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Tumor Biology

, Volume 36, Issue 2, pp 1029–1038 | Cite as

The hOGG1 Ser326Cys polymorphism contributes to digestive system cancer susceptibility: evidence from 48 case–control studies

  • Yang Wang
  • Xujie Gao
  • Feng Wei
  • Xinwei Zhang
  • Jinpu Yu
  • Hua Zhao
  • Qian Sun
  • Fan Yan
  • Cihui Yan
  • Hui Li
  • Xiubao Ren
Research Article

Abstract

The Ser326Cys polymorphism in the human 8-oxogunaine DNA glycosylase (hOGG1) gene had been implicated in cancer susceptibility. Studies investigating the associations between the Ser326Cys polymorphism and digestion cancer susceptibility showed conflicting results. Therefore, a meta-analysis was performed to derive a more precise estimation of the relationship. We conducted a meta-analysis of 48 studies that included 12,073 cancer cases and 19,557 case-free controls. We assessed the strength of the association using odds ratios (ORs) with 95 % confidence intervals (CIs). In our analysis, the hOGG1 Ser326Cys polymorphism was significantly associated with the risk of digestive system cancers (Cys/Cys vs. Ser/Ser: OR = 1.17, 95 % CI = 1.00–1.35, P < 0.001; Cys/Cys vs. Cys/Ser + Ser/Ser: OR = 1.14, 95 % CI = 1.00–1.29, P < 0.001). In subgroup analyses by cancer types, we found that the hOGG1 Ser326Cys polymorphism may increase hepatocellular cancer and colorectal cancer risks, but decrease the risk of oral cancer. These findings supported that hOGG1 Ser326Cys polymorphism may contribute to the susceptibility of digestive cancers.

Keywords

Digestive cancer hOGG1 Polymorphism Meta-analysis 

Notes

Acknowledgments

This manuscript is supported by the National Basic Research Program of China (973program) No. 2012CB9333004.

References

  1. 1.
    Barrowman JA, Rahman A, Lindstrom MB, Borgstrom B. Intestinal absorption and metabolism of hydrocarbons. Prog Lipid Res. 1989;28:189–203.CrossRefPubMedGoogle Scholar
  2. 2.
    Bingham SA, Hughes R, Cross AJ. Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. J Nutr. 2002;132:3522S–5S.PubMedGoogle Scholar
  3. 3.
    Knize MG, Salmon CP, Pais P, Felton JS. Food heating and the formation of heterocyclic aromatic amine and polycyclic aromatic hydrocarbon mutagens/carcinogens. Adv Exp Med Biol. 1999;459:179–93.CrossRefPubMedGoogle Scholar
  4. 4.
    Kobayashi M, Tsubono Y, Sasazuki S, Sasaki S, Tsugane S. Vegetables, fruit and risk of gastric cancer in Japan: a 10-year follow-up of the JPHC Study Cohort I. Int J Cancer. 2002;102:39–44.CrossRefPubMedGoogle Scholar
  5. 5.
    Levi F, Pasche C, La Vecchia C, Lucchini F, Franceschi S. Food groups and colorectal cancer risk. Br J Cancer. 1999;79:1283–7.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Floyd RA. The role of 8-hydroxyguanine in carcinogenesis. Carcinogenesis. 1990;11:1447–50.CrossRefPubMedGoogle Scholar
  7. 7.
    Loft S, Deng XS, Tuo J, Wellejus A, Sorensen M, Poulsen HE. Experimental study of oxidative DNA damage. Free Radic Res. 1998;29:525–39.CrossRefPubMedGoogle Scholar
  8. 8.
    Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis. 2000;21:361–70.CrossRefPubMedGoogle Scholar
  9. 9.
    Jaruga P, Zastawny TH, Skokowski J, Dizdaroglu M, Olinski R. Oxidative DNA base damage and antioxidant enzyme activities in human lung cancer. FEBS Lett. 1994;341:59–64.CrossRefPubMedGoogle Scholar
  10. 10.
    Roldan-Arjona T, Wei YF, Carter KC, Klungland A, Anselmino C, Wang RP, et al. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc Natl Acad Sci U S A. 1997;94:8016–20.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Wood RD, Mitchell M, Sgouros J, Lindahl T. Human DNA repair genes. Science. 2001;291:1284–9.CrossRefPubMedGoogle Scholar
  12. 12.
    Chatterjee A, Mambo E, Zhang Y, Deweese T, Sidransky D. Targeting of mutant hogg1 in mammalian mitochondria and nucleus: effect on cellular survival upon oxidative stress. BMC Cancer. 2006;6:235.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Elahi A, Zheng Z, Park J, Eyring K, McCaffrey T, Lazarus P. The human OGG1 DNA repair enzyme and its association with orolaryngeal cancer risk. Carcinogenesis. 2002;23:1229–34.CrossRefPubMedGoogle Scholar
  14. 14.
    Sakamoto T, Higaki Y, Hara M, Ichiba M, Horita M, Mizuta T, et al. hOGG1 Ser326Cys polymorphism and risk of hepatocellular carcinoma among Japanese. J Epidemiol. 2006;16:233–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Speina E, Arczewska KD, Gackowski D, Zielinska M, Siomek A, Kowalewski J, et al. Contribution of hMTH1 to the maintenance of 8-oxoguanine levels in lung DNA of non-small-cell lung cancer patients. J Natl Cancer Inst. 2005;97:384–95.CrossRefPubMedGoogle Scholar
  16. 16.
    Poplawski T, Arabski M, Kozirowska D, Blasinska-Morawiec M, Morawiec Z, Morawiec-Bajda A, et al. DNA damage and repair in gastric cancer—a correlation with the hOGG1 and RAD51 genes polymorphisms. Mutat Res. 2006;601:83–91.CrossRefPubMedGoogle Scholar
  17. 17.
    Park HW, Kim IJ, Kang HC, Jang SG, Ahn SA, Lee JS, et al. The hOGG1 Ser326Cys polymorphism is not associated with colorectal cancer risk. J Epidemiol. 2007;17:156–60.CrossRefPubMedGoogle Scholar
  18. 18.
    Radicella JP, Dherin C, Desmaze C, Fox MS, Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1997;94:8010–5.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Aburatani H, Hippo Y, Ishida T, Takashima R, Matsuba C, Kodama T, et al. Cloning and characterization of mammalian 8-hydroxyguanine-specific DNA glycosylase/apurinic, apyrimidinic lyase, a functional mutM homologue. Cancer Res. 1997;57:2151–6.PubMedGoogle Scholar
  20. 20.
    Kohno T, Shinmura K, Tosaka M, Tani M, Kim SR, Sugimura H, et al. Genetic polymorphisms and alternative splicing of the hOGG1 gene, that is involved in the repair of 8-hydroxyguanine in damaged DNA. Oncogene. 1998;16:3219–25.CrossRefPubMedGoogle Scholar
  21. 21.
    Li D, Suzuki H, Liu B, Morris J, Liu J, Okazaki T, et al. DNA repair gene polymorphisms and risk of pancreatic cancer. Clin Cancer Res. 2009;15:740–6.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    McWilliams RR, Bamlet WR, Cunningham JM, Goode EL, de Andrade M, Boardman LA, et al. Polymorphisms in DNA repair genes, smoking, and pancreatic adenocarcinoma risk. Cancer Res. 2008;68:4928–35.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Jiao X, Huang J, Wu S, Lv M, Hu Y, Jianfu S. X, Luo C, Ce B. hOGG1 Ser326Cys polymorphism and susceptibility to gallbladder cancer in a Chinese population. Int J Cancer. 2007;121:501–5.CrossRefPubMedGoogle Scholar
  24. 24.
    Srivastava A, Srivastava K, Pandey SN, Choudhuri G, Mittal B. Single-nucleotide polymorphisms of DNA repair genes OGG1 and XRCC1: association with gallbladder cancer in North Indian population. Ann Surg Oncol. 2009;16:1695–703.CrossRefPubMedGoogle Scholar
  25. 25.
    Srivastava K, Srivastava A, Mittal B. Polymorphisms in ERCC2, MSH2, and OGG1 DNA repair genes and gallbladder cancer risk in a population of Northern India. Cancer. 2010;116:3160–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Huang WY, Gao YT, Rashid A, Sakoda LC, Deng J, Shen MC, et al. Selected base excision repair gene polymorphisms and susceptibility to biliary tract cancer and biliary stones: a population-based case–control study in China. Carcinogenesis. 2008;29:100–5.CrossRefPubMedGoogle Scholar
  27. 27.
    Canbay E, Agachan B, Gulluoglu M, Isbir T, Balik E, Yamaner S, et al. Possible associations of APE1 polymorphism with susceptibility and HOGG1 polymorphism with prognosis in gastric cancer. Anticancer Res. 2010;30:1359–64.PubMedGoogle Scholar
  28. 28.
    Capella G, Pera G, Sala N, Agudo A, Rico F, Del GG, et al. DNA repair polymorphisms and the risk of stomach adenocarcinoma and severe chronic gastritis in the EPIC-EURGAST study. Int J Epidemiol. 2008;37:1316–25.CrossRefPubMedGoogle Scholar
  29. 29.
    Engin AB, Karahalil B, Engin A, Karakaya AE. DNA repair enzyme polymorphisms and oxidative stress in a Turkish population with gastric carcinoma. Mol Biol Rep. 2011;38:5379–86.CrossRefPubMedGoogle Scholar
  30. 30.
    Farinati F, Cardin R, Bortolami M, Nitti D, Basso D, de Bernard M, et al. Oxidative DNA damage in gastric cancer: CagA status and OGG1 gene polymorphism. Int J Cancer. 2008;123:51–5.CrossRefPubMedGoogle Scholar
  31. 31.
    Hanaoka T, Sugimura H, Nagura K, Ihara M, Li XJ, Hamada GS, et al. hOGG1 exon7 polymorphism and gastric cancer in case–control studies of Japanese Brazilians and non-Japanese Brazilians. Cancer Lett. 2001;170:53–61.CrossRefPubMedGoogle Scholar
  32. 32.
    Liu X, Xiao N, Guo W, Wu Y, Cai Z, He Q, et al. The hOGG1 gene 5′-UTR variant c.-53G > C contributes to the risk of gastric cancer but not colorectal cancer in the Chinese population: the functional variation of hOGG1 for gastric cancer risk. J Cancer Res Clin Oncol. 2011;137:1477–85.CrossRefPubMedGoogle Scholar
  33. 33.
    Malik MA, Zargar SA, Mittal B. Lack of influence of DNA repair gene OGG1 codon 326 polymorphisms of gastric cancer risk in the Kashmir valley. Asian Pac J Cancer Prev. 2010;11:165–8.PubMedGoogle Scholar
  34. 34.
    Palli D, Polidoro S, D’Errico M, Saieva C, Guarrera S, Calcagnile AS, et al. Polymorphic DNA repair and metabolic genes: a multigenic study on gastric cancer. Mutagenesis. 2010;25:569–75.CrossRefPubMedGoogle Scholar
  35. 35.
    Sun LM, Shang Y, Zeng YM, Deng YY, Cheng JF. HOGG1 polymorphism in atrophic gastritis and gastric cancer after Helicobacter pylori eradication. World J Gastroenterol. 2010;16:4476–82.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Takezaki T, Gao CM, Wu JZ, Li ZY, Wang JD, Ding JH, et al. hOGG1 Ser(326)Cys polymorphism and modification by environmental factors of stomach cancer risk in Chinese. Int J Cancer. 2002;99:624–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Tsukino H, Hanaoka T, Otani T, Iwasaki M, Kobayashi M, Hara M, et al. hOGG1 Ser326Cys polymorphism, interaction with environmental exposures, and gastric cancer risk in Japanese populations. Cancer Sci. 2004;95:977–83.CrossRefPubMedGoogle Scholar
  38. 38.
    Shinmura K, Kohno T, Kasai H, Koda K, Sugimura H, Yokota J. Infrequent mutations of the hOGG1 gene, that is involved in the excision of 8-hydroxyguanine in damaged DNA, in human gastric cancer. Jpn J Cancer Res. 1998;89:825–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Brevik A, Joshi AD, Corral R, Onland-Moret NC, Siegmund KD, Le Marchand L, et al. Polymorphisms in base excision repair genes as colorectal cancer risk factors and modifiers of the effect of diets high in red meat. Cancer Epidemiol Biomarkers Prev. 2010;19:3167–73.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Canbay E, Cakmakoglu B, Zeybek U, Sozen S, Cacina C, Gulluoglu M, et al. Association of APE1 and hOGG1 polymorphisms with colorectal cancer risk in a Turkish population. Curr Med Res Opin. 2011;27:1295–302.CrossRefPubMedGoogle Scholar
  41. 41.
    Curtin K, Samowitz WS, Wolff RK, Ulrich CM, Caan BJ, Potter JD, et al. Assessing tumor mutations to gain insight into base excision repair sequence polymorphisms and smoking in colon cancer. Cancer Epidemiol Biomarkers Prev. 2009;18:3384–8.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Engin AB, Karahalil B, Engin A, Karakaya AE. Oxidative stress, Helicobacter pylori, and OGG1 Ser326Cys, XPC Lys939Gln, and XPD Lys751Gln polymorphisms in a Turkish population with colorectal carcinoma. Genet Test Mol Biomarkers. 2010;14:559–64.CrossRefPubMedGoogle Scholar
  43. 43.
    Hansen R, Saebo M, Skjelbred CF, Nexo BA, Hagen PC, Bock G, et al. GPX Pro198Leu and OGG1 Ser326Cys polymorphisms and risk of development of colorectal adenomas and colorectal cancer. Cancer Lett. 2005;229:85–91.CrossRefPubMedGoogle Scholar
  44. 44.
    Hansen RD, Krath BN, Frederiksen K, Tjonneland A, Overvad K, Roswall N, et al. GPX1 Pro(198)Leu polymorphism, erythrocyte GPX activity, interaction with alcohol consumption and smoking, and risk of colorectal cancer. Mutat Res. 2009;664:13–9.CrossRefPubMedGoogle Scholar
  45. 45.
    Kasahara M, Osawa K, Yoshida K, Miyaishi A, Osawa Y, Inoue N, et al. Association of MUTYH Gln324His and APEX1 Asp148Glu with colorectal cancer and smoking in a Japanese population. J Exp Clin Cancer Res. 2008;27:49.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kim JI, Park YJ, Kim KH, Kim JI, Song BJ, Lee MS, et al. hOGG1 Ser326Cys polymorphism modifies the significance of the environmental risk factor for colon cancer. World J Gastroenterol. 2003;9:956–60.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Moreno V, Gemignani F, Landi S, Gioia-Patricola L, Chabrier A, Blanco I, et al. Polymorphisms in genes of nucleotide and base excision repair: risk and prognosis of colorectal cancer. Clin Cancer Res. 2006;12:2101–8.CrossRefPubMedGoogle Scholar
  48. 48.
    Obtulowicz T, Swoboda M, Speina E, Gackowski D, Rozalski R, Siomek A, et al. Oxidative stress and 8-oxoguanine repair are enhanced in colon adenoma and carcinoma patients. Mutagenesis. 2010;25:463–71.CrossRefPubMedGoogle Scholar
  49. 49.
    Sliwinski T, Krupa R, Wisniewska-Jarosinska M, Pawlowska E, Lech J, Chojnacki J, et al. Common polymorphisms in the XPD and hOGG1 genes are not associated with the risk of colorectal cancer in a Polish population. Tohoku J Exp Med. 2009;218:185–91.CrossRefPubMedGoogle Scholar
  50. 50.
    Stern MC, Conti DV, Siegmund KD, Corral R, Yuan JM, Koh WP, et al. DNA repair single-nucleotide polymorphisms in colorectal cancer and their role as modifiers of the effect of cigarette smoking and alcohol in the Singapore Chinese Health Study. Cancer Epidemiol Biomarkers Prev. 2007;16:2363–72.CrossRefPubMedGoogle Scholar
  51. 51.
    Pardini B, Naccarati A, Novotny J, Smerhovsky Z, Vodickova L, Polakova V, et al. DNA repair genetic polymorphisms and risk of colorectal cancer in the Czech Republic. Mutat Res. 2008;638:146–53.CrossRefPubMedGoogle Scholar
  52. 52.
    Ferguson HR, Wild CP, Anderson LA, Murphy SJ, Johnston BT, Murray LJ, et al. No association between hOGG1, XRCC1, and XPD polymorphisms and risk of reflux esophagitis, Barrett’s esophagus, or esophageal adenocarcinoma: results from the factors influencing the Barrett’s adenocarcinoma relationship case–control study. Cancer Epidemiol Biomarkers Prev. 2008;17:736–9.CrossRefPubMedGoogle Scholar
  53. 53.
    Hao B, Wang H, Zhou K, Li Y, Chen X, Zhou G, et al. Identification of genetic variants in base excision repair pathway and their associations with risk of esophageal squamous cell carcinoma. Cancer Res. 2004;64:4378–84.CrossRefPubMedGoogle Scholar
  54. 54.
    Lagadu S, Lechevrel M, Sichel F, Breton J, Pottier D, Couderc R, et al. 8-oxo-7,8-dihydro-2'-deoxyguanosine as a biomarker of oxidative damage in oesophageal cancer patients: lack of association with antioxidant vitamins and polymorphism of hOGG1 and GST. J Exp Clin Cancer Res. 2010;29:157.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Li QD, Li H, Wang MS, Diao TY, Zhou ZY, Fang QX, et al. Multi-susceptibility genes associated with the risk of the development stages of esophageal squamous cell cancer in Feicheng County. BMC Gastroenterol. 2011;11:74.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Upadhyay R, Malik MA, Zargar SA, Mittal B. OGG1 Ser326Cys polymorphism and susceptibility to esophageal cancer in low and high at-risk populations of northern India. J Gastrointest Cancer. 2010;41:110–5.CrossRefPubMedGoogle Scholar
  57. 57.
    Xing DY, Tan W, Song N, Lin DX. Ser326Cys polymorphism in hOGG1 gene and risk of esophageal cancer in a Chinese population. Int J Cancer. 2001;95:140–3.CrossRefPubMedGoogle Scholar
  58. 58.
    Tse D, Zhai R, Zhou W, Heist RS, Asomaning K, Su L, et al. Polymorphisms of the NER pathway genes, ERCC1 and XPD are associated with esophageal adenocarcinoma risk. Cancer Causes Control. 2008;19:1077–83.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Tsou YA, Hua CH, Tseng HC, Hsu CF, Tsai CW, Sun SS, et al. The joint effect of hOGG1 single nucleotide polymorphism and betel quid chewing on oral cancer in Taiwan. Anticancer Res. 2010;30:4205–8.PubMedGoogle Scholar
  60. 60.
    Gorgens H, Muller A, Kruger S, Kuhlisch E, Konig IR, Ziegler A, et al. Analysis of the base excision repair genes MTH1, OGG1 and MUTYH in patients with squamous oral carcinomas. Oral Oncol. 2007;43:791–5.CrossRefPubMedGoogle Scholar
  61. 61.
    Yuan T, Wei J, Luo J, Liu M, Deng S, Chen P. Polymorphisms of base-excision repair genes hOGG1 326cys and XRCC1 280His increase hepatocellular carcinoma risk. Dig Dis Sci. 2012;57:2451–7.CrossRefPubMedGoogle Scholar
  62. 62.
    Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med. 1997;127:820–6.CrossRefPubMedGoogle Scholar
  63. 63.
    Berman NG, Parker RA. Meta-analysis: neither quick nor easy. BMC Med Res Methodol. 2002;2:10.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.CrossRefPubMedGoogle Scholar
  65. 65.
    MANTEL N, HAENSZEL W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22:719–48.PubMedGoogle Scholar
  66. 66.
    Hayashino Y, Noguchi Y, Fukui T. Systematic evaluation and comparison of statistical tests for publication bias. J Epidemiol. 2005;15:235–43.CrossRefPubMedGoogle Scholar
  67. 67.
    Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Comparison of two methods to detect publication bias in meta-analysis. JAMA. 2006;295:676–80.CrossRefPubMedGoogle Scholar
  68. 68.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRefPubMedGoogle Scholar
  69. 69.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.CrossRefPubMedGoogle Scholar
  70. 70.
    Ames BN. Endogenous oxidative DNA damage, aging, and cancer. Free Radic Res Commun. 1989;7:121–8.CrossRefPubMedGoogle Scholar
  71. 71.
    Shibutani S, Takeshita M, Grollman AP. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature. 1991;349:431–4.CrossRefPubMedGoogle Scholar
  72. 72.
    Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res. 1997;387:147–63.CrossRefPubMedGoogle Scholar
  73. 73.
    Greim H, Csanady G, Filser JG, Kreuzer P, Schwarz L, Wolff T, et al. Biomarkers as tools in human health risk assessment. Clin Chem. 1995;41:1804–8.PubMedGoogle Scholar
  74. 74.
    Nishioka K, Ohtsubo T, Oda H, Fujiwara T, Kang D, Sugimachi K, et al. Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs. Mol Biol Cell. 1999;10:1637–52.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Weiss JM, Goode EL, Ladiges WC, Ulrich CM. Polymorphic variation in hOGG1 and risk of cancer: a review of the functional and epidemiologic literature. Mol Carcinog. 2005;42:127–41.CrossRefPubMedGoogle Scholar
  76. 76.
    Wang W, Wang M, Chen Y, Zhang Z, Wang S, Xu M, et al. The hOGG1 Ser326Cys polymorphism contributes to cancer susceptibility: evidence from 83 case–control studies. Mutagenesis. 2012;27:329–36.CrossRefPubMedGoogle Scholar
  77. 77.
    Dizdaroglu M, Olinski R, Doroshow JH, Akman SA. Modification of DNA bases in chromatin of intact target human cells by activated human polymorphonuclear leukocytes. Cancer Res. 1993;53:1269–72.PubMedGoogle Scholar
  78. 78.
    Obst B, Wagner S, Sewing KF, Beil W. Helicobacter pylori causes DNA damage in gastric epithelial cells. Carcinogenesis. 2000;21:1111–5.CrossRefPubMedGoogle Scholar
  79. 79.
    Bagchi D, McGinn TR, Ye X, Bagchi M, Krohn RL, Chatterjee A, et al. Helicobacter pylori-induced oxidative stress and DNA damage in a primary culture of human gastric mucosal cells. Dig Dis Sci. 2002;47:1405–12.CrossRefPubMedGoogle Scholar
  80. 80.
    Church DF, Pryor WA. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect. 1985;64:111–26.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Chen J, Geissler C, Parpia B, Li J, Campbell TC. Antioxidant status and cancer mortality in China. Int J Epidemiol. 1992;21:625–35.CrossRefPubMedGoogle Scholar
  82. 82.
    Cheng KK, Day NE. Nutrition and esophageal cancer. Cancer Causes Control. 1996;7:33–40.CrossRefPubMedGoogle Scholar
  83. 83.
    Glei M, Latunde-Dada GO, Klinder A, Becker TW, Hermann U, Voigt K, et al. Iron-overload induces oxidative DNA damage in the human colon carcinoma cell line HT29 clone 19A. Mutat Res. 2002;519:151–61.CrossRefPubMedGoogle Scholar
  84. 84.
    Boiteux S, Radicella JP. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch Biochem Biophys. 2000;377:1–8.CrossRefPubMedGoogle Scholar
  85. 85.
    Dianov GL, Souza-Pinto N, Nyaga SG, Thybo T, Stevnsner T, Bohr VA. Base excision repair in nuclear and mitochondrial DNA. Prog Nucleic Acid Res Mol Biol. 2001;68:285–97.CrossRefPubMedGoogle Scholar
  86. 86.
    Karahalil B, Hogue BA, de Souza-Pinto NC, Bohr VA. Base excision repair capacity in mitochondria and nuclei: tissue-specific variations. FASEB J. 2002;16:1895–902.CrossRefPubMedGoogle Scholar
  87. 87.
    Gu D, Wang M, Zhang Z, Chen J. Lack of association between the hOGG1 Ser326Cys polymorphism and breast cancer risk: evidence from 11 case–control studies. Breast Cancer Res Treat. 2010;122:527–31.CrossRefPubMedGoogle Scholar
  88. 88.
    Niwa Y, Matsuo K, Ito H, Hirose K, Tajima K, Nakanishi T, et al. Association of XRCC1 Arg399Gln and OGG1 Ser326Cys polymorphisms with the risk of cervical cancer in Japanese subjects. Gynecol Oncol. 2005;99:43–9.CrossRefPubMedGoogle Scholar
  89. 89.
    Albano E. Free radical mechanisms in immune reactions associated with alcoholic liver disease. Free Radic Biol Med. 2002;32:110–4.CrossRefPubMedGoogle Scholar
  90. 90.
    Shimoda R, Nagashima M, Sakamoto M, Yamaguchi N, Hirohashi S, Yokota J, et al. Increased formation of oxidative DNA damage, 8-hydroxydeoxyguanosine, in human livers with chronic hepatitis. Cancer Res. 1994;54:3171–2.PubMedGoogle Scholar
  91. 91.
    Asami S, Hirano T, Yamaguchi R, Tomioka Y, Itoh H, Kasai H. Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking. Cancer Res. 1996;56:2546–9.PubMedGoogle Scholar
  92. 92.
    Shacter E,Weitzman SA. Chronic inflammation and cancer. Oncology (Williston Park). 2002;16:217–26, 229; discussion 230–2Google Scholar
  93. 93.
    Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer. 1992;18:1–29.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2014

Authors and Affiliations

  • Yang Wang
    • 1
    • 3
    • 4
  • Xujie Gao
    • 1
    • 3
    • 4
  • Feng Wei
    • 1
    • 3
    • 4
  • Xinwei Zhang
    • 2
    • 3
    • 4
  • Jinpu Yu
    • 1
    • 3
    • 4
  • Hua Zhao
    • 1
    • 3
    • 4
  • Qian Sun
    • 1
    • 3
    • 4
  • Fan Yan
    • 1
    • 3
    • 4
  • Cihui Yan
    • 1
    • 3
    • 4
  • Hui Li
    • 1
    • 3
    • 4
  • Xiubao Ren
    • 2
    • 3
    • 4
  1. 1.Department of ImmunologyTianjin Medical University Cancer Institute and HospitalTianjinChina
  2. 2.Department of BiotherapyTianjin Medical University Cancer Institute and HospitalTianjinChina
  3. 3.National Clinical Research Center of CancerTianjinChina
  4. 4.Key Laboratory of Cancer Immunology and BiotherapyTianjinChina

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