–282PubMedCrossRefGoogle Scholar
  32. Davis AJ, Chen DJ (2013) DNA double strand break repair via non-homologous end-joining. Transl Cancer Res 2:130–143PubMedPubMedCentralGoogle Scholar
  33. de Laat WL, Jaspers NGJ, Hoeijmakers JHJ (1999) Molecular mechanism of nucleotide excision repair. Genes Dev 13:768–785PubMedCrossRefGoogle Scholar
  34. De Ruyck K, Szaumkessel M, De Rudder I, Dehoorne A, Vral A, Claes K, Velghe A, Van Meerbeeck J, Thierens H (2007) Polymorphisms in base-excision repair and nucleotide-excision repair genes in relation to lung cancer risk. Mutat Res 631:101–110PubMedCrossRefGoogle Scholar
  35. De Vos M, Schreiber V, Dantzer F (2012) The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem Pharmacol 84:137–146PubMedCrossRefGoogle Scholar
  36. Dherin C, Radicella JP, Dizdaroglu M, Boiteux S (1999) Excision of oxidatively damaged DNA bases by the human alpha-hOgg1 protein and the polymorphic alpha-hOgg1(Ser326Cys) protein which is frequently found in human populations. Nucleic Acids Res 27:4001–4007PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ding DP, He XF, Zhang Y (2011) Lack of association between XPG Asp1104His and XPF Arg415Gln polymorphism and breast cancer risk: a meta-analysis of case-control studies. Breast Cancer Res Treat 129:203–209PubMedCrossRefGoogle Scholar
  38. Duan WX, Hua RX, Yi W, Shen LJ, Jin ZX, Zhao YH, Yi DH, Chen WS, Yu SQ (2012) The association between OGG1 Ser326Cys polymorphism and lung cancer susceptibility: a meta-analysis of 27 studies. PLoS ONE 7:e35970PubMedPubMedCentralCrossRefGoogle Scholar
  39. Emmert S, Schneider TD, Khan SG, Kraemer KH (2001) The human XPG gene: gene architecture, alternative splicing and single nucleotide polymorphisms. Nucleic Acids Res 29:1443–1452PubMedPubMedCentralCrossRefGoogle Scholar
  40. Eustermann S, Videler H, Yang JC, Cole PT, Gruszka D, Veprintsev D, Neuhaus D (2011) The DNA-binding domain of human PARP-1 interacts with DNA single-strand breaks as a monomer through its second zinc finger. J Mol Biol 407:149–170PubMedPubMedCentralCrossRefGoogle Scholar
  41. Evans E, Fellows J, Coffer A, Wood RD (1997a) Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein. EMBO J 16:625–638PubMedPubMedCentralCrossRefGoogle Scholar
  42. Evans E, Moggs JG, Hwang JR, Egly J-M, Wood RD (1997b) Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J 16:6559–6573PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fang F, Wang J, Yao L, Yu XJ, Yu L (2011) Relationship between XRCC3 T241M polymorphism and gastric cancer risk: a meta-analysis. Med Oncol 28:999–1003PubMedCrossRefGoogle Scholar
  44. Feng J, Sun X, Sun N, Qin S, Li F, Cheng H, Chen B, Cao Y, Ma J, Cheng L, Lu Z, Ji J, Zhou Y (2009) XPA A23G polymorphism is associated with the elevated response to platinum-based chemotherapy in advanced non-small cell lung cancer. Acta Biochim Biophys Sin (Shanghai) 41:429–435CrossRefGoogle Scholar
  45. Figueroa JD, Malats N, Rothman N, Real FX, Silverman D, Kogevinas M, Chanock S, Yeager M, Welch R, Dosemeci M, Tardon A, Serra C, Carrato A, Garcia-Closas R, Castano-Vinyals G, Garcia-Closas M (2007) Evaluation of genetic variation in the double-strand break repair pathway and bladder cancer risk. Carcinogenesis 28:1788–1793PubMedCrossRefGoogle Scholar
  46. Fousteri M, Mullenders LH (2008) Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18:73–84PubMedCrossRefGoogle Scholar
  47. Freedman ML, Penney KL, Stram DO, Le Marchand L, Hirschhorn JN, Kolonel LN, Altshuler D, Henderson BE, Haiman CA (2004) Common variation in BRCA2 and breast cancer risk: a haplotype-based analysis in the multiethnic cohort. Hum Mol Genet 13:2431–2441PubMedCrossRefGoogle Scholar
  48. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2005) DNA repair and mutagenesis. ASM Press, Washington, DCGoogle Scholar
  49. Fu YP, Yu JC, Cheng TC, Lou MA, Hsu GC, Wu CY, Chen ST, Wu HS, Wu PE, Shen CY (2003) Breast cancer risk associated with genotypic polymorphism of the nonhomologous end-joining genes: a multigenic study on cancer susceptibility. Cancer Res 63:2440–2446PubMedGoogle Scholar
  50. Garcia-Closas M, Egan KM, Newcomb PA, Brinton LA, Titus-Ernstoff L, Chanock S, Welch R, Lissowska J, Peplonska B, Szeszenia-Dabrowska N, Zatonski W, Bardin-Mikolajczak A, Struewing JP (2006) Polymorphisms in DNA double-strand break repair genes and risk of breast cancer: two population-based studies in USA and Poland, and meta-analyses. Hum Genet 119:376–388PubMedCrossRefGoogle Scholar
  51. Giglia-Mari G, Coin F, Ranish JA, Hoogstraten D, Theil A, Wijgers N, Jaspers NG, Raams A, Argentini M, van der Spek PJ, Botta E, Stefanini M, Egly JM, Aebersold R, Hoeijmakers JH, Vermeulen W (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 36:714–719PubMedCrossRefGoogle Scholar
  52. Gil J, Ramsey D, Stembalska A, Karpinski P, Pesz KA, Laczmanska I, Leszczynski P, Grzebieniak Z, Sasiadek MM (2012) The C/A polymorphism in intron 11 of the XPC gene plays a crucial role in the modulation of an individual’s susceptibility to sporadic colorectal cancer. Mol Biol Rep 39:527–534PubMedCrossRefGoogle Scholar
  53. Gresner P, Gromadzinska J, Polanska K, Twardowska E, Jurewicz J, Wasowicz W (2012) Genetic variability of Xrcc3 and Rad51 modulates the risk of head and neck cancer. Gene 504:166–174PubMedCrossRefGoogle Scholar
  54. Guo W, Zhou RM, Wan LL, Wang N, Li Y, Zhang XJ, Dong XJ (2008) Polymorphisms of the DNA repair gene xeroderma pigmentosum groups A and C and risk of esophageal squamous cell carcinoma in a population of high incidence region of North China. J Cancer Res Clin Oncol 134:263–270PubMedCrossRefGoogle Scholar
  55. Gurubhagavatula S, Liu G, Park S, Zhou W, Su L, Wain JC, Lynch TJ, Neuberg DS, Christiani DC (2004) XPD and XRCC1 genetic polymorphisms are prognostic factors in advanced non-small-cell lung cancer patients treated with platinum chemotherapy. J Clin Oncol 22:2594–2601PubMedCrossRefGoogle Scholar
  56. Haber JE (2000) Partners and pathwaysrepairing a double-strand break. Trends Genet 16:259–264PubMedCrossRefGoogle Scholar
  57. Hamann I, Schwerdtle T, Hartwig A (2009) Establishment of a non-radioactive cleavage assay to assess the DNA repair capacity towards oxidatively damaged DNA in subcellular and cellular systems and the impact of copper. Mutat Res 669:122–130PubMedCrossRefGoogle Scholar
  58. Han S, Zhang HT, Wang Z, Xie Y, Tang R, Mao Y, Li Y (2006) DNA repair gene XRCC3 polymorphisms and cancer risk: a meta-analysis of 48 case-control studies. Eur J Hum Genet 14:1136–1144PubMedCrossRefGoogle Scholar
  59. Hao B, Wang H, Zhou K, Li Y, Chen X, Zhou G, Zhu Y, Miao X, Tan W, Wei Q, Lin D, He F (2004) Identification of genetic variants in base excision repair pathway and their associations with risk of esophageal squamous cell carcinoma. Cancer Res 64:4378–4384PubMedCrossRefGoogle Scholar
  60. Hao B, Miao X, Li Y, Zhang X, Sun T, Liang G, Zhao Y, Zhou Y, Wang H, Chen X, Zhang L, Tan W, Wei Q, Lin D, He F (2006) A novel T-77C polymorphism in DNA repair gene XRCC1 contributes to diminished promoter activity and increased risk of non-small cell lung cancer. Oncogene 25:3613–3620PubMedCrossRefGoogle Scholar
  61. Hayden PJ, Tewari P, Morris DW, Staines A, Crowley D, Nieters A, Becker N, de Sanjose S, Foretova L, Maynadie M, Cocco PL, Boffetta P, Brennan P, Chanock SJ, Browne PV, Lawler M (2007) Variation in DNA repair genes XRCC3, XRCC4, XRCC5 and susceptibility to myeloma. Hum Mol Genet 16:3117–3127PubMedCrossRefGoogle Scholar
  62. He X, Ye F, Zhang J, Cheng Q, Shen J, Chen H (2008) Susceptibility of XRCC3, XPD, and XPG genetic variants to cervical carcinoma. Pathobiology 75:356–363PubMedCrossRefGoogle Scholar
  63. He XF, Wei W, Su J, Yang ZX, Liu Y, Zhang Y, Ding DP, Wang W (2012) Association between the XRCC3 polymorphisms and breast cancer risk: meta-analysis based on case-control studies. Mol Biol Rep 39:5125–5134PubMedCrossRefGoogle Scholar
  64. Healey CS, Dunning AM, Teare MD, Chase D, Parker L, Burn J, Chang-Claude J, Mannermaa A, Kataja V, Huntsman DG, Pharoah PD, Luben RN, Easton DF, Ponder BA (2000) A common variant in BRCA2 is associated with both breast cancer risk and prenatal viability. Nat Genet 26:362–364PubMedCrossRefGoogle Scholar
  65. Ho T, Li G, Lu J, Zhao C, Wei Q, Sturgis EM (2007) X-ray repair cross-complementing group 1 (XRCC1) single-nucleotide polymorphisms and the risk of salivary gland carcinomas. Cancer 110:318–325PubMedCrossRefGoogle Scholar
  66. Hochegger H, Dejsuphong D, Fukushima T, Morrison C, Sonoda E, Schreiber V, Zhao GY, Saberi A, Masutani M, Adachi N, Koyama H, de Murcia G, Takeda S (2006) Parp-1 protects homologous recombination from interference by Ku and ligase IV in vertebrate cells. EMBO J 25:1305–1314PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475–1485PubMedCrossRefGoogle Scholar
  68. Hu JJ, Smith TR, Miller MS, Mohrenweiser HW, Golden A, Case LD (2001) Amino acid substitution variants of APE1 and XRCC1 genes associated with ionizing radiation sensitivity. Carcinogenesis 22:917–922PubMedCrossRefGoogle Scholar
  69. Hu Z, Wei Q, Wang X, Shen H (2004) DNA repair gene XPD polymorphism and lung cancer risk: a meta-analysis. Lung Cancer 46:1–10PubMedCrossRefGoogle Scholar
  70. Hu Z, Wang Y, Wang X, Liang G, Miao X, Xu Y, Tan W, Wei Q, Lin D, Shen H (2005) DNA repair gene XPC genotypes/haplotypes and risk of lung cancer in a Chinese population. Int J Cancer 115:478–483PubMedCrossRefGoogle Scholar
  71. Hu YY, Yuan H, Jiang GB, Chen N, Wen L, Leng WD, Zeng XT, Niu YM (2012) Associations between XPD Asp312Asn polymorphism and risk of head and neck cancer: a meta-analysis based on 7,122 subjects. PLoS ONE 7:e35220PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hung RJ, Brennan P, Canzian F, Szeszenia-Dabrowska N, Zaridze D, Lissowska J, Rudnai P, Fabianova E, Mates D, Foretova L, Janout V, Bencko V, Chabrier A, Borel S, Hall J, Boffetta P (2005) Large-scale investigation of base excision repair genetic polymorphisms and lung cancer risk in a multicenter study. J Natl Cancer Inst 97:567–576PubMedCrossRefGoogle Scholar
  73. Hung RJ, Christiani DC, Risch A, Popanda O, Haugen A, Zienolddiny S, Benhamou S, Bouchardy C, Lan Q, Spitz MR, Wichmann HE, LeMarchand L, Vineis P, Matullo G, Kiyohara C, Zhang ZF, Pezeshki B, Harris C, Mechanic L, Seow A, Ng DP, Szeszenia-Dabrowska N, Zaridze D, Lissowska J, Rudnai P, Fabianova E, Mates D, Foretova L, Janout V, Bencko V, Caporaso N, Chen C, Duell EJ, Goodman G, Field JK, Houlston RS, Hong YC, Landi MT, Lazarus P, Muscat J, McLaughlin J, Schwartz AG, Shen H, Stucker I, Tajima K, Matsuo K, Thun M, Yang P, Wiencke J, Andrew AS, Monnier S, Boffetta P, Brennan P (2008) International Lung Cancer Consortium: pooled analysis of sequence variants in DNA repair and cell cycle pathways. Cancer Epidemiol Biomark Prev 17:3081–3089CrossRefGoogle Scholar
  74. Hussien YM, Gharib AF, Awad HA, Karam RA, Elsawy WH (2012) Impact of DNA repair genes polymorphism (XPD and XRCC1) on the risk of breast cancer in Egyptian female patients. Mol Biol Rep 39:1895–1901PubMedCrossRefGoogle Scholar
  75. Ishitobi M, Miyoshi Y, Ando A, Hasegawa S, Egawa C, Tamaki Y, Monden M, Noguchi S (2003) Association of BRCA2 polymorphism at codon 784 (Met/Val) with breast cancer risk and prognosis. Clin Cancer Res 9:1376–1380PubMedGoogle Scholar
  76. Janik J, Swoboda M, Janowska B, Ciesla JM, Gackowski D, Kowalewski J, Olinski R, Tudek B, Speina E (2011) 8-Oxoguanine incision activity is impaired in lung tissues of NSCLC patients with the polymorphism of OGG1 and XRCC1 genes. Mutat Res 709–710:21–31PubMedCrossRefGoogle Scholar
  77. Janssen K, Schlink K, Gotte W, Hippler B, Kaina B, Oesch F (2001) DNA repair activity of 8-oxoguanine DNA glycosylase 1 (OGG1) in human lymphocytes is not dependent on genetic polymorphism Ser326/Cys326. Mutat Res 486:207–216PubMedCrossRefGoogle Scholar
  78. Jeon HS, Kim KM, Park SH, Lee SY, Choi JE, Lee GY, Kam S, Park RW, Kim IS, Kim CH, Jung TH, Park JY (2003) Relationship between XPG codon 1104 polymorphism and risk of primary lung cancer. Carcinogenesis 24:1677–1681PubMedCrossRefGoogle Scholar
  79. Jiao X, Ren J, Chen H, Ma J, Rao S, Huang K, Wu S, Fu J, Su X, Luo C, Shi J, Broelsch CE (2011) Ala499Val (C>T) and Lys939Gln (A>C) polymorphisms of the XPC gene: their correlation with the risk of primary gallbladder adenocarcinoma—a case–control study in China. Carcinogenesis 32:496–501PubMedCrossRefGoogle Scholar
  80. Jin T, Wang Y, Li G, Du S, Yang H, Geng T, Hou P, Gong Y (2015) Analysis of difference of association between polymorphisms in the XRCC5, RPA3 and RTEL1 genes and glioma, astrocytoma and glioblastoma. Am J Cancer Res 5:2294–2300PubMedPubMedCentralGoogle Scholar
  81. Jorgensen TJ, Visvanathan K, Ruczinski I, Thuita L, Hoffman S, Helzlsouer KJ (2007) Breast cancer risk is not associated with polymorphic forms of xeroderma pigmentosum genes in a cohort of women from Washington County, Maryland. Breast Cancer Res Treat 101:65–71PubMedCrossRefGoogle Scholar
  82. Jungmichel S, Rosenthal F, Altmeyer M, Lukas J, Hottiger MO, Nielsen ML (2013) Proteome-wide identification of poly(ADP-ribosyl)ation targets in different genotoxic stress responses. Mol Cell 52:272–285PubMedCrossRefGoogle Scholar
  83. Kakarougkas A, Jeggo PA (2014) DNA DSB repair pathway choice: an orchestrated handover mechanism. Br J Radiol 87:20130685PubMedPubMedCentralCrossRefGoogle Scholar
  84. Kang SY, Lee KG, Lee W, Shim JY, Ji SI, Chung KW, Chung YK, Kim NK (2007) Polymorphisms in the DNA repair gene XRCC1 associated with basal cell carcinoma and squamous cell carcinoma of the skin in a Korean population. Cancer Sci 98:716–720PubMedCrossRefGoogle Scholar
  85. Khan SG, Metter EJ, Tarone RE, Bohr VA, Grossman L, Hedayati M, Bale SJ, Emmert S, Kraemer KH (2000) A new xeroderma pigmentosum group C poly(AT) insertion/deletion polymorphism. Carcinogenesis 21:1821–1825PubMedCrossRefGoogle Scholar
  86. Kim YJ, Wilson DM 3rd (2012) Overview of base excision repair biochemistry. Curr Mol Pharmacol 5:3–13PubMedPubMedCentralCrossRefGoogle Scholar
  87. King MC, Marks JH, Mandell JB (2003) Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 302:643–646PubMedCrossRefGoogle Scholar
  88. Kiyohara C, Yoshimasu K (2007) Genetic polymorphisms in the nucleotide excision repair pathway and lung cancer risk: a meta-analysis. Int J Med Sci 4:59–71PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ko HL, Ren EC (2012) Functional aspects of PARP1 in DNA repair and transcription. Biomolecules 2:524–548PubMedPubMedCentralCrossRefGoogle Scholar
  90. Köberle B, Grimaldi KA, Sunters A, Hartley JA, Kelland LR, Masters JR (1997) DNA repair capacity and cisplatin sensitivity of human testis tumour cells. Int J Cancer 70:551–555PubMedCrossRefGoogle Scholar
  91. Köberle B, Wittschieben J, Wood RD (2005) DNA repair and cancer. In: Knowles M, Selby PJ (eds) Cellular and molecular biology of cancer. Oxford University Press, OxfordGoogle Scholar
  92. Köberle B, Roginskaya V, Wood RD (2006) XPA protein as a limiting factor for nucleotide excision repair and UV sensitivity in human cells. DNA Repair 5:641–648PubMedCrossRefGoogle Scholar
  93. Kohno T, Shinmura K, Tosaka M, Tani M, Kim SR, Sugimura H, Nohmi T, Kasai H, Yokota J (1998) Genetic polymorphisms and alternative splicing of the hOGG1 gene, that is involved in the repair of 8-hydroxyguanine in damaged DNA. Oncogene 16:3219–3225PubMedCrossRefGoogle Scholar
  94. Kozak M (1996) Interpreting cDNA sequences: some insights from studies on translation. Mamm Genome 7:563–574PubMedCrossRefGoogle Scholar
  95. Krejci L, Altmannova V, Spirek M, Zhao X (2012) Homologous recombination and its regulation. Nucleic Acids Res 40:5795–5818PubMedPubMedCentralCrossRefGoogle Scholar
  96. Krokan HE, Bjoras M (2013) Base excision repair. Cold Spring Harb Perspect Biol 5:a012583PubMedPubMedCentralCrossRefGoogle Scholar
  97. Krupa R, Sliwinski T, Wisniewska-Jarosinska M, Chojnacki J, Wasylecka M, Dziki L, Morawiec J, Blasiak J (2011) Polymorphisms in RAD51, XRCC2 and XRCC3 genes of the homologous recombination repair in colorectal cancer—a case control study. Mol Biol Rep 38:2849–2854PubMedCrossRefGoogle Scholar
  98. Kumar R, Hoglund L, Zhao C, Forsti A, Snellman E, Hemminki K (2003) Single nucleotide polymorphisms in the XPG gene: determination of role in DNA repair and breast cancer risk. Int J Cancer 103:671–675PubMedCrossRefGoogle Scholar
  99. Kuschel B, Chenevix-Trench G, Spurdle AB, Chen X, Hopper JL, Giles GG, McCredie M, Chang-Claude J, Gregory CS, Day NE, Easton DF, Ponder BA, Dunning AM, Pharoah PD (2005) Common polymorphisms in ERCC2 (xeroderma pigmentosum D) are not associated with breast cancer risk. Cancer Epidemiol Biomark Prev 14:1828–1831CrossRefGoogle Scholar
  100. Laine JP, Mocquet V, Bonfanti M, Braun C, Egly JM, Brousset P (2007) Common XPD (ERCC2) polymorphisms have no measurable effect on nucleotide excision repair and basal transcription. DNA Repair (Amst) 6:1264–1270CrossRefGoogle Scholar
  101. Langelier MF, Pascal JM (2013) PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol 23:134–143PubMedPubMedCentralCrossRefGoogle Scholar
  102. Le Marchand L, Donlon T, Lum-Jones A, Seifried A, Wilkens LR (2002) Association of the hOGG1 Ser326Cys polymorphism with lung cancer risk. Cancer Epidemiol Biomark Prev 11:409–412Google Scholar
  103. Lee GY, Jang JS, Lee SY, Jeon HS, Kim KM, Choi JE, Park JM, Chae MH, Lee WK, Kam S, Kim IS, Lee JT, Jung TH, Park JY (2005) XPC polymorphisms and lung cancer risk. Int J Cancer 115:807–813PubMedCrossRefGoogle Scholar
  104. Lehmann AR (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85:1101–1111PubMedCrossRefGoogle Scholar
  105. Li R, Yang Y, An Y, Zhou Y, Liu Y, Yu Q, Lu D, Wang H, Jin L, Zhou W, Qian J, Shugart YY (2011) Genetic polymorphisms in DNA double-strand break repair genes XRCC5, XRCC6 and susceptibility to hepatocellular carcinoma. Carcinogenesis 32:530–536PubMedCrossRefGoogle Scholar
  106. Li F, Wang J, Chen M (2016) Single nucleotide polymorphisms in DNA repair genes and the risk of laryngeal cancer: a meta-analysis. Biomed Pharmacother 78:92–100PubMedCrossRefGoogle Scholar
  107. Liang G, Xing D, Miao X, Tan W, Yu C, Lu W, Lin D (2003) Sequence variations in the DNA repair gene XPD and risk of lung cancer in a Chinese population. Int J Cancer 105:669–673PubMedCrossRefGoogle Scholar
  108. Lindahl T (2000) Suppression of spontaneous mutagenesis in human cells by DNA base excision-repair. Mutat Res Rev Mutat Res 462:129–135CrossRefGoogle Scholar
  109. Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286:1897–1905PubMedCrossRefGoogle Scholar
  110. Liu N, Lamerdin JE, Tebbs RS, Schild D, Tucker JD, Shen MR, Brookman KW, Siciliano MJ, Walter CA, Fan WF, Narayana LS, Zhou ZQ, Adamson AW, Sorensen KJ, Chen DJ, Jones NJ, Thompson LH (1998) XRCC2 and XRCC3, new human RAD51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol Cell 1:783–793PubMedCrossRefGoogle Scholar
  111. Liu J, Zhang Z, Cao XL, Lei DP, Wang ZQ, Jin T, Pan XL (2012) XPA A23G polymorphism and susceptibility to cancer: a meta-analysis. Mol Biol Rep 39:6791–6799PubMedCrossRefGoogle Scholar
  112. Lockett KL, Hall MC, Xu J, Zheng SL, Berwick M, Chuang SC, Clark PE, Cramer SD, Lohman K, Hu JJ (2004) The ADPRT V762A genetic variant contributes to prostate cancer susceptibility and deficient enzyme function. Cancer Res 64:6344–6348PubMedCrossRefGoogle Scholar
  113. Lockett KL, Snowhite IV, Hu JJ (2005) Nucleotide-excision repair and prostate cancer risk. Cancer Lett 220:125–135PubMedCrossRefGoogle Scholar
  114. Loizidou MA, Michael T, Neuhausen SL, Newbold RF, Marcou Y, Kakouri E, Daniel M, Papadopoulos P, Malas S, Hadjisavvas A, Kyriacou K (2009) DNA-repair genetic polymorphisms and risk of breast cancer in Cyprus. Breast Cancer Res Treat 115:623–627PubMedCrossRefGoogle Scholar
  115. Lopes-Aguiar L, Costa EF, Nogueira GA, Lima TR, Visacri MB, Pincinato EC, Calonga L, Mariano FV, Altemani AM, Altemani JM, Coutinho-Camillo CM, Alves MA, Moriel P, Ramos CD, Chone CT, Lima CS (2016) XPD c.934G>A polymorphism of nucleotide excision repair pathway in outcome of head and neck squamous cell carcinoma patients treated with cisplatin chemoradiation. Oncotarget. doi: 10.18632/oncotarget.7668 PubMedGoogle Scholar
  116. Lunn RM, Langlois RG, Hsieh LL, Thompson CL, Bell DA (1999) XRCC1 polymorphisms: effects on aflatoxin B1-DNA adducts and glycophorin A variant frequency. Cancer Res 59:2557–2561PubMedGoogle Scholar
  117. Mari PO, Florea BI, Persengiev SP, Verkaik NS, Bruggenwirth HT, Modesti M, Giglia-Mari G, Bezstarosti K, Demmers JA, Luider TM, Houtsmuller AB, van Gent DC (2006) Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc Natl Acad Sci USA 103:18597–18602PubMedPubMedCentralCrossRefGoogle Scholar
  118. Marin MS, Lopez-Cima MF, Garcia-Castro L, Pascual T, Marron MG, Tardon A (2004) Poly (AT) polymorphism in intron 11 of the XPC DNA repair gene enhances the risk of lung cancer. Cancer Epidemiol Biomark Prev 13:1788–1793Google Scholar
  119. Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JH (2014) Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol 15:465–481PubMedCrossRefGoogle Scholar
  120. Martin AM, Weber BL (2000) Genetic and hormonal risk factors in breast cancer. J Natl Cancer Inst 92:1126–1135PubMedCrossRefGoogle Scholar
  121. Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enomoto T, Takio K, Tanaka K, van der Spek PJ, Bootsma D, Hoeijmakers JHJ, Hanaoka F (1994) Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J 13:1831–1843PubMedPubMedCentralGoogle Scholar
  122. Matsumura Y, Nishigori C, Yagi T, Imamura S, Takebe H (1998) Characterization of molecular defects in xeroderma pigmentosum group F in relation to its clinically mild symptoms. Hum Mol Genet 7:969–974PubMedCrossRefGoogle Scholar
  123. Matullo G, Guarrera S, Carturan S, Peluso M, Malaveille C, Davico L, Piazza A, Vineis P (2001a) DNA repair gene polymorphisms, bulky DNA adducts in white blood cells and bladder cancer in a case-control study. Int J Cancer 92:562–567PubMedCrossRefGoogle Scholar
  124. Matullo G, Palli D, Peluso M, Guarrera S, Carturan S, Celentano E, Krogh V, Munnia A, Tumino R, Polidoro S, Piazza A, Vineis P (2001b) XRCC1, XRCC3, XPD gene polymorphisms, smoking and (32)P-DNA adducts in a sample of healthy subjects. Carcinogenesis 22:1437–1445PubMedCrossRefGoogle Scholar
  125. McKean-Cowdin R, Barnholtz-Sloan J, Inskip PD, Ruder AM, Butler M, Rajaraman P, Razavi P, Patoka J, Wiencke JK, Bondy ML, Wrensch M (2009) Associations between polymorphisms in DNA repair genes and glioblastoma. Cancer Epidemiol Biomark Prev 18:1118–1126CrossRefGoogle Scholar
  126. Mellon I, Hock T, Reid R, Porter PC, States JC (2002) Polymorphisms in the human xeroderma pigmentosum group A gene and their impact on cell survival and nucleotide excision repair. DNA Repair (Amst) 1:531–546CrossRefGoogle Scholar
  127. Miller KL, Karagas MR, Kraft P, Hunter DJ, Catalano PJ, Byler SH, Nelson HH (2006) XPA, haplotypes, and risk of basal and squamous cell carcinoma. Carcinogenesis 27:1670–1675PubMedCrossRefGoogle Scholar
  128. Mohrenweiser HW, Xi T, Vazquez-Matias J, Jones IM (2002) Identification of 127 amino acid substitution variants in screening 37 DNA repair genes in humans. Cancer Epidemiol Biomark Prev 11:1054–1064Google Scholar
  129. Mort R, Mo L, McEwan C, Melton DW (2003) Lack of involvement of nucleotide excision repair gene polymorphisms in colorectal cancer. Br J Cancer 89:333–337PubMedPubMedCentralCrossRefGoogle Scholar
  130. Moser J, Kool H, Giakzidis I, Caldecott K, Mullenders LH, Fousteri MI (2007) Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol Cell 27:311–323PubMedCrossRefGoogle Scholar
  131. Mutamba JT, Svilar D, Prasongtanakij S, Wang XH, Lin YC, Dedon PC, Sobol RW, Engelward BP (2011) XRCC1 and base excision repair balance in response to nitric oxide. DNA Repair (Amst) 10:1282–1293CrossRefGoogle Scholar
  132. Ng PC, Henikoff S (2002) Accounting for human polymorphisms predicted to affect protein function. Genome Res 12:436–446PubMedPubMedCentralCrossRefGoogle Scholar
  133. Nouspikel T (2009) DNA repair in mammalian cells: nucleotide excision repair: variations on versatility. Cell Mol Life Sci 66:994–1009PubMedCrossRefGoogle Scholar
  134. O’Donovan A, Davies AA, Moggs JG, West SC, Wood RD (1994) XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature 371:432–435PubMedCrossRefGoogle Scholar
  135. Pabalan N, Francisco-Pabalan O, Sung L, Jarjanazi H, Ozcelik H (2010) Meta-analysis of two ERCC2 (XPD) polymorphisms, Asp312Asn and Lys751Gln, in breast cancer. Breast Cancer Res Treat 124:531–541PubMedCrossRefGoogle Scholar
  136. Palli D, Polidoro S, D’Errico M, Saieva C, Guarrera S, Calcagnile AS, Sera F, Allione A, Gemma S, Zanna I, Filomena A, Testai E, Caini S, Moretti R, Gomez-Miguel MJ, Nesi G, Luzzi I, Ottini L, Masala G, Matullo G, Dogliotti E (2010) Polymorphic DNA repair and metabolic genes: a multigenic study on gastric cancer. Mutagenesis 25:569–575PubMedCrossRefGoogle Scholar
  137. Park CH, Mu D, Reardon JT, Sancar A (1995) The general transcription-repair factor TFIIH is recruited to the excision-repair complex by the XPA protein independent of the TFIIE transcription factor. J Biol Chem 270:4896–4902PubMedCrossRefGoogle Scholar
  138. Park DJ, Stoehlmacher J, Zhang W, Tsao-Wei DD, Groshen S, Lenz HJ (2001) A xeroderma pigmentosum group D gene polymorphism predicts clinical outcome to platinum-based chemotherapy in patients with advanced colorectal cancer. Cancer Res 61:8654–8658PubMedGoogle Scholar
  139. Park JY, Lee SY, Jeon HS, Bae NC, Chae SC, Joo S, Kim CH, Park JH, Kam S, Kim IS, Jung TH (2002) Polymorphism of the DNA repair gene XRCC1 and risk of primary lung cancer. Cancer Epidemiol Biomark Prev 11:23–27Google Scholar
  140. Pei XH, Yang Z, Lv XQ, Li HX (2014) Genetic variation in ERCC1 and XPF genes and breast cancer risk. Genet Mol Res 13:2259–2267PubMedCrossRefGoogle Scholar
  141. Pierce AJ, Johnson RD, Thompson LH, Jasin M (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13:2633–2638PubMedPubMedCentralCrossRefGoogle Scholar
  142. Popanda O, Schattenberg T, Phong CT, Butkiewicz D, Risch A, Edler L, Kayser K, Dienemann H, Schulz V, Drings P, Bartsch H, Schmezer P (2004) Specific combinations of DNA repair gene variants and increased risk for non-small cell lung cancer. Carcinogenesis 25:2433–2441PubMedCrossRefGoogle Scholar
  143. Porter PC, Mellon I, States JC (2005) XP-A cells complemented with Arg228Gln and Val234Leu polymorphic XPA alleles repair BPDE-induced DNA damage better than cells complemented with the wild type allele. DNA Repair (Amst) 4:341–349CrossRefGoogle Scholar
  144. Povey JE, Darakhshan F, Robertson K, Bisset Y, Mekky M, Rees J, Doherty V, Kavanagh G, Anderson N, Campbell H, MacKie RM, Melton DW (2007) DNA repair gene polymorphisms and genetic predisposition to cutaneous melanoma. Carcinogenesis 28:1087–1093PubMedCrossRefGoogle Scholar
  145. Qian B, Zhang H, Zhang L, Zhou X, Yu H, Chen K (2011) Association of genetic polymorphisms in DNA repair pathway genes with non-small cell lung cancer risk. Lung Cancer 73:138–146PubMedCrossRefGoogle Scholar
  146. Qiao Y, Spitz MR, Shen H, Guo Z, Shete S, Hedayati M, Grossman L, Mohrenweiser H, Wei Q (2002) Modulation of repair of ultraviolet damage in the host-cell reactivation assay by polymorphic XPC and XPD/ERCC2 genotypes. Carcinogenesis 23:295–299PubMedCrossRefGoogle Scholar
  147. Qin Q, Lu J, Zhu H, Xu L, Cheng H, Zhan L, Yang X, Zhang C, Sun X (2014) PARP-1 Val762Ala polymorphism and risk of cancer: a meta-analysis based on 39 case-control studies. PLoS ONE 9:e98022PubMedPubMedCentralCrossRefGoogle Scholar
  148. Qiu L, Wang Z, Shi X (2008) Associations between XPC polymorphisms and risk of cancers: a meta-analysis. Eur J Cancer 44:2241–2253PubMedCrossRefGoogle Scholar
  149. Ramensky V, Bork P, Sunyaev S (2002) Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30:3894–3900PubMedPubMedCentralCrossRefGoogle Scholar
  150. Reynolds P, Cooper S, Lomax M, O’Neill P (2015) Disruption of PARP1 function inhibits base excision repair of a sub-set of DNA lesions. Nucleic Acids Res 43:4028–4038PubMedPubMedCentralCrossRefGoogle Scholar
  151. Robins P, Jones CJ, Biggerstaff M, Lindahl T, Wood RD (1991) Complementation of DNA repair in xeroderma pigmentosum group A cell extracts by a protein with affinity for damaged DNA. EMBO J 10:3913–3921PubMedPubMedCentralGoogle Scholar
  152. Romanowicz-Makowska H, Smolarz B, Zadrozny M, Westfal B, Baszczynski J, Polac I, Sporny S (2011) Single nucleotide polymorphisms in the homologous recombination repair genes and breast cancer risk in Polish women. Tohoku J Exp Med 224:201–208PubMedCrossRefGoogle Scholar
  153. Roszak A, Lianeri M, Sowinska A, Jagodzinski PP (2013) Involvement of PARP-1 Val762Ala polymorphism in the onset of cervical cancer in caucasian women. Mol Diagn Ther 17:239–245PubMedPubMedCentralCrossRefGoogle Scholar
  154. Rouissi K, Bahria IB, Bougatef K, Marrakchi R, Stambouli N, Hamdi K, Cherif M, Ben Slama MR, Sfaxi M, Othman FB, Chebil M, Elgaaied AB, Ouerhani S (2011) The effect of tobacco, XPC, ERCC2 and ERCC5 genetic variants in bladder cancer development. BMC Cancer 11:101PubMedPubMedCentralCrossRefGoogle Scholar
  155. Rybicki BA, Conti DV, Moreira A, Cicek M, Casey G, Witte JS (2004) DNA repair gene XRCC1 and XPD polymorphisms and risk of prostate cancer. Cancer Epidemiol Biomarkers Prev 13:23–29PubMedCrossRefGoogle Scholar
  156. Ryu JS, Hong YC, Han HS, Lee JE, Kim S, Park YM, Kim YC, Hwang TS (2004) Association between polymorphisms of ERCC1 and XPD and survival in non-small-cell lung cancer patients treated with cisplatin combination chemotherapy. Lung Cancer 44:311–316PubMedCrossRefGoogle Scholar
  157. Sak SC, Barrett JH, Paul AB, Bishop DT, Kiltie AE (2006) Comprehensive analysis of 22 XPC polymorphisms and bladder cancer risk. Cancer Epidemiol Biomark Prev 15:2537–2541CrossRefGoogle Scholar
  158. Salagovic J, Klimcakova L, Ilencikova D, Kafkova A (2012) Association of follicular lymphoma risk with BRCA2 N372H polymorphism in Slovak population. Med Oncol 29:1173–1178PubMedCrossRefGoogle Scholar
  159. Saldivar JS, Lu KH, Liang D, Gu J, Huang M, Vlastos AT, Follen M, Wu X (2007) Moving toward individualized therapy based on NER polymorphisms that predict platinum sensitivity in ovarian cancer patients. Gynecol Oncol 107:S223–S229PubMedCrossRefGoogle Scholar
  160. Sanyal S, Festa F, Sakano S, Zhang Z, Steineck G, Norming U, Wijkstrom H, Larsson P, Kumar R, Hemminki K (2004) Polymorphisms in DNA repair and metabolic genes in bladder cancer. Carcinogenesis 25:729–734PubMedCrossRefGoogle Scholar
  161. Schaeffer L, Moncollin V, Roy R, Staub A, Mezzina M, Sarasin A, Weeda G, Hoeijmakers JHJ, Egly JM (1994) The ERCC2/DNA repair protein is associated with the class-II BTF2/TFIIH transcription factor. EMBO J 13:2388–2392PubMedPubMedCentralGoogle Scholar
  162. Schärer OD (2013) Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol 5:a012609PubMedPubMedCentralCrossRefGoogle Scholar
  163. Seker H, Butkiewicz D, Bowman ED, Rusin M, Hedayati M, Grossman L, Harris CC (2001) Functional significance of XPD polymorphic variants: attenuated apoptosis in human lymphoblastoid cells with the XPD 312 Asp/Asp genotype. Cancer Res 61:7430–7434PubMedGoogle Scholar
  164. Shao J, Gu M, Xu Z, Hu Q, Qian L (2007) Polymorphisms of the DNA gene XPD and risk of bladder cancer in a Southeastern Chinese population. Cancer Genet Cytogenet 177:30–36PubMedCrossRefGoogle Scholar
  165. Shao N, Li J, Xu B, Wang Y, Lu X, Feng N (2014) Role of the functional variant (−652T>G) in the XRCC4 promoter in prostate cancer. Mol Biol Rep 41:7463–7470PubMedCrossRefGoogle Scholar
  166. Shen H, Sturgis EM, Khan SG, Qiao Y, Shahlavi T, Eicher SA, Xu Y, Wang X, Strom SS, Spitz MR, Kraemer KH, Wei Q (2001) An intronic poly (AT) polymorphism of the DNA repair gene XPC and risk of squamous cell carcinoma of the head and neck: a case–control study. Cancer Res 61:3321–3325PubMedGoogle Scholar
  167. Shen M, Hung RJ, Brennan P, Malaveille C, Donato F, Placidi D, Carta A, Hautefeuille A, Boffetta P, Porru S (2003) Polymorphisms of the DNA repair genes XRCC1, XRCC3, XPD, interaction with environmental exposures, and bladder cancer risk in a case-control study in northern Italy. Cancer Epidemiol Biomark Prev 12:1234–1240Google Scholar
  168. Shen Q, Tian Y, Li K, Jiang Q, Xue H, Yang S (2015) Association of single nucleotide polymorphisms of DNA repair gene and susceptibility to pancreatic cancer. Int J Clin Exp Pathol 8:3180–3185PubMedPubMedCentralGoogle Scholar
  169. Shi TY, He J, Qiu LX, Zhu ML, Wang MY, Zhou XY, Han J, Yu H, Zang RY, Wei Q (2012) Association between XPF polymorphisms and cancer risk: a meta-analysis. PLoS ONE 7:e38606PubMedPubMedCentralCrossRefGoogle Scholar
  170. Shuck SC, Short EA, Turchi JJ (2008) Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 18:64–72PubMedPubMedCentralCrossRefGoogle Scholar
  171. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei Y-F, Moggs JG, Carter KC, Shell BK, Evans E, de Jong MC, Rademakers S, de Rooij J, Jaspers NGJ, Hoeijmakers JHJ, Wood RD (1996) Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86:811–822PubMedCrossRefGoogle Scholar
  172. Silva SN, Tomar M, Paulo C, Gomes BC, Azevedo AP, Teixeira V, Pina JE, Rueff J, Gaspar JF (2010) Breast cancer risk and common single nucleotide polymorphisms in homologous recombination DNA repair pathway genes XRCC2, XRCC3, NBS1 and RAD51. Cancer Epidemiol 34:85–92PubMedCrossRefGoogle Scholar
  173. Smart DJ, Chipman JK, Hodges NJ (2006) Activity of OGG1 variants in the repair of pro-oxidant-induced 8-oxo-2′-deoxyguanosine. DNA Repair (Amst) 5:1337–1345CrossRefGoogle Scholar
  174. Spurdle AB, Hopper JL, Chen X, Dite GS, Cui J, McCredie MR, Giles GG, Ellis-Steinborner S, Venter DJ, Newman B, Southey MC, Chenevix-Trench G (2002) The BRCA2 372 HH genotype is associated with risk of breast cancer in Australian women under age 60 years. Cancer Epidemiol Biomark Prev 11:413–416Google Scholar
  175. Stern MC, Johnson LR, Bell DA, Taylor JA (2002) XPD codon 751 polymorphism, metabolism genes, smoking, and bladder cancer risk. Cancer Epidemiol Biomark Prev 11:1004–1011Google Scholar
  176. Ström CE, Johansson F, Uhlen M, Szigyarto CA, Erixon K, Helleday T (2011) Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res 39:3166–3175PubMedCrossRefGoogle Scholar
  177. Sturgis EM, Zheng R, Li L, Castillo EJ, Eicher SA, Chen M, Strom SS, Spitz MR, Wei Q (2000) XPD/ERCC2 polymorphisms and risk of head and neck cancer: a case–control analysis. Carcinogenesis 21:2219–2223PubMedCrossRefGoogle Scholar
  178. Sturgis EM, Zhao C, Zheng R, Wei Q (2005) Radiation response genotype and risk of differentiated thyroid cancer: a case–control analysis. Laryngoscope 115:938–945PubMedCrossRefGoogle Scholar
  179. Sugasawa K, Ng JMY, Masutani C, Iwai S, van der Spek PJ, Eker APM, Hanaoka F, Bootsma D, Hoeijmakers JHJ (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2:223–232PubMedCrossRefGoogle Scholar
  180. Sugimura H, Kohno T, Wakai K, Nagura K, Genka K, Igarashi H, Morris BJ, Baba S, Ohno Y, Gao C, Li Z, Wang J, Takezaki T, Tajima K, Varga T, Sawaguchi T, Lum JK, Martinson JJ, Tsugane S, Iwamasa T, Shinmura K, Yokota J (1999) hOGG1 Ser326Cys polymorphism and lung cancer susceptibility. Cancer Epidemiol Biomark Prev 8:669–674Google Scholar
  181. Swindall AF, Stanley JA, Yang ES (2013) PARP-1: friend or foe of DNA damage and repair in tumorigenesis? Cancers (Basel) 5:943–958CrossRefGoogle Scholar
  182. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, Yamaguchiiwai Y, Shinohara A, Takeda S (1998) Homologous recombination and nonhomologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 17:5497–5508PubMedPubMedCentralCrossRefGoogle Scholar
  183. Takata M, Sasaki MS, Tachiiri S, Fukushima T, Sonoda E, Schild D, Thompson LH, Takeda S (2001) Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol Cell Biol 21:2858–2866PubMedPubMedCentralCrossRefGoogle Scholar
  184. Thacker J (2005) The RAD51 gene family, genetic instability and cancer. Cancer Lett 219:125–135PubMedCrossRefGoogle Scholar
  185. Tranah GJ, Giovannucci E, Ma J, Fuchs C, Hankinson SE, Hunter DJ (2004) XRCC2 and XRCC3 polymorphisms are not associated with risk of colorectal adenoma. Cancer Epidemiol Biomark Prev 13:1090–1091Google Scholar
  186. Usanova S, Piee-Staffa A, Sied U, Thomale J, Schneider A, Kaina B, Koberle B (2010) Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression. Mol Cancer 9:248PubMedPubMedCentralCrossRefGoogle Scholar
  187. Venkitaraman AR (2002) Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108:171–182PubMedCrossRefGoogle Scholar
  188. Vidal AE, Boiteux S, Hickson ID, Radicella JP (2001) XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein–protein interactions. EMBO J 20:6530–6539PubMedPubMedCentralCrossRefGoogle Scholar
  189. Vogel U, Overvad K, Wallin H, Tjonneland A, Nexo BA, Raaschou-Nielsen O (2005) Combinations of polymorphisms in XPD, XPC and XPA in relation to risk of lung cancer. Cancer Lett 222:67–74PubMedCrossRefGoogle Scholar
  190. Wakasugi M, Shimizu M, Morioka H, Linn S, Nikaido O, Matsunaga T (2001) Damaged DNA-binding protein DDB stimulates the excision of cyclobutane pyrimidine dimers in vitro in concert with XPA and replication protein A. J Biol Chem 276:15434–15440PubMedCrossRefGoogle Scholar
  191. Wallace SS (2014) Base excision repair: a critical player in many games. DNA Repair (Amst) 19:14–26CrossRefGoogle Scholar
  192. Wang M, Wu W, Rosidi B, Zhang L, Wang H, Iliakis G (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34:6170–6182PubMedPubMedCentralCrossRefGoogle Scholar
  193. Wang XG, Wang ZQ, Tong WM, Shen Y (2007) PARP1 Val762Ala polymorphism reduces enzymatic activity. Biochem Biophys Res Commun 354:122–126PubMedCrossRefGoogle Scholar
  194. Wang X, Ma KW, Zhao YG, Wang GJ, Li W (2015) XRCC1 rs25487 polymorphism is associated with lung cancer risk in epidemiologically susceptible Chinese people. Genet Mol Res 14:15530–15538PubMedCrossRefGoogle Scholar
  195. Weiss JM, Weiss NS, Ulrich CM, Doherty JA, Chen C (2006) Nucleotide excision repair genotype and the incidence of endometrial cancer: effect of other risk factors on the association. Gynecol Oncol 103:891–896PubMedCrossRefGoogle Scholar
  196. Wikman H, Risch A, Klimek F, Schmezer P, Spiegelhalder B, Dienemann H, Kayser K, Schulz V, Drings P, Bartsch H (2000) hOGG1 polymorphism and loss of heterozygosity (LOH): significance for lung cancer susceptibility in a caucasian population. Int J Cancer 88:932–937PubMedCrossRefGoogle Scholar
  197. Willems P, Claes K, Baeyens A, Vandersickel V, Werbrouck J, De Ruyck K, Poppe B, Van den Broecke R, Makar A, Marras E, Perletti G, Thierens H, Vral A (2008) Polymorphisms in nonhomologous end-joining genes associated with breast cancer risk and chromosomal radiosensitivity. Genes Chromosomes Cancer 47:137–148PubMedCrossRefGoogle Scholar
  198. Willems P, De Ruyck K, Van den Broecke R, Makar A, Perletti G, Thierens H, Vral A (2009) A polymorphism in the promoter region of Ku70/XRCC6, associated with breast cancer risk and oestrogen exposure. J Cancer Res Clin Oncol 135:1159–1168PubMedCrossRefGoogle Scholar
  199. Winsey SL, Haldar NA, Marsh HP, Bunce M, Marshall SE, Harris AL, Wojnarowska F, Welsh KI (2000) A variant within the DNA repair gene XRCC3 is associated with the development of melanoma skin cancer. Cancer Res 60:5612–5616PubMedGoogle Scholar
  200. Wood RD (1997) Nucleotide excision repair in mammalian cells. J Biol Chem 272:23465–23468PubMedCrossRefGoogle Scholar
  201. Wood R, Shivji M (1997) Which DNA polymerases are used for DNA repair in eukaryotes? Carcinogenesis 18:605–610PubMedCrossRefGoogle Scholar
  202. Worrillow L, Roman E, Adamson PJ, Kane E, Allan JM, Lightfoot TJ (2009) Polymorphisms in the nucleotide excision repair gene ERCC2/XPD and risk of non-Hodgkin lymphoma. Cancer Epidemiol 33:257–260PubMedCrossRefGoogle Scholar
  203. Wu X, Zhao H, Wei Q, Amos CI, Zhang K, Guo Z, Qiao Y, Hong WK, Spitz MR (2003) XPA polymorphism associated with reduced lung cancer risk and a modulating effect on nucleotide excision repair capacity. Carcinogenesis 24:505–509PubMedCrossRefGoogle Scholar
  204. Wu CN, Liang SY, Tsai CW, Bau DT (2008) The role of XRCC4 in carcinogenesis and anticancer drug discovery. Recent Pat Anticancer Drug Discov 3:209–219PubMedCrossRefGoogle Scholar
  205. Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–383PubMedCrossRefGoogle Scholar
  206. Xi T, Jones IM, Mohrenweiser HW (2004) Many amino acid substitution variants identified in DNA repair genes during human population screenings are predicted to impact protein function. Genomics 83:970–979PubMedCrossRefGoogle Scholar
  207. Xing DY, Tan W, Song N, Lin DX (2001) Ser326Cys polymorphism in hOGG1 gene and risk of esophageal cancer in a Chinese population. Int J Cancer 95:140–143PubMedCrossRefGoogle Scholar
  208. Xing D, Tan W, Wei Q, Lin D (2002) Polymorphisms of the DNA repair gene XPD and risk of lung cancer in a Chinese population. Lung Cancer 38:123–129PubMedCrossRefGoogle Scholar
  209. Xu J, Zheng SL, Turner A, Isaacs SD, Wiley KE, Hawkins GA, Chang BL, Bleecker ER, Walsh PC, Meyers DA, Isaacs WB (2002) Associations between hOGG1 sequence variants and prostate cancer susceptibility. Cancer Res 62:2253–2257PubMedGoogle Scholar
  210. Yang H, Jeffrey PD, Miller J, Kinnucan E, Sun Y, Thoma NH, Zheng N, Chen PL, Lee WH, Pavletich NP (2002) BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297:1837–1848PubMedCrossRefGoogle Scholar
  211. Yarosh DB, Pena A, Brown DA (2005) DNA repair gene polymorphisms affect cytotoxicity in the National Cancer Institute Human Tumour Cell Line Screening Panel. Biomarkers 10:188–202PubMedCrossRefGoogle Scholar
  212. Yin J, Vogel U, Ma Y, Qi R, Wang H (2009) Association of DNA repair gene XRCC1 and lung cancer susceptibility among nonsmoking Chinese women. Cancer Genet Cytogenet 188:26–31PubMedCrossRefGoogle Scholar
  213. Yokoi M, Masutani C, Maekawa T, Sugasawa K, Ohkuma Y, Hanaoka F (2000) The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J Biol Chem 275:9870–9875PubMedCrossRefGoogle Scholar
  214. Yu H, Zhao H, Wang LE, Han Y, Chen WV, Amos CI, Rafnar T, Sulem P, Stefansson K, Landi MT, Caporaso N, Albanes D, Thun M, McKay JD, Brennan P, Wang Y, Houlston RS, Spitz MR, Wei Q (2011) An analysis of single nucleotide polymorphisms of 125 DNA repair genes in the Texas genome-wide association study of lung cancer with a replication for the XRCC4 SNPs. DNA Repair (Amst) 10:398–407CrossRefGoogle Scholar
  215. Zamble DB, Lippard SJ (1995) Cisplatin and DNA-repair in cancer-chemotherapy. Trends Biochem Sci 20:435–439PubMedCrossRefGoogle Scholar
  216. Shao N, Jiang WY, Qiao D, Zhang, SG, Wu Y, Zhang XX, Hua LX, Ding Y, Feng NH (2012/2013) An updated meta-analysis of XRCC4 polymorphisms and cancer risk based on 31 case-control studies. Cancer Biomark 12:37–47Google Scholar
  217. Zhang X, Miao X, Liang G, Hao B, Wang Y, Tan W, Li Y, Guo Y, He F, Wei Q, Lin D (2005) Polymorphisms in DNA base excision repair genes ADPRT and XRCC1 and risk of lung cancer. Cancer Res 65:722–726PubMedGoogle Scholar
  218. Zienolddiny S, Campa D, Lind H, Ryberg D, Skaug V, Stangeland L, Phillips DH, Canzian F, Haugen A (2006) Polymorphisms of DNA repair genes and risk of non-small cell lung cancer. Carcinogenesis 27:560–567PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Food Chemistry and ToxicologyKarlsruhe Institute of TechnologyKarlsruheGermany

Personalised recommendations