Skip to main content
SpringerLink
Log in

Glutathione S-transferase M1 null genotype contributes to increased risk of esophageal carcinoma in Chinese population

  • Research Article
  • Published:
Tumor Biology

Abstract

Glutathione S-transferases (GSTs) play important roles in the detoxification of electrophilic carcinogens, and GSTM1 null genotype is associated with the dysfunction of GSTs. Previous studies investigating the association between GSTM1 null genotype and risk of esophageal carcinoma in Chinese provided inconsistent findings. To provide a more precise estimation on the association between GSTM1 null genotype and risk of esophageal carcinoma in Chinese population, a meta-analysis was performed. Eligible studies were searched in PubMed, Embase, and China National Knowledge Infrastructure databases. Odds ratio (OR) with the corresponding 95 % confidence interval (95 %CI) was used to assess the association. A total of 18 case–control studies involving 1,947 cases and 3,506 controls were finally included in the meta-analysis. Meta-analysis of those 18 studies showed that GSTM1 null genotype was associated with an increased risk of esophageal carcinoma in Chinese (random effect model OR = 1.49, 95 %CI = 1.11–2.00, P = 0.008). The findings from cumulative meta-analysis showed that the association was more obvious as the data increased by publication year. There was no risk of publication bias in the meta-analysis. Therefore, the findings from our meta-analysis provide a strong evidence for the association between GSTM1 null genotype and risk of esophageal carcinoma in Chinese population, and GSTM1 null genotype contributes to increased risk of esophageal carcinoma in Chinese.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Lao-Sirieix P, Fitzgerald RC. Screening for oesophageal cancer. Nat Rev Clin Oncol. 2012;9:278–87.

    Article  PubMed  Google Scholar 

  2. Wheeler JB, Reed CE. Epidemiology of esophageal cancer. Surg Clin North Am. 2012;92:1077–87.

    Article  PubMed  Google Scholar 

  3. Denlinger CE, Thompson RK. Molecular basis of esophageal cancer development and progression. Surg Clin North Am. 2012;92:1089–103.

    Article  PubMed  Google Scholar 

  4. Bennett C, Vakil N, Bergman J, Harrison R, Odze R, Vieth M, et al. Consensus statements for management of barrett's dysplasia and early-stage esophageal adenocarcinoma, based on a delphi process. Gastroenterology. 2012;143:336–46.

    Article  PubMed  Google Scholar 

  5. Tejani MA, Burtness BA. Multi-modality therapy for cancer of the esophagus and ge junction. Curr Treat Options in Oncol. 2012;13:390–402.

    Article  Google Scholar 

  6. 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.

    Article  PubMed  Google Scholar 

  7. Ginsberg G, Smolenski S, Hattis D, Guyton KZ, Johns DO, Sonawane B. Genetic polymorphism in glutathione transferases (GST): population distribution of GSTM1, T1, and P1 conjugating activity. J Toxicol Environ Health B Crit Rev. 2009;12:389–439.

    Article  PubMed  CAS  Google Scholar 

  8. Jancova P, Anzenbacher P, Anzenbacherova E. Phase II drug metabolizing enzymes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2010;154:103–16.

    Article  PubMed  CAS  Google Scholar 

  9. Wang B, Huang G, Wang D, Li A, Xu Z, Dong R, et al. Null genotypes of GSTM1 and GSTT1 contribute to hepatocellular carcinoma risk: evidence from an updated meta-analysis. J Hepatol. 2010;53:508–18.

    Article  PubMed  Google Scholar 

  10. Zhang Y, Liu C. The interaction between smoking and GSTM1 variant on lung cancer in the Chinese population. Tumour Biol. 2013;34:395–401.

    Article  PubMed  CAS  Google Scholar 

  11. Lin DX, Tang YM, Peng Q, Lu SX, Ambrosone CB, Kadlubar FF. Susceptibility to esophageal cancer and genetic polymorphisms in glutathione S-transferases T1, P1, and M1 and cytochrome P450 2E1. Cancer Epidemiol Biomarkers Prev. 1998;7:1013–8.

    PubMed  CAS  Google Scholar 

  12. Tan W, Song N, Wang GQ, Liu Q, Tang HJ, Kadlubar FF, et al. Impact of genetic polymorphisms in cytochrome p450 2e1 and glutathione S-transferases M1, T1, and P1 on susceptibility to esophageal cancer among high-risk individuals in China. Cancer Epidemiol Biomarkers Prev. 2000;9:551–6.

    PubMed  CAS  Google Scholar 

  13. Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, et al. Glutathione-S-transferases M1 (GSTM1) and GSTT1 genotype, smoking, consumption of alcohol and tea and risk of esophageal and stomach cancers: a case–control study of a high-incidence area in Jiangsu Province, China. Cancer Lett. 2002;188:95–102.

    Article  PubMed  CAS  Google Scholar 

  14. Roth MJ, Abnet CC, Johnson LL, Mark SD, Dong ZW, Taylor PR, et al. Polymorphic variation of Cyp1A1 is associated with the risk of gastric cardia cancer: a prospective case-cohort study of cytochrome P-450 1A1 and GST enzymes. Cancer Causes Control. 2004;15:1077–83.

    Article  PubMed  Google Scholar 

  15. Wang AH, Sun CS, Li LS, Huang JY, Chen QS, Xu DZ. Genetic susceptibility and environmental factors of esophageal cancer in Xi'an. World J Gastroenterol. 2004;10:940–4.

    PubMed  Google Scholar 

  16. Lu XM, Zhang YM, Lin RY, Arzi G, Wang X, Zhang YL, et al. Relationship between genetic polymorphisms of metabolizing enzymes CYP2E1, GSTM1 and Kazakh's esophageal squamous cell cancer in Xinjiang, China. World J Gastroenterol. 2005;11:3651–4.

    PubMed  CAS  Google Scholar 

  17. Dong C, Wu J, Jin Y, Zhang J. Correlation between genetic polymorphism of CYP2E1, GSTM1 and esophageal cancer in Gansu. Chin J Gastroenterol Hepatol. 2007;16:115–8.

    CAS  Google Scholar 

  18. Liu R, Yin L, Pu Y, Li Y, Liang G, Zhang J, et al. Functional alterations in the glutathione S-transferase family associated with enhanced occurrence of esophageal carcinoma in China. J Toxicol Environ Health A. 2010;73:471–82.

    Article  PubMed  CAS  Google Scholar 

  19. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.

    Article  PubMed  Google Scholar 

  20. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.

    Article  PubMed  CAS  Google Scholar 

  21. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22:719–48.

    PubMed  CAS  Google Scholar 

  22. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.

    Article  PubMed  CAS  Google Scholar 

  23. Shao G, Su Y, Huang G, Wen B. Relationship between CYP1A1, GSTM1 genetic polymorphisms and susceptibility to esophageal squamous cell carcinoma. Zhonghua Liu Xing Bing Xue Za Zhi. 2000;21:420–3.

    PubMed  CAS  Google Scholar 

  24. Shi Y, Zhou X, Zhou Y, Ren S. Analysis of CYP2E1, GSTM1 genetic polymorphisms in relation to human lung cancer and esophageal carcinoma. J Huazhong Univ Sci Technol (Heal Sci). 2002;31:14–7.

    CAS  Google Scholar 

  25. Wang LD, Zheng S, Liu B, Zhou JX, Li YJ, Li JX. CYP1A1, GSTS and MEH polymorphisms and susceptibility to esophageal carcinoma: study of population from a high- incidence area in north China. World J Gastroenterol. 2003;9:1394–7.

    PubMed  CAS  Google Scholar 

  26. Han Y, Feng X, Li P, Niu Z. Case–control study on relationship of CYP1A1 and GSTM1 polymorphisms and susceptibility to esophageal squamous carcinoma. Chin J Public Health. 2005;21:3–6.

    CAS  Google Scholar 

  27. Yi L, Pu Y, Song Y, Hu X, Liu Y, Kai H. Polymorphisms of susceptible genes for esophageal cancer risk in Huaian population in Jiangsu Province. Tumor. 2005;25:357–61.

    Google Scholar 

  28. Lu XM, Yang T, Xu SY, Wen H, Wang X, Ren ZH, et al. Glutathione-S-transferase M1 polymorphisms on the susceptibility to esophageal cancer among three Chinese minorities: Kazakh, Tajik and Uygur. World J Gastroenterol. 2006;12:7758–61.

    PubMed  CAS  Google Scholar 

  29. Li Y, Zhu WC, Lin Z, Wu H, Ye Z. Correlation between smoking and the polymorphism of gene GSTM1 and esophageal carcinoma. Heilongjiang Med J. 2008;32:18–20.

    Google Scholar 

  30. Ji R, Wu J, Zhou Y, Zhang B, Zhang Z, Yang Z. Relationship between CYP1A1, GSTM1 and GSTT1 genetic polymorphisms and susceptibility of esophageal cancer in Wuwei, Gansu Province. J Lanzhou Univ (Med Sci). 2010;36:29–34.

    CAS  Google Scholar 

  31. Chen Y, Zhang H, Yi D, Wang H, Wang Y, Deng Y, Ma Y: Relationship between GSTM1 gene polymorphism and interaction of gene environment and susceptibility of esophageal cancer. Modern Preventive Medicine 2012;39:1235–9.

    Google Scholar 

  32. Gao P, Qian Y, Ye X, Ge J, Zang D, Xu W. Study of CTPIA1, GSTT1, GSTM1 polymorphisms and susceptibility on esophageal carcinoma in Ningxia Hui nationality. Ningxia Med J. 2012;34:196–9.

    CAS  Google Scholar 

  33. Zheng S, Vuitton L, Sheyhidin I, Vuitton DA, Zhang Y, Lu X. Northwestern China: a place to learn more on oesophageal cancer. Part two: gene alterations and polymorphisms. Eur J Gastroenterol Hepatol. 2011;23:1087–99.

    Article  PubMed  Google Scholar 

  34. Jana S, Mandlekar S. Role of phase II drug metabolizing enzymes in cancer chemoprevention. Curr Drug Metab. 2009;10:595–616.

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Institute of Biomedicine and School of Medicine, Tsinghua University, Beijing, 100084, People’s Republic of China

    Shan Zhong & Zhijie Chang

  2. Department of Biochemistry and Molecular Biology, Second Military Medical University, Shanghai, 200433, People’s Republic of China

    Shan Zhong & Binhua Jiao

  3. Shanghai Food and Drug Packaging Material Control Center, Shanghai, 201203, People’s Republic of China

    Wei Zhao

  4. Department of Cardiothoracic Surgery, Changhai Hospital Second Military Medical University, Shanghai, 200438, People’s Republic of China

    Chaojing Lu, Bailing Li, Yang Yuan & Lixin Yang

  5. The Second Detachment of the Chinese People’s Armed Police Force Shanghai Corps, Shanghai, 200081, People’s Republic of China

    Danfeng Guo

Authors
  1. Shan Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chaojing Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bailing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yang Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Danfeng Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhijie Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Binhua Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lixin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lixin Yang.

Additional information

Shan Zhong and Wei Zhao contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhong, S., Zhao, W., Lu, C. et al. Glutathione S-transferase M1 null genotype contributes to increased risk of esophageal carcinoma in Chinese population. Tumor Biol. 34, 2403–2407 (2013). https://doi.org/10.1007/s13277-013-0790-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13277-013-0790-3

Keywords

Search

Navigation