Abstract
The conclusions of the published reports on the relationship between glutathione S-transferase P1 (GSTP1) gene polymorphism and the risk of lung cancer are still debated. GSTP1 is one of the important mutant sites reported at present. This meta-analysis was performed to evaluate the association between GSTP1 and the risk of lung cancer. The association investigations were identified from PubMed and Cochrane Library, and eligible studies were included and synthesized using meta-analysis method. Forty-four reports were included into this meta-analysis for the association of GSTP1 A/G gene polymorphism and lung cancer susceptibility, consisting of 12,363 patients with lung cancer and 13,948 controls. The association between GSTPI G allele and lung cancer risk was found in this meta-analysis (OR 1.08, 95 % CI 1.02–1.15, P = 0.01). However, the GG genotype and AA genotype were not associated with the susceptibility of lung cancer. Furthermore, there was no association between GSTP1 A/G gene polymorphism and the risk of lung cancer in Caucasians, and East-Asians. In conclusion, GSTP1 G allele is associated with the lung cancer susceptibility. However, more studies on the relationship between GSTP1 A/G gene polymorphism and the risk of lung cancer should be performed in the future.
Similar content being viewed by others
References
Chen L, He Z, Qin L, Li Q, Shi X, Zhao S, Chen L, Zhong N, Chen X (2011) Antitumor effect of malaria parasite infection in a murine Lewis lung cancer model through induction of innate and adaptive immunity. PLoS One 6:24407
Zhang C, Elkahloun AG, Robertson M, Gills JJ, Tsurutani J, Shih JH, Fukuoka J, Hollander MC, Harris CC, Travis WD, Jen J, Dennis PA (2011) Loss of cytoplasmic CDK1 predicts poor survival in human lung cancer and confers chemotherapeutic resistance. PLoS One 6:23849
Ihsan R, Chauhan PS, Mishra AK, Yadav DS, Kaushal M, Sharma JD, Zomawia E, Verma Y, Kapur S, Saxena S (2011) Multiple analytical approaches reveal distinct gene-environment interactions in smokers and non smokers in lung cancer. PLoS One 6:29431
Yang L, Li Y, Ling X, Liu L, Liu B, Xu K, Bin X, Ji W, Lu J (2011) A common genetic variant (97906C>A) of DAB2IP/AIP1 is associated with an increased risk and early onset of lung cancer in Chinese males. PLoS One 6:26944
VanderWeele TJ, Asomaning K, Tchetgen TE, Han Y, Spitz MR, Shete S, Wu X, Gaborieau V, Wang Y, McLaughlin J, Hung RJ, Brennan P, Amos CI, Christiani DC, Lin X (2012) Genetic variants on 15q25.1, smoking, and lung cancer: an assessment of mediation and interaction. Am J Epidemiol 175:1013–1020
Tew KD, Townsend DM (2012) Glutathione-S-transferases as determinants of cell survival and death. Antioxid Redox Signal. doi:10.1089/ars.2012.4640
Board PG, Webb GC, Coggan M (1989) Isolation of a cDNA clone and localization of the human glutathione S-transferase 3 genes to chromosome bands 11q13 and 12q13-14. Ann Hum Genet 53:205–213
Ramalhinho AC, Fonseca-Moutinho JA, Breitenfeld L (2011) Glutathione S-transferase M1, T1, and P1 genotypes and breast cancer risk: a study in a Portuguese population. Mol Cell Biochem 355:265–271
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 (2007) Polymorphisms in genes involved in DNA repair and metabolism of xenobiotics in individual susceptibility to sporadic diffuse gastric cancer. Clin Chem Lab Med 45:822–828
Qin YH, Zhou TB, Su LN, Lei FY, Zhao YJ, Huang WF (2010) The efficacy of different dose intravenous immunoglobulin in treating acute idiopathic thrombocytopenic purpura: a meta-analysis of 13 randomized controlled trials. Blood Coagul Fibrinolysis 21:713–721
Zhou TB, Qin YH, Su LN, Lei FY, Huang WF, Zhao YJ (2011) ACE I/D gene polymorphism can’t predict the steroid responsiveness in Asian children with idiopathic nephrotic syndrome: a meta-analysis. PLoS One 6:19599
Zhou TB, Liu YG, Lin N, Qin YH, Huang K, Shao MB, Peng DD (2012) Relationship between angiotensin-converting enzyme insertion/deletion gene polymorphism and systemic Lupus erythematosus/lupus nephritis: a systematic review and metaanalysis. J Rheumatol 39:686–693
Zhang LF, Mi YY, Qin C, Wang Y, Cao Q, Wei JF, Zhou YJ, Feng NH, Zhang W (2011) RNASEL-1385G/A polymorphism and cancer risk: a meta-analysis based on 21 case-control studies. Mol Biol Rep 38:5099–5105
Zhou TB, Qin YH, Ou C, Su LN, Lei FY, Huang WF, Zhao YJ, Pang YS (2012) A meta-analysis of the association between angiotensin-converting enzyme insertion/deletion gene polymorphism and steroid-sensitive nephrotic syndrome in children. J Renin Angiotensin Aldosterone Syst 13:175–183
Zhou TB, Qin YH, Su LN, Lei FY, Huang WF, Zhao YJ, Pang YS, Yang KP (2011) The association between angiotensin-converting enzyme insertion/deletion gene variant and risk of focal segmental glomerulosclerosis: a systematic review and meta-analysis. J Renin Angiotensin Aldosterone Syst 12:624–633
Wang JJ, Zheng Y, Sun L, Wang L, Yu PB, Dong JH, Zhang L, Xu J, Shi W, Ren YC (2011) TP53 codon 72 polymorphism and colorectal cancer susceptibility: a meta-analysis. Mol Biol Rep 38:4847–4853
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101
Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
Ryberg D, Skaug V, Hewer A, Phillips DH, Harries LW, Wolf CR, Ogreid D, Ulvik A, Vu P, Haugen A (1997) Genotypes of glutathione transferase M1 and P1 and their significance for lung DNA adduct levels and cancer risk. Carcinogenesis 18:1285–1289
Harris MJ, Coggan M, Langton L, Wilson SR, Board PG (1998) Polymorphism of the Pi class glutathione S-transferase in normal populations and cancer patients. Pharmacogenetics 8:27–31
Jourenkova-Mironova N, Wikman H, Bouchardy C, Voho A, Dayer P, Benhamou S, Hirvonen A (1998) Role of glutathione S-transferase GSTM1, GSTM3, GSTP1 and GSTT1 genotypes in modulating susceptibility to smoking-related lung cancer. Pharmacogenetics 8:495–502
Saarikoski ST, Voho A, Reinikainen M, Anttila S, Karjalainen A, Malaveille C, Vainio H, Husgafvel-Pursiainen K, Hirvonen A (1998) Combined effect of polymorphic GST genes on individual susceptibility to lung cancer. Int J Cancer 77:516–521
Katoh T, Kaneko S, Takasawa S, Nagata N, Inatomi H, Ikemura K, Itoh H, Matsumoto T, Kawamoto T, Bell DA (1999) Human glutathione S-transferase P1 polymorphism and susceptibility to smoking related epithelial cancer; oral, lung, gastric, colorectal and urothelial cancer. Pharmacogenetics 9:165–169
Kihara M, Kihara M, Noda K (1999) Lung cancer risk of the GSTM1 null genotype is enhanced in the presence of the GSTP1 mutated genotype in male Japanese smokers. Cancer Lett 137:53–60
To-Figueras J, Gene M, Gomez-Catalan J, Pique E, Borrego N, Carrasco JL, Ramon J, Corbella J (1999) Genetic polymorphism of glutathione S-transferase P1 gene and lung cancer risk. Cancer Causes Control 10:65–70
Kiyohara C, Yamamura KI, Nakanishi Y, Takayama K, Hara N (2000) Polymorphism in GSTM1, GSTT1, and GSTP1 and susceptibility to lung cancer in a Japanese population. Asian Pac J Cancer Prev 1:293–298
Risch A, Wikman H, Thiel S, Schmezer P, Edler L, Drings P, Dienemann H, Kayser K, Schulz V, Spiegelhalder B, Bartsch H (2001) Glutathione-S-transferase M1, M3, T1 and P1 polymorphisms and susceptibility to non-small-cell lung cancer subtypes and hamartomas. Pharmacogenetics 11:757–764
Lewis SJ, Cherry NM, Niven RM, Barber PV, Povey AC (2002) GSTM1, GSTT1 and GSTP1 polymorphisms and lung cancer risk. Cancer Lett 180:165–171
Perera FP, Mooney LA, Stampfer M, Phillips DH, Bell DA, Rundle A, Cho S, Tsai WY, Ma J, Blackwood A, Tang D (2002) Associations between carcinogen-DNA damage, glutathione S-transferase genotypes, and risk of lung cancer in the prospective Physicians’ Health Cohort Study. Carcinogenesis 23:1641–1646
Stucker I, Hirvonen A, de Waziers I, Cabelguenne A, Mitrunen K, Cenee S, Koum-Besson E, Hemon D, Beaune P, Loriot MA (2002) Genetic polymorphisms of glutathione S-transferases as modulators of lung cancer susceptibility. Carcinogenesis 23:1475–1481
Lin P, Hsueh YM, Ko JL, Liang YF, Tsai KJ, Chen CY (2003) Analysis of NQO1, GSTP1, and MnSOD genetic polymorphisms on lung cancer risk in Taiwan. Lung Cancer J Iaslc 40:123–129
Nazar-Stewart V, Vaughan TL, Stapleton P, Van Loo J, Nicol-Blades B, Eaton DL (2003) A population-based study of glutathione S-transferase M1, T1 and P1 genotypes and risk for lung cancer. Lung Cancer J Iaslc 40:247–258
Reszka E, Wasowicz W, Rydzynski K, Szeszenia-Dabrowska N, Szymczak W (2003) Glutathione S-transferase M1 and P1 metabolic polymorphism and lung cancer predisposition. Neoplasma 50:357–362
Wang J, Deng Y, Cheng J, Ding J, Tokudome S (2003) GST genetic polymorphisms and lung adenocarcinoma susceptibility in a Chinese population. Cancer Lett 201:185–193
Wang Y, Spitz MR, Schabath MB, Ali-Osman F, Mata H, Wu X (2003) Association between glutathione S-transferase p1 polymorphisms and lung cancer risk in Caucasians: a case–control study. Lung Cancer-J Iaslc 40:25–32
Chan-Yeung M, Tan-Un KC, Ip MS, Tsang KW, Ho SP, Ho JC, Chan H, Lam WK (2004) Lung cancer susceptibility and polymorphisms of glutathione-S-transferase genes in Hong Kong. Lung Cancer J Iaslc 45:155–160
Schneider J, Bernges U, Philipp M, Woitowitz HJ (2004) GSTM1, GSTT1, and GSTP1 polymorphism and lung cancer risk in relation to tobacco smoking. Cancer Lett 208:65–74
Yang P, Bamlet WR, Ebbert JO, Taylor WR, de Andrade M (2004) Glutathione pathway genes and lung cancer risk in young and old populations. Carcinogenesis 25:1935–1944
Chan EC, Lam SY, Fu KH, Kwong YL (2005) Polymorphisms of the GSTM1, GSTP1, MPO, XRCC1, and NQO1 genes in Chinese patients with non-small cell lung cancers: relationship with aberrant promoter methylation of the CDKN2A and RARB genes. Cancer Genet Cytogenet 162:10–20
Cote ML, Kardia SL, Wenzlaff AS, Land SJ, Schwartz AG (2005) Combinations of glutathione S-transferase genotypes and risk of early-onset lung cancer in Caucasians and African Americans: a population-based study. Carcinogenesis 26:811–819
Liang G, Pu Y, Yin L (2005) Rapid detection of single nucleotide polymorphisms related with lung cancer susceptibility of Chinese population. Cancer Lett 223:265–274
Wenzlaff AS, Cote ML, Bock CH, Land SJ, Schwartz AG (2005) GSTM1, GSTT1 and GSTP1 polymorphisms, environmental tobacco smoke exposure and risk of lung cancer among never smokers: a population-based study. Carcinogenesis 26:395–401
Chen HC, Cao YF, Hu WX, Liu XF, Liu QX, Zhang J, Liu J (2006) Genetic polymorphisms of phase II metabolic enzymes and lung cancer susceptibility in a population of Central South China. Dis Markers 22:141–152
Larsen JE, Colosimo ML, Yang IA, Bowman R, Zimmerman PV, Fong KM (2006) CYP1A1 Ile462Val and MPO G-463A interact to increase risk of adenocarcinoma but not squamous cell carcinoma of the lung. Carcinogenesis 27:525–532
Miller DP, Asomaning K, Liu G, Wain JC, Lynch TJ, Neuberg D, Su L, Christiani DC (2006) An association between glutathione S-transferase P1 gene polymorphism and younger age at onset of lung carcinoma. Cancer 107:1570–1577
Loft S, Svoboda P, Kasai H, Tjonneland A, Moller P, Sorensen M, Overvad K, Autrup H, Raaschou-Nielsen O (2007) Prospective study of urinary excretion of 7-methylguanine and the risk of lung cancer: effect modification by mu class glutathione-S-transferases. Int J Cancer 121:1579–1584
Reszka E, Wasowicz W, Gromadzinska J (2007) Antioxidant defense markers modulated by glutathione S-transferase genetic polymorphism: results of lung cancer case–control study. Genes Nutr 2:287–294
Sorensen M, Raaschou-Nielsen O, Brasch-Andersen C, Tjonneland A, Overvad K, Autrup H (2007) Interactions between GSTM1, GSTT1 and GSTP1 polymorphisms and smoking and intake of fruit and vegetables in relation to lung cancer. Lung Cancer J Iaslc 55:137–144
Sreeja L, Syamala V, Hariharan S, Syamala VS, Raveendran PB, Sivanandan CD, Madhavan J, Ankathil R (2008) Glutathione S-transferase M1, T1 and P1 polymorphisms: susceptibility and outcome in lung cancer patients. J Exp Ther Oncol 7:73–85
Yang M, Choi Y, Hwangbo B, Lee JS (2007) Combined effects of genetic polymorphisms in six selected genes on lung cancer susceptibility. Lung Cancer J Iaslc 57:135–142
Yoon KA, Kim JH, Gil HJ, Hwang H, Hwangbo B, Lee JS (2008) CYP1B1, CYP1A1, MPO, and GSTP1 polymorphisms and lung cancer risk in never-smoking Korean women. Lung Cancer J Iaslc 60:40–46
Honma HN, De Capitani EM, Jr Perroud MW, Barbeiro AS, Toro IF, Costa DB, Lima CS, Zambon L (2008) Influence of p53 codon 72 exon 4, GSTM1, GSTT1 and GSTP1*B polymorphisms in lung cancer risk in a Brazilian population. Lung Cancer J Iaslc 61:152–162
Sobti RC, Kaur P, Kaur S, Janmeja AK, Jindal SK, Kishan J, Raimondi S (2008) Combined effect of GSTM1, GSTT1 and GSTP1 polymorphisms on histological subtypes of lung cancer. Biomarkers 13:282–295
Zienolddiny S, Campa D, Lind H, Ryberg D, Skaug V, Stangeland LB, Canzian F, Haugen A (2008) A comprehensive analysis of phase I and phase II metabolism gene polymorphisms and risk of non-small cell lung cancer in smokers. Carcinogenesis 29:1164–1169
Kumar M, Agarwal SK, Goel SK (2009) Lung cancer risk in north Indian population: role of genetic polymorphisms and smoking. Mol Cell Biochem 322:73–79
Gervasini G, San JC, Carrillo JA, Benitez J, Cabanillas A (2010) GST polymorphisms interact with dietary factors to modulate lung cancer risk: study in a high-incidence area. Nutr Cancer 62:750–758
Lam TK, Rotunno M, Lubin JH, Wacholder S, Consonni D, Pesatori AC, Bertazzi PA, Chanock SJ, Burdette L, Goldstein AM, Tucker MA, Caporaso NE, Subar AF, Landi MT (2010) Dietary quercetin, quercetin-gene interaction, metabolic gene expression in lung tissue and lung cancer risk. Carcinogenesis 31:634–642
Timofeeva M, Kropp S, Sauter W, Beckmann L, Rosenberger A, Illig T, Jager B, Mittelstrass K, Dienemann H, Bartsch H, Bickeboller H, Chang-Claude J, Risch A, Wichmann HE (2010) Genetic polymorphisms of MPO, GSTT1, GSTM1, GSTP1, EPHX1 and NQO1 as risk factors of early-onset lung cancer. Int J Cancer 127:1547–1561
Vural B, Yakar F, Derin D, Saip P, Yakar A, Demirkan A, Karabulut A, Ugurel E, Cine N, Kilicaslan Z, Tuzun E, Ozbek U (2012) Evaluation of glutathione S-transferase P1 polymorphisms (Ile105Val and Ala114Val) in patients with small cell lung cancer. Genet Test Mol Biomarkers 16:701–706
Ada AO, Kunak SC, Hancer F, Soydas E, Alpar S, Gulhan M, Iscan M (2012) Association between GSTM1, GSTT1, and GSTP1 polymorphisms and lung cancer risk in a Turkish population. Mol Biol Rep 39:5985–5993
Kiyohara C, Horiuchi T, Takayama K, Nakanishi Y (2012) Genetic polymorphisms involved in carcinogen metabolism and DNA repair and lung cancer risk in a Japanese population. J Thorac Oncol 7:954–962
Pliarchopoulou K, Voutsinas G, Papaxoinis G, Florou K, Skondra M, Kostaki K, Roussou P, Syrigos K, Pectasides D (2012) Correlation of CYP1A1, GSTP1 and GSTM1 gene polymorphisms and lung cancer risk among smokers. Oncol Lett 3:1301–1306
Dai L, Duan F, Wang P, Song C, Wang K, Zhang J (2012) XRCC1 gene polymorphisms and lung cancer susceptibility: a meta-analysis of 44 case–control studies. Mol Biol Rep 39:9535–9547
Ji YN, Wang Q, Lin XQ, Suo LJ (2012) CYP1A1 MspI polymorphisms and lung cancer risk: an updated meta-analysis involving 20,209 subjects. Cytokine 59:324–334
Guan P, Huang D, Yin Z, Zhou B (2011) Association of the hOGG1 Ser326Cys polymorphism with increased lung cancer susceptibility in Asians: a meta-analysis of 18 studies including 7592 cases and 8129 controls. Asian Pac J Cancer Prev 12:1067–1072
Liu F, He Y, Peng X, Wang W, Yang X (2010) Association of the 8473T>C cyclooxygenase-2 (COX-2) gene polymorphism with lung cancer risk in Asians. Asian Pac J Cancer Prev 11:1257–1262
Gong M, Dong W, An R (2012) Glutathione S-transferase T1 polymorphism contributes to bladder cancer risk: a meta-analysis involving 50 studies. DNA Cell Biol 31:1187–1197
Cote ML, Chen W, Smith DW, Benhamou S, Bouchardy C, Butkiewicz D, Fong KM, Gene M, Hirvonen A, Kiyohara C, Larsen JE, Lin P, Raaschou-Nielsen O, Povey AC, Reszka E, Risch A, Schneider J, Schwartz AG, Sorensen M, To-Figueras J, Tokudome S, Pu Y, Yang P, Wenzlaff AS, Wikman H, Taioli E (2009) Meta- and pooled analysis of GSTP1 polymorphism and lung cancer: a HuGE-GSEC review. Am J Epidemiol 169:802–814
Bin Q, Luo J (2012) The role of polymorphisms of the GSTM1, GSTT1 and GSTP1 Ile105Val in Hodgkin’s and non-Hodgkin’s lymphoma risk: a HUGE review. Leuk Lymphoma. doi:10.3109/10428194.2012.706284
Yao L, Ji G, Gu A, Zhao P, Liu N (2012) An updated pooled analysis of glutathione S-transferase genotype polymorphisms and risk of adult gliomas. Asian Pac J Cancer Prev 13:157–163
Zhao ZQ, Guan QK, Yang FY, Zhao P, Zhou B, Chen ZJ (2012) System review and metaanalysis of the relationships between five metabolic gene polymorphisms and colorectal adenoma risk. Tumour Biol 33:523–535
Conflict of interest
The authors declare no competing interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Xu Feng and Jun-Jie Shi are joint First Authors.
Rights and permissions
About this article
Cite this article
Feng, X., Zheng, BS., Shi, JJ. et al. Association of glutathione S-transferase P1 gene polymorphism with the susceptibility of lung cancer. Mol Biol Rep 39, 10313–10323 (2012). https://doi.org/10.1007/s11033-012-1908-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-1908-1