Methods and Findings

Background Glutathione S-transferases (GSTs) are known to abolish or reduce the activities of intracellular enzymes that help detoxify environmental carcinogens, such as those found in tobacco smoke. It has been suggested that polymorphisms in the GST genes are risk factors for lung cancer, but a large number of studies have reported apparently conflicting results. Methods and Findings Literature-based meta-analysis was supplemented by tabular data from investigators of all relevant studies of five GST polymorphisms ( GSTM1 null, GSTT1 null, I105V, and A114V polymorphisms in the GSTP1 genes, and GSTM3 intron 6 polymorphism) available before August, 2005, with investigation of potential sources of heterogeneity. Included in the present meta-analysis were 130 studies, involving a total of 23,452 lung cancer cases and 30,397 controls. In a combined analysis, the relative risks for lung cancer of the GSTM1 null and GSTT1 null polymorphisms were 1.18 (95% confidence interval [CI]: 1.14–1.23) and 1.09 (95% CI: 1.02–1.16), respectively, but in the larger studies they were only 1.04 (95% CI: 0.95–1.14) and 0.99 (95% CI: 0.86–1.11), respectively. In addition to size of study, ethnic background was a significant source of heterogeneity among studies of the GSTM1 null genotype, with possibly weaker associations in studies of individuals of European continental ancestry. Combined analyses of studies of the 105V, 114V, and GSTM3*B variants showed no significant overall associations with lung cancer, yielding per-allele relative risks of 1.04 (95% CI: 0.99–1.09), 1.15 (95% CI: 0.95–1.39), and 1.05 (95% CI: 0.89–1.23), respectively. Conclusions The risk of lung cancer is not strongly associated with the I105V and A114V polymorphisms in the GSTP1 gene or with GSTM3 intron 6 polymorphism. Given the non-significant associations in the larger studies, the relevance of the weakly positive overall associations with the GSTM1 null and the GSTT1 null polymorphisms is uncertain. As lung cancer has important environmental causes, understanding any genetic contribution to it in general populations will require the conduct of particularly large and comprehensive studies.

[1]  T. Sellers,et al.  Examining Population Stratification via Individual Ancestry Estimates versus Self-Reported Race , 2005, Cancer Epidemiology Biomarkers & Prevention.

[2]  Qinghua Zhou,et al.  [Relationship between genetic polymorphism of GSTT1 gene and inherent susceptibility to lung cancer in Han population in Sichuan, China]. , 2005, Zhongguo fei ai za zhi = Chinese journal of lung cancer.

[3]  N. Rothman,et al.  Green tea consumption, genetic susceptibility, PAH-rich smoky coal, and the risk of lung cancer. , 2005, Mutation research.

[4]  S. Kardia,et al.  Combinations of glutathione S-transferase genotypes and risk of early-onset lung cancer in Caucasians and African Americans: a population-based study. , 2005, Carcinogenesis.

[5]  Qinghua Zhou,et al.  [Study on the association between genetic polymorphism of CYP2E1, GSTM1 and susceptibility of lung cancer]. , 2005, Zhongguo fei ai za zhi = Chinese journal of lung cancer.

[6]  S. Land,et al.  GSTM1, GSTT1 and GSTP1 polymorphisms, environmental tobacco smoke exposure and risk of lung cancer among never smokers: a population-based study. , 2004, Carcinogenesis.

[7]  Yi-ming Wu,et al.  Research on Relationship between GSTMI Gene Deletion and Lung Cancer Genetic Susceptibility , 2005 .

[8]  Sidong Chen,et al.  Interaction between serum selenium level and polymorphism of GSTM1 in lung cancer , 2005 .

[9]  B. Lai,et al.  [The relationship between genetic polymorphism of metabolizing enzymes and the genetic susceptibility to lung cancer]. , 2004, Zhonghua liu xing bing xue za zhi = Zhonghua liuxingbingxue zazhi.

[10]  D. Neuberg,et al.  Dietary intake of Cruciferous vegetables, Glutathione S-transferase (GST) polymorphisms and lung cancer risk in a Caucasian population , 2004, Cancer Causes & Control.

[11]  R. Sobti,et al.  Genetic polymorphism of the CYP1A1, CYP2E1, GSTM1 and GSTT1 genes and lung cancer susceptibility in a north Indian population , 2004, Molecular and Cellular Biochemistry.

[12]  S. Wacholder,et al.  CYP1A1 and GSTM1 polymorphisms in relation to lung cancer risk in Chinese women. , 2004, Cancer letters.

[13]  W. Bamlet,et al.  Glutathione pathway genes and lung cancer risk in young and old populations. , 2004, Carcinogenesis.

[14]  L. Yin,et al.  [Studies of the genes related to lung cancer susceptibility in Nanjing Han population, China]. , 2004, Yi chuan = Hereditas.

[15]  Hua Zhao,et al.  Genetic susceptibility to tobacco-related cancer , 2004, Oncogene.

[16]  M. Chan-yeung,et al.  Lung cancer susceptibility and polymorphisms of glutathione-S-transferase genes in Hong Kong. , 2004, Lung cancer.

[17]  Yusuke Nakamura,et al.  Variation of gene-based SNPs and linkage disequilibrium patterns in the human genome. , 2004, Human molecular genetics.

[18]  Richard Doll,et al.  Mortality in relation to smoking: 22 years' observations on female British doctors. , 1980, British medical journal.

[19]  A. Tjønneland,et al.  Glutathione S‐transferase T1 null‐genotype is associated with an increased risk of lung cancer , 2004, International journal of cancer.

[20]  M. Warholm,et al.  Influence of CYP1A1, GSTM1, GSTT1, and NQO1 genotypes and cumulative smoking dose on lung cancer risk in a Swedish population. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[21]  Q. Lan,et al.  Molecular epidemiological studies on the relationship between indoor coal burning and lung cancer in Xuan Wei, China. , 2004, Toxicology.

[22]  J. Schneider,et al.  GSTM1, GSTT1, and GSTP1 polymorphism and lung cancer risk in relation to tobacco smoking. , 2004, Cancer letters.

[23]  E. Imyanitov,et al.  A novel approach for assessment of cancer predisposing roles of GSTM1 and GSTT1 genes: use of putatively cancer resistant elderly tumor-free smokers as the referents. , 2004, Lung cancer.

[24]  BaoGuo Wang,et al.  [A case control study on the impact of CYP450 MSPI and GST-M1 polymorphisms on the risk of lung cancer]. , 2004, Zhonghua zhong liu za zhi [Chinese journal of oncology].

[25]  J. Gómez-catalán,et al.  Genetic polymorphism of glutathione S-transferase P1 gene and lung cancer risk , 1999, Cancer Causes & Control.

[26]  M. Spitz,et al.  Polymorphisms in the glutathione S-transferase class mu and theta genes interact and increase susceptibility to lung cancer in minority populations (Texas, United States) , 1997, Cancer Causes & Control.

[27]  Xiping Xu,et al.  A case-control study of cytochrome P450 1A1, glutathione S-transferase M1, cigarette smoking and lung cancer susceptibility (Massachusetts, United States) , 1997, Cancer Causes & Control.

[28]  Ye Wei Study on relationship between GSTM1 polymorphism,diet factors and lung cancer , 2004 .

[29]  Cao Yan Study on the Relationship Between the Genetic Polymorphisms of GSTM1 and GSTT1 Genes and Lung Cancer Susceptibility in the Population of Hunan Province of China , 2004 .

[30]  Wang Bao-guo A Case-Control Study of the Impact of Glutathione S-transferase M1 on the Risk of Lung Cancer , 2004 .

[31]  I. Kalina,et al.  Combined analysis of polymorphisms in glutathione S-transferase M1 and microsomal epoxide hydrolase in lung cancer patients. , 2004, Neoplasma.

[32]  G. Morgan-Villela,et al.  GSTT1 Gene Deletion Is Associated with Lung Cancer in Mexican Patients , 2004, Disease markers.

[33]  K. Buetow,et al.  Genetic susceptibility and dietary patterns in lung cancer. , 2004, Lung cancer.

[34]  Jingweng Wang,et al.  GST genetic polymorphisms and lung adenocarcinoma susceptibility in a Chinese population. , 2003, Cancer letters.

[35]  I. Yaylim,et al.  GST M1 and CYP1A1 gene polymorphism and daily fruit consumption in Turkish patients with non-small cell lung carcinomas. , 2003, In vivo.

[36]  D. Spandidos,et al.  Genetic polymorphisms of CYP1A1, GSTM1 and GSTT1 genes and lung cancer risk. , 2003, Oncology reports.

[37]  M. Ando,et al.  Risk modification by CYP1A1 and GSTM1 polymorphisms in the association of environmental tobacco smoke and lung cancer: A case‐control study in Japanese nonsmoking women , 2003, International Journal of Cancer.

[38]  Z. Seyfikli,et al.  Strong association between the GSTM1-null genotype and lung cancer in a Turkish population. , 2003, Cancer genetics and cytogenetics.

[39]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[40]  K. Buetow,et al.  Genetic susceptibility and dietary patterns in lung cancer , 2003 .

[41]  A. Ruano-Raviña,et al.  GSTM1 and GSTT1 polymorphisms, tobacco and risk of lung cancer: a case-control study from Galicia, Spain. , 2003, Anticancer research.

[42]  D. Neuberg,et al.  Smoking and the Risk of Lung Cancer: Susceptibility with GSTP1 Polymorphisms , 2003, Epidemiology.

[43]  J. Wall,et al.  Haplotype blocks and linkage disequilibrium in the human genome , 2003, Nature Reviews Genetics.

[44]  T. Vaughan,et al.  Glutathione S-transferase M1, T1, and P1 polymorphisms and survival among lung cancer patients. , 2003, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[45]  T. Vaughan,et al.  A population-based study of glutathione S-transferase M1, T1 and P1 genotypes and risk for lung cancer. , 2003, Lung cancer.

[46]  Y. Hsueh,et al.  Analysis of NQO1, GSTP1, and MnSOD genetic polymorphisms on lung cancer risk in Taiwan. , 2003, Lung cancer.

[47]  K. Kuriki,et al.  Association of GSTM1, CYP1A1 and CYP2E1 genetic polymorphisms with susceptibility to lung adenocarcinoma: A case‐control study in Chinese population , 2003, Cancer science.

[48]  M. Spitz,et al.  Association between glutathione S-transferase p1 polymorphisms and lung cancer risk in Caucasians: a case-control study. , 2003, Lung cancer.

[49]  J. Zwischenberger,et al.  Combined effect of MPO, GSTM1 and GSTT1 polymorphisms on chromosome aberrations and lung cancer risk. , 2003, International journal of hygiene and environmental health.

[50]  E. Reszka,et al.  Glutathione S-transferase M1 and P1 metabolic polymorphism and lung cancer predisposition. , 2003, Neoplasma.

[51]  W. Tan,et al.  Genetic polymorphism in myeloperoxidase but not GSTM1 is associated with risk of lung squamous cell carcinoma in a Chinese population , 2002, International journal of cancer.

[52]  A. Cittadini,et al.  Glutathione S-transferase (GST) polymorphisms as risk factors for cancer in a highly homogeneous population from southern Italy. , 2002, Anticancer research.

[53]  David H Phillips,et al.  Associations between carcinogen-DNA damage, glutathione S-transferase genotypes, and risk of lung cancer in the prospective Physicians' Health Cohort Study. , 2002, Carcinogenesis.

[54]  M. Loriot,et al.  Genetic polymorphisms of glutathione S-transferases as modulators of lung cancer susceptibility. , 2002, Carcinogenesis.

[55]  J. Yokota,et al.  Contribution of the NQO1 and GSTT1 polymorphisms to lung adenocarcinoma susceptibility. , 2002, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[56]  L. Le Marchand,et al.  Meta- and pooled analyses of the effects of glutathione S-transferase M1 polymorphisms and smoking on lung cancer risk. , 2002, Carcinogenesis.

[57]  Sarah J Lewis,et al.  GSTM1, GSTT1 and GSTP1 polymorphisms and lung cancer risk. , 2002, Cancer letters.

[58]  D. Christiani,et al.  Combinations of the variant genotypes of GSTP1, GSTM1, and p53 are associated with an increased lung cancer risk. , 2002, Cancer research.

[59]  Z. Ji Study on Genetic Polymorphisms of GSTM1 and GSTT1 Related with Inherent Susceptibility to Lung Cancer in Women , 2002 .

[60]  Chang-Qing Ying A study of genetic polymorphism of GSTM1 gene in normal population and lung cancer population in Yunnan , 2002 .

[61]  W. Ahrens,et al.  Cruciferous vegetable intake, GSTM1 genotype and lung cancer risk in a non-smoking population. , 2002, IARC scientific publications.

[62]  D. Christiani,et al.  Differential association of the codon 72 p53 and GSTM1 polymorphisms on histological subtype of non-small cell lung carcinoma. , 2001, Cancer research.

[63]  L. Quiñones,et al.  CYP1A1, CYP2E1 and GSTM1 genetic polymorphisms. The effect of single and combined genotypes on lung cancer susceptibility in Chilean people. , 2001, Cancer letters.

[64]  H. Dienemann,et al.  Glutathione-S-transferase M1, M3, T1 and P1 polymorphisms and susceptibility to non-small-cell lung cancer subtypes and hamartomas. , 2001, Pharmacogenetics.

[65]  J. Gómez-catalán,et al.  Lung cancer susceptibility in relation to combined polymorphisms of microsomal epoxide hydrolase and glutathione S-transferase P1. , 2001, Cancer letters.

[66]  M. Teh,et al.  Dietary isothiocyanates, glutathione S-transferase -M1, -T1 polymorphisms and lung cancer risk among Chinese women in Singapore. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[67]  K. Xue,et al.  Polymorphisms of the CYP1A1 and GSTM1 genes in relation to individual susceptibility to lung carcinoma in Chinese population. , 2001, Mutation research.

[68]  K. Trieb,et al.  Genetic polymorphisms of CYP1A1 and GSTM1 and lung cancer risk. , 2001, Anticancer research.

[69]  S. Chen,et al.  [Polymorphisms of the CYP1A1 and GSTM1 genes and their combined effects on individual susceptibility to lung cancer in a Chinese population]. , 2001, Zhonghua yi xue yi chuan xue za zhi = Zhonghua yixue yichuanxue zazhi = Chinese journal of medical genetics.

[70]  K. Hemminki,et al.  Differential interactions between GSTM1 and NAT2 genotypes on aromatic DNA adduct level and HPRT mutant frequency in lung cancer patients and population controls. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[71]  F. Nyberg,et al.  Glutathione S‐transferase T1‐null genotype interacts synergistically with heavy smoking on lung cancer risk , 2001, Environmental and molecular mutagenesis.

[72]  James F. Babb,et al.  Gender differences in genetic susceptibility for lung cancer. , 2000, Lung cancer.

[73]  E. Taioli,et al.  Glutathione S-transferase M1 polymorphism and lung cancer risk in African-Americans. , 2000, Carcinogenesis.

[74]  P. Beaune,et al.  Relation between inducibility of CYP1A1, GSTM1 and lung cancer in a French population. , 2000, Pharmacogenetics.

[75]  M. Spitz,et al.  Dietary intake of isothiocyanates: evidence of a joint effect with glutathione S-transferase polymorphisms in lung cancer risk. , 2000, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[76]  T. V. Kondratieva,et al.  GSTM1 genotypes in elderly tumour-free smokers and non-smokers. , 2000, Lung cancer.

[77]  G. Coetzee,et al.  CYP1A1 I462V genetic polymorphism and lung cancer risk in a cohort of men in Shanghai, China. , 2000, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[78]  G. Coetzee,et al.  Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: a prospective study of men in Shanghai, China , 2000, The Lancet.

[79]  W. Ahrens,et al.  Lung cancer risk in nonsmokers and GSTM1 and GSTT1 genetic polymorphism. , 2000, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[80]  N. Rothman,et al.  Indoor coal combustion emissions, GSTM1 and GSTT1 genotypes, and lung cancer risk: a case-control study in Xuan Wei, China. , 2000, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[81]  R. Tweedie,et al.  A Nonparametric “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis , 2000 .

[82]  D. Ryberg,et al.  GSTM1 and NAT2 polymorphisms in operable and non-operable lung cancer patients. , 2000, Carcinogenesis.

[83]  Y. Nakanishi,et al.  [Lung cancer risk and genetic polymorphism at the glutathione S-transferase P1 locus in male Japanese]. , 2000, Fukuoka igaku zasshi = Hukuoka acta medica.

[84]  Y. Nakanishi,et al.  Polymorphism in GSTM1, GSTT1, and GSTP1 and Susceptibility to Lung Cancer in a Japanese Population. , 2000, Asian Pacific journal of cancer prevention : APJCP.

[85]  N. Bhat,et al.  Effect of vitamin intervention on the relationship between GSTM1, smoking, and lung cancer risk among male smokers. , 1999, Cancer Epidemiology, Biomarkers and Prevention.

[86]  P. Beaune,et al.  GSTM1, smoking and lung cancer: a case-control study. , 1999, International journal of epidemiology.

[87]  Q. Zhang,et al.  Polymorphisms of the GSTM1 and CYP2D6 genes associated with susceptibility to lung cancer in Chinese. , 1999, Mutation research.

[88]  R. Houlston Glutathione S-transferase M1 status and lung cancer risk: a meta-analysis. , 1999, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[89]  C. Harris,et al.  GSTM1, GSTP1, CYP1A1 and CYP2D6 polymorphisms in lung cancer patients from an environmentally polluted region of Poland: correlation with lung DNA adduct levels. , 1999, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[90]  M. Ingelman-Sundberg,et al.  Genetic polymorphism of xenobiotic metabolizing enzymes among Chinese lung cancer patients , 1999, International journal of cancer.

[91]  K. Noda,et al.  Lung cancer risk of the GSTM1 null genotype is enhanced in the presence of the GSTP1 mutated genotype in male Japanese smokers. , 1999, Cancer letters.

[92]  A. Hirvonen Polymorphisms of xenobiotic-metabolizing enzymes and susceptibility to cancer. , 1999, Environmental health perspectives.

[93]  Q. Lan,et al.  [Glutathione S-transferase GSTM1 and GSTT1 genotypes and susceptibility to lung cancer]. , 1999, Wei sheng yan jiu = Journal of hygiene research.

[94]  P. Lin,et al.  Influence of polymorphism at p53, CYP1A1 and GSTM1 loci on p53 mutation and association of p53 mutation with prognosis in lung cancer. , 1999, Zhonghua yi xue za zhi = Chinese medical journal; Free China ed.

[95]  J. Chang,et al.  Polymorphism of the CYP1A1 and glutathione-S-transferase gene in Korean lung cancer patients , 1998, Experimental & Molecular Medicine.

[96]  P. Dayer,et al.  Role of glutathione S-transferase GSTM1, GSTM3, GSTP1 and GSTT1 genotypes in modulating susceptibility to smoking-related lung cancer. , 1998, Pharmacogenetics.

[97]  L. Marchand,et al.  Associations of CYP1A1, GSTM1, and CYP2E1 polymorphisms with lung cancer suggest cell type specificities to tobacco carcinogens. , 1998, Cancer research.

[98]  F P Perera,et al.  Associations between both genetic and environmental biomarkers and lung cancer: evidence of a greater risk of lung cancer in women smokers. , 1998, Carcinogenesis.

[99]  K. Hemminki,et al.  Glutathione S-transferase mu1 and N-acetyltransferase 2 genetic polymorphisms and exposure to tobacco smoke in nonsmoking and smoking lung cancer patients and population controls. , 1998, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[100]  E. Biros,et al.  Genetic polymorphism of glutathione S-transferases M1 and T1 as a risk factor in lung cancer , 1998 .

[101]  S. Anttila,et al.  Combined effect of polymorphic GST genes on individual susceptibility to lung cancer , 1998, International journal of cancer.

[102]  K. Hemminki,et al.  GSTM1 AND NAT2 GENETIC POLYMORPHISMS AND EXPOSURE TO TOBACCO SMOKE IN NONSMOKING AND SMOKING LUNG CANCER PATIENTS AND POPULATION CONTROLS , 1998 .

[103]  Qiang Zhang,et al.  [CYP2D6 and GSTM1 genetic polymorphism and lung cancer susceptibility]. , 1998, Zhonghua zhong liu za zhi [Chinese journal of oncology].

[104]  S. R. Wilson,et al.  Polymorphism of the Pi class glutathione S-transferase in normal populations and cancer patients. , 1998, Pharmacogenetics.

[105]  E. Biros,et al.  Genetic polymorphism of glutathione S-transferases M1 and T1 as a risk factor in lung and bladder cancers. , 1998, Neoplasma.

[106]  P. Dayer,et al.  Effects of glutathione S-transferases GSTM1 and GSTT1 genotypes on lung cancer risk in smokers. , 1997, Pharmacogenetics.

[107]  S. Z. Abdel‐Rahman,et al.  Combined genetic polymorphism and risk for development of lung cancer. , 1997, Mutation research.

[108]  T. Rebbeck Molecular epidemiology of the human glutathione S-transferase genotypes GSTM1 and GSTT1 in cancer susceptibility. , 1997, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[109]  J. Gómez-catalán,et al.  Glutathione S-transferase M1 (GSTM1) and T1 (GSTT1) polymorphisms and lung cancer risk among Northwestern Mediterraneans. , 1997, Carcinogenesis.

[110]  L. Harries,et al.  Genotypes of glutathione transferase M1 and P1 and their significance for lung DNA adduct levels and cancer risk. , 1997, Carcinogenesis.

[111]  D. Lamb,et al.  Frequency of glutathione S-transferase M1 deletion in smokers with emphysema and lung cancer , 1997, Human & experimental toxicology.

[112]  J. Pi,et al.  Gene deficiency of glutathione S-transferase mu isoform associated with susceptibility to lung cancer in a Chinese population. , 1997, Cancer letters.

[113]  J. Buolamwini,et al.  Molecular Cloning, Characterization, and Expression in Escherichia coli of Full-length cDNAs of Three Human Glutathione S -Transferase Pi Gene Variants EVIDENCE FOR DIFFERENTIAL CATALYTIC ACTIVITY OF THE ENCODED PROTEINS* , 1997 .

[114]  W. Au,et al.  Interactions between genetic predisposition and environmental toxicants for development of lung cancer , 1997, Environmental and molecular mutagenesis.

[115]  M. Lung,et al.  Analysis of L-myc and GSTM1 genotypes in Chinese non-small cell lung carcinoma patients. , 1996, Lung cancer.

[116]  J. Lear,et al.  Polymorphism at the glutathione S-transferase locus GSTM3: interactions with cytochrome P450 and glutathione S-transferase genotypes as risk factors for multiple cutaneous basal cell carcinoma. , 1996, Cancer research.

[117]  D. Bell,et al.  Glutathione S-transferase GSTT1 genotypes and susceptibility to cancer: studies of interactions with GSTM1 in lung, oral, gastric and colorectal cancers. , 1996, Carcinogenesis.

[118]  Yang Cuihong,et al.  Apoptosis of tumor cells in lectin-dependent lymphokine-activated killer cell-mediated cytotoxicity , 1996 .

[119]  J. Rueff,et al.  Glutathione S-transferase mu polymorphism and susceptibility to lung cancer in the Portuguese population. , 1996, Teratogenesis, carcinogenesis, and mutagenesis.

[120]  A. Fryer,et al.  Identification of polymorphism at the glutathione S-transferase, GSTM3 locus: evidence for linkage with GSTM1*A. , 1995, The Biochemical journal.

[121]  K. Noda,et al.  Risk of smoking for squamous and small cell carcinomas of the lung modulated by combinations of CYP1A1 and GSTM1 gene polymorphisms in a Japanese population. , 1995, Carcinogenesis.

[122]  D. Christiani,et al.  Comparison of sister chromatid exchange frequency in peripheral lymphocytes in lung cancer cases and controls. , 1995, Mutation research.

[123]  K. Richert-Boe,et al.  Glutathione S-transferase M1 (GSTM1) deficiency and lung cancer risk. , 1995, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[124]  S. London,et al.  Polymorphism of glutathione S-transferase M1 and lung cancer risk among African-Americans and Caucasians in Los Angeles County, California. , 1995, Journal of the National Cancer Institute.

[125]  E. Bowman,et al.  Human Lung Carcinogen—DNA Adduct Levels Mediated by Genetic Polymorphisms In Vivo , 1995 .

[126]  Q. Zheng,et al.  [The study of GST mu gene deletion as the hereditary marker for susceptibility to lung cancer]. , 1995, Zhonghua jie he he hu xi za zhi = Zhonghua jiehe he huxi zazhi = Chinese journal of tuberculosis and respiratory diseases.

[127]  K. Kawajiri,et al.  Genetic polymorphisms of drug-metabolizing enzymes and lung cancer susceptibility. , 1995, Pharmacogenetics.

[128]  E. Bowman,et al.  Human lung carcinogen-DNA adduct levels mediated by genetic polymorphisms in vivo. , 1995, Journal of the National Cancer Institute.

[129]  K. Noda,et al.  Distribution of GSTM1 null genotype in relation to gender, age and smoking status in Japanese lung cancer patients. , 1995, Pharmacogenetics.

[130]  T. Katoh [The frequency of glutathione-S-transferase M1 (GSTM1) gene deletion in patients with lung and oral cancer]. , 1994, Sangyo igaku. Japanese journal of industrial health.

[131]  C. Begg,et al.  Operating characteristics of a rank correlation test for publication bias. , 1994, Biometrics.

[132]  A. Rannug,et al.  Genetic susceptibility to lung cancer with special emphasis on CYP1A1 and GSTM1: a study on host factors in relation to age at onset, gender and histological cancer types. , 1994, Carcinogenesis.

[133]  K. Noda,et al.  Lung cancer risk of GSTM1 null genotype is dependent on the extent of tobacco smoke exposure. , 1994, Carcinogenesis.

[134]  K. Becker,et al.  Characterization of hUCRBP (YY1, NF-E1, delta): a transcription factor that binds the regulatory regions of many viral and cellular genes. , 1994, Gene.

[135]  H Vainio,et al.  The GSTM1 null genotype as a potential risk modifier for squamous cell carcinoma of the lung. , 1993, Carcinogenesis.

[136]  K. Nakachi,et al.  Polymorphisms of the CYP1A1 and glutathione S-transferase genes associated with susceptibility to lung cancer in relation to cigarette dose in a Japanese population. , 1993, Cancer research.

[137]  J. Brockmöller,et al.  Genotype and Phenotype of Glutathione S-Transferase Class µ Isoenzymes µ and ψ in Lung Cancer Patients and Controls , 1993 .

[138]  J. Brockmöller,et al.  Genotype and phenotype of glutathione S-transferase class mu isoenzymes mu and psi in lung cancer patients and controls. , 1993, Cancer research.

[139]  G. Talaska,et al.  The human glutathione S-transferase supergene family, its polymorphism, and its effects on susceptibility to lung cancer. , 1992, Environmental health perspectives.

[140]  K. Kawajiri,et al.  High Susceptibility to Lung Cancer Analyzed in Terms of Combined Genotypes of P450IA1 and Mu‐class Glutathione S‐Transferase Genes , 1992, Japanese journal of cancer research : Gann.

[141]  S. Heckbert,et al.  Glutathione S-transferase and epoxide hydrolase activity in human leukocytes in relation to risk of lung cancer and other smoking-related cancers. , 1992, Journal of the National Cancer Institute.

[142]  A Whitehead,et al.  A general parametric approach to the meta-analysis of randomized clinical trials. , 1991, Statistics in medicine.

[143]  C. Wolf,et al.  Glutathione S-transferase mu locus: use of genotyping and phenotyping assays to assess association with lung cancer susceptibility. , 1991, Carcinogenesis.

[144]  B. Ketterer Protective role of glutathione and glutathione transferases in mutagenesis and carcinogenesis. , 1988, Mutation research.

[145]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.