Genetic variants of glutathione S-transferase as possible risk factors for hepatocellular carcinoma: A HuGE systematic review and meta-analysis

American Journal of Epidemiology

Volumn 167, Issue 4, 2008, Pages 377-389

  White, Donna L ^a   Li, Donghui ^b   Nurgalieva, Zhannat ^a   El Serag, Hashem B ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Carcinoma, hepatocellular; Epidemiology; Genetics; Glutathione S transferase pi; Glutathione transferase; Humans; Liver neoplasms; Meta analysis

Indexed keywords

GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE A1; GLUTATHIONE TRANSFERASE A4; GLUTATHIONE TRANSFERASE M1; GLUTATHIONE TRANSFERASE M2; GLUTATHIONE TRANSFERASE M3; GLUTATHIONE TRANSFERASE O1; GLUTATHIONE TRANSFERASE O2; GLUTATHIONE TRANSFERASE P1; GLUTATHIONE TRANSFERASE T1; UNCLASSIFIED DRUG;

ENZYME; GENETIC VARIATION; GENOTYPE; HETEROGENEITY; META-ANALYSIS; POLYMORPHISM; RISK FACTOR; TUMOR;

CANCER INCIDENCE; CANCER RISK; CONFIDENCE INTERVAL; DETOXIFICATION; GENE INTERACTION; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HUMAN; LIVER CELL CARCINOMA; REVIEW; RISK ASSESSMENT; RISK FACTOR; SYSTEMATIC REVIEW;

CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; CONFIDENCE INTERVALS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; GLUTATHIONE S-TRANSFERASE PI; GLUTATHIONE TRANSFERASE; HUMANS; INCIDENCE; ISOENZYMES; LIVER NEOPLASMS; ODDS RATIO; POLYMORPHISM, GENETIC; RISK FACTORS; TUMOR MARKERS, BIOLOGICAL; UNITED STATES;

AFRICA; ASIA; EURASIA; EUROPE;

EID: 39349093336     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kwm315     Document Type: Review

References (75)

1. Parkin DM. Global cancer statistics in the year 2000. Lancet Oncol 2001;2:533-43.
2. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 2004;127(suppl 1):S27-34.
3. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol 2005;45:51-88.
4. Landi S. Mammalian class theta GST and differential susceptibility to carcinogens: a review. Mutat Res 2000;463:247-83.
5. Salama SA, Abdel-Rahman SZ, Sierra-Torres CH, et al. Role of polymorphic GSTM1 and GSTT1 genotypes on NNK-induced genotoxicity. Pharmacogenetics 1999;9:735-43.
6. Strange RC, Spiteri MA, Ramachandran S, et al. Glutathione- S-transferase family of enzymes. Mutat Res 2001;482:21-6.
7. Okcu MF, Selvan M,Wang LE, et al. Glutathione S-transferase polymorphisms and survival in primary malignant glioma. Clin Cancer Res 2004;10:2618-25.
8. Daniel V. Glutathione S-transferases: gene structure and regulation of expression. Crit Rev Biochem Mol Biol 1993;28:173-207.
9. Rebbeck TR. Molecular epidemiology of the human glutathione S-transferase genotypes GSTM1 and GSTT1 in cancer susceptibility. Cancer Epidemiol Biomarkers Prev 1997;6:733-43.
10. Yang G, Shu XO, Ruan ZX, et al. Genetic polymorphisms in glutathione-S-transferase genes (GSTM1, GSTT1, GSTP1) and survival after chemotherapy for invasive breast carcinoma. Cancer 2005;103:52-8.
11. Stoehlmacher J, Park DJ, Zhang W, et al. Association between glutathione S-transferase P1, T1, and M1 genetic polymorphism and survival of patients with metastatic colorectal cancer. J Natl Cancer Inst 2002;94:936-42.
12. Hohaus S, Di RA, Di FA, et al. Glutathione S-transferase P1 genotype and prognosis in Hodgkin's lymphoma. Clin Cancer Res 2005;11:2175-9.
13. Ambrosone CB, Sweeney C, Coles BF, et al. Polymorphisms in glutathione S-transferases (GSTM1 and GSTT1) and survival after treatment for breast cancer. Cancer Res 2001;61:7130-5.
14. Hayes JD, Strange RC. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 2000;61:154-66.
15. Norppa H. Cytogenetic biomarkers and genetic polymorphisms. Toxicol Lett 2004;149:309-34.
16. Garte S, Gaspari L, Alexandrie AK, et al. Metabolic gene polymorphism frequencies in control populations. Cancer Epidemiol Biomarkers Prev 2001;10:1239-48.
17. Hagen TM, Huang S, Curnutte J, et al. Extensive oxidative DNA damage in hepatocytes of transgenic mice with chronic active hepatitis destined to develop hepatocellular carcinoma. Proc Natl Acad Sci U S A 1994;91:12808-12.
18. Harris MJ, Coggan M, Langton L, et al. Polymorphism of the Pi class glutathione S-transferase in normal populations and cancer patients. Pharmacogenetics 1998;8:27-31.
19. Ali-Osman F, Akande O, Antoun G, et al. Molecular cloning, characterization, and expression in Escherichia coli of full-length cDNAs of three human glutathione S-transferase Pi gene variants. Evidence for differential catalytic activity of the encoded proteins. J Biol Chem 1997;272:10004-12.
20. Watson MA, Stewart RK, Smith GB, et al. Human glutathione S-transferase P1 polymorphisms: relationship to lung tissue enzyme activity and population frequency distribution. Carcinogenesis 1998;19:275-80.
21. Packer BR, Yeager M, Burdett L, et al. SNP500Cancer: a public resource for sequence validation, assay development, and frequency analysis for genetic variation in candidate genes. Nucleic Acids Res 2006;34(database issue):D617-21. (http://snp500cancer.nci.nih.gov/home.cfm). (Accessed December 1, 2006).
22. Khoury MJ, Little J. Human genome epidemiologic reviews: the beginning of something HuGE. Am J Epidemiol 2000;151:2-3.
23. Little J, Khoury MJ. Mendelian randomisation: a new spin or real progress? Lancet 2003;362:930-1.
24. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-Analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008-12.
25. Petitti DB. Meta-analysis, decision analysis, and cost-effectiveness analysis: methods for quantitative synthesis in medicine. 2nd ed. New York, NY: Oxford University Press, 2000.
26. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58.
27. Dersimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88.
28. Egger M, Davey SG, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34.
29. 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 Biomarkers Prev 2005;14:373-9.
30. Covolo L, Gelatti U, Talamini R, et al. Alcohol dehydrogenase 3, glutathione S-transferase M1 and T1 polymorphisms, alcohol consumption and hepatocellular carcinoma (Italy). Cancer Causes Control 2005;16:831-8.
31. 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;34:1310-18.
32. Deng ZL, Wei YP, Ma Y. Polymorphism of glutathione S-transferase mu 1 and theta 1 genes and hepatocellular carcinoma in southern Guangxi, China. World J Gastroenterol 2005;11:272-4.
33. Yu MW, Chiu YH, Chiang YC, et al. Plasma carotenoids, glutathione S-transferase M1 and T1 genetic polymorphisms, and risk of hepatocellular carcinoma: independent and interactive effects. Am J Epidemiol 1999;149:621-9.
34. Tiemersma EW, Omer RE, Bunschoten A, et al. Role of genetic polymorphism of glutathione-S-transferase T1 and microsomal epoxide hydrolase in aflatoxin-associated hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev 2001;10:785-91.
35. Ladero JM, Martinez C, Garcia-Martin E, et al. Glutathione S-transferase M1 and T1 genetic polymorphisms are not related to the risk of hepatocellular carcinoma: a study in the Spanish population. Eur J Cancer 2006;42:73-7.
36. Munaka M, Kohshi K, Kawamoto T, et al. Genetic polymorphisms of tobacco- and alcohol-related metabolizing enzymes and the risk of hepatocellular carcinoma. J Cancer Res Clin Oncol 2003;129:355-60.
37. Sun CA, Wang LY, Chen CJ, et al. Genetic polymorphisms of glutathione S-transferases M1 and T1 associated with susceptibility to aflatoxin-related hepatocarcinogenesis among chronic hepatitis B carriers: a nested case-control study in Taiwan. Carcinogenesis 2001;22:1289-94.
38. Liu CZ, Bian JC, Jiang F, et al. Genetic polymorphisms of glutathione S-transferases M1, T1, P1 on susceptibility hepatocellular carcinoma. (In Chinese). China Public Health 2002;18:935-6.
39. Zhu MH, Chen XH, Zhou LF. Association of genetic polymorphisms in glutathione S-transferases M1 with hepatitis beta-related hepatocellular carcinoma. (In Chinese). Zhejiang Da Xue Xue Bao Yi Xue Ban 2005;34:126-30.
40. 1 related hepatocellular carcinoma in Guangxi. (In Chinese). Zhonghua Liu Xing Bing Xue Za Zhi 2005;26:777-81.
41. Marahatta SB, Punyarit P, Bhudisawasdi V, et al. Polymorphism of glutathione S-transferase omega gene and risk of cancer. Cancer Lett 2006;236:276-81.
42. 1-related hepatocellular carcinoma in Guangxi population, China. Hepatol Res 2006;36:48-55.
43. Gelatti U, Covolo L, Talamini R, et al. N-Acetyltransferase-2, glutathione S-transferase M1 and T1 genetic polymorphisms, cigarette smoking and hepatocellular carcinoma: a case-control study. Int J Cancer 2005;115:301-6.
44. 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.
45. Chen CJ, Yu MW, Liaw YF, et al. Chronic hepatitis B carriers with null genotypes of glutathione S-transferase M1 and T1 polymorphisms who are exposed to aflatoxin are at increased risk of hepatocellular carcinoma. Am J Hum Genet 1996;59:128-34.
46. Hsieh LL, Huang RC, Yu MW, et al. L-myc, GST M1 genetic polymorphism and hepatocellular carcinoma risk among chronic hepatitis B carriers. Cancer Lett 1996;103:171-6.
47. Ma Y, Deng Z, Wei YP. Study of the deletion mutation of glutathione S transferase M1 gene and its role in susceptibility to hepatocellular carcinoma. Chin J Cancer Res 2001;13:176-8.
48. Deng Z, Wei Y, Ma Y. Glutathione-S-transferase M1 genotype in patients with hepatocellular carcinoma. (In Chinese). Zhonghua Zhong Liu Za Zhi 2001;23:477-9.
49. Yu MW, Gladek-Yarborough A, Chiamprasert S, et al. Cytochrome P450 2E1 and glutathione S-transferase M1 polymorphisms and susceptibility to hepatocellular carcinoma. Gastroenterology 1995;109:1266-73.
50. Omer RE, Verhoef L, Van't Veer P, et al. Peanut butter intake, GSTM1 genotype and hepatocellular carcinoma: a case-control study in Sudan. Cancer Causes Control 2001;12:23-32.
51. 1-related primary hepatocellular carcinoma in mice and humans. Cancer Res 2003;63:4594-601.
52. London WT, Evans AA, Buetow K, et al. Molecular and genetic epidemiology of hepatocellular carcinoma: studies in China and Senegal. Princess Takamatsu Symp 1995;25:51-60.
53. Bian JC, Shen FM, Shen L, et al. Susceptibility to hepatocellular carcinoma associated with null genotypes of GSTM1 and GSTT1. World J Gastroenterol 2000;6:228-30.
54. Bian JC, Shen F, Shen L, et al. Susceptibility to hepatocellular carcinoma is associated with the null genotypes of GSTM1 and GSTT1. (In Chinese). Chin J Dig 1999;19:87-90.
55. 1-related hepatocellular carcinoma. (In Chinese). Zhonghua Gan Zang Bing Za Zhi 2005;13:668-70.
56. Zhou T, Evans AA, London WT, et al. Glutathione S-transferase expression in hepatitis B virus-associated human hepatocellular carcinogenesis. Cancer Res 1997;57:2749-53.
57. Chen SY, Wang LY, Lunn RM, et al. Polycyclic aromatic hydrocarbon-DNA adducts in liver tissues of hepatocellular carcinoma patients and controls. Int J Cancer 2002;99:14-21.
58. 1. Proc Natl Acad Sci U S A 1995;92:2384-7.
59. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 1999;340:745-50.
60. Brind AM, Hurlstone A, Edrisinghe D, et al. The role of polymorphisms of glutathione S-transferases GSTM1, M3, P1, T1 and A1 in susceptibility to alcoholic liver disease. Alcohol Alcohol 2004;39:478-83.
61. Savolainen VT, Pjarinen J, Perola M, et al. Glutathione- S-transferase GST M1 "null" genotype and the risk of alcoholic liver disease. Alcohol Clin Exp Res 1996;20:1340-5.
62. Angulo P. GI epidemiology: nonalcoholic fatty liver disease. Aliment Pharmacol Ther 2007;25:883-9.
63. Nobili V, Pastore A, Gaeta LM, et al. Glutathione metabolism and antioxidant enzymes in patients affected by nonalcoholic steatohepatitis. Clin Chim Acta 2005;355:105-11.
64. Wiencke JK, Pemble S, Ketterer B, et al. Gene deletion of glutathione S-transferase theta: correlation with induced genetic damage and potential role in endogenous mutagenesis. Cancer Epidemiol Biomarkers Prev 1995;4:253-9.
65. Duell EJ, Holly EA, Bracci PM, et al. A population-based, case-control study of polymorphisms in carcinogen-metabolizing genes, smoking, and pancreatic adenocarcinoma risk. J Natl Cancer Inst 2002;94:297-306.
66. Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted? Stat Med 2002;21:1559-73.
67. Trikalinos TA, Ntzani EE, Contopoulos-Ioannidis DG, et al. Establishment of genetic associations for complex diseases is independent of early study findings. Eur J Hum Genet 2004;12:762-9.
68. Ioannidis JP, Trikalinos TA. Early extreme contradictory estimates may appear in published research: the Proteus phenomenon in molecular genetics research and randomized trials. J Clin Epidemiol 2005;58:543-9.
69. Rothman K, Greenland S. Causation and causal inference. In: Rothman K, Greenland S, eds. Modern epidemiology. Philadelphia, PA: Lippincott-Raven, 1998:7-28.
70. Yang Q, Khoury MJ, Friedman J, et al. How many genes underlie the occurrence of common complex diseases in the population? Int J Epidemiol 2005;34:1129-37.
71. Lohmueller KE, Pearce CL, Pike M, et al. Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat Genet 2003;33:177-82.
72. Hattersley AT, McCarthy MI. What makes a good genetic association study? Lancet 2005;366:1315-23.
73. Thakkinstian A, Bowe S, McEvoy M. Association between apolipoprotein E polymorphisms and age-related macular degeneration: a HuGE review and meta-analysis. Am J Epidemiol 2006;164:813-22.
74. Greenland S, O'Rourke K. On the bias produced by quality scores in meta-analysis, and a hierarchical view of proposed solutions. Biostatistics 2001;2:463-71.
75. Hoffmann R, Valencia A. A gene network for navigating the literature. (Letter). Nat Genet 2004;36:664.