European Journal of Cancer
Volume 46, Issue 9 , Pages 1617-1631 , June 2010

GSTM1, GSTT1, GSTP1, GSTA1 and colorectal cancer risk: A comprehensive meta-analysis

  • Konstantinos P. Economopoulos

      Affiliations

    • School of Medicine, National University of Athens, Greece
    • Society of Junior Doctors, Athens, Greece
    • Corresponding Author InformationCorresponding author: Address: Society of Junior Doctors, 5 Menalou Street, Maroussi, Athens 15123, Greece. Tel.: +306942462812; fax: +302105593860.
    web address
  • ,
  • Theodoros N. Sergentanis

      Affiliations

    • School of Medicine, National University of Athens, Greece
    • Society of Junior Doctors, Athens, Greece

Received 21 November 2009 ,Revised 2 February 2010 ,Accepted 8 February 2010.

References 

  1. Cotton SC, Sharp L, Little J, Brockton N. Glutathione S-transferase polymorphisms and colorectal cancer: a HuGE review. Am J Epidemiol. 2000;151:7–32
  2. Bolt HM, Thier R. Relevance of the deletion polymorphisms of the glutathione S-transferases GSTT1 and GSTM1 in pharmacology and toxicology. Curr Drug Metab. 2006;7:613–628
  3. Raimondi S, Botteri E, Iodice S, Lowenfels AB, Maisonneuve P. Gene-smoking interaction on colorectal adenoma and cancer risk: review and meta-analysis. Mutat Res. 2009;670:6–14
  4. Gao Y, Pan X, Su T, et al. Glutathione S-transferase P1 Ile105Val polymorphism and colorectal cancer risk: A meta-analysis and HuGE review. Eur J Cancer. 2009;(July):[Epub ahead of print]
  5. Hengstler JG, Arand M, Herrero ME, Oesch F. Polymorphisms of N-acetyltransferases, glutathione S-transferases, microsomal epoxide hydrolase and sulfotransferases: influence on cancer susceptibility. Recent Results Cancer Res. 1998;154:47–85
  6. Dalhoff K, Buus Jensen K, Enghusen Poulsen H. Cancer and molecular biomarkers of phase 2. Methods Enzymol. 2005;400:618–627
  7. Dong LM, Potter JD, White E, et al. Genetic susceptibility to cancer: the role of polymorphisms in candidate genes. JAMA. 2008;299:2423–2436
  8. Liao C, Cao Y, Wu L, Huang J, Gao F. An updating meta-analysis of the glutathione S-transferase T1 polymorphisms and colorectal cancer risk: a HuGE review. Int J Colorectal Dis. 2009;(October):[Epub ahead of print]
  9. Sachse C, Smith G, Wilkie MJ, et al. A pharmacogenetic study to investigate the role of dietary carcinogens in the etiology of colorectal cancer. Carcinogenesis. 2002;23:1839–1849
  10. Sgambato A, Campisi B, Zupa A, et al. Glutathione S-transferase (GST) polymorphisms as risk factors for cancer in a highly homogeneous population from southern Italy. Anticancer Res. 2002;22:3647–3652
  11. van der Hel OL, Bueno de Mesquita HB, Roest M, et al. No modifying effect of NAT1, GSTM1, and GSTT1 on the relation between smoking and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev. 2003;12:681–682
  12. Rajagopal R, Deakin M, Fawole AS, et al. Glutathione S-transferase T1 polymorphisms are associated with outcome in colorectal cancer. Carcinogenesis. 2005;26:2157–2163
  13. Probst-Hensch NM, Sun CL, Van Den Berg D, et al. The effect of the cyclin D1 (CCND1) A870G polymorphism on colorectal cancer risk is modified by glutathione-S-transferase polymorphisms and isothiocyanate intake in the Singapore Chinese Health Study. Carcinogenesis. 2006;27:2475–2482
  14. Skjelbred CF, Saebo M, Hjartaker A, et al. Meat, vegetables, genetic polymorphisms, the risk of colorectal carcinomas, adenomas. BMC Cancer. 2007;7:228
  15. Cotterchio M, Boucher BA, Manno M, et al. Red meat intake, doneness, polymorphisms in genes that encode carcinogen-metabolizing enzymes, and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev. 2008;17:3098–3107
  16. Csejtei A, Tibold A, Varga Z, et al. GSTM, GSTT and p53 polymorphisms as modifiers of clinical outcome in colorectal cancer. Anticancer Res. 2008;28:1917–1922
  17. Matakova T, Sivonova M, Halasova E, et al. Polymorphisms of biotransforming enzymes (GSTs) and their association with colorectal cancer in the Slovak population. Neoplasma. 2009;56:422–427
  18. Harries LW, Stubbins MJ, Forman D, Howard GC, Wolf CR. Identification of genetic polymorphisms at the glutathione S-transferase Pi locus and association with susceptibility to bladder, testicular and prostate cancer. Carcinogenesis. 1997;18:641–644
  19. Sun XF, Ahmadi A, Arbman G, et al. Polymorphisms in sulfotransferase 1A1 and glutathione S-transferase P1 genes in relation to colorectal cancer risk and patients’ survival. World J Gastroenterol. 2005;11:6875–6879
  20. Katoh T, Kaneko S, Takasawa S, et al. Human glutathione S-transferase P1 polymorphism and susceptibility to smoking related epithelial cancer; oral, lung, gastric, colorectal and urothelial cancer. Pharmacogenetics. 1999;9:165–169
  21. Yoshioka M, Katoh T, Nakano M, et al. Glutathione S-transferase (GST) M1, T1, P1, N-acetyltransferase (NAT) 1 and 2 genetic polymorphisms and susceptibility to colorectal cancer. J UOEH. 1999;21:133–147
  22. Houlston RS, Tomlinson IP. Polymorphisms and colorectal tumor risk. Gastroenterology. 2001;121:282–301
  23. de Jong MM, Nolte IM, te Meerman GJ, et al. Low-penetrance genes and their involvement in colorectal cancer susceptibility. Cancer Epidemiol Biomarkers Prev. 2002;11:1332–1352
  24. Ye Z, Parry JM. A meta-analysis of 20 case-control studies of the glutathione S-transferase M1 (GSTM1) status and colorectal cancer risk. Med Sci Monit. 2003;9:SR83–SR91
  25. Chen K, Jiang QT, He HQ. Relationship between metabolic enzyme polymorphism and colorectal cancer. World J Gastroenterol. 2005;11:331–335
  26. Economopoulos KP, Sergentanis TN. Differential effects of MDM2 SNP309 polymorphism on breast cancer risk along with race: a meta-analysis. Breast Cancer Res Treat. 2010;120:211–216
  27. Economopoulos KP, Sergentanis TN. XRCC3 Thr241Met polymorphism and breast cancer risk: a meta-analysis. Breast Cancer Res Treat. 2009;(September):[Epub ahead of print]
  28. Sergentanis TN, Economopoulos KP. GSTT1 and GSTP1 polymorphisms and breast cancer risk: a meta-analysis. Breast Cancer Res Treat. 2009;(September):[Epub ahead of print]
  29. Sergentanis TN, Economopoulos KP. Four polymorphisms in cytochrome P450 1A1 (CYP1A1) gene and breast cancer risk: a meta-analysis. Breast Cancer Res Treat. 2009;(December):[Epub ahead of print]
  30. Sergentanis TN, Economopoulos KP. Association of two CASP8 polymorphisms with breast cancer risk: a meta-analysis. Breast Cancer Res Treat. 2010;120:229–234
  31. Economopoulos KP, Sergentanis TN. Three polymorphisms in cytochrome P450 1B1 (CYP1B1) gene and breast cancer risk: a meta-analysis. Breast Cancer Res Treat. 2010;(January):[Epub ahead of print]
  32. Cavalli-Sforza LL, Piazza A, Menozzi P, Mountain J. Reconstruction of human evolution: bringing together genetic, archaeological, and linguistic data. Proc Natl Acad Sci USA. 1988;85:6002–6006
  33. Cavalli-Sforza LL, Feldman MW. The application of molecular genetic approaches to the study of human evolution. Nat Genet. 2003;33(Suppl.):266–275
  34. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560
  35. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634
  36. Thakkinstian A, McElduff P, D’Este C, Duffy D, Attia J. A method for meta-analysis of molecular association studies. Stat Med. 2005;24:1291–1306
  37. Rohlfs RV, Weir BS. Distributions of Hardy–Weinberg equilibrium test statistics. Genetics. 2008;180:1609–1616
  38. Inoue H, Kiyohara C, Marugame T, et al. Cigarette smoking, CYP1A1 MspI and GSTM1 genotypes, and colorectal adenomas. Cancer Res. 2000;60:3749–3752
  39. Lin HJ, Probst-Hensch NM, Louie AD, et al. Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev. 1998;7:647–652
  40. Tijhuis MJ, Wark PA, Aarts JM, et al. GSTP1 and GSTA1 polymorphisms interact with cruciferous vegetable intake in colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev. 2005;14:2943–2951
  41. Murtaugh MA, Ma KN, Sweeney C, Caan BJ, Slattery ML. Meat consumption patterns and preparation, genetic variants of metabolic enzymes, and their association with rectal cancer in men and women. J Nutr. 2004;134:776–784
  42. Turner F, Smith G, Sachse C, et al. Vegetable, fruit and meat consumption and potential risk modifying genes in relation to colorectal cancer. Int J Cancer. 2004;112:259–264
  43. Yeh CC, Hsieh LL, Tang R, Chang-Chieh CR, Sung FC. Vegetable/fruit, smoking, glutathione S-transferase polymorphisms and risk for colorectal cancer in Taiwan. World J Gastroenterol. 2005;11:1473–1480
  44. Seow A, Yuan JM, Sun CL, et al. Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study. Carcinogenesis. 2002;23:2055–2061
  45. Chen K, Jiang QT, Ma XY, et al. Associations between genetic polymorphisms of glutathione S-transferase M1 and T1, smoking and susceptibility to colorectal cancer: a case-control study. Zhonghua Zhong Liu Za Zhi. 2004;26:645–648
  46. Chen K, Jin MJ, Fan CH, et al. A case-control study on the association between genetic polymorphisms of metabolic enzymes and the risk of colorectal cancer. Zhonghua Liu Xing Bing Xue Za Zhi. 2005;26:659–664
  47. Slattery ML, Potter JD, Ma KN. Western diet, family history of colorectal cancer, NAT2, GSTM-1 and risk of colon cancer. Cancer Causes Control. 2000;11:1–8
  48. Kampman E, Slattery ML, Bigler J, et al. Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case-control study. Cancer Epidemiol Biomarkers Prev. 1999;8:15–24
  49. Coles B, Nowell SA, MacLeod SL, et al. The role of human glutathione S-transferases (hGSTs) in the detoxification of the food-derived carcinogen metabolite N-acetoxy-PhIP, and the effect of a polymorphism in hGSTA1 on colorectal cancer risk. Mutat Res. 2001;482:3–10
  50. 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;94:936–942
  51. Luchtenborg M, Weijenberg MP, Kampman E, et al. Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am J Epidemiol. 2005;161:806–815
  52. Moisio AL, Sistonen P, Mecklin JP, Jarvinen H, Peltomaki P. Genetic polymorphisms in carcinogen metabolism and their association to hereditary nonpolyposis colon cancer. Gastroenterology. 1998;115:1387–1394
  53. Smits KM, Gaspari L, Weijenberg MP, et al. Interaction between smoking, GSTM1 deletion and colorectal cancer: results from the GSEC study. Biomarkers. 2003;8:299–310
  54. de Bruin WC, Wagenmans MJ, Board PG, Peters WH. Expression of glutathione S-transferase theta class isoenzymes in human colorectal and gastric cancers. Carcinogenesis. 1999;20:1453–1457
  55. Strange RC, Matharoo B, Faulder GC, et al. The human glutathione S-transferases: a case-control study of the incidence of the GST1 0 phenotype in patients with adenocarcinoma. Carcinogenesis. 1991;12:25–28
  56. Zhong S, Wyllie AH, Barnes D, Wolf CR, Spurr NK. Relationship between the GSTM1 genetic polymorphism and susceptibility to bladder, breast and colon cancer. Carcinogenesis. 1993;14:1821–1824
  57. Zupa A, Sgambato A, Bianchino G, et al. GSTM1 and NAT2 polymorphisms and colon, lung and bladder cancer risk: a case-control study. Anticancer Res. 2009;29:1709–1714
  58. Epplein M, Wilkens LR, Tiirikainen M, et al. Urinary isothiocyanates; glutathione S-transferase M1, T1, and P1 polymorphisms; and risk of colorectal cancer: the Multiethnic Cohort Study. Cancer Epidemiol Biomarkers Prev. 2009;18:314–320
  59. Kury S, Buecher B, Robiou-du-Pont S, et al. Low-penetrance alleles predisposing to sporadic colorectal cancers: a French case-controlled genetic association study. BMC Cancer. 2008;8:326
  60. Vlaykova T, Miteva L, Gulubova M, Stanilova S. Ile105Val GSTP1 polymorphism and susceptibility to colorectal carcinoma in Bulgarian population. Int J Colorectal Dis. 2007;22:1209–1215
  61. Yoshida K, Osawa K, Kasahara M, et al. Association of CYP1A1, CYP1A2, GSTM1 and NAT2 gene polymorphisms with colorectal cancer and smoking. Asian Pac J Cancer Prev. 2007;8:438–444
  62. Yeh CC, Sung FC, Tang R, Chang-Chieh CR, Hsieh LL. Association between polymorphisms of biotransformation and DNA-repair genes and risk of colorectal cancer in Taiwan. J Biomed Sci. 2007;14:183–193
  63. Martinez C, Martin F, Fernandez JM, et al. Glutathione S-transferases mu 1, theta 1, pi 1, alpha 1 and mu 3 genetic polymorphisms and the risk of colorectal and gastric cancers in humans. Pharmacogenomics. 2006;7:711–718
  64. Little J, Sharp L, Masson LF, et al. Colorectal cancer and genetic polymorphisms of CYP1A1, GSTM1 and GSTT1: a case-control study in the Grampian region of Scotland. Int J Cancer. 2006;119:2155–2164
  65. Huang K, Sandler RS, Millikan RC, et al. GSTM1 and GSTT1 polymorphisms, cigarette smoking, and risk of colon cancer: a population-based case-control study in North Carolina (United States). Cancer Causes Control. 2006;17:385–394
  66. Fan CH, Jin MJ, Zhang Y, et al. Association between genetic polymorphisms of metabolic enzymes and susceptibility of colorectal cancer. Zhonghua Yu Fang Yi Xue Za Zhi. 2006;40:13–17
  67. Landi S, Gemignani F, Moreno V, et al. A comprehensive analysis of phase I and phase II metabolism gene polymorphisms and risk of colorectal cancer. Pharmacogenet Genomics. 2005;15:535–546
  68. Ates NA, Tamer L, Ates C, et al. Glutathione S-transferase M1, T1, P1 genotypes and risk for development of colorectal cancer. Biochem Genet. 2005;43:149–163
  69. van der Logt EM, Bergevoet SM, Roelofs HM, et al. Genetic polymorphisms in UDP-glucuronosyltransferases and glutathione S-transferases and colorectal cancer risk. Carcinogenesis. 2004;25:2407–2415
  70. Kiss I, Nemeth A, Bogner B, et al. Polymorphisms of glutathione-S-transferase and arylamine N-acetyltransferase enzymes and susceptibility to colorectal cancer. Anticancer Res. 2004;24:3965–3970
  71. Slattery ML, Edwards S, Curtin K, Schaffer D, Neuhausen S. Associations between smoking, passive smoking, GSTM-1, NAT2, and rectal cancer. Cancer Epidemiol Biomarkers Prev. 2003;12:882–889
  72. Nascimento H, Coy CS, Teori MT, et al. Possible influence of glutathione S-transferase GSTT1 null genotype on age of onset of sporadic colorectal adenocarcinoma. Dis Colon Rectum. 2003;46:510–515
  73. Zhu Y, Deng C, Zhang Y, Zhou X, He X. The relationship between GSTM1, GSTT1 gene polymorphisms and susceptibility to sporadic colorectal adenocarcinoma. Zhonghua Nei Ke Za Zhi. 2002;41:538–540
  74. Ye Z, Parry JM. Genetic polymorphisms in the cytochrome P450 1A1, glutathione S-transferase M1 and T1, and susceptibility to colon cancer. Teratog Carcinog Mutagen. 2002;22:385–392
  75. Tiemersma EW, Kampman E, Bueno de Mesquita HB, et al. Meat consumption, cigarette smoking, and genetic susceptibility in the etiology of colorectal cancer: results from a Dutch prospective study. Cancer Causes Control. 2002;13:383–393
  76. Sweeney C, Coles BF, Nowell S, Lang NP, Kadlubar FF. Novel markers of susceptibility to carcinogens in diet: associations with colorectal cancer. Toxicology. 2002;181–182:83–87
  77. Laso N, Lafuente MJ, Mas S, et al. Glutathione S-transferase (GSTM1 and GSTT1)-dependent risk for colorectal cancer. Anticancer Res. 2002;22:3399–3403
  78. Saadat I, Saadat M. Glutathione S-transferase M1 and T1 null genotypes and the risk of gastric and colorectal cancers. Cancer Lett. 2001;169:21–26
  79. Loktionov A, Watson MA, Gunter M, et al. Glutathione-S-transferase gene polymorphisms in colorectal cancer patients: interaction between GSTM1 and GSTM3 allele variants as a risk-modulating factor. Carcinogenesis. 2001;22:1053–1060
  80. Butler WJ, Ryan P, Roberts-Thomson IC. Metabolic genotypes and risk for colorectal cancer. J Gastroenterol Hepatol. 2001;16:631–635
  81. Kiss I, Sandor J, Pajkos G, et al. Colorectal cancer risk in relation to genetic polymorphism of cytochrome P450 1A1, 2E1, and glutathione-S-transferase M1 enzymes. Anticancer Res. 2000;20:519–522
  82. Zhang H, Ahmadi A, Arbman G, et al. Glutathione S-transferase T1 and M1 genotypes in normal mucosa, transitional mucosa and colorectal adenocarcinoma. Int J Cancer. 1999;84:135–138
  83. Welfare M, Monesola Adeokun A, Bassendine MF, Daly AK. Polymorphisms in GSTP1, GSTM1, and GSTT1 and susceptibility to colorectal cancer. Cancer Epidemiol Biomarkers Prev. 1999;8:289–292
  84. Gawronska-Szklarz B, Lubinski J, Kladny J, et al. Polymorphism of GSTM1 gene in patients with colorectal cancer and colonic polyps. Exp Toxicol Pathol. 1999;51:321–325
  85. Abdel-Rahman SZ, Soliman AS, Bondy ML, et al. Polymorphism of glutathione S-transferase loci GSTM1 and GSTT1 and susceptibility to colorectal cancer in Egypt. Cancer Lett. 1999;142:97–104
  86. Slattery ML, Potter JD, Samowitz W, et al. NAT2, GSTM-1, cigarette smoking, and risk of colon cancer. Cancer Epidemiol Biomarkers Prev. 1998;7:1079–1084
  87. Lee E, Huang Y, Zhao B, et al. Genetic polymorphism of conjugating enzymes and cancer risk: GSTM1, GSTT1, NAT1 and NAT2. J Toxicol Sci. 1998;23(Suppl. 2):140–142
  88. Gertig DM, Stampfer M, Haiman C, et al. Glutathione S-transferase GSTM1 and GSTT1 polymorphisms and colorectal cancer risk: a prospective study. Cancer Epidemiol Biomarkers Prev. 1998;7:1001–1005
  89. Harris MJ, Coggan M, Langton L, Wilson SR, Board PG. Polymorphism of the Pi class glutathione S-transferase in normal populations and cancer patients. Pharmacogenetics. 1998;8:27–31
  90. Katoh T, Nagata N, Kuroda Y, et al. Glutathione S-transferase M1 (GSTM1) and T1 (GSTT1) genetic polymorphism and susceptibility to gastric and colorectal adenocarcinoma. Carcinogenesis. 1996;17:1855–1859
  91. Guo JY, Wan DS, Zeng RP, Zhang Q. The polymorphism of GSTM1, mutagen sensitivity in colon cancer and healthy control. Mutat Res. 1996;372:17–22
  92. Deakin M, Elder J, Hendrickse C, et al. Glutathione S-transferase GSTT1 genotypes and susceptibility to cancer: studies of interactions with GSTM1 in lung, oral, gastric and colorectal cancers. Carcinogenesis. 1996;17:881–884
  93. Chenevix-Trench G, Young J, Coggan M, Board P. Glutathione S-transferase M1 and T1 polymorphisms: susceptibility to colon cancer and age of onset. Carcinogenesis. 1995;16:1655–1657
  94. Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions version 5.0.1. The Cochrane Collaboration; 2008. Available from www.cochrane-handbook.org [accessed 29.08.09].
  95. Boccia S, La Torre G, Gianfagna F, Mannocci A, Ricciardi G. Glutathione S-transferase T1 status and gastric cancer risk: a meta-analysis of the literature. Mutagenesis. 2006;21:115–123
  96. La Torre G, Boccia S, Ricciardi G. Glutathione S-transferase M1 status and gastric cancer risk: a meta-analysis. Cancer Lett. 2005;217:53–60
  97. Higdon JV, Delage B, Williams DE, Dashwood RH. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res. 2007;55:224–236

PII: S0959-8049(10)00112-7

doi: 10.1016/j.ejca.2010.02.009

European Journal of Cancer
Volume 46, Issue 9 , Pages 1617-1631 , June 2010