Advertisement

Tumor Biology

, Volume 37, Issue 8, pp 10229–10234 | Cite as

Glutathione S-transferase M1 null genotype related to poor prognosis of colorectal cancer

Original Article

Abstract

Published studies showed controversial findings about the relationship between glutathione S-transferase M1 (GSTM1) null genotype and clinical outcomes of patients with colorectal cancer. We performed a meta-analysis to quantitatively assess the association between GSTM1 null genotype and prognosis of patients with colorectal cancer. We systematically searched Pubmed, Embase, and Web of Science to identify prospective or retrospective cohort studies assessing the association of GSTM1 null genotype with overall survival (OS) or disease-free survival (DFS) in colorectal cancer. The hazard ratios (HRs) and 95 % confidence intervals (95 % CIs) were used to assess the association of GSTM1 null genotype with OS or DFS. Finally, 15 studies from 14 publications with 4326 colorectal cancer patients were included into the meta-analysis. There was no heterogeneity in the meta-analysis relating OS (I 2 = 0 %) and DFS (I 2 = 0 %). Overall, GSTM1 null genotype was significantly associated with poor OS in patients with colorectal cancer (HR = 1.18, 95 % CI 1.07–1.30, P = 0.001). In addition, GSTM1 null genotype was also significantly associated with poor DFS in patients with colorectal cancer (HR = 1.15, 95 % CI 1.03–1.28, P = 0.015). No obvious risk of publication bias was observed. GSTM1 null genotype is significantly associated with poor OS and DFS in patients with colorectal cancer, which suggests that GSTM1 null genotype confers poor effect on the prognosis of colorectal cancer.

Keywords

Colorectal cancer Glutathione S-transferase M1 Prognosis 

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation (81430062). This work was also supported in part by the program for Development of Innovative Research Team in the First Affiliated Hospital of NJMU and the Priority Academic Program of Jiangsu Higher Education Institutions.

Compliance with ethical standards

Conflicts of interest

None

References

  1. 1.
    Cunningham D, Atkin W, Lenz HJ, Lynch HT, Minsky B, Nordlinger B, et al. Colorectal cancer. Lancet. 2010;375:1030–47.CrossRefPubMedGoogle Scholar
  2. 2.
    Ferlitsch M, Reinhart K, Pramhas S, Wiener C, Gal O, Bannert C, et al. Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA. 2011;306:1352–8.CrossRefPubMedGoogle Scholar
  3. 3.
    Price TJ, Segelov E, Burge M, Haller DG, Ackland SP, Tebbutt NC, et al. Current opinion on optimal treatment for colorectal cancer. Expert Rev Anticancer Ther. 2013;13:597–611.CrossRefPubMedGoogle Scholar
  4. 4.
    Audisio RA, Papamichael D. Treatment of colorectal cancer in older patients. Nat Rev Gastroenterol Hepatol. 2012;9:716–25.CrossRefPubMedGoogle Scholar
  5. 5.
    Marin JJ, Sanchez de Medina F, Castano B, Bujanda L, Romero MR, Martinez-Augustin O, et al. Chemoprevention, chemotherapy, and chemoresistance in colorectal cancer. Drug Metab Rev. 2012;44:148–72.CrossRefPubMedGoogle Scholar
  6. 6.
    Blumenstein I, Tacke W, Bock H, Filmann N, Lieber E, Zeuzem S, et al. Prevalence of colorectal cancer and its precursor lesions in symptomatic and asymptomatic patients undergoing total colonoscopy: results of a large prospective, multicenter, controlled endoscopy study. Eur J Gastroenterol Hepatol. 2013;25:556–61.CrossRefPubMedGoogle Scholar
  7. 7.
    Rossi L, Vakiarou F, Zoratto F, Bianchi L, Papa A, Basso E, et al. Factors influencing choice of chemotherapy in metastatic colorectal cancer (mCRC). Cancer Manag Res. 2013;5:377–85.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Di Pietro G, Magno LA, Rios-Santos F. Glutathione S-transferases: an overview in cancer research. Expert Opin Drug Metab Toxicol. 2010;6:153–70.CrossRefPubMedGoogle Scholar
  9. 9.
    Tew KD, Townsend DM. Glutathione-s-transferases as determinants of cell survival and death. Antioxid Redox Signal. 2012;17:1728–37.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Lo HW, Ali-Osman F. Genetic polymorphism and function of glutathione S-transferases in tumor drug resistance. Curr Opin Pharmacol. 2007;7:367–74.CrossRefPubMedGoogle Scholar
  11. 11.
    Katoh T, Yamano Y, Tsuji M, Watanabe M. Genetic polymorphisms of human cytosol glutathione S-transferases and prostate cancer. Pharmacogenomics. 2008;9:93–104.CrossRefPubMedGoogle Scholar
  12. 12.
    Fang J, Wang S, Zhang S, Su S, Song Z, Deng Y, et al. Association of the glutathione s-transferase m1, t1 polymorphisms with cancer: evidence from a meta-analysis. PLoS One. 2013;8:e78707.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Cai Q, Wang Z, Zhang W, Guo X, Shang Z, Jiang N, et al. Association between glutathione S-transferases M1 and T1 gene polymorphisms and prostate cancer risk: a systematic review and meta-analysis. Tumour Biol. 2014;35:247–56.CrossRefPubMedGoogle Scholar
  14. 14.
    Cai X, Yang L, Chen H, Wang C. An updated meta-analysis of the association between GSTM1 polymorphism and colorectal cancer in Asians. Tumour Biol. 2014;35:949–53.CrossRefPubMedGoogle Scholar
  15. 15.
    Wang X, Huang ZH. Predictive potential role of glutathione S-transferase polymorphisms in the prognosis of breast cancer. Genet Mol Res. 2015;14:10236–41.CrossRefPubMedGoogle Scholar
  16. 16.
    Li GN, Li XM, Liu YQ, Bao ZQ, Yang LX, Wang X, et al. Association between glutathione S-transferases M1 and T1 gene polymorphisms and esophageal cancer prognosis. Int J Clin Exp Med. 2015;8:3300–8.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Kap EJ, Richter S, Rudolph A, Jansen L, Ulrich A, Hoffmeister M, et al. Genetic variants in the glutathione S-transferase genes and survival in colorectal cancer patients after chemotherapy and differences according to treatment with oxaliplatin. Pharmacogenet Genomics. 2014;24:340–7.CrossRefPubMedGoogle Scholar
  18. 18.
    Negandhi AA, Hyde A, Dicks E, Pollett W, Younghusband BH, Parfrey P, et al. MTHFR Glu429Ala and ERCC5 His46His polymorphisms are associated with prognosis in colorectal cancer patients: analysis of two independent cohorts from Newfoundland. PLoS One. 2013;8:e61469.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    McLeod HL, Sargent DJ, Marsh S, Green EM, King CR, Fuchs CS, et al. Pharmacogenetic predictors of adverse events and response to chemotherapy in metastatic colorectal cancer: results from North American Gastrointestinal Intergroup Trial N9741. J Clin Oncol. 2010;28:3227–33.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Funke S, Timofeeva M, Risch A, Hoffmeister M, Stegmaier C, Seiler CM, et al. Genetic polymorphisms in GST genes and survival of colorectal cancer patients treated with chemotherapy. Pharmacogenomics. 2010;11:33–41.CrossRefPubMedGoogle Scholar
  21. 21.
    Boige V, Mendiboure J, Pignon JP, Loriot MA, Castaing M, Barrois M, et al. Pharmacogenetic assessment of toxicity and outcome in patients with metastatic colorectal cancer treated with LV5FU2, FOLFOX, and FOLFIRI: FFCD 2000–05. J Clin Oncol. 2010;28:2556–64.CrossRefPubMedGoogle Scholar
  22. 22.
    Jones BA, Christensen AR, Wise Sr JP, Yu H. Glutathione S-transferase polymorphisms and survival in African-American and white colorectal cancer patients. Cancer Epidemiol. 2009;33:249–56.CrossRefPubMedGoogle Scholar
  23. 23.
    Funke S, Risch A, Nieters A, Hoffmeister M, Stegmaier C, Seiler CM, et al. Genetic polymorphisms in genes related to oxidative stress (GSTP1, GSTM1, GSTT1, CAT, MnSOD, MPO, eNOS) and survival of rectal cancer patients after radiotherapy. J Cancer Epidemiol. 2009;2009:302047.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ruzzo A, Graziano F, Loupakis F, Rulli E, Canestrari E, Santini D, et al. Pharmacogenetic profiling in patients with advanced colorectal cancer treated with first-line FOLFOX-4 chemotherapy. J Clin Oncol. 2007;25:1247–54.CrossRefPubMedGoogle Scholar
  25. 25.
    Holley SL, Rajagopal R, Hoban PR, Deakin M, Fawole AS, Elder JB, et al. Polymorphisms in the glutathione S-transferase mu cluster are associated with tumour progression and patient outcome in colorectal cancer. Int J Oncol. 2006;28:231–6.PubMedGoogle Scholar
  26. 26.
    Gordon MA, Gil J, Lu B, Zhang W, Yang D, Yun J, et al. Genomic profiling associated with recurrence in patients with rectal cancer treated with chemoradiation. Pharmacogenomics. 2006;7:67–88.CrossRefPubMedGoogle Scholar
  27. 27.
    Stoehlmacher J, Park DJ, Zhang W, Yang D, Groshen S, Zahedy S, et al. A multivariate analysis of genomic polymorphisms: prediction of clinical outcome to 5-FU/oxaliplatin combination chemotherapy in refractory colorectal cancer. Br J Cancer. 2004;91:344–54.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Stoehlmacher J, Park DJ, Zhang W, Groshen S, Tsao-Wei DD, Yu MC, 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.CrossRefPubMedGoogle Scholar
  29. 29.
    Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101–29.CrossRefGoogle Scholar
  30. 30.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.CrossRefPubMedGoogle Scholar
  32. 32.
    Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22:719–48.PubMedGoogle Scholar
  33. 33.
    Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Csejtei A, Tibold A, Varga Z, Koltai K, Ember A, Orsos Z, et al. GSTM, GSTT and p53 polymorphisms as modifiers of clinical outcome in colorectal cancer. Anticancer Res. 2008;28:1917–22.PubMedGoogle Scholar
  35. 35.
    Lai CY, Hsieh LL, Sung FC, Tang R, Bai CH, Wu FY, et al. Tumor site- and stage-specific associations between allelic variants of glutathione S-transferase and DNA-repair genes and overall survival in colorectal cancer patients receiving 5-fluorouracil-based chemotherapy. PLoS One. 2013;8:e69039.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Chen J, Ye Y, Sun H, Shi G. Association between KRAS codon 13 mutations and clinical response to anti-EGFR treatment in patients with metastatic colorectal cancer: results from a meta-analysis. Cancer Chemother Pharmacol. 2013;71:265–72.CrossRefPubMedGoogle Scholar
  37. 37.
    Ye F, Liu Z, Tan A, Liao M, Mo Z, Yang X. XRCC1 and GSTP1 polymorphisms and prognosis of oxaliplatin-based chemotherapy in colorectal cancer: a meta-analysis. Cancer Chemother Pharmacol. 2013;71:733–40.CrossRefPubMedGoogle Scholar
  38. 38.
    Deboever G, Hiltrop N, Cool M, Lambrecht G. Alternative treatment options in colorectal cancer patients with 5-fluorouracil- or capecitabine-induced cardiotoxicity. Clin Colorectal Cancer. 2013;12:8–14.CrossRefPubMedGoogle Scholar
  39. 39.
    Sharma R, Yang Y, Sharma A, Awasthi S, Awasthi YC. Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal. 2004;6:289–300.CrossRefPubMedGoogle Scholar
  40. 40.
    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;7:613–28.CrossRefPubMedGoogle Scholar
  41. 41.
    Frank M, Mittendorf T. Influence of pharmacogenomic profiling prior to pharmaceutical treatment in metastatic colorectal cancer on cost effectiveness: a systematic review. Pharmacoeconomics. 2013;31:215–28.CrossRefPubMedGoogle Scholar
  42. 42.
    Ouaissi A, Ouaissi M, Sereno D. Glutathione S-transferases and related proteins from pathogenic human parasites behave as immunomodulatory factors. Immunol Lett. 2002;81:159–64.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  • Shushan Yan
    • 1
    • 2
    • 3
  • Zengfang Wang
    • 4
  • Zengyan Wang
    • 5
  • Quanhong Duan
    • 2
  • Xiaochen Wang
    • 1
  • Jun Li
    • 6
    • 1
  • Beicheng Sun
    • 1
  1. 1.Liver Transplantation Center of the First Affiliated HospitalNanjing Medical UniversityNanjingChina
  2. 2.Department of Surgical OncologyThe Eighty-First Hospital of People’s Liberation ArmyNanjingChina
  3. 3.Department of Anorectal Surgerythe Affiliated Hospital of Weifang Medical UniversityWeifangChina
  4. 4.Department of Gynaecology and ObstetricsMaternal and Children Health’s HospitalWeifangChina
  5. 5.Operating Room of People’s Hospital of ZhuchengZhuchengChina
  6. 6.Department of General Surgerythe Affiliated Jiangning Hospital of Nanjing Medical UniversityNanjingChina

Personalised recommendations