Tumor Biology

, Volume 34, Issue 3, pp 1431–1440 | Cite as

RETRACTED ARTICLE: Association of GSTT1 gene polymorphisms with the risk of prostate cancer: an updating meta-analysis

  • Jihong Wang
  • Yuemin Xu
  • Qiang Fu
  • Jianjun Yu
  • Zhong Chen
  • Zhangshun Liu
  • Chao Li
  • Hui Guo
  • Mingkai Xie
Research Article

Abstract

It has been demonstrated that the glutathione S-transferase (GST) superfamily helps remove carcinogens from the body and thus might be associated with prostate cancer risk. In recent years, GSTT1 polymorphism has been extensively studied as a potential prostate cancer risk factor; however, the results are inconsistent. To investigate the association between GSTT1 and prostate cancer, we conducted a meta-analysis of 33 studies with 6,697 prostate patients and 7,643 controls. For GSTM1 null versus present genotype, the random effects odds ratio was 0.98 (95 % confidence interval (CI) 0.83–1.16) based on a wide population. Subgroup analyses in the different ethnic groups and different controls were performed. The OR was 1.01 (95 % CI 0.86–1.19) in Caucasians, 1.01 (95 % CI 0.70–1.47) in Asians, and 0.77 (95 % CI 0.42–1.42) in Africans. The OR was 0.98 (95 % CI 0.82–1.16) in non-benign prostate hyperplasia (BPH) controls and 1.09 (95 % CI 0.66–1.79) in BPH controls. In conclusion, our present meta-analysis demonstrates that there is no association between GSTT1 polymorphism and prostate cancer, even in the sub-analysis concerning different races and control sources. The direction of further research should focus not only on the simple relationship of GSTT1 and prostate cancer but also on gene–environment interaction and distinctions of different GSTs.

Keywords

Prostate cancer Susceptibility Glutathione transferase GSTT1 Genetic polymorphism 

Notes

Conflicts of interest

None

References

  1. 1.
    Meyer UA. Overview of enzymes of drug metabolism. J Pharmacokinet Biopharm. 1996;24:449–59.CrossRefPubMedGoogle Scholar
  2. 2.
    Taningher M, Malacarne D, Izzotti A, Ugolini D, Parodi S. Drug metabolism polymorphisms as modulators of cancer susceptibility. Mutat Res. 1999;436:227–61.CrossRefPubMedGoogle Scholar
  3. 3.
    Ryberg D, Skaug V, Hewer A, Phillips DH, Harries LW, Wolf CR, Ogreid D, Ulvik A, Vu P, Haugen A. Genotypes of glutathione transferase m1 and p1 and their significance for lung DNA adduct levels and cancer risk. Carcinogenesis. 1997;18:1285–9.CrossRefPubMedGoogle Scholar
  4. 4.
    Hayes JD, Pulford DJ. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol. 1995;30:445–600.CrossRefPubMedGoogle Scholar
  5. 5.
    Pemble S, Schroeder KR, Spencer SR, Meyer DJ, Hallier E, Bolt HM, Ketterer B, Taylor JB. Human glutathione S-transferase theta (GSTT1): cDNA cloning and the characterization of a genetic polymorphism. Biochem J. 1994;300(Pt 1):271–6.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    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.PubMedGoogle Scholar
  7. 7.
    Ntais C, Polycarpou A, Ioannidis JP. Association of GSTM1, GSTT1, and GSTP1 gene polymorphisms with the risk of prostate cancer: a meta-analysis. Cancer Epidemiol Biomarkers Prev. 2005;14:176–81.PubMedGoogle Scholar
  8. 8.
    Mo Z, Gao Y, Cao Y, Gao F, Jian L. An updating meta-analysis of the GSTM1, GSTT1, and GSTP1 polymorphisms and prostate cancer: a huge review. Prostate. 2009;69:662–88.CrossRefPubMedGoogle Scholar
  9. 9.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Autrup JL, Thomassen LH, Olsen JH, Wolf H, Autrup H. Glutathione S-transferases as risk factors in prostate cancer. Eur J Cancer Prev. 1999;8:525–32.CrossRefPubMedGoogle Scholar
  11. 11.
    Rebbeck TR, Walker AH, Jaffe JM, White DL, Wein AJ, Malkowicz SB. Glutathione S-transferase-mu (GSTM1) and -theta (GSTT1) genotypes in the etiology of prostate cancer. Cancer Epidemiol Biomarkers Prev. 1999;8:283–7.PubMedGoogle Scholar
  12. 12.
    Steinhoff C, Franke KH, Golka K, Thier R, Romer HC, Rotzel C, Ackermann R, Schulz WA. Glutathione transferase isozyme genotypes in patients with prostate and bladder carcinoma. Arch Toxicol. 2000;74:521–6.CrossRefPubMedGoogle Scholar
  13. 13.
    Gsur A, Haidinger G, Hinteregger S, Bernhofer G, Schatzl G, Madersbacher S, Marberger M, Vutuc C, Micksche M. Polymorphisms of glutathione-S-transferase genes (GSTP1, GSTM1 and GSTT1) and prostate-cancer risk. Int J Cancer. 2001;95:152–5.CrossRefPubMedGoogle Scholar
  14. 14.
    Kote-Jarai Z, Easton D, Edwards SM, Jefferies S, Durocher F, Jackson RA, Singh R, Ardern-Jones A, Murkin A, Dearnaley DP, Shearer R, Kirby R, Houlston R, Eeles R. Collaborators CBUFPCS: relationship between glutathione S-transferase M1, P1 and T1 polymorphisms and early onset prostate cancer. Pharmacogenetics. 2001;11:325–30.CrossRefPubMedGoogle Scholar
  15. 15.
    Murata M, Watanabe M, Yamanaka M, Kubota Y, Ito H, Nagao M, Katoh T, Kamataki T, Kawamura J, Yatani R, Shiraishi T. Genetic polymorphisms in cytochrome P450 (CYP) 1A1, CYP1A2, CYP2E1, glutathione S-transferase (GST) M1 and GSTT1 and susceptibility to prostate cancer in the japanese population. Cancer Lett. 2001;165:171–7.CrossRefPubMedGoogle Scholar
  16. 16.
    Beer TM, Evans AJ, Hough KM, Lowe BA, McWilliams JE, Henner WD. Polymorphisms of GSTP1 and related genes and prostate cancer risk. Prostate Cancer Prostatic Dis. 2002;5:22–7.CrossRefPubMedGoogle Scholar
  17. 17.
    Kidd LC, Woodson K, Taylor PR, Albanes D, Virtamo J, Tangrea JA. Polymorphisms in glutathione-S-transferase genes (GST-M1, GST-T1 and GST-P1) and susceptibility to prostate cancer among male smokers of the atbc cancer prevention study. Eur J Cancer Prev. 2003;12:317–20.CrossRefPubMedGoogle Scholar
  18. 18.
    Nakazato H, Suzuki K, Matsui H, Koike H, Okugi H, Ohtake N, Takei T, Nakata S, Hasumi M, Ito K, Kurokawa K, Yamanaka H. Association of genetic polymorphisms of glutathione-S-transferase genes (GSTM1, GSTT1 and GSTP1) with familial prostate cancer risk in a Japanese population. Anticancer Res. 2003;23:2897–902.PubMedGoogle Scholar
  19. 19.
    Nam RK, Zhang WW, Trachtenberg J, Jewett MA, Emami M, Vesprini D, Chu W, Ho M, Sweet J, Evans A, Toi A, Pollak M, Narod SA. Comprehensive assessment of candidate genes and serological markers for the detection of prostate cancer. Cancer Epidemiol Biomarkers Prev. 2003;12:1429–37.PubMedGoogle Scholar
  20. 20.
    Joseph MA, Moysich KB, Freudenheim JL, Shields PG, Bowman ED, Zhang Y, Marshall JR, Ambrosone CB. Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutr Cancer. 2004;50:206–13.CrossRefPubMedGoogle Scholar
  21. 21.
    Medeiros R, Vasconcelos A, Costa S, Pinto D, Ferreira P, Lobo F, Morais A, Oliveira J, Lopes C. Metabolic susceptibility genes and prostate cancer risk in a southern european population: the role of glutathione S-transferases GSTM1, GSTM3, and GSTT1 genetic polymorphisms. Prostate. 2004;58:414–20.CrossRefPubMedGoogle Scholar
  22. 22.
    Mittal RD, Srivastava DS, Mandhani A, Kumar A, Mittal B. Polymorphism of GSTM1 and GSTT1 genes in prostate cancer: a study from north india. Indian J Cancer. 2004;41:115–9.PubMedGoogle Scholar
  23. 23.
    Caceres DD, Iturrieta J, Acevedo C, Huidobro C, Varela N, Quinones L. Relationship among metabolizing genes, smoking and alcohol used as modifier factors on prostate cancer risk: exploring some gene–gene and gene–environment interactions. Eur J Epidemiol. 2005;20:79–88.CrossRefPubMedGoogle Scholar
  24. 24.
    Komiya Y, Tsukino H, Nakao H, Kuroda Y, Imai H, Katoh T. Human glutathione S-transferase A1, T1, M1, and P1 polymorphisms and susceptibility to prostate cancer in the Japanese population. J Cancer Res Clin Oncol. 2005;131:238–42.CrossRefPubMedGoogle Scholar
  25. 25.
    Srivastava DS, Mandhani A, Mittal B, Mittal RD. Genetic polymorphism of glutathione S-transferase genes (GSTM1, GSTT1 and GSTP1) and susceptibility to prostate cancer in northern India. BJU Int. 2005;95:170–3.CrossRefPubMedGoogle Scholar
  26. 26.
    Agalliu I, Langeberg WJ, Lampe JW, Salinas CA, Stanford JL. Glutathione S-transferase M1, T1, and P1 polymorphisms and prostate cancer risk in middle-aged men. Prostate. 2006;66:146–56.CrossRefPubMedGoogle Scholar
  27. 27.
    Mittal RD, Mishra DK, Mandhani A. Evaluating polymorphic status of glutathione-S-transferase genes in blood and tissue samples of prostate cancer patients. Asian Pac J Cancer Prev. 2006;7:444–6.PubMedGoogle Scholar
  28. 28.
    Silig Y, Pinarbasi H, Gunes S, Ayan S, Bagci H, Cetinkaya O. Polymorphisms of CYP1A1, GSTM1, GSTT1, and prostate cancer risk in turkish population. Cancer Invest. 2006;24:41–5.CrossRefPubMedGoogle Scholar
  29. 29.
    Yang J, Wu HF, Zhang W, Gu M, Hua LX, Sui YG, Zhang ZD, Zhou JW, Wang XR, Zou C, Qian LX. Polymorphisms of metabolic enzyme genes, living habits and prostate cancer susceptibility. Front Biosci. 2006;11:2052–60.PubMedGoogle Scholar
  30. 30.
    Mallick S, Romana M, Blanchet P, Multigner L. GSTM1 and GSTT1 polymorphisms and the risk of prostate cancer in a caribbean population of african descent. Urology. 2007;69:1165–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Lima Jr MM, Oliveira MN, Granja F, Trindade AC, De Castro Santos LE, Ward LS. Lack of association of GSTT1, GSTM1, GSTO1, GSTP1 and CYP1A1 polymorphisms for susceptibility and outcome in brazilian prostate cancer patients. Folia Biol (Praha). 2008;54:102–8.Google Scholar
  32. 32.
    Lavender NA, Benford ML, VanCleave TT, Brock GN, Kittles RA, Moore JH, Hein DW, Kidd LC. Examination of polymorphic glutathione S-transferase (GST) genes, tobacco smoking and prostate cancer risk among men of african descent: a case–control study. BMC Cancer. 2009;9:397.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sivonova M, Waczulikova I, Dobrota D, Matakova T, Hatok J, Racay P, Kliment J. Polymorphisms of glutathione-S-transferase M1, T1, P1 and the risk of prostate cancer: a case–control study. J Exp Clin Cancer Res. 2009;28:32.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Souiden Y, Mahdouani M, Chaieb K, Elkamel R, Mahdouani K. Polymorphisms of glutathione-S-transferase M1 and T1 and prostate cancer risk in a Tunisian population. Cancer Epidemiol. 2010;34:598–603.CrossRefPubMedGoogle Scholar
  35. 35.
    Ashtiani ZO, Hasheminasab SM, Ayati M, Goulian BS, Modarressi MH. Are GSTM1, GSTT1 and CAG repeat length of androgen receptor gene polymorphisms associated with risk of prostate cancer in iranian patients? Pathol Oncol Res. 2011;17:269–75.CrossRefPubMedGoogle Scholar
  36. 36.
    Kumar V, Yadav CS, Datta SK, Singh S, Ahmed RS, Goel S, Gupta S, Mustafa M, Grover RK, Banerjee BD. Association of GSTM1 and GSTT1 polymorphism with lipid peroxidation in benign prostate hyperplasia and prostate cancer: a pilot study. Dis Markers. 2011;30:163–9.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kwon DD, Lee JW, Han DY, Seo IY, Park SC, Jeong HJ, Yang YS, Chae SC, Na KS, Mo KJ, Kim JJ, Rim JS. Relationship between the glutathione-S-transferase P1, M1, and T1 genotypes and prostate cancer risk in Korean subjects. Korean J Urol. 2011;52:247–52.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Rodrigues IS, Kuasne H, Losi-Guembarovski R, Fuganti PE, Gregorio EP, Kishima MO, Ito K, de Freitas Rodrigues MA, de Syllos Colus IM. Evaluation of the influence of polymorphic variants CYP1A1 2B, CYP1B1 2, CYP3A4 1B, GSTM1 0, and GSTT1 0 in prostate cancer. Urol Oncol. 2011;29:654–63.CrossRefPubMedGoogle Scholar
  39. 39.
    Safarinejad MR, Shafiei N, Safarinejad SH. Glutathione S-transferase gene polymorphisms (GSTM1, GSTT1, GSTP1) and prostate cancer: a case–control study in Tehran, Iran. Prostate Cancer Prostatic Dis. 2011;14:105–13.CrossRefPubMedGoogle Scholar
  40. 40.
    Thakur H, Gupta L, Sobti RC, Janmeja AK, Seth A, Singh SK. Association of GSTM1T1 genes with copd and prostate cancer in north Indian population. Mol Biol Rep. 2011;38:1733–9.CrossRefPubMedGoogle Scholar
  41. 41.
    Catsburg C, Joshi AD, Corral R, Lewinger JP, Koo J, John EM, Ingles SA, Stern MC. Polymorphisms in carcinogen metabolism enzymes, fish intake, and risk of prostate cancer. Carcinogenesis. 2012;33:1352–9.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Choubey VK, Sankhwar SN, Tewari R, Sankhwar P, Singh BP, Rajender S: Null genotypes at the GSTM1 and GSTT1 genes and the risk of benign prostatic hyperplasia: a case–control study and a meta-analysis. Prostate. 2013;73:146–52.CrossRefPubMedGoogle Scholar
  43. 43.
    Haas GP, Sakr WA. Epidemiology of prostate cancer. CA Cancer J Clin. 1997;47:273–87.CrossRefPubMedGoogle Scholar
  44. 44.
    Fost U, Hallier E, Ottenwalder H, Bolt HM, Peter H. Distribution of ethylene oxide in human blood and its implications for biomonitoring. Hum Exp Toxicol. 1991;10:25–31.CrossRefPubMedGoogle Scholar
  45. 45.
    Hallier E, Deutschmann S, Reichel C, Bolt HM, Peter H. A comparative investigation of the metabolism of methyl bromide and methyl iodide in human erythrocytes. Int Arch Occup Environ Health. 1990;62:221–5.CrossRefPubMedGoogle Scholar
  46. 46.
    Hallier E, Schroder KR, Asmuth K, Dommermuth A, Aust B, Goergens HW. Metabolism of dichloromethane (methylene chloride) to formaldehyde in human erythrocytes: influence of polymorphism of glutathione transferase theta (GST T1-1). Arch Toxicol. 1994;68:423–7.CrossRefPubMedGoogle Scholar
  47. 47.
    Guengerich FP, Thier R, Persmark M, Taylor JB, Pemble SE, Ketterer B. Conjugation of carcinogens by theta class glutathione S-transferases: mechanisms and relevance to variations in human risk. Pharmacogenetics. 1995;5 Spec No:S103–7.CrossRefPubMedGoogle Scholar
  48. 48.
    Wiencke JK, Pemble S, Ketterer B, Kelsey KT. 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.PubMedGoogle Scholar
  49. 49.
    Taioli E, Flores-Obando RE, Agalliu I, Blanchet P, Bunker CH, Ferrell RE, Jackson M, Kidd LC, Kolb S, Lavender NA, McFarlane-Anderson N, Morrison SS, Multigner L, Ostrande EA, Park JY, Patrick AL, Rebbeck TR, Romana M, Stanford JL, Ukoli F, Vancleave TT, Zeigler-Johnson CM, Mutetwa B, Ragin C. Multi-institutional prostate cancer study of genetic susceptibility in populations of African descent. Carcinogenesis. 2011;32:1361–5.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Gronberg H. Prostate cancer epidemiology. Lancet. 2003;361:859–64.CrossRefPubMedGoogle Scholar
  51. 51.
    Wei B, Xu Z, Zhou Y, Ruan J, Cheng H, Xi B, Zhu M, Jin K, Zhou D, Hu Q, Wang Q, Wang Z, Yan Z, Xuan F, Huang X, Zhang J, Zhou H. Association of gstm1 null allele with prostate cancer risk: evidence from 36 case–control studies. PLoS One. 2012;7:e46982.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Nemesure B, Wu SY, Hennis A, Leske MC. Family history of prostate cancer in a black population. J Immigr Minor Health 2012; doi: 10.1007/s10903-012-9710-7
  53. 53.
    Zuccolo L, Lewis SJ, Donovan JL, Hamdy FC, Neal DE, Smith GD. Alcohol consumption and PSA-detected prostate cancer risk—a case–control nested in the protect study. Int J Cancer. 2013;132:2176–85.CrossRefPubMedGoogle Scholar
  54. 54.
    Nock NL, Tang D, Rundle A, Neslund-Dudas C, Savera AT, Bock CH, Monaghan KG, Koprowski A, Mitrache N, Yang JJ, Rybicki BA. Associations between smoking, polymorphisms in polycyclic aromatic hydrocarbon (PAH) metabolism and conjugation genes and PAH-DNA adducts in prostate tumors differ by race. Cancer Epidemiol Biomarkers Prev. 2007;16:1236–45.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Mannervik B, Awasthi YC, Board PG, Hayes JD, Di Ilio C, Ketterer B, Listowsky I, Morgenstern R, Muramatsu M, Pearson WR, et al. Nomenclature for human glutathione transferases. Biochem J. 1992;282(Pt 1):305–6.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Widersten M, Pearson WR, Engstrom A, Mannervik B. Heterologous expression of the allelic variant mu-class glutathione transferases mu and psi. Biochem J. 1991;276(Pt 2):519–24.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Lof A, Johanson G, Rannug A, Warholm M. Glutathione transferase T1 phenotype affects the toxicokinetics of inhaled methyl chloride in human volunteers. Pharmacogenetics. 2000;10:645–53.CrossRefPubMedGoogle Scholar
  58. 58.
    Thier R, Lewalter J, Kempkes M, Selinski S, Bruning T, Bolt HM. Haemoglobin adducts of acrylonitrile and ethylene oxide in acrylonitrile workers, dependent on polymorphisms of the glutathione transferases GSTT1 and GSTM1. Arch Toxicol. 1999;73:197–202.CrossRefPubMedGoogle Scholar
  59. 59.
    Seidegard J, Pero RW, Miller DG, Beattie EJ. A glutathione transferase in human leukocytes as a marker for the susceptibility to lung cancer. Carcinogenesis. 1986;7:751–3.CrossRefPubMedGoogle Scholar
  60. 60.
    Kawajiri K, Nakachi K, Imai K, Watanabe J, Hayashi S. The CYP1A1 gene and cancer susceptibility. Crit Rev Oncol Hematol. 1993;14:77–87.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2013

Authors and Affiliations

  • Jihong Wang
    • 1
  • Yuemin Xu
    • 1
  • Qiang Fu
    • 1
  • Jianjun Yu
    • 1
  • Zhong Chen
    • 1
  • Zhangshun Liu
    • 1
  • Chao Li
    • 1
  • Hui Guo
    • 1
  • Mingkai Xie
    • 1
  1. 1.Department of Urology, Affiliated Sixth People’s HospitalShanghai Jiaotong UniversityShanghaiChina

Personalised recommendations