Skip to main content
Top
Published in: Diagnostic Pathology 1/2014

Open Access 01-12-2014 | Research

Glutathione S-transferase M1 null genotype meta-analysis on gastric cancer risk

Authors: Xianhong Meng, Yong Liu, Bona Liu

Published in: Diagnostic Pathology | Issue 1/2014

Login to get access

Abstract

Background

Glutathione S-transferases (GSTs) have proved to be involved in the detoxifying several carcinogens and may play an important role in carcinogenesis of cancer. Previous studies on the association between Glutathione S-transferase M1 (GSTM1) polymorphism and gastric cancer (GC) risk reported inconclusive results. To get a precise result, we conducted this present meta-analysis through pooling all eligible studies.

Methods

A comprehensive databases of Pubmed, Embase, Web of Science, and the Chinese Biomedical Database (CBM) were searched for case–control studies investigating the association between GSTM1 null genotype and GC risk. Odds ratios (OR) and 95% confidence intervals (95% CI) were used to assess this possible association. A χ2-based Q-test was used to examine the heterogeneity assumption. Begg’s and Egger’s test were used to examine the potential publication bias. The leave-one-out sensitivity analysis was conducted to determine whether our assumptions or decisions have a major effect on the results of present work. Statistical analyses were performed with the software program STATA 12.0.

Results

A total of 47 eligible case–control studies were identified, including 6,678 cases and 12,912 controls. Our analyses suggested that GSTM1 null genotype was significantly associated with increased risk of GC (OR = 1.186, 95% CI = 1.057-1.329, Pheterogenetiy = 0.000, P = 0.004). Significant association was also found in Asians (OR = 1.269, 95% CI = 1.106-1.455, Pheterogenetiy = 0.002, P = 0.001). However, GSTM1 null genotype was not contributed to GC risk in Caucasians (OR = 1.115, 95% CI = 0.937-1.326, Pheterogenetiy = 0.000, P = 0.222). In the subgroup analysis stratified by sources of controls, significant association was detected in hospital-based studies (OR = 1.355, 95% CI = 1.179-1.557, Pheterogenetiy = 0.001, P = 0.000), while there was no significant association detected in population-based studies (OR = 1.017, 95% CI = 0.862-1.200, Pheterogenetiy = 0.000, P = 0.840).

Conclusion

This meta-analysis showed the evidence that GSTM1 null genotype contributed to the development of GC.

Virtual Slides

The virtual slide(s) for this article can be found here: http://​www.​diagnosticpathol​ogy.​diagnomx.​eu/​vs/​1644180505119533​.
Literature
1.
go back to reference Oliveira C, Seruca R, Carneiro F: Genetics, pathology, and clinicsof familial gastric cancer. Int J SurgPathol. 2006, 14: 21-33. Oliveira C, Seruca R, Carneiro F: Genetics, pathology, and clinicsof familial gastric cancer. Int J SurgPathol. 2006, 14: 21-33.
2.
go back to reference Boccia S, Sayed-Tabatabaei FA, Persiani R, Gianfagna F, Rausei S, Arzani D, La Greca A, D'Ugo D, La Torre G, van Duijn CM, Ricciardi G: Polymorphisms in metabolic genes, their combination and interaction with tobacco smoke and alcohol consumption and risk of gastric cancer: a case–control study in an Italian population. BMC Cancer. 2007, 7: 206-213.PubMedPubMedCentralCrossRef Boccia S, Sayed-Tabatabaei FA, Persiani R, Gianfagna F, Rausei S, Arzani D, La Greca A, D'Ugo D, La Torre G, van Duijn CM, Ricciardi G: Polymorphisms in metabolic genes, their combination and interaction with tobacco smoke and alcohol consumption and risk of gastric cancer: a case–control study in an Italian population. BMC Cancer. 2007, 7: 206-213.PubMedPubMedCentralCrossRef
3.
go back to reference 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 asouthernEuropean population: the role of glutathione S-transferases GSTM1, GSTM3, and GSTT1 genetic polymorphisms. Prostate. 2004, 58: 414-420.PubMedCrossRef 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 asouthernEuropean population: the role of glutathione S-transferases GSTM1, GSTM3, and GSTT1 genetic polymorphisms. Prostate. 2004, 58: 414-420.PubMedCrossRef
4.
go back to reference Hayes JD, Pulford DJ: The glutathione S-transferase super-gene 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.PubMedCrossRef Hayes JD, Pulford DJ: The glutathione S-transferase super-gene 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.PubMedCrossRef
5.
go back to reference de Bruin W, Wagenmans M, Peters W: Expression of glutathioneS-transferase alpha, P1-1 and T1-1 in the human gastrointestinal tract. Jpn J Cancer Res. 2000, 91: 310-316.PubMedCrossRef de Bruin W, Wagenmans M, Peters W: Expression of glutathioneS-transferase alpha, P1-1 and T1-1 in the human gastrointestinal tract. Jpn J Cancer Res. 2000, 91: 310-316.PubMedCrossRef
6.
go back to reference Clavel J, Bellec S, Rebouissou S, Ménégaux F, Feunteun J, Bonaïti-Pellié C, Baruchel A, Kebaili K, Lambilliotte A, Leverger G, Sommelet D, Lescoeur B, Beaune P, Hémon D, Loriot MA: Childhood leukaemia, polymorphisms ofmetabolism enzyme genes, and interactions with maternal tobacco, coffee and alcohol consumption during pregnancy. Eur J CancerPrev. 2005, 14: 531-540.CrossRef Clavel J, Bellec S, Rebouissou S, Ménégaux F, Feunteun J, Bonaïti-Pellié C, Baruchel A, Kebaili K, Lambilliotte A, Leverger G, Sommelet D, Lescoeur B, Beaune P, Hémon D, Loriot MA: Childhood leukaemia, polymorphisms ofmetabolism enzyme genes, and interactions with maternal tobacco, coffee and alcohol consumption during pregnancy. Eur J CancerPrev. 2005, 14: 531-540.CrossRef
7.
go back to reference La Torre G, Boccia S, Ricciardi G: Glutathione S-transferase M1 status andgastric cancer risk: a meta-analysis. Cancer Lett. 2005, 217: 53-60.PubMedCrossRef La Torre G, Boccia S, Ricciardi G: Glutathione S-transferase M1 status andgastric cancer risk: a meta-analysis. Cancer Lett. 2005, 217: 53-60.PubMedCrossRef
8.
go back to reference Zhang AP, Liu BH, Wang L, Gao Y, Li F, Sun SX: Glutathione S-transferasegene polymorphisms and risk of gastric cancer in a Chinese population. Asian Pac J Cancer Prev. 2011, 12: 3421-3425.PubMed Zhang AP, Liu BH, Wang L, Gao Y, Li F, Sun SX: Glutathione S-transferasegene polymorphisms and risk of gastric cancer in a Chinese population. Asian Pac J Cancer Prev. 2011, 12: 3421-3425.PubMed
11.
go back to reference Cochran WG: The combination of estimates from different experiments. Biometrics. 1954, 10 (1): 101-129.CrossRef Cochran WG: The combination of estimates from different experiments. Biometrics. 1954, 10 (1): 101-129.CrossRef
12.
go back to reference DerSimonian R, Laird N: Meta-analysis in clinical trials. Control Clin Trials. 1986, 7 (3): 177-188.PubMedCrossRef DerSimonian R, Laird N: Meta-analysis in clinical trials. Control Clin Trials. 1986, 7 (3): 177-188.PubMedCrossRef
13.
go back to reference Mantel N, Haenszel W: Statistical aspects of the analysis of data fromretrospective studies of disease. J Natl Cancer Inst. 1959, 22 (4): 719-748.PubMed Mantel N, Haenszel W: Statistical aspects of the analysis of data fromretrospective studies of disease. J Natl Cancer Inst. 1959, 22 (4): 719-748.PubMed
14.
go back to reference Begg CB, Mazumdar M: Operating characteristics of a rank correlationtest for publication bias. Biometrics. 1994, 50 (4): 1088-1101.PubMedCrossRef Begg CB, Mazumdar M: Operating characteristics of a rank correlationtest for publication bias. Biometrics. 1994, 50 (4): 1088-1101.PubMedCrossRef
17.
go back to reference Strange RC, Matharoo B, Faulder GC, Jones P, Cotton W, Elder JB, Deakin M: 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.PubMedCrossRef Strange RC, Matharoo B, Faulder GC, Jones P, Cotton W, Elder JB, Deakin M: 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.PubMedCrossRef
18.
go back to reference Harada S, Misawa S, Nakamura T, Tanaka N, Ueno E, Nozoe M: Detection of GST1 genedeletion by the polymerase chain reaction and its possible correlation with stomach cancer in Japanese. Hum Genet. 1992, 90: 62-64.PubMedCrossRef Harada S, Misawa S, Nakamura T, Tanaka N, Ueno E, Nozoe M: Detection of GST1 genedeletion by the polymerase chain reaction and its possible correlation with stomach cancer in Japanese. Hum Genet. 1992, 90: 62-64.PubMedCrossRef
19.
go back to reference Kato S, Onda M, Matsukura N, Tokunaga A, Matsuda N, Yamashita K, Shields PG: Genetic polymorphisms ofthe cancer-related gene and Helicobacter pylori infection inJapanese gastric cancer patients: an age and gender matchedcase-control study. Cancer. 1996, 77: 1654-1661.PubMedCrossRef Kato S, Onda M, Matsukura N, Tokunaga A, Matsuda N, Yamashita K, Shields PG: Genetic polymorphisms ofthe cancer-related gene and Helicobacter pylori infection inJapanese gastric cancer patients: an age and gender matchedcase-control study. Cancer. 1996, 77: 1654-1661.PubMedCrossRef
20.
go back to reference Katoh T, Nagata N, Kuroda Y, Itoh H, Kawahara A, Kuroki N, Ookuma R, Bell DA: Glutathione S-transferaseM1 (GSTM1) and T1 (GSTT1) genetic polymorphism and susceptibility to gastric and colorectal adenocarcinoma. Carcinogenesis. 1996, 17: 1855-1859.PubMedCrossRef Katoh T, Nagata N, Kuroda Y, Itoh H, Kawahara A, Kuroki N, Ookuma R, Bell DA: Glutathione S-transferaseM1 (GSTM1) and T1 (GSTT1) genetic polymorphism and susceptibility to gastric and colorectal adenocarcinoma. Carcinogenesis. 1996, 17: 1855-1859.PubMedCrossRef
21.
go back to reference Deakin M, Elder J, Hendrickse C, Peckham D, Baldwin D, Pantin C, Wild N, Leopard P, Bell DA, Jones P, Duncan H, Brannigan K, Alldersea J, Fryer AA, Strange RC: Glutathione S-transferaseGSTT1 genotypes and susceptibility to cancer: studies of interactions with GSTM1 in lung, oral, gastric and colorectal cancers. Carcinogenesis. 1996, 17: 881-884.PubMedCrossRef Deakin M, Elder J, Hendrickse C, Peckham D, Baldwin D, Pantin C, Wild N, Leopard P, Bell DA, Jones P, Duncan H, Brannigan K, Alldersea J, Fryer AA, Strange RC: Glutathione S-transferaseGSTT1 genotypes and susceptibility to cancer: studies of interactions with GSTM1 in lung, oral, gastric and colorectal cancers. Carcinogenesis. 1996, 17: 881-884.PubMedCrossRef
22.
go back to reference Ng EK, Sung JJ, Ling TK, Ip SM, Lau JY, Chan AC, Liew CT, Chung SC: Helicobacter pylori and thenull genotype of glutathione-S-transferase-mu in patients withgastric adenocarcinoma. Cancer. 1998, 82: 268-273.PubMedCrossRef Ng EK, Sung JJ, Ling TK, Ip SM, Lau JY, Chan AC, Liew CT, Chung SC: Helicobacter pylori and thenull genotype of glutathione-S-transferase-mu in patients withgastric adenocarcinoma. Cancer. 1998, 82: 268-273.PubMedCrossRef
23.
go back to reference Martins G, Alves M: Glutathione S transferase mu polymorphism and gastric cancer in the Portuguese population. Biomarkers. 1998, 3: 441-447.CrossRef Martins G, Alves M: Glutathione S transferase mu polymorphism and gastric cancer in the Portuguese population. Biomarkers. 1998, 3: 441-447.CrossRef
24.
go back to reference Oda Y, Kobayashi M, Ooi A, Muroishi Y, Nakanishi I: Genotypes of glutathione S-transferase M1 and N-acetyltransferase 2in Japanese patients with gastric cancer. Gastric Cancer. 1999, 2: 158-164.PubMedCrossRef Oda Y, Kobayashi M, Ooi A, Muroishi Y, Nakanishi I: Genotypes of glutathione S-transferase M1 and N-acetyltransferase 2in Japanese patients with gastric cancer. Gastric Cancer. 1999, 2: 158-164.PubMedCrossRef
25.
go back to reference Cai L, Yu SZ, Zhang ZF: Glutathione S-transferases M1, T1genotypes and the risk of gastric cancer: a case–control study. World J Gastroenterol. 2001, 7: 506-509.PubMed Cai L, Yu SZ, Zhang ZF: Glutathione S-transferases M1, T1genotypes and the risk of gastric cancer: a case–control study. World J Gastroenterol. 2001, 7: 506-509.PubMed
26.
go back to reference Setiawan VW, Zhang ZF, Yu GP, Li YL, Lu ML, Tsai CJ, Cordova D, Wang MR, Guo CH, Yu SZ, Kurtz RC: GSTT1 and GSTM1 null genotypes and the risk of gastric cancer: a case–control study in a Chinese population. Cancer Epidemiol Biomarkers Prev. 2000, 9: 73-80.PubMed Setiawan VW, Zhang ZF, Yu GP, Li YL, Lu ML, Tsai CJ, Cordova D, Wang MR, Guo CH, Yu SZ, Kurtz RC: GSTT1 and GSTM1 null genotypes and the risk of gastric cancer: a case–control study in a Chinese population. Cancer Epidemiol Biomarkers Prev. 2000, 9: 73-80.PubMed
27.
go back to reference Lan Q, Chow WH, Lissowska J, Hein DW, Buetow K, Engel LS, Ji B, Zatonski W, Rothman N: Glutathione S-transferase genotypes and stomach cancer in a population-based case–control study in Warsaw, Poland. Pharmacogenetics. 2001, 11: 655-661.PubMedCrossRef Lan Q, Chow WH, Lissowska J, Hein DW, Buetow K, Engel LS, Ji B, Zatonski W, Rothman N: Glutathione S-transferase genotypes and stomach cancer in a population-based case–control study in Warsaw, Poland. Pharmacogenetics. 2001, 11: 655-661.PubMedCrossRef
28.
go back to reference Saadat I, Saadat M: Glutathione S-transferase M1 and T1 nullgenotypes and the risk of gastric and colorectal cancers. Cancer Lett. 2001, 169: 21-26.PubMedCrossRef Saadat I, Saadat M: Glutathione S-transferase M1 and T1 nullgenotypes and the risk of gastric and colorectal cancers. Cancer Lett. 2001, 169: 21-26.PubMedCrossRef
29.
go back to reference Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, Ding JH, Su P, Hu X, Xu TL, Sugimura H, Tajima K: 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.PubMedCrossRef Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, Ding JH, Su P, Hu X, Xu TL, Sugimura H, Tajima K: 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.PubMedCrossRef
30.
go back to reference Wu MS, Chen CJ, Lin MT, Wang HP, Shun CT, Sheu JC, Lin JT: Genetic polymorphisms ofcytochrome p450 2E1, glutathione S-transferase M1 and T1, andsusceptibility to gastric carcinoma in Taiwan. Int J Colorectal Dis. 2002, 17: 338-343.PubMedCrossRef Wu MS, Chen CJ, Lin MT, Wang HP, Shun CT, Sheu JC, Lin JT: Genetic polymorphisms ofcytochrome p450 2E1, glutathione S-transferase M1 and T1, andsusceptibility to gastric carcinoma in Taiwan. Int J Colorectal Dis. 2002, 17: 338-343.PubMedCrossRef
31.
go back to reference Sgambato A, Campisi B, Zupa A, Bochicchio A, Romano G, Tartarone A, Galasso R, Traficante A, Cittadini A: Glutathione S-transferase (GST) polymorphisms as risk factors for cancer in a highly homogeneous population from southern Italy. Anticancer Res. 2002, 22: 3647-3652.PubMed Sgambato A, Campisi B, Zupa A, Bochicchio A, Romano G, Tartarone A, Galasso R, Traficante A, Cittadini A: Glutathione S-transferase (GST) polymorphisms as risk factors for cancer in a highly homogeneous population from southern Italy. Anticancer Res. 2002, 22: 3647-3652.PubMed
32.
go back to reference Choi SC, Yun KJ, Kim TH, Kim HJ, Park SG, Oh GJ, Chae SC, Oh GJ, Nah YH, Kim JJ, Chung HT: Prognostic potential of glutathione S-transferase M1 and T1 null genotypes for gastric cancer progression. Cancer Lett. 2003, 195: 169-175.PubMedCrossRef Choi SC, Yun KJ, Kim TH, Kim HJ, Park SG, Oh GJ, Chae SC, Oh GJ, Nah YH, Kim JJ, Chung HT: Prognostic potential of glutathione S-transferase M1 and T1 null genotypes for gastric cancer progression. Cancer Lett. 2003, 195: 169-175.PubMedCrossRef
33.
go back to reference Roth MJ, Abnet CC, Johnson LL, Mark SD, Dong ZW, Taylor PR, Dawsey SM, Qiao YL: 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: 1077-1083.PubMedCrossRef Roth MJ, Abnet CC, Johnson LL, Mark SD, Dong ZW, Taylor PR, Dawsey SM, Qiao YL: 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: 1077-1083.PubMedCrossRef
34.
go back to reference Suzuki S, Muroishi Y, Nakanishi I, Oda Y: Relationship between genetic polymorphisms of drug-metabolizing enzymes (CYP1A1, CYP2E1, GSTM1, and NAT2), drinking habits, histological subtypes, and p53 gene point mutations in Japanese patients with gastric cancer. J Gastroenterol. 2004, 39: 220-230.PubMedCrossRef Suzuki S, Muroishi Y, Nakanishi I, Oda Y: Relationship between genetic polymorphisms of drug-metabolizing enzymes (CYP1A1, CYP2E1, GSTM1, and NAT2), drinking habits, histological subtypes, and p53 gene point mutations in Japanese patients with gastric cancer. J Gastroenterol. 2004, 39: 220-230.PubMedCrossRef
35.
go back to reference Colombo J, Rossit AR, Caetano A, Borim AA, Wornrath D, Silva AE: GSTT1, GSTM1 andCYP2E1 genetic polymorphisms in gastric cancer and chronicgastritis in a Brazilian population. World J Gastroenterol. 2004, 10: 1240-1245.PubMedPubMedCentral Colombo J, Rossit AR, Caetano A, Borim AA, Wornrath D, Silva AE: GSTT1, GSTM1 andCYP2E1 genetic polymorphisms in gastric cancer and chronicgastritis in a Brazilian population. World J Gastroenterol. 2004, 10: 1240-1245.PubMedPubMedCentral
36.
go back to reference Lai KC, Chen WC, Tsai FJ, Li SY, Chou MC, Jeng LB: Glutathione S-transferase M1gene null genotype and gastric cancer risk in Taiwan. Hepato-Gastroenterol. 2005, 52: 1916-1919. Lai KC, Chen WC, Tsai FJ, Li SY, Chou MC, Jeng LB: Glutathione S-transferase M1gene null genotype and gastric cancer risk in Taiwan. Hepato-Gastroenterol. 2005, 52: 1916-1919.
37.
go back to reference Li H, Chen XL, Li HQ: Polymorphism of CYPIA1 and GSTM1genes associated with susceptibility of gastric cancer in Shandong Province of China. World J Gastroenterol. 2005, 11: 5757-5762.PubMedPubMedCentralCrossRef Li H, Chen XL, Li HQ: Polymorphism of CYPIA1 and GSTM1genes associated with susceptibility of gastric cancer in Shandong Province of China. World J Gastroenterol. 2005, 11: 5757-5762.PubMedPubMedCentralCrossRef
38.
go back to reference Mu LN, Lu QY, Yu SZ, Jiang QW, Cao W, You NC, Setiawan VW, Zhou XF, Ding BG, Wang RH, Zhao J, Cai L, Rao JY, Heber D, Zhang ZF: Green tea drinking and multigenetic index on the risk of stomach cancer in a Chinese population. Int J Cancer. 2005, 116: 972-983.PubMedPubMedCentralCrossRef Mu LN, Lu QY, Yu SZ, Jiang QW, Cao W, You NC, Setiawan VW, Zhou XF, Ding BG, Wang RH, Zhao J, Cai L, Rao JY, Heber D, Zhang ZF: Green tea drinking and multigenetic index on the risk of stomach cancer in a Chinese population. Int J Cancer. 2005, 116: 972-983.PubMedPubMedCentralCrossRef
39.
go back to reference Nan HM, Park JW, Song YJ, Yun HY, Park JS, Hyun T, Youn SJ, Kim YD, Kang JW, Kim H: Kimchi and soybean pastes arerisk factors of gastric cancer. World J Gastroenterol. 2005, 11: 3175-3181.PubMedPubMedCentralCrossRef Nan HM, Park JW, Song YJ, Yun HY, Park JS, Hyun T, Youn SJ, Kim YD, Kang JW, Kim H: Kimchi and soybean pastes arerisk factors of gastric cancer. World J Gastroenterol. 2005, 11: 3175-3181.PubMedPubMedCentralCrossRef
40.
go back to reference Shen J, Wang RT, Xu YC, Wang LW, Wang XR: Interaction models of CYP1A1, GSTM1 polymorphisms and tobacco smoking in intestinal gastric cancer. World J Gastroenterol. 2005, 11: 6056-6060.PubMedPubMedCentralCrossRef Shen J, Wang RT, Xu YC, Wang LW, Wang XR: Interaction models of CYP1A1, GSTM1 polymorphisms and tobacco smoking in intestinal gastric cancer. World J Gastroenterol. 2005, 11: 6056-6060.PubMedPubMedCentralCrossRef
41.
go back to reference Palli D, Saieva C, Gemma S, Masala G, Gomez-Miguel MJ, Luzzi I, D'Errico M, Matullo G, Ozzola G, Manetti R, Nesi G, Sera F, Zanna I, Dogliotti E, Testai E: GSTT1 and GSTM1 gene polymorphisms and gastric cancer in a high-risk Italian population. Int J Cancer. 2005, 115: 284-289.PubMedCrossRef Palli D, Saieva C, Gemma S, Masala G, Gomez-Miguel MJ, Luzzi I, D'Errico M, Matullo G, Ozzola G, Manetti R, Nesi G, Sera F, Zanna I, Dogliotti E, Testai E: GSTT1 and GSTM1 gene polymorphisms and gastric cancer in a high-risk Italian population. Int J Cancer. 2005, 115: 284-289.PubMedCrossRef
42.
go back to reference Tamer L, Ateş NA, Ateş C, Ercan B, Elipek T, Yildirim H, Camdeviren H, Atik U, Aydin S: Glutathione S-transferase M1, T1 and P1 genetic polymorphisms, cigarette smoking and gastric cancer risk. Cell Biochem Funct. 2005, 23: 267-272.PubMedCrossRef Tamer L, Ateş NA, Ateş C, Ercan B, Elipek T, Yildirim H, Camdeviren H, Atik U, Aydin S: Glutathione S-transferase M1, T1 and P1 genetic polymorphisms, cigarette smoking and gastric cancer risk. Cell Biochem Funct. 2005, 23: 267-272.PubMedCrossRef
43.
go back to reference Nan HM, Song YJ, Yun HY, Park JS, Kim H: Effects of dietary intake and genetic factors on hyper methylation of the hMLH1 gene promoter in gastric cancer. World J Gastroenterol. 2005, 11: 3834-3841.PubMedPubMedCentralCrossRef Nan HM, Song YJ, Yun HY, Park JS, Kim H: Effects of dietary intake and genetic factors on hyper methylation of the hMLH1 gene promoter in gastric cancer. World J Gastroenterol. 2005, 11: 3834-3841.PubMedPubMedCentralCrossRef
44.
go back to reference Hong SH, Kim JW, Kim HG, Park IK, Ryoo JW, Lee CH, Sohn YK, Lee JY: Glutathione S-transferases (GSTM1, GSTT1 and GSTP1) and N-acetyl transferase 2 polymorphisms and the risk of gastric cancer. J Prev Med Pub Health. 2006, 39: 135-140. Hong SH, Kim JW, Kim HG, Park IK, Ryoo JW, Lee CH, Sohn YK, Lee JY: Glutathione S-transferases (GSTM1, GSTT1 and GSTP1) and N-acetyl transferase 2 polymorphisms and the risk of gastric cancer. J Prev Med Pub Health. 2006, 39: 135-140.
45.
go back to reference Agudo A, Sala N, Pera G, Capellá G, Berenguer A, García N, Palli D, Boeing H, Del Giudice G, Saieva C, Carneiro F, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Simán H, Stenling R, Hallmans G, Martínez C, Amiano P, Barricarte A, Navarro C, Quirós JR, Allen N, Key T, Bingham S, Khaw KT, Linseisen J, Nagel G, et al.: No association between polymorphisms in CYP2E1, GSTM1, NAT1, NAT2 and the risk of gastric adenocarcinoma in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev. 2006, 15: 1043-1045.PubMedCrossRef Agudo A, Sala N, Pera G, Capellá G, Berenguer A, García N, Palli D, Boeing H, Del Giudice G, Saieva C, Carneiro F, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Simán H, Stenling R, Hallmans G, Martínez C, Amiano P, Barricarte A, Navarro C, Quirós JR, Allen N, Key T, Bingham S, Khaw KT, Linseisen J, Nagel G, et al.: No association between polymorphisms in CYP2E1, GSTM1, NAT1, NAT2 and the risk of gastric adenocarcinoma in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev. 2006, 15: 1043-1045.PubMedCrossRef
46.
go back to reference Martinez C, Martín F, Fernández JM, García-Martín E, Sastre J, Díaz-Rubio M, Agúndez JA, Ladero JM: 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. Pharmaco Genomics. 2006, 7: 711-718. Martinez C, Martín F, Fernández JM, García-Martín E, Sastre J, Díaz-Rubio M, Agúndez JA, Ladero JM: 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. Pharmaco Genomics. 2006, 7: 711-718.
47.
go back to reference Ruzzo A, Canestrari E, Maltese P, Pizzagalli F, Graziano F, Santini D, Catalano V, Ficarelli R, Mari D, Bisonni R, Giordani P, Giustini L, Lippe P, Silva R, Mattioli R, Torresi U, Latini L, Magnani M: Polymorphisms in genes involved in DNA repair and metabolism of xenobiotics in individual susceptibility to sporadic diffuse gastric cancer. Clin Chem Lab Med. 2007, 45: 822-828.PubMedCrossRef Ruzzo A, Canestrari E, Maltese P, Pizzagalli F, Graziano F, Santini D, Catalano V, Ficarelli R, Mari D, Bisonni R, Giordani P, Giustini L, Lippe P, Silva R, Mattioli R, Torresi U, Latini L, Magnani M: Polymorphisms in genes involved in DNA repair and metabolism of xenobiotics in individual susceptibility to sporadic diffuse gastric cancer. Clin Chem Lab Med. 2007, 45: 822-828.PubMedCrossRef
48.
go back to reference Wideroff L, Vaughan TL, Farin FM, Gammon MD, Risch H, Stanford JL, Chow WH: GST, NAT1, CYP1A1polymorphisms and risk of esophageal and gastric adenocarcinomas. Cancer Detect Prev. 2007, 31: 233-236.PubMedPubMedCentralCrossRef Wideroff L, Vaughan TL, Farin FM, Gammon MD, Risch H, Stanford JL, Chow WH: GST, NAT1, CYP1A1polymorphisms and risk of esophageal and gastric adenocarcinomas. Cancer Detect Prev. 2007, 31: 233-236.PubMedPubMedCentralCrossRef
49.
go back to reference Tripathi S, Ghoshal U, Ghoshal UC, Mittal B, Krishnani N, Chourasia D, Agarwal AK, Singh K: Gastric carcinogenesis: possible role of polymorphisms of GSTM1, GSTT1, and GSTP1 genes. Scand J Gastroenterol. 2008, 43: 431-439.PubMedCrossRef Tripathi S, Ghoshal U, Ghoshal UC, Mittal B, Krishnani N, Chourasia D, Agarwal AK, Singh K: Gastric carcinogenesis: possible role of polymorphisms of GSTM1, GSTT1, and GSTP1 genes. Scand J Gastroenterol. 2008, 43: 431-439.PubMedCrossRef
50.
go back to reference Al-Moundhri MS, Alkindy M, Al-Nabhani M, Al-Bahrani B, Burney IA, Al-Habsi H, Ganguly SS, Tanira M: Combined polymorphism analysis of glutathione S-transferase M1/G1 andinterleukin-1B (IL-1B)/interleukin 1-receptor antagonist (IL-1RN) and gastric cancer risk in an Omani Arab population. J Clin Gastroenterol. 2009, 43: 152-156.PubMedCrossRef Al-Moundhri MS, Alkindy M, Al-Nabhani M, Al-Bahrani B, Burney IA, Al-Habsi H, Ganguly SS, Tanira M: Combined polymorphism analysis of glutathione S-transferase M1/G1 andinterleukin-1B (IL-1B)/interleukin 1-receptor antagonist (IL-1RN) and gastric cancer risk in an Omani Arab population. J Clin Gastroenterol. 2009, 43: 152-156.PubMedCrossRef
51.
go back to reference Masoudi M, Saadat I, Omidvari S, Saadat M: Genetic polymorphisms of GSTO2, GSTM1, and GSTT1 and risk of gastriccancer. Mol Biol Rep. 2009, 36: 781-784.PubMedCrossRef Masoudi M, Saadat I, Omidvari S, Saadat M: Genetic polymorphisms of GSTO2, GSTM1, and GSTT1 and risk of gastriccancer. Mol Biol Rep. 2009, 36: 781-784.PubMedCrossRef
52.
go back to reference Malik MA, Upadhyay R, Mittal RD, Zargar SA, Modi DR, Mittal B: Role of xenobiotic-metabolizing enzyme gene polymorphisms and interactions with environmental factors in susceptibility to gastric cancer in Kashmir Valley. J Gastrointest Cancer. 2009, 40: 26-32.PubMedCrossRef Malik MA, Upadhyay R, Mittal RD, Zargar SA, Modi DR, Mittal B: Role of xenobiotic-metabolizing enzyme gene polymorphisms and interactions with environmental factors in susceptibility to gastric cancer in Kashmir Valley. J Gastrointest Cancer. 2009, 40: 26-32.PubMedCrossRef
53.
go back to reference Moy KA, Yuan JM, Chung FL, Wang XL, Van Den Berg D, Wang R, Gao YT, Yu MC: Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms and gastric cancer risk: a prospective study of men in Shanghai, China. Int J Cancer. 2009, 125: 2652-2659.PubMedPubMedCentralCrossRef Moy KA, Yuan JM, Chung FL, Wang XL, Van Den Berg D, Wang R, Gao YT, Yu MC: Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms and gastric cancer risk: a prospective study of men in Shanghai, China. Int J Cancer. 2009, 125: 2652-2659.PubMedPubMedCentralCrossRef
54.
go back to reference Zendehdel K, Bahmanyar S, McCarthy S, Nyren O, Andersson B, Ye W: Genetic polymorphisms of glutathione S-transferase genes GSTP1, GSTM1, and GSTT1 and risk of esophageal and gastric cardia cancers. Cancer Causes Control. 2009, 20: 2031-2038.PubMedCrossRef Zendehdel K, Bahmanyar S, McCarthy S, Nyren O, Andersson B, Ye W: Genetic polymorphisms of glutathione S-transferase genes GSTP1, GSTM1, and GSTT1 and risk of esophageal and gastric cardia cancers. Cancer Causes Control. 2009, 20: 2031-2038.PubMedCrossRef
55.
go back to reference Palli D, Polidoro S, D'Errico M, Saieva C, Guarrera S, Calcagnile AS, Sera F, Allione A, Gemma S, Zanna I, Filomena A, Testai E, Caini S, Moretti R, Gomez-Miguel MJ, Nesi G, Luzzi I, Ottini L, Masala G, Matullo G, Dogliotti E: Polymorphic DNA repair and metabolic genes: a multigenic study on gastric cancer. Mutagenesis. 2010, 25: 569-575.PubMedCrossRef Palli D, Polidoro S, D'Errico M, Saieva C, Guarrera S, Calcagnile AS, Sera F, Allione A, Gemma S, Zanna I, Filomena A, Testai E, Caini S, Moretti R, Gomez-Miguel MJ, Nesi G, Luzzi I, Ottini L, Masala G, Matullo G, Dogliotti E: Polymorphic DNA repair and metabolic genes: a multigenic study on gastric cancer. Mutagenesis. 2010, 25: 569-575.PubMedCrossRef
56.
go back to reference Yadav DS, Devi TR, Ihsan R, Mishra AK, Kaushal M, Chauhan PS, Bagadi SA, Sharma J, Zamoawia E, Verma Y, Nandkumar A, Saxena S, Kapur S: Polymorphisms of glutathione-S-transferase genes and the risk of aero digestive tract cancers in the Northeast Indian population. Genet Test Mol Biomarkers. 2010, 14: 715-723.PubMedCrossRef Yadav DS, Devi TR, Ihsan R, Mishra AK, Kaushal M, Chauhan PS, Bagadi SA, Sharma J, Zamoawia E, Verma Y, Nandkumar A, Saxena S, Kapur S: Polymorphisms of glutathione-S-transferase genes and the risk of aero digestive tract cancers in the Northeast Indian population. Genet Test Mol Biomarkers. 2010, 14: 715-723.PubMedCrossRef
57.
go back to reference Luo YP, Chen HC, Khan MA, Chen FZ, Wan XX, Tan B, Ou-Yang FD, Zhang DZ: Genetic polymorphisms of metabolic enzymes-CYP1A1, CYP2D6, GSTM1, and GSTT1, and gastric carcinoma susceptibility. Tumour Biol. 2011, 32: 215-222.PubMedCrossRef Luo YP, Chen HC, Khan MA, Chen FZ, Wan XX, Tan B, Ou-Yang FD, Zhang DZ: Genetic polymorphisms of metabolic enzymes-CYP1A1, CYP2D6, GSTM1, and GSTT1, and gastric carcinoma susceptibility. Tumour Biol. 2011, 32: 215-222.PubMedCrossRef
58.
go back to reference Nguyen TV, Janssen MJ, van Oijen MG: Genetic polymorphisms in GSTA1, GSTP1, GSTT1, and GSTM1 and gastric cancer risk in a Vietnamese population. Oncol Res. 2010, 18: 349-355.PubMedCrossRef Nguyen TV, Janssen MJ, van Oijen MG: Genetic polymorphisms in GSTA1, GSTP1, GSTT1, and GSTM1 and gastric cancer risk in a Vietnamese population. Oncol Res. 2010, 18: 349-355.PubMedCrossRef
59.
go back to reference Darazy M, Balbaa M, Mugharbil A, Saeed H, Sidani H, Abdel-Razzak Z: CYP1A1, CYP2E1, and GSTM1 gene polymorphisms and susceptibility to colorectal and gastric cancer among Lebanese. Genet Test Mol Bio markers. 2011, 15 (6): 423-429.CrossRef Darazy M, Balbaa M, Mugharbil A, Saeed H, Sidani H, Abdel-Razzak Z: CYP1A1, CYP2E1, and GSTM1 gene polymorphisms and susceptibility to colorectal and gastric cancer among Lebanese. Genet Test Mol Bio markers. 2011, 15 (6): 423-429.CrossRef
60.
go back to reference García-González MA, Quintero E, Bujanda L, Nicolás D, Benito R, Strunk M, Santolaria S, Sopeña F, Badía M, Hijona E, Pérez-Aísa MA, Méndez-Sánchez IM, Thomson C, Carrera P, Piazuelo E, Jiménez P, Espinel J, Campo R, Manzano M, Geijo F, Pellisé M, González-Huix F, Espinós J, Titó L, Zaballa M, Pazo R, Lanas A: Relevance of GSTM1, GSTT1, and GSTP1 gene polymorphisms to gastric cancer susceptibility and phenotype. Mutagenesis. 2011, 27 (6): 771-777.CrossRef García-González MA, Quintero E, Bujanda L, Nicolás D, Benito R, Strunk M, Santolaria S, Sopeña F, Badía M, Hijona E, Pérez-Aísa MA, Méndez-Sánchez IM, Thomson C, Carrera P, Piazuelo E, Jiménez P, Espinel J, Campo R, Manzano M, Geijo F, Pellisé M, González-Huix F, Espinós J, Titó L, Zaballa M, Pazo R, Lanas A: Relevance of GSTM1, GSTT1, and GSTP1 gene polymorphisms to gastric cancer susceptibility and phenotype. Mutagenesis. 2011, 27 (6): 771-777.CrossRef
61.
go back to reference Malakar M, Devi KR, Phukan RK, Kaur T, Deka M, Puia L, Barua D, Mahanta J, Narain K: Genetic polymorphism of glutathione S-transferases M1 and T1, tobacco habits and risk of stomach cancer in Mizoram, India. Asian Pac J Cancer Prev. 2012, 13 (9): 4725-4732.PubMedCrossRef Malakar M, Devi KR, Phukan RK, Kaur T, Deka M, Puia L, Barua D, Mahanta J, Narain K: Genetic polymorphism of glutathione S-transferases M1 and T1, tobacco habits and risk of stomach cancer in Mizoram, India. Asian Pac J Cancer Prev. 2012, 13 (9): 4725-4732.PubMedCrossRef
62.
go back to reference Jing C, Huang ZJ, Duan YQ, Wang PH, Zhang R, Luo KS, Xiao XR: Glulathione-S-transferases gene polymorphism in prediction of gastric cancer risk by smoking and Helicobacter pylori infection status. Asian Pac J Cancer Prev. 2012, 13 (7): 3325-3328.PubMedCrossRef Jing C, Huang ZJ, Duan YQ, Wang PH, Zhang R, Luo KS, Xiao XR: Glulathione-S-transferases gene polymorphism in prediction of gastric cancer risk by smoking and Helicobacter pylori infection status. Asian Pac J Cancer Prev. 2012, 13 (7): 3325-3328.PubMedCrossRef
63.
go back to reference Xiaowen L, Hongmei Y, Hong C, Yanong W: The expression and clinical significance of miR-132 in gastric cancer patients. Diagn Pathol. 2014, 9: 57-CrossRef Xiaowen L, Hongmei Y, Hong C, Yanong W: The expression and clinical significance of miR-132 in gastric cancer patients. Diagn Pathol. 2014, 9: 57-CrossRef
64.
go back to reference Ming G, Lin W, Xin C, Ruixue C, Peifeng L: The association between chemosensitivity and Pgp, GST- and Topo II expression in gastric cancer. Diagn Pathol. 2013, 8: 198-CrossRef Ming G, Lin W, Xin C, Ruixue C, Peifeng L: The association between chemosensitivity and Pgp, GST- and Topo II expression in gastric cancer. Diagn Pathol. 2013, 8: 198-CrossRef
65.
go back to reference Ketterer B, Harris JM, Talaska G, Meyer DJ, Pemble SE, Taylor JB, Lang NP, Kadlubar FF: The human glutathione S-transferase supergene family, its polymorphism, and its effects on susceptibility to lung cancer. Environ Health Perspect. 1992, 98: 87-94.PubMedPubMedCentralCrossRef Ketterer B, Harris JM, Talaska G, Meyer DJ, Pemble SE, Taylor JB, Lang NP, Kadlubar FF: The human glutathione S-transferase supergene family, its polymorphism, and its effects on susceptibility to lung cancer. Environ Health Perspect. 1992, 98: 87-94.PubMedPubMedCentralCrossRef
66.
go back to reference Dan C, Huimin S, Kan Z, Lingling Y, Guohua Z: RAD51 gene 135G/C polymorphism and the risk of four types of common cancers: a meta-analysis. Diagn Pathol. 2014, 9: 18-CrossRef Dan C, Huimin S, Kan Z, Lingling Y, Guohua Z: RAD51 gene 135G/C polymorphism and the risk of four types of common cancers: a meta-analysis. Diagn Pathol. 2014, 9: 18-CrossRef
67.
go back to reference Xue Q, Peng Q, Qin A, Chen Z, Lin L, Deng Y, Xie L, Xu J, Li H, Li T, Li S, Zhao J: Association of COMT Val158Met polymorphism and breast cancer risk: an updated meta-analysis. Diagn Pathol. 2012, 7: 136-CrossRef Xue Q, Peng Q, Qin A, Chen Z, Lin L, Deng Y, Xie L, Xu J, Li H, Li T, Li S, Zhao J: Association of COMT Val158Met polymorphism and breast cancer risk: an updated meta-analysis. Diagn Pathol. 2012, 7: 136-CrossRef
68.
go back to reference Saadat M: Genetic polymorphisms of glutathione S-transferase T1 (GSTT1) and susceptibility to gastric cancer: a meta-analysis. Cancer Sci. 2006, 97: 505-509.PubMedCrossRef Saadat M: Genetic polymorphisms of glutathione S-transferase T1 (GSTT1) and susceptibility to gastric cancer: a meta-analysis. Cancer Sci. 2006, 97: 505-509.PubMedCrossRef
69.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
70.
go back to reference Darazy M, Balbaa M, Mugharbil A, Saeed H, Hassan S, Ziad AR: CYP1A1, CYP2E1, and GSTM1 gene polymorphisms and susceptibility to colorectal and gastric cancer among Lebanese. Genetic Test Mol Biomarkers. 2011, 15 (6): 1-7.CrossRef Darazy M, Balbaa M, Mugharbil A, Saeed H, Hassan S, Ziad AR: CYP1A1, CYP2E1, and GSTM1 gene polymorphisms and susceptibility to colorectal and gastric cancer among Lebanese. Genetic Test Mol Biomarkers. 2011, 15 (6): 1-7.CrossRef
71.
go back to reference Piao JM, Shin MH, Kweon SS, Kim HN, Choi JS, Bae WK, Shim HJ, Kim HR, Park YK, Choi YD, Kim SH: Glutathione-S-transferase (GSTM1, GSTT1) and the risk of gastrointestinal cancer in a Korean population. World J Gastroenterol. 2009, 15: 5716-5721.PubMedPubMedCentralCrossRef Piao JM, Shin MH, Kweon SS, Kim HN, Choi JS, Bae WK, Shim HJ, Kim HR, Park YK, Choi YD, Kim SH: Glutathione-S-transferase (GSTM1, GSTT1) and the risk of gastrointestinal cancer in a Korean population. World J Gastroenterol. 2009, 15: 5716-5721.PubMedPubMedCentralCrossRef
72.
go back to reference Qiu LX, Wang K, Lv FF, Chen ZY, Liu X, Zheng CL, Li WH, Zhu XD, Guo WJ, Li J: GSTM1 null allele is a risk factor for gastric cancer development in Asians. Cytokine. 2011, 55 (1): 122-125.PubMedCrossRef Qiu LX, Wang K, Lv FF, Chen ZY, Liu X, Zheng CL, Li WH, Zhu XD, Guo WJ, Li J: GSTM1 null allele is a risk factor for gastric cancer development in Asians. Cytokine. 2011, 55 (1): 122-125.PubMedCrossRef
Metadata
Title
Glutathione S-transferase M1 null genotype meta-analysis on gastric cancer risk
Authors
Xianhong Meng
Yong Liu
Bona Liu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2014
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/1746-1596-9-122

Other articles of this Issue 1/2014

Diagnostic Pathology 1/2014 Go to the issue