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The XRCC1 Arg399Gln Genetic Polymorphism Contributes to Hepatocellular Carcinoma Susceptibility: An Updated Meta-analysis

  • Pan, Yan (Department of Integrative Oncology, Fudan University Shanghai Cancer Center) ;
  • Zhao, Lei (School of Chinese Medicine, Research Center of Heart, Brain, Hormone & Healthy Aging, The University of Hong Kong) ;
  • Chen, Xing-Miao (School of Chinese Medicine, Research Center of Heart, Brain, Hormone & Healthy Aging, The University of Hong Kong) ;
  • Gu, Yong (School of Chinese Medicine, Research Center of Heart, Brain, Hormone & Healthy Aging, The University of Hong Kong) ;
  • Shen, Jian-Gang (School of Chinese Medicine, Research Center of Heart, Brain, Hormone & Healthy Aging, The University of Hong Kong) ;
  • Liu, Lu-Ming (Department of Integrative Oncology, Fudan University Shanghai Cancer Center)
  • Published : 2013.10.30

Abstract

The potential correlation of X-ray repair cross-complementing group 1 (XRCC1) Arg399Gln polymorphism with hepatocellular carcinoma (HCC) susceptibility is ambiguous. Taking account of inconsistent results of previous meta-analyses and new emerging literatures, we conducted a meta-analysis covering 15 case-control datasets to evaluate the relationship. Relevant studies from Medline, Embase and CNKI were retrieved. A fixed-effect model or a random-effect model, depending on between-study heterogeneity, were applied to estimate the association between XRCC1 polymorphism Arg399Gln and HCC risk with the results presented as odds ratios (ORs) and 95% confidence intervals (95% CIs). In accordance with Hardy-Weinberg equilibrium, 15 studies with data for 6,556 individuals were enrolled in this systematic review. For overall HCC,thr XRCC1 polymorphism Arg399Gln was significantly associated with HCC susceptibility in a homozygote model as well as in a dominant model (G/G vs. A/A, OR=1.253, p=0.028; G/G+A/G vs. A/A, OR= 1.281, p=0.047, respectively), but not in a heterozygote model (A/G vs. A/A, OR=1.271, p=0.066) or a recessive model (G/G vs. A/G + A/A, OR= 1.049, p=0.542). Similar results were also observed on stratification analysis by ethnicity (A/G vs. A/A, OR=1.357, p=0.025; G/G vs. A/A, OR=1.310, p=0.011; G/G+A/G vs. A/A, OR= 1.371, p=0.013). However, no potential contribution of XRCC1 Arg399Gln polymorphism to HCC susceptibility in HBV/HCV subgroups was identified. No publication bias was found in this study. In conclusion, the XRCC1 Arg399Gln polymorphism contributes to HCC susceptibility. Due to the lack of studies in Western countries, further large-sample and rigorous studies are needed to validate the findings.

Keywords

Hepatocellular carcinoma;meta-analysis;SNPs;X-ray repair cross-complementing group 1

References

  1. Akinyinka OO, Falade AG, Ogunbiyi O, Johnson AO (2001). Hepatocellular carcinoma in Nigerian children. Ann Trop Paediatr, 21, 165-8. https://doi.org/10.1080/02724930120058250
  2. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50, 1088-101. https://doi.org/10.2307/2533446
  3. Borentain P, Gerolami V, Ananian P, et al (2007). DNA-repair and carcinogen- metabilising enzymes genetic polymorphisms as an independent risk factor for hepatocellular carcinoma in Caucasian liver-transplanted patients. Eur J Cancer, 43, 2479-86. https://doi.org/10.1016/j.ejca.2007.08.006
  4. Bose S, Tripathi DM, Sukriti, et al (2013). Genetic polymorphisms of CYP2E1 and DNA repair genes HOGG1 and XRCC1 Association with hepatitis B related advanced liver disease and cancer. Gene, 519, 231-7. https://doi.org/10.1016/j.gene.2013.02.025
  5. DerSimonian R, Laird N (1986). Meta-analysis in clinical trials. Control Clin Trials, 7, 177-88. https://doi.org/10.1016/0197-2456(86)90046-2
  6. Chacko P, Rajan B, Joseph T, Mathew BS, Pillai MR (2005). Polymorphisms in DNA repair gene XRCC1 and increased genetic susceptibility to breast cancer. Breast Cancer Res Treat, 89, 15-21. https://doi.org/10.1007/s10549-004-1004-x
  7. Chen CC, Yang SY, Liu CY, et al (2005). Association of cytokine and DNA repair gene polymorphisms with hepatitis B-related hepatocellular carcinoma. Int J Epidemiol, 34, 1310-8. https://doi.org/10.1093/ije/dyi191
  8. Cochran WG (1954). The combination of estimates from different experiments. Biometrics, 10, 101-29. https://doi.org/10.2307/3001666
  9. Ding F, Chen YY, Xie YA (2012). Correlations between XRCC1 genetic polymorphism Arg399Gln and susceptibility to hepa-tocellular carcinoma in liver cancer family clusters in Fusui county, Guangxi. Chin J of Oncol Prev and Treat, 4, 33-7. (article in Chinese)
  10. Egger M, Davey Smith G, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315, 629-34. https://doi.org/10.1136/bmj.315.7109.629
  11. Geng J, Zhang Q, Zhu C, Wang J, Chen L (2009). XRCC1 genetic polymorphism Arg399Gln and prostate cancer risk: a meta-analysis. Urology, 74, 648-53. https://doi.org/10.1016/j.urology.2009.02.046
  12. Geng J, Zhang YW, Huang GC, Chen LB (2008). XRCC1 genetic polymorphism Arg399Gln and gastric cancer risk: a meta-analysis. World J Gastroenterol, 14, 6733-7. https://doi.org/10.3748/wjg.14.6733
  13. Gulnaz A, Sayyed AH, Amin F, et al (2013). Association of XRCC1, XRCC3, and XPD genetic polymorphism with an increased risk of hepatocellular carcinoma because of the hepatitis B and C virus. Eur J Gastroenterol Hepatol, 25, 166-79. https://doi.org/10.1097/MEG.0b013e328359a775
  14. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003). Measuring inconsistency in meta- analyses. BMJ, 327, 557-60. https://doi.org/10.1136/bmj.327.7414.557
  15. Guo LY, Jin XP, Niu W, et al (2012). Association of XPD and XRCC1 Genetic Polymorphisms with Hepatocellular Carcinoma Risk. Asian Pac J Cancer Prev, 13, 4423-6. https://doi.org/10.7314/APJCP.2012.13.9.4423
  16. Han X, Xing Q, Li Y, et al (2012). Study on the DNA repair gene XRCC1 and XRCC3 polymorphism in prediction and prognosis of hepatocellular carcinoma risk. Hepatogastroenterology, 59, 2285-9.
  17. Han YN, Yang JL, Zhen SG (2004). Study on the association of human XRCC1-399 single nucleotide polymorphism and primary hepatocytic carcinoma. Liver, 12, 235-7. (article in Chinese)
  18. Hirschhorn JN, Lohmueller K, Byrne E, Hirschhorn K (2002). A comprehensive review of genetic association studies. Genet Med, 4, 45-61. https://doi.org/10.1097/00125817-200203000-00002
  19. Hu Z, Ma H, Chen F, Wei Q, Shen H (2005). XRCC1 polymorphisms and cancer risk: meta-analysis of 38 case-control studies. Cancer Epidemiol Biomarkers Prev, 14, 1810-8. https://doi.org/10.1158/1055-9965.EPI-04-0793
  20. Jia ZF, Su HY, Li XL, et al (2010). Polymorphisms of UGT1A7 and XRCC1 are associated with an increased risk of hepatocellular carcinoma in Northeast China. Chin J Cancer Res, 22, 260-6. https://doi.org/10.1007/s11670-010-0260-z
  21. Jung SW, Park NH, Shin JW, et al (2012). Polymorphisms of DNA repair genes in Korean hepatocellular carcinoma patients with chronic hepatitis B. J Hepatol, 57, 621-7. https://doi.org/10.1016/j.jhep.2012.04.039
  22. Kiran M, Chawla YK, Jain M, Kaur J (2009). Haplotypes of microsomal epoxide hydrolase and x-ray cross-complementing group 1 genes in Indian hepatocellular carcinoma patients. DNA Cell Biol, 28, 573-7. https://doi.org/10.1089/dna.2009.0921
  23. Lahtz C, Pfeifer GP (2011). Epigenetic changes of DNA repair genes in cancer. J Mol Cell Biol, 3, 51-8. https://doi.org/10.1093/jmcb/mjq053
  24. Kiran M, Saxena R, Chawla YK, Kaur J (2009). Polymorphism of DNA repair gene XRCC1 and hepatitis-related hepatocellular carcinoma risk in Indian population. Mol Cell Biochem, 327, 7-13. https://doi.org/10.1007/s11010-009-0035-3
  25. Kirk GD, Turner PC, Gong Y, et al (2005). Hepatocellular carcinoma and polymorphism in carcinogen-metabolizing and DNA repair enzymes in a population with aflatoxin exposure and hepatitis B virus endemicity. Cancer Epidemiol Biomarkers Prev, 14, 373-9. https://doi.org/10.1158/1055-9965.EPI-04-0161
  26. Kiyohara C, Takayama K, Nakanishi Y (2006). Association of genetic polymorphisms in the base excision repair pathway with lung cancer risk: a meta-analysis. Lung Cancer, 54, 267-83. https://doi.org/10.1016/j.lungcan.2006.08.009
  27. Lamerdin JE, Montgomery MA, Stilwagen SA, et al (1995). Genomic sequence comparison of human and mouse XRCC1 DNA repair gene regions. Genomics, 25, 547-54. https://doi.org/10.1016/0888-7543(95)80056-R
  28. Li J, Li Z, Feng L, Guo W, Zhang S (2013). Polymorphisms of DNA repair gene XRCC1 and hepatocellular carcinoma risk among East Asians: a meta-analysis. Tumor Biol, 34, 261-9. https://doi.org/10.1007/s13277-012-0546-5
  29. Li QW, Lu CR, Ye M, Xiao WH, Liang J (2012). Evaluation of DNA repair gene XRCC1 polymorphism in prediction and prognosis of hepatocellular carcinoma risk. Asian Pac J Cancer Prev, 13, 191-4. https://doi.org/10.7314/APJCP.2012.13.1.191
  30. Lindahl T, Wood RD (1999). Quality control by DNA repair. Science, 286, 1897-905. https://doi.org/10.1126/science.286.5446.1897
  31. Liu F, Li B, Wei Y, et al (2011). XRCC1 genetic polymorphism Arg399Gln and hepatocellular carcinoma risk: a meta-analysis. Liver Int, 31, 802-9. https://doi.org/10.1111/j.1478-3231.2011.02508.x
  32. Long XD, Ma Y, Wei YP, Deng ZL (2006). The polymorphisms of GSTM1, GSTT1, HYL1*2, and XRCC1, and aflatoxin B1-related hepatocellular carcinoma in Guangxi population, China. Hepatol Res, 36, 48-55. https://doi.org/10.1016/j.hepres.2006.06.004
  33. Long XD (2004). Polymorphism of DNA repair gene XRCC1 and risk of aflatoxin B1-related hepatocellular carcinoma. Available at http://dlib.cnki.net/kns50/detail.aspx?dbname = CMFD2004&filename = 200480557.nh (accessed 30 April 2013) (article in Chinese)
  34. Long XD, Ma Y, Huang HD, et al (2008). Polymorphism of XRCC1 and the frequency of mutation in codon 249 of the p53 gene in hepatocellular carcinoma among guangxi population, China. Mol Carcinog, 47, 295-300. https://doi.org/10.1002/mc.20384
  35. Long XD, Ma Y, Wei YP (2005). X-ray repair cross-complementing group1 (XRCC1) Arg399Gln polymorphism and aflatoxin B1 (AFB1)-related hepatocellular carcinoma (HCC) in Guangxi population. Chin J Cancer Res, 17, 17-21. https://doi.org/10.1007/s11670-005-0004-7
  36. Lopez LJ, Marrero JA (2004). Hepatocellular carcinoma. Curr Opin Gastroenterol, 20, 248-53. https://doi.org/10.1097/00001574-200405000-00009
  37. Mantel N, Haenszel W (1959). Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst, 22, 719-48.
  38. McKillop IH, Moran DM, Jin X, Koniaris LG (2006). Molecular pathogenesis of hepatocellular carcinoma. J Surg Res, 136, 125-35. https://doi.org/10.1016/j.jss.2006.04.013
  39. Miller MC 3rd, Mohrenweiser HW, Bell DA (2001). Genetic variability in susceptibility and response to toxicants. Toxicol Lett, 120, 269-80. https://doi.org/10.1016/S0378-4274(01)00279-X
  40. Mohana Devi S, Balachandar V, Arun M, et al (2013). Analysis of genetic damage and gene polymorphism in hepatocellular carcinoma (HCC) patients in a South Indian population. Dig Dis Sci, 58, 759-67. https://doi.org/10.1007/s10620-012-2409-8
  41. Saadat M, Ansari-Lari M (2009). Polymorphism of XRCC1 (at codon 399) and susceptibility to breast cancer, a meta-analysis of the literature. Breast Cancer Res Treat, 115, 137-44. https://doi.org/10.1007/s10549-008-0051-0
  42. Pan HZ, Liang J, Yu Z, et al (2011). Polymorphism of DNA repair gene XRCC1 and hepatocellular carcinoma risk in Chinese population. Asian Pac J Cancer Prev, 12, 2947-50.
  43. Price BD, D'Andrea AD (2013). Chromatin remodeling at DNA double-strand breaks. Cell, 152, 1344-54. https://doi.org/10.1016/j.cell.2013.02.011
  44. Ren Y, Wang DS, Li Z (2008). Study on the relationship between gene XRCC1 codon 399 single nucleotide polymorphisms and primary hepatic carcinoma in Han nationality. Chin J Clin Hepatol, 24, 361-5. (article in Chinese)
  45. Salanti G, Amountza G, Ntzani EE, loannidis JP (2005). Hardy-Weinberg equilibrium in genetic association studies: an empirical evaluation of reporting, deviations, and power. Eur J Hum Genet, 13, 840-8. https://doi.org/10.1038/sj.ejhg.5201410
  46. Seeberg E, Eide L, Bjoras M (1995). The base excision repair pathway. Trends Biochem Sci, 20, 391-7. https://doi.org/10.1016/S0968-0004(00)89086-6
  47. Siegel R, Naishadham D, Jemal A (2012). Cancer statistics, 2012. CA Cancer J Clin, 62, 10-29. https://doi.org/10.3322/caac.20138
  48. Smith TR, Miler MS, Lohman K, et al (2003). Polymorphisms of XRCC1 and XRCC3 genes and susceptibility to breast cancer. Cancer Lett, 190, 183-90. https://doi.org/10.1016/S0304-3835(02)00595-5
  49. Stern MC, Umbach DM, Lunn RM, Taylor JA (2002). DNA repair gene XRCC3 codon 241 polymorphism, its interaction with smoking and XRCC1 polymorphisms, and bladder cancer risk. Cancer Epidemiol Biomarkers Prev, 11, 939-43.
  50. 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, 6530-9. https://doi.org/10.1093/emboj/20.22.6530
  51. Su HY (2008). A case-control study on association between genetic polymorphisms of DNA repair and hepatic cell cancer susceptibility. Available at http://dlib.cnki.net/kns50/detail/aspx?dbname = CDFD2008&filename = 2008083042.nh (accessed 30 April 2013) (article in Chinese)
  52. Tang YT, Li XP, Liu TQ, et al (2011). Genetic polymorphisms of DNA repair genes in patients with hepatocellular carcinoma. Shandong Med J, 51, 19-20. (article in Chinese)
  53. Trikalinos TA, Salanti G, Khoury MJ, loannidis JP (2006). Impact of violations and deviations in Hardy-Weinberg equilibrium on postulated gene-disease associations. Am J Epidermiol, 163, 300-9.
  54. Wang B, Wang D, Huang G, et al (2010). XRCC1 polymorphisms and risk of colorectal cancer: a meta-analysis. Int J Colorectal Dis, 25, 313-21 https://doi.org/10.1007/s00384-009-0866-0
  55. Wang C, Sun Y, Han R (2008). XRCC1 genetic polymorphisms and bladder cancer susceptibility: a meta-analysis. Urology, 72, 869-72. https://doi.org/10.1016/j.urology.2007.12.059
  56. Wang DS (2006). Serological diagnosis and DNA repair gene XRCC1 polymorphism in patients with primary liver cancer. Available at http://dlib.cnki.net/kns50/detail.aspx?dbname = CMFD2007&filename = 2007101142.nh (accessed 30 April 2013) (article in Chinese)
  57. Whitehouse CJ, Taylor RM, Thistlethwaite A, et al (2001). XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell, 104, 107-17. https://doi.org/10.1016/S0092-8674(01)00195-7
  58. Yang JL, Han YN, Zhen SG (2004). Influence of human XRCC1-399 single nucleotide polymorphism on primary hepatocytic carcinoma. Tumor, 24, 322-4. (article in Chinese)
  59. Wu H (2009). Correlation between DNA Pepair Gene XRCC1 Single Nucleotide Polymorphism and Susceptibility to Hepatocellular Carcinoma in Fusui County of Guangxi. Available at http://dlib.cnki.net/kns50/detail.aspx?dbname = CMFD 2009&filename = 2009132690.nh. (accessed 30 April 2013) (article in Chinese)
  60. Wu H (2009). Correlation between DNA repair gene XRCC1 single nucleotide polymorphism and susceptibility to hepatocellular carcinoma in Fusui County of Guangxi. Available at http://dlib.cnki.net/kns50/detail.aspx?dbname=CMFD2009&filename=2009132690.nh (accessed 30 April 2013) (article in Chinese)
  61. Xie T, Wang ZG, Zhang JL, Liu H (2012). X-ray repair cross-complementing group 1 polymorphisms and hepatocellular carcinoma: a meta-analysis. World J Gastroenterol, 18, 4207 -14. https://doi.org/10.3748/wjg.v18.i31.4207
  62. Yu MW, Yang SY, Pan IJ, et al (2003). Polymorphisms in XRCC1 and glutathione S-transferase genes and hepatitis B-related hepatocellular carcinoma. J Natl Cancer Inst, 95, 1485-8. https://doi.org/10.1093/jnci/djg051
  63. Zeng XY, Huang JM, Xu JW, et al (2013). Meta-analysis demonstrates lack of a relationship between XRCC1 399 gene polymorphisms and susceptibility to hepatocellular carcinoma. Genet Mol Res, 12, 1916-23. https://doi.org/10.4238/2013.March.15.5
  64. Zeng XY, Yu HP, Qiu XQ, et al (2010). A case-control study of polymorphism of XRCC1 gene and the risk of hepatocellular carcinoma. Chin J Dis Control Prev, 14, 760-3. (article in Chinese)
  65. Zhang H, Wang P, Dai L, et al (2010). Meta-analysis of the relationship between polymorphisms of 399 point of X-ray repair cross complementing gene group 1 and hepatocellular carcinoma. Wei Sheng Yan Jiu, 39, 664-8. (article in Chinese)

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