XRCC1 genetic polymorphism Arg399Gln and hepatocellular carcinoma risk: a meta-analysis
Fei Liu
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorBo Li
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorYonggang Wei
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorLvnan Yan
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorTianfu Wen
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorJichun Zhao
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorMingqing Xu
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorFei Liu
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorBo Li
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorYonggang Wei
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorLvnan Yan
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorTianfu Wen
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorJichun Zhao
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorMingqing Xu
Department of Liver and Vascular Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
Search for more papers by this authorAbstract
Background: Studies investigating the association between X-ray repair cross-complementing group 1 (XRCC1) genetic polymorphism Arg399Gln and hepatocellular carcinoma (HCC) risk report conflicting results. The aim of this study was to quantitatively summarize the evidence for such a relationship.
Methods: Two investigators independently searched the Medline, Embase, CNKI and Chinese Biomedicine Database. Summary odds ratios (ORs) and 95% confidence intervals (95% CIs) for XRCC1 polymorphism and HCC were calculated in a fixed-effects model (the Mantel–Haenszel method) and a random-effects model (the DerSimonian and Laird method) when appropriate. The pooled ORs were performed for a codominant model (Gln/Gln vs. Arg/Arg, Arg/Gln vs. Arg/Arg), a dominant model (Gln/Gln+Arg/Gln vs. Arg/Arg) and a recessive model (Gln/Gln vs. Arg/Gln+Arg/Arg).
Results: This meta-analysis included 11 case–control studies, which included 2208 HCC cases and 3265 controls. Overall, the variant genotypes (Gln/Gln and Arg/Gln) of Arg399Gln were not associated with HCC risk when compared with the wild-type Arg/Arg homozygote (Gln/Gln vs. Arg/Arg, OR=1.01, 95% CI=0.79–1.28; Arg/Gln vs. Arg/Arg, OR=1.09, 95% CI=0.81–1.45). Similarly, no associations were found in the dominant and recessive models (dominant model, OR=1.12, 95% CI=0.85–1.47; recessive model, OR=0.99, 95% CI=0.79–1.25). Limiting the analysis to the studies within Hardy–Weinberg equilibrium, the results were persistent and robust. When stratifying for ethnicity, country/region and source of controls, no evidence of a significant association was observed in any subgroup. No publication bias was found in the present study.
Conclusion: No association is found between the XRCC1 polymorphism Arg399Gln and the risk of HCC.
References
- 1 Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74–108.
- 2 Michielsen PP, Francque SM, van Dongen JL. Viral hepatitis and hepatocellular carcinoma. World J Surg Oncol 2005; 3: 27.
- 3 Faivre S, Bouattour M, Raymond E. Novel molecular therapies in hepatocellular carcinoma. Liver Int 2011; 31 (Suppl. 1): 151–60.
- 4 Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005; 436: 946–52.
- 5 Smith TR, Miler MS, Lohman KK, et al. Polymorphisms of XRCC1 and XRCC3 genes and susceptibility to breast cancer. Cancer Lett 2003; 190: 183–90.
- 6 Seeberg E, Eide L, Bjoras M. The base excision repair pathway. Trends Biochem Sci 1995; 20: 397–401.
- 7
Lee JM,
Lee YC,
Yang SY, et al. Genetic polymorphisms of XRCC1 and risk of the esophageal cancer.
Int J Cancer
2001; 95: 240–6.
10.1002/1097-0215(20010720)95:4<240::AID-IJC1041>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- 8 Lamerdin J, Montegomery M, Stilwagen S, et al. Genomic sequence comparison of human and mouse XRCC1 DNA repair gene regions. Genomics 1995; 25: 547–54.
- 9 Lindahl T, Wood RD. Quality control by DNA repair. Science 1999; 286: 1897–905.
- 10 Shen MR, Jones LM, Mohrenweiser H. Nonconservative amino acid substitution variants exist at polymorphic frequency in DNA repair genes in healthy humans. Cancer Res 1998; 58: 604–8.
- 11 Cochran WG. The combination of estimates from different experiments. Biometrics 1954; 10: 101–29.
- 12 Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557–60.
- 13 Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959; 22: 719–48.
- 14 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177–88.
- 15 Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50: 1088–101.
- 16 Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629–34.
- 17 Kiran M, Chawla YK, Jain M, Kaur J. Haplotypes of microsomal epoxide hydrolase and x-ray cross-complementing group 1 genes in Indian hepatocellular carcinoma patients. DNA Cell Biol 2009; 28: 573–7.
- 18 Kiran M, Saxena R, Chawla YK, Kaur J. Polymorphism of DNA repair gene XRCC1 and hepatitis-related hepatocellular carcinoma risk in Indian population. Mol Cell Biochem 2009; 327: 7–13.
- 19 Borentain P, Gérolami V, Ananian P, et al. DNA-repair and carcinogen-metabolising enzymes genetic polymorphisms as an independent risk factor for hepatocellular carcinoma in Caucasian liver-transplanted patients. Eur J Cancer 2007; 43: 2479–86.
- 20 Long XD, Ma Y, Wei YP, Deng ZL. The polymorphisms of GSTM1, GSTT1, HYL1*2, and XRCC1, and aflatoxin B1-related hepatocellular carcinoma in Guangxi population, China. Hepatol Res 2006; 36: 48–55.
- 21 Chen CC, Yang SY, Liu CJ, et al. Association of cytokine and DNA repair gene polymorphisms with hepatitis B-related hepatocellular carcinoma. Int J Epidemiol 2005; 34: 1310–8.
- 22 Kirk GD, Turner PC, Gong Y, et al. Hepatocellular carcinoma and polymorphisms in carcinogen-metabolizing and DNA repair enzymes in a population with aflatoxin exposure and hepatitis B virus endemicity. Cancer Epidemiol Biomark Prev 2005; 14: 373–9.
- 23 Yu MW, Yang SY, Pan IJ, et al. Polymorphisms in XRCC1 and glutathione S-transferase genes and hepatitis B-related hepatocellular carcinoma. J Natl Cancer Inst 2003; 95: 1485–8.
- 24 Ren Y, Wang DS, Li Z, et al. Study on the relationship between Gene XRCC1 Codon 399 S ingle Nucleotide Polymorphisms and Primary Hepatic Carcinoma in Han Nationality. Chin J Clin Hepatol 2008; 24: 361–4 (article in Chinese).
- 25 Yang JL, Han YN, Zheng SG. Influence of human XRCC1-399 single nucleotide polymorphism on primary hepatocytic carcinoma. Zhong Liu 2004; 24: 322–4 (article in Chinese).
- 26 Long XD, Ma Y, Wei YP, Deng ZL. Polymorphism of DNA repair gene XRCC1 and risk of hepatocellular carcinoma. J Guang Xi Med. Univ. 2004; 21: 313–5 (article in Chinese).
- 27 Su HY. A case–control study on association between genetic polymorphisms of DNA repair and hepatic cell cancer susceptibility, 2008 (article in Chinese). Available at http://dlib3.edu.cnki.net/kns50/detail.aspx?dbname=CDFD2008&filename=2008083042.nh (accessed 10 March 2011).
- 28 Wu H. Correlation between DNA repair gene XRCC1 single nucleotide polymorphism and susceptibility to hepatocellular carcinoma in Fusui County of Guangxi, 2009 (article in Chinese). Available at http://dlib3.edu.cnki.net/kns50/detail.aspx?dbname=CMFD2009&filename=2009132690.nh (accessed 10 March 2011).
- 29 Long XD. Polymorphism of DNA repair gene XRCC1 and risk of aflatoxin B1-related hepatocellular carcinoma, 2004 (article in Chinese). Available at http://dlib3.edu.cnki.net/kns50/detail.aspx?dbname=CMFD2004&filename=2004080557.nh (accessed 10 March 2011).
- 30 Wang DS. Serological diagnosis and DNA repair gene XRCC1 polymorphism in patients with primary liver cancer, 2006 (article in Chinese). Available at http://dlib3.edu.cnki.net/kns50/detail.aspx?dbname=CMFD2007&filename=2007101142.nh (accessed 10 March 2011).
- 31 Han YN, Yang JL, Zheng SG, Wu YQ. Study on the association of human XRCC1-399 single nucleotide polymorphism and primary hepatocytic carcinoma. Gan Zang 2004; 9: 235–7 (article in Chinese).
- 32 Basso D, Navaglia F, Fogar P, et al. DNA repair pathways and mitochondrial DNA mutations in gastrointestinal carcinogenesis. Clin Chim Acta 2007; 381: 50–5.
- 33 Tudek B. Base excision repair modulation as a risk factor for human cancers. Mol Aspects Med 2007; 28: 258–75.
- 34 Xing D, Qi J, Miao X, et al. Polymorphisms of DNA repair genes XRCC1 and XPD and their associations with risk of esophageal squamous cell carcinoma in a Chinese population. Int J Cancer 2002; 100: 600–5.
- 35 Divine KK, Gilliland FD, Crowell RE, et al. The XRCC1 399 glutamine allele is a risk factor for adenocarcinoma of the lung. Mutat Res 2001; 461: 273–8.
- 36 Olshan AF, Watson MA, Weissler MC, Bell DA. XRCC1 polymorphisms and head and neck cancer. Cancer Lett 2002; 178: 181–6.
- 37 Duell EJ, Holly EA, Bracci PM, Wiencke JK, Kelsey KT. A population-based study of the Arg399Gln polymorphism in X-ray repair cross-complementing group 1 (XRCC1) and risk of pancreatic adenocarcinoma. Cancer Res 2002; 62: 4630–6.
- 38 van Gils CH, Bostick RM, Stern MC, Taylor JA. Differences in base excision repair capacity may modulate the effect of dietary antioxidant intake on prostate cancer risk: an example of polymorphisms in the XRCC1 gene. Cancer Epidemiol Biomarkers Prev 2002; 11: 1279–84.
- 39 Shen M, Hung RJ, Brennan P, et al. 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 Biomarkers Prev 2003; 12: 1234–40.
- 40 Shu XO, Cai Q, Gao YT, et al. A population based case–control study of the Arg399Gln polymorphism in DNA repair gene XRCC1 and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2003; 12: 1462–7.
- 41 Matsuo K, Hamajima N, Suzuki R, et al. Lack of association between DNA base excision repair gene XRCC1 Gln399Arg polymorphism and risk of malignant lymphoma in Japan. Cancer Genet Cytogenet 2004; 149: 77–80.
- 42 Figueiredo JC, Knight JA, Briollais L, Andrulis IL, Ozcelik H. 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 2004; 13: 583–91.
- 43 Geng J, Zhang YW, Huang GC, Chen LB. XRCC1 genetic polymorphism Arg399Gln and gastric cancer risk: a meta-analysis. World J Gastroenterol 2008; 14: 6733–7.
- 44 Wang B, Wang D, Huang G, et al. XRCC1 polymorphisms and risk of colorectal cancer: a meta-analysis. Int J Colorectal Dis 2010; 25: 313–21.
- 45 Wang C, Sun Y, Han R. XRCC1genetic polymorphisms and bladder cancer susceptibility: a meta-analysis. Urology 2008; 72: 869–72.
- 46 Saadat M, Ansari-Lari M. Polymorphism of XRCC1 (at codon 399) and susceptibility to breast cancer, a meta-analysis of the literatures. Breast Cancer Res Treat 2009; 115: 137–44.
- 47 Geng J, Zhang Q, Zhu C, Wang J, Chen L. XRCC1 genetic polymorphism Arg399Gln and prostate cancer risk: a meta-analysis. Urology 2009; 72: 4648–53.
- 48 Kiyohara C, Takayama K, Nakanishi Y. Association of genetic polymorphisms in the base excision repair pathway with lung cancer risk: a meta-analysis. Lung Cancer 2006; 54: 267–83.
- 49 Mitchell AA, Cutler DJ, Chakravarti A. Undetected genotyping errors cause apparent overtransmission of common alleles in the transmission/disequilibrium test. Am J Hum Genet 2003; 72: 598–610.
- 50 Hosking L, Lumsden S, Lewis K, et al. Detection of genotyping errors by Hardy–Weinberg equilibrium testing. Eur J Hum Genet 2004; 12: 395–9.
- 51 Salanti G, Amountza G, Ntzani EE, Ioannidis JP. Hardy–Weinberg equilibrium in genetic association studies: an empirical evaluation of reporting, deviations, and power. Eur J Hum Genet 2005; 13: 840–8.
- 52 Trikalinos TA, Salanti G, Khoury MJ, Ioannidis JP. Impact of violations and deviations in Hardy–Weinberg equilibrium on postulated gene–disease associations. Am J Epidemiol 2006; 163: 300–9.
- 53 Benhamou S, Lee WJ, Alexandrie AK, et al. Meta- and pooled analyses of the effects of glutathione S-transferase M1 polymorphisms and smoking on lung cancer risk. Carcinogenesis 2002; 23: 1343–50.
- 54 Stephens JC, Schneider JA, Tanguay DA, et al. Haplotype variation and linkage disequilibrium in 313 human genes. Science 2001; 293: 489–93.
- 55 Juson R, Stephens JC, Windemuth A. The predictive power of haplotypes in clinical response. Pharmacogenomics 2000; 1: 15–26.
- 56 Fallin D, Cohen A, Essioux L, et al. Genetic analysis of case/control data using estimated haplotype frequencies: application to APOE locus variation and Alzheimer's disease. Genome Res 2001; 11: 143–51.
- 57 Lao T, Gu W, Huang Q. A meta-analysis on XRCC1 R399Q and R194W polymorphisms, smoking and bladder cancer risk. Mutagenesis 23: 523–32.