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Meta-analysis of genetic polymorphisms in xenobiotic metabolizing enzymes and their association with breast cancer risk

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Abstract

Studies on the association of cytochrome p450 A1 (m1, m2), catechol-O-methyltransferase (COMT) H108L, glutathione S-transferase (GST) T1 and M1 polymorphisms with breast cancer risk were inconclusive. The current study was aimed to clarify the ambiguity in genetic associations of these enzymes with breast cancer risk on a global perspective. A systematic literature search was carried out in PubMed, Google Scholar and Medline, covering all the case–control studies published until September 2017. A meta-analysis was performed based on the random-effect and fixed-effect models to calculate the overall association of each genetic variant with breast cancer risk. Of the five polymorphisms studied, GSTT1 (OR: 1.07, 95% CI: 1.02–1.12 and OR: 1.08, 95% CI: 1.01–1.15 for fixed-effect and random-effect models, respectively) and GSTM1 (OR: 1.22, 95% CI: 1.17–1.26 and OR: 1.25, 95% CI: 1.12–1.35 for fixed-effect and random-effect models, respectively) null polymorphisms exhibited an increased risk for breast cancer in both the models. Cochrane Q-test and \(I^{2}\) statistics revealed heterogeneity in association with these polymorphisms (\(P < 0.0001\)) with no evidence of publication bias. Thus, GSTT1 and GSTM1 null polymorphisms are risk factors for breast cancer.

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References

  • Ahsan H., Chen Y., Whittemore A. S., Kibriya M. G., Gurvich I., Senie R. T. and Santella R. M. 2004 A family-based genetic association study of variants in estrogen-metabolism genes COMT and CYP1B1 and breast cancer risk. Breast Cancer Res. Treat. 85, 121–131.

    Article  PubMed  CAS  Google Scholar 

  • Ambrosone C. B., Freudenheim J. L., Graham S., Marshall J. R., Vena J. E., Brasure J. R., et al. 1995 Cytochrome P4501A1 and glutathione S-transferase (M1) genetic polymorphisms and postmenopausal breast cancer risk. Cancer Res. 55, 3483–3485.

    PubMed  CAS  Google Scholar 

  • Amrani I., Bulatova N., Awidi A., Yousef A. M., Melhem J. M., Al-Masri M. and Tahoun L. A. 2016 Lack of association between CYP1A1 M2 and M4 polymorphisms and breast carcinoma in Jordanian women: a case-control study. Asian Pac. J. Cancer Prev. 17, 387–393.

    Article  PubMed  Google Scholar 

  • Bailey L. R., Roodi N., Verrier C. S., Yee C. J., Dupont W. D. and Parl F. F. 1998 Breast cancer and CYP1A1, GSTM1, and GSTT1 polymorphisms: evidence of a lack of associations in Caucasians and African Americans. Cancer Res. 58, 65–70.

    PubMed  CAS  Google Scholar 

  • Basham V. M., Pharoah P. D., Healey C. S., Luben R. N., Day N. E., Easton D. F. et al. 2001 Polymorphisms in CYP1A1 and smoking: no association with breast cancer risk. Carcinogenesis 22, 1797–1800.

    Article  PubMed  CAS  Google Scholar 

  • Boyapati S. M., Shu X. O., Gao Y. T., Cai Q., ** F. and Zheng W. 2005 Polymorphisms in CYP1A1 and breast carcinoma risk in a population-based case-control study of Chinese women. Cancer 103, 2228–2235.

    Article  PubMed  CAS  Google Scholar 

  • Cavalieri E. L. and Rogan E. G. 2010 Depurinating estrogen-DNA adducts in the etiology and prevention of breast and other human cancers. Future Oncol. 6, 75–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cerne J. Z., Pohar-Perme M., Novakovic S., Frkovic-Grazio S., Stegel V. and Gersak K. 2011 Combined effect of CYP1B1, COMT, GSTP1, and MnSOD genotypes and risk of postmenopausal breast cancer. J. Gynecol. Oncol. 22, 110–119.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chacko P., Joseph T., Mathew B. S., Rajan B. and Pillai M. R. 2005 Role of xenobiotic metabolizing gene polymorphisms in breast cancer susceptibility and treatment outcome. Mutat. Res. 581, 153–163.

    Article  PubMed  CAS  Google Scholar 

  • Chang T. W., Wang S. M., Guo Y. L., Tsai P. C., Huang C. J. and Huang W. 2006 Glutathione S-transferase polymorphisms associated with risk of breast cancer in southern Taiwan. Breast 15, 754–761.

    Article  PubMed  Google Scholar 

  • Chang Y. L,, Li J., Yao S. Q., Hu W. N., Jiang S. F., Guo Z. et al. 2008 A case-control study on serum organochlorines residues, genetic polymorphisms of glutathione S-transferase T1 and the risks of breast cancer. Zhonghua Liu **ng Bing Xue Za Zhi. 29, 763–766.

    PubMed  CAS  Google Scholar 

  • Chen C., Huang Y., Li Y., Mao Y. and **e Y. 2007 Cytochrome P450 1A1 (CYP1A1) T3801C and A2455G polymorphisms in breast cancer risk: a meta-analysis. J. Hum. Gen. 52, 423–435.

    Article  CAS  Google Scholar 

  • Cheng T. C., Chen S. T., Huang C. S., Fu Y. P., Yu J. C., Cheng C. W. et al. 2005 Breast cancer risk associated with genotype polymorphism of the catechol estrogen-metabolizing genes: a multigenic study on cancer susceptibility. Int. J. Cancer 113, 345–353.

    Article  PubMed  CAS  Google Scholar 

  • Cochran W. G. 1955 Research techniques in the study of human beings. Milbank Mem. Fund Q. 33, 121–136.

    Article  PubMed  CAS  Google Scholar 

  • Comings D. E., Gade-Andavolu R., Cone L. A., Muhleman D. and MacMurray J. P. 2003 A multigene test for the risk of sporadic breast carcinoma. Cancer 97, 2160–2170.

    Article  PubMed  CAS  Google Scholar 

  • Cribb A. E., Joy Knight M., Guernsey J., Dryer D., Hender K., Shawwa A. et al. 2011 CYP17, catechol-o-methyltransferase, and glutathione transferase M1 genetic polymorphisms, lifestyle factors, and breast cancer risk in women on Prince Edward Island. Breast J. 17, 24–31.

    Article  PubMed  Google Scholar 

  • Curran J. E., Weinstein S. R. and Griffiths L. R. 2000 Polymorphisms of glutathione S-transferase genes (GSTM1, GSTP1 and GSTT1) and breast cancer susceptibility. Cancer Lett. 153, 113–120.

    Article  PubMed  CAS  Google Scholar 

  • Delort L., Satih S., Kwiatkowski F., Bignon Y. J. and Bernard-Gallon D. J. 2010 Evaluation of breast cancer risk in a multigenic model including low penetrance genes involved in xenobiotic and estrogen metabolisms. Nutr. Cancer 62, 243–251.

    Article  PubMed  CAS  Google Scholar 

  • Dorszewska J., Prendecki M., Oczkowska A., Rozycka A., Lianeri M. and Kozubski W. 2013 Polymorphism of the COMT, MAO, DAT, NET and 5-HTT Genes, and biogenic amines in Parkinson’s disease. Curr. Genomics 14, 518–533.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Egan K. M., Cai Q., Shu X. O., ** F., Zhu T. L., Dai Q. et al. 2004 Genetic polymorphisms in GSTM1, GSTP1, and GSTT1 and the risk for breast cancer: results from the Shanghai breast cancer study and meta-analysis. Cancer Epidemiol. Biomarkers Prev. 13, 197–204.

    Article  PubMed  CAS  Google Scholar 

  • Fontana X., Peyrottes I., Rossi C., Leblanc-Talent P., Ettore F., Namer M. and Bussière F. 1998 Study of the frequencies of CYP1A1 gene polymorphisms and glutathione S-transferase mu1 gene in primary breast cancers: an update with an additional 114 cases. Mutat. Res. 403, 45–53.

    Article  PubMed  CAS  Google Scholar 

  • Fowke J. H., Chung F. L., ** F., Qi D., Cai Q., Conaway C. et al. 2003 Urinary isothiocyanate levels, brassica, and human breast cancer. Cancer Res. 63, 3980–3986.

    PubMed  CAS  Google Scholar 

  • Gago-Dominguez M., Castelao J. E., Sun C. L., Van Den Berg D., Koh W. P., Lee H. P. and Yu M. C. 2004 Marine n-3 fatty acid intake, glutathione S-transferase polymorphisms and breast cancer risk in post-menopausal Chinese women in Singapore. Carcinogenesis 25, 2143–2147.

    Article  PubMed  CAS  Google Scholar 

  • Gallicchio L., Berndt S. I., McSorley M. A., Newschaffer C. J., Thuita L. W., Argani P. et al. 2006 Polymorphisms in estrogen-metabolizing and estrogen receptor genes and the risk of develo** breast cancer among a cohort of women with benign breast disease. BMC Cancer 6, 173.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Closas M., Kelsey K. T., Hankinson S. E., Spiegelman D., Springer K., Willett W. C. et al. 1999 Glutathione S-transferase mu and theta polymorphisms and breast cancer susceptibility. J. Natl. Cancer Inst. 91, 1960–1964.

    Article  PubMed  Google Scholar 

  • Gaudet M. M., Chanock S., Lissowska J., Berndt S. I., Peplonska B., Brinton L. A. et al. 2006 Comprehensive assessment of genetic variation of catechol-o-methyltransferase and breast cancer risk. Cancer Res. 66, 9781–9785.

    Article  PubMed  CAS  Google Scholar 

  • Ghisari M., Long M. and Bonefeld-Jørgensen E. C. 2013 Genetic polymorphisms in CYP1A1, CYP1B1 and COMT genes in Greenlandic inuit and Europeans. Int. J. Circumpolar Health 72, 21113.

    Article  PubMed  Google Scholar 

  • Goodman J. E., Lavigne J. A., Hengstler J. G., Tanner B., Helzlsouer K. J. and Yager J. D. 2000 Catechol-O-methyltransferase polymorphism is not associated with ovarian cancer risk. Cancer Epidemiol. Biomarkers Prev. 9, 1373–1376.

    PubMed  CAS  Google Scholar 

  • Goodman J. E., Lavigne J. A., Wu K., Helzlsouer K. J., Strickland P. T., Selhub J. and Yager J. D. 2001 COMT genotype, micronutrients in the folate metabolic pathway and breast cancer risk. Carcinogenesis 22, 1661–1665.

    Article  PubMed  CAS  Google Scholar 

  • Hamajima N., Matsuo K., Tajima K., Mizutani M., Iwata H., Iwase T. et al. 2001 Limited association between a catechol-o-methyltransferase (COMT) polymorphism and breast cancer risk in Japan. Int. J. Clin. Oncol. 6, 13–18.

    Article  PubMed  CAS  Google Scholar 

  • Hashemi M., Eskandari-Nasab E., Fazaeli A., Taheri M., Rezaei H., Mashhadi M. et al. 2012 Association between polymorphisms of glutathione S-transferase genes (GSTM1, GSTP1 and GSTT1) and breast cancer risk in a sample Iranian population. Biomark Med. 6, 797–803.

    Article  PubMed  CAS  Google Scholar 

  • He C., Tamimi R. M., Hankinson S. E., Hunter D. J. and Han J. 2009 A prospective study of genetic polymorphism in MPO, antioxidant status, and breast cancer risk. Breast Cancer Res. Treat. 113, 585–594.

    Article  PubMed  CAS  Google Scholar 

  • Hefler L. A., Tempfer C. B., Grimm C., Lebrecht A., Ulbrich E., Heinze G. et al. 2004 Estrogen-metabolizing gene polymorphisms in the assessment of breast carcinoma risk and fibroadenoma risk in Caucasian women. Cancer 101, 264–269.

    Article  PubMed  CAS  Google Scholar 

  • Henmi M. and Copas J. B. 2010 Confidence intervals for random effects meta-analysis and robustness to publication bias. Stat. Med. 29, 2969–1983.

    Article  PubMed  Google Scholar 

  • Hu Z., Song C. G., Lu J. S., Luo J. M., Shen Z. Z., Huang W. and Shao Z. M. 2007 A multigenic study on breast cancer risk associated with genetic polymorphisms of ER Alpha, COMT and CYP19 gene in BRCA1/BRCA2 negative Shanghai women with early onset breast cancer or affected relatives. J. Cancer Res. Clin. Oncol. 133, 969–978.

    Article  PubMed  CAS  Google Scholar 

  • Huang C. S., Shen C. Y., Chang K. J., Hsu S. M. and Chern H. D. 1999 Cytochrome P4501A1 polymorphism as a susceptibility factor for breast cancer in postmenopausal Chinese women in Taiwan. Br. J. Cancer. 80, 1838–1843.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jakubowska A., Gronwald J., Menkiszak J., Górski B., Huzarski T., Byrski T. et al. 2010 BRCA1-associated breast and ovarian cancer risks in Poland: no association with commonly studied polymorphisms. Breast Cancer Res Treat. 119, 201–211.

    Article  PubMed  Google Scholar 

  • Kadouri L., Kote-Jarai Z., Hubert A., Baras M., Abeliovich D., Hamburger T. et al. 2008 Glutathione-S-transferase M1, T1 and P1 polymorphisms, and breast cancer risk, in BRCA1/2 mutation carriers. Br. J. Cancer. 98, 2006–2010.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kakkoura M. G., Demetriou, C. A., Loizidou M. A., Loucaides G., Neophytou I., Marcou Y. et al. 2015 Single-nucleotide polymorphisms in one-carbon metabolism genes, Mediterranean diet and breast cancer risk: a case-control study in the Greek-Cypriot female population. Genes Nutr. 10(2), 453.

    Article  PubMed  CAS  Google Scholar 

  • Kakkoura M. G., Sokratous K., Demetriou C. A., Loizidou M. A., Loucaides G., Kakouri E. et al. 2017a Mediterranean diet-gene interactions: a targeted metabolomics study in Greek-Cypriot women. Mol. Nutr. Food Res. 61.

  • Kakkoura M. G., Loizidou M. A., Demetriou C. A., Loucaides G., Daniel M., Kyriacou K. and Hadjisavvas A. 2017b The synergistic effect between the Mediterranean diet and GSTP1 or NAT2 SNPs decreases breast cancer risk in Greek-Cypriot women. Eur. J. Nutr. 56, 545–555.

  • Kang D. 2003 Genetic polymorphisms and cancer susceptibility of breast cancer in Korean women. J. Biochem. Mol. Biol. 36, 28–34.

    PubMed  CAS  Google Scholar 

  • Kaushal M., Mishra A. K., Raju B. S., Ihsan R., Chakraborty A., Sharma J. et al. 2010 Betel quid chewing as an environmental risk factor for breast cancer. Mutat. Res. 703, 143–148.

    Article  PubMed  CAS  Google Scholar 

  • Kelsey K. T., Hankinson S. E., Colditz G. A., Springer K., Garcia-Closas M., Spiegelman D. et al. 1997 Glutathione S-transferase class mu deletion polymorphism and breast cancer: results from prevalent versus incident cases. Cancer Epidemiol. Biomarkers Prev. 6, 511–515.

    PubMed  CAS  Google Scholar 

  • Khedhaier A., Remadi S., Corbex M., Ahmed S. B., Bouaouina N., Mestiri S. et al. 2003 Glutathione S-transferases (GSTT1 and GSTM1) gene deletions in Tunisians: susceptibility and prognostic implications in breast carcinoma. Br. J. Cancer. 89, 1502–1507.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kimi L., Ghatak S., Yadav R. P., Chhuani L., Lallawmzuali D., Pautu J. L. and Kumar N. S. 2016 Relevance of GSTM1, GSTT1 and GSTP1 Gene Polymorphism to Breast Cancer Susceptibility in Mizoram Population, Northeast India. Biochem. Genet. 54, 41–49.

    Article  PubMed  CAS  Google Scholar 

  • Kiruthiga P. V., Kannan M. R., Saraswathi C., Pandian S. K. and Devi K. P. 2011 CYP1A1 gene polymorphisms: lack of association with breast cancer susceptibility in the southern region (Madurai) of India. Asian Pac. J. Cancer Prev. 12, 2133–2138.

    PubMed  CAS  Google Scholar 

  • Kocabaş N. A., Sardaş S., Cholerton S., Daly A. K. and Karakaya A. E. 2002 Cytochrome P450 CYP1B1 and catechol O-methyltransferase (COMT) genetic polymorphisms and breast cancer susceptibility in a Turkish population. Arch. Toxicol. 76, 643–649.

    Article  PubMed  CAS  Google Scholar 

  • Kra**ovic M., Ghadirian P., Richer C., Sinnett H., Gandini S., Perret C. et al. 2001 Genetic susceptibility to breast cancer in French-Canadians: role of carcinogen-metabolizing enzymes and gene-environment interactions. Int. J. Cancer. 92, 220–225.

    Article  PubMed  CAS  Google Scholar 

  • Kuptsova N., Chang-Claude J., Kropp S., Helmbold I., Schmezer P., von Fournier D. et al. 2008 Genetic predictors of long-term toxicities after radiation therapy for breast cancer. Int. J. Cancer. 122, 1333–1339.

    Article  PubMed  CAS  Google Scholar 

  • Lavigne J. A., Helzlsouer K. J., Huang H. Y., Strickland P. T., Bell D. A., Selmin O. et al. 1997 An association between the allele coding for a low activity variant of catechol-o-methyltransferase and the risk for breast cancer. Cancer Res. 57, 5493–5497.

    PubMed  CAS  Google Scholar 

  • Le Marchand L., Donlon T., Kolonel L. N., Henderson B. E. and Wilkens L. R. 2005 Estrogen metabolism-related genes and breast cancer risk: the multiethnic cohort study. Cancer Epidemiol. Biomarkers Prev. 14, 1998–2003.

    Article  PubMed  CAS  Google Scholar 

  • Lee K. M., Park S. K., Kim S. U., Doll M. A., Yoo K. Y., Ahn S. H. et al. 2003 N-acetyltransferase (NAT1, NAT2) and glutathione S-transferase (GSTM1, GSTT1) polymorphisms in breast cancer. Cancer Lett. 196, 179–186.

    Article  PubMed  CAS  Google Scholar 

  • Li Y., Millikan R. C., Bell D. A., Cui L., Tse C. K., Newman B. and Conway K. 2004 Cigarette smoking, cytochrome P4501A1 polymorphisms and breast cancer among African-American and white women. Breast Cancer Res. 6, 460–473.

    Article  CAS  Google Scholar 

  • Li J. Y., Long Q. M., Tao P., Hu R., Li H., Lei F. M. et al. 2008 Using MSR model to analyze the impact of gene-gene interaction with related to the genetic polymorphism of metabolism enzymes on the risk of breast cancer. Sichuan Da Xue Xue Bao Yi Xue Ban. 39, 780–783. Chinese.

  • Li K., Li W. and Zou H. 2014 Catechol-O-methyltransferase Val158Met polymorphism and breast cancer risk in Asian population. Tumor Biol. 35, 2343–2350.

    Article  CAS  Google Scholar 

  • Lin W. Y., Chou Y. C., Wu M. H., Jeng Y. L., Huang H. B., You S. L. et al. 2005 Polymorphic catechol-O-methyltransferase gene, duration of estrogen exposure, and breast cancer risk: a nested case-control study in Taiwan. Cancer Detect. Prev. 29, 427–432.

    Article  PubMed  CAS  Google Scholar 

  • Luo J., Gao Y. T., Chow W. H., Shu X. O., Li H., Yang G. et al. 2012 Urinary polyphenols, glutathione s-transferases copy number variation, and breast cancer risk: results from the Shanghai Women’s Health Study. Mol. Carcinog. 51, 379–388.

    Article  PubMed  CAS  Google Scholar 

  • Manzanares M. Á., Solanas M., Moral R., Escrich R., Vela E., Costa I. and Escrich E. 2015 Dietary extra-virgin olive oil and corn oil differentially modulate the mRNA expression of xenobiotic-metabolizing enzymes in the liver and in the mammary gland in a rat chemically induced breast cancer model. Eur. J. Cancer Prev. 24, 215–222.

    Article  PubMed  CAS  Google Scholar 

  • Marie-Genica Consortium on Genetic Susceptibility for Menopausal Hormone Therapy Related Breast Cancer Risk 2010 Genetic polymorphisms in phase I and phase II enzymes and breast cancer risk associated with menopausal hormone therapy in postmenopausal women. Breast Cancer Res Treat. 119, 463–474.

  • Martínez-Ramírez O. C., Pérez-Morales R., Castro C., Flores-Díaz A., Soto-Cruz K. E., Astorga-Ramos A. et al. 2013 Polymorphisms of catechol estrogens metabolism pathway genes and breast cancer risk in Mexican women. Breast 2, 335–343.

    Article  Google Scholar 

  • Masoudi M., Saadat I., Omidvari S. and Saadat M. 2010 Additive effects of genetic variations of xenobiotic detoxification enzymes and DNA repair gene XRCC1 on the susceptibility to breast cancer. Breast Cancer Res. Treat. 120, 263–265.

    Article  PubMed  Google Scholar 

  • Matsui A., Ikeda T., Enomoto K., Hosoda K., Nakashima H., Omae K. et al. 2000 Increased formation of oxidative DNA damage, 8-hydroxy-2’-deoxyguanosine, in human breast cancer tissue and its relationship to GSTP1 and COMT genotypes. Cancer Lett. 151, 87–95.

    Article  PubMed  CAS  Google Scholar 

  • Mavaddat N., Antoniou A. C., Easton D. F. and Garcia-Closas M. 2010 Genetic susceptibility to breast cancer. Mol. Oncol. 4, 174–191.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCarty K. M., Santella R. M., Steck S. E., Cleveland R. J., Ahn J., Ambrosone C. B. et al. 2009 PAH-DNA adducts, cigarette smoking, GST polymorphisms, and breast cancer risk. Environ. Health Perspect. 117, 552–558.

    Article  PubMed  CAS  Google Scholar 

  • McPherson K., Steel C. M. and Dixon J. M. 2000 Breast cancer—epidemiology, risk factors, and genetics. BMJ 321, 624–628.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Millikan R. C., Pittman G. S., Tse C. K., Duell E., Newman B., Savitz D. et al. 1998 Catechol-O-methyltransferase and breast cancer risk. Carcinogenesis 19, 1943–1947.

    Article  PubMed  CAS  Google Scholar 

  • Millikan R., Pittman G., Tse C. K., Savitz D. A., Newman B. and Bell D. 2000 Glutathione S-transferases M1, T1, and P1 and breast cancer. Cancer Epidemiol. Biomarkers Prev. 9, 567–573.

    PubMed  CAS  Google Scholar 

  • Mitrunen K., Jourenkova N., Kataja V., Eskelinen M., Kosma V. M., Benhamou S. et al. 2001 Polymorphic catechol-o-methyltransferase gene and breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 10, 635–640.

    PubMed  CAS  Google Scholar 

  • Miyoshi Y., Takahashi Y., Egawa C. and Noguchi S. 2002 Breast cancer risk associated with CYP1A1 genetic polymorphisms in Japanese women. Breast J. 8, 209–215.

    Article  PubMed  CAS  Google Scholar 

  • Modugno F., Zmuda J. M., Potter D., Cai C., Ziv E., Cummings S. R. et al. 2005 Estrogen metabolizing polymorphisms and breast cancer risk among older white women. Breast Cancer Res. Treat. 93, 261–270.

    Article  PubMed  CAS  Google Scholar 

  • Naushad S. M., Reddy C. A., Rupasree Y., Pavani A., Digumarti R. R., Gottumukkala S. R. et al. 2011 Cross-talk between one-carbon metabolism and xenobiotic metabolism: implications on oxidative DNA damage and susceptibility to breast cancer. Cell Biochem. Biophys. 61, 715–723.

    Article  PubMed  CAS  Google Scholar 

  • Naushad S. M., Ramaiah M. J., Pavithrakumari M., Jayapriya J., Hussain T., Alrokayan S. A. et al. 2016 Artificial neural network-based exploration of gene-nutrient interactions in folate and xenobiotic metabolic pathways that modulate susceptibility to breast cancer. Gene 580, 159–168.

    Article  PubMed  CAS  Google Scholar 

  • Nosheen M., Malik F. A. and Kayani M. A. 2011 Lack of influence of glutathione S-transferase gene deletions in sporadic breast cancer in Pakistan. Asian Pac. J. Cancer Prev. 12, 1749–1752.

    PubMed  Google Scholar 

  • Okobia M., Bunker C., Zmuda J., Kammerer C., Vogel V., Uche E. et al. 2005 Cytochrome P4501A1 genetic polymorphisms and breast cancer risk in Nigerian women. Breast Cancer Res. Treat. 94, 285–293.

    Article  PubMed  CAS  Google Scholar 

  • Oliveira A. L., Rodrigues F. F., Santos R. E., Aoki T., Rocha M. N., Longui C. A. and Melo M. B. 2010 GSTT1, GSTM1, and GSTP1 polymorphisms and chemotherapy response in locally advanced breast cancer. Genet. Mol. Res. 9, 1045–1053.

    Article  PubMed  CAS  Google Scholar 

  • Onay V. U., Briollais L., Knight J. A., Shi E., Wang Y., Wells S. et al. 2006 SNP-SNP interactions in breast cancer susceptibility. BMC Cancer. 6, 114.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Onay U. V., Aaltonen K., Briollais L., Knight J. A., Pabalan N., Kilpivaara O. et al. 2008 Combined effect of CCND1 and COMT polymorphisms and increased breast cancer risk. BMC Cancer 8, 1–10.

    Article  CAS  Google Scholar 

  • Pabalan N., Singh N., Singian E., Barbosa C. P., Bianco B. and Jarjanazi H. 2015 Associations of CYP1A1 gene polymorphisms and risk of breast cancer in Indian women: a meta-analysis. AIMS Genet. 2, 250–262.

    Article  Google Scholar 

  • Parada H. Jr., Steck S. E., Cleveland R. J., Teitelbaum S. L., Neugut A. I., Santella R. M., and Gammon M. D. 2017 Genetic polymorphisms of phase I metabolizing enzyme genes, their interaction with lifetime grilled and smoked meat intake, and breast cancer incidence. Ann. Epidemiol. 27, 208–214.

    Article  PubMed  Google Scholar 

  • Park S. K., Yim D. S., Yoon K. S., Choi I. M., Choi J. Y., Yoo K. Y. et al. 2004 Combined effect of GSTM1, GSTT1, and COMT genotypes in individual breast cancer risk. Breast Cancer Res. Treat. 88, 55–62.

    Article  PubMed  CAS  Google Scholar 

  • Peterson N. B., Trentham-Dietz A., Garcia-Closas M., Newcomb P. A., Titus-Ernstoff L., Huang Y. et al. 2010 Association of COMT haplotypes and breast cancer risk in caucasian women. Anticancer Res. 30, 217–220.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Petrakis N. L. 1977 Genetic factors in the etiology of breast cancer. Cancer 39, 2709–2715.

    Article  PubMed  CAS  Google Scholar 

  • Pongtheerat T., Treetrisool M. and Purisa W. 2009 Glutathione s-transferase polymorphisms in breast cancers of Thai patients. Asian Pac. J. Cancer Prev. 10, 127–132.

    PubMed  Google Scholar 

  • Possuelo L. G., Peraça C. F., Eisenhardt M. F., Dotto M. L., Cappelletti L., Foletto E. and Valim A. R. 2013 Polymorphisms of GSTM1 and GSTT1 genes in breast cancer susceptibility: a case-control study. Rev. Bras. Ginecol. Obstet. 35, 569–574.

    Article  PubMed  Google Scholar 

  • Qiu L. X., Yuan H., Yu K. D., Mao C., Chen B., Zhan P. et al. 2010 Glutathione S-transferase M1 polymorphism and breast cancer susceptibility: a meta-analysis involving 46,281 subjects. Breast Cancer Res. Treat. 121, 703–708.

    Article  PubMed  CAS  Google Scholar 

  • Qin X., Peng Q., Qin A., Chen Z., Lin L., Deng Y. et al. 2012 Association of COMT Val158Met polymorphism and breast cancer risk: an updated meta-analysis. Diagn Pathol. 7, 136.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qin J., Zhang J. X., Li X. P., Wu B. Q., Chen G. B. and He X. F. 2014 Association between the CYP1A1 A2455G polymorphism and risk of cancer: evidence from 272 case–control studies. Tumor Biol. 35, 3363–3376.

    Article  CAS  Google Scholar 

  • Rai V., Yadav U. and Kumar P. 2017 Impact of catechol-o-methyltransferase Val 158Met (rs4680) polymorphism on breast cancer susceptibility in Asian population. Asian Pac. J. Cancer Prev. 18, 1243–1250.

  • Rajkumar T., Samson M., Rama R., Sridevi V., Mahji U., Swaminathan R. and Nancy N. K. 2008 TGFbeta1 (Leu10Pro), p53 (Arg72Pro) can predict for increased risk for breast cancer in south Indian women and TGFbeta1 Pro (Leu10Pro) allele predicts response to neo-adjuvant chemo-radiotherapy. Breast Cancer Res Treat. 112, 81–87.

    Article  PubMed  CAS  Google Scholar 

  • Ralph D. A., Zhao L. P., Aston C. E., Manjeshwar S., Pugh T. W., DeFreese D. C. et al. 2007 Age-specific association of steroid hormone pathway gene polymorphisms with breast cancer risk. Cancer 109,1940-8.

    Article  PubMed  CAS  Google Scholar 

  • Ramalhinho A. C., Fonseca-Moutinho J. A. and 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.

    Article  PubMed  CAS  Google Scholar 

  • Reding K. W., Weiss N. S., Chen C., Li C. I., Carlson C. S., Wilkerson H. W. et al. 2009 Genetic polymorphisms in the catechol estrogen metabolism pathway and breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 18, 1461–1467.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robins J., Greenland S. and Breslow N. E. 1986 A general estimator for the variance of the Mantel-Haenszel odds ratio. Am. J. Epidemiol. 124, 719–723.

    Article  PubMed  CAS  Google Scholar 

  • Roodi N., Dupont W. D., Moore J. H. and Parl F. F. 2004 Association of homozygous wild-type glutathione S-transferase M1 genotype with increased breast cancer risk. Cancer Res. 64, 1233–1236.

    Article  PubMed  CAS  Google Scholar 

  • Rutherford K., Bennion B. J., Parson W. W. and Daggett V. 2006 The 108M polymorph of human catechol O-methyltransferase is prone to deformation at physiological temperatures. Biochemistry 45, 2178–2188.

    Article  PubMed  CAS  Google Scholar 

  • Sakoda L. C., Blackston C. R., Xue K., Doherty J. A., Ray R. M., Lin M. G. et al. 2008 Glutathione S-transferase M1 and P1 polymorphisms and risk of breast cancer and fibrocystic breast conditions in Chinese women. Breast Cancer Res. Treat. 109, 143–155.

    Article  PubMed  CAS  Google Scholar 

  • Samson M., Swaminathan R., Rama R., Sridevi V., Nancy K. N. and Rajkumar T. 2007 Role of GSTM1 (Null/Present), GSTP1 (Ile105Val) and P53 (Arg72Pro) genetic polymorphisms and the risk of breast cancer: a case control study from South India. Asian Pac. J. Cancer Prev. 8, 253–257.

    PubMed  Google Scholar 

  • Sangrajrang S., Sato Y., Sakamoto H., Ohnami S., Laird N. M., Khuhaprema T. et al. 2009 Genetic polymorphisms of estrogen metabolizing enzyme and breast cancer risk in Thai women. Int. J. Cancer. 125, 837–843.

    Article  PubMed  CAS  Google Scholar 

  • Sarmanová J., Su̇sová S., Gut I., Mrhalová M., Kodet R., Adámek J. et al. 2004 Breast cancer: role of polymorphisms in biotransformation enzymes. Eur. J. Hum. Genet. 12, 848–54.

  • Saxena A., Dhillon V. S., Raish M., Asim M., Rehman S., Shukla N. K. et al. 2009 Detection and relevance of germline genetic polymorphisms in glutathione S-transferases (GSTs) in breast cancer patients from northern Indian population. Breast Cancer Res. Treat. 115, 537–543.

    Article  PubMed  CAS  Google Scholar 

  • Sazci A., Ergul E., Utkan N. Z., Canturk N. Z. and Kaya G. 2004 Catechol-o-methyltransferase Val 108/158 Met polymorphism in premenopausal breast cancer patients. Toxicology 204, 197–202.

    Article  PubMed  CAS  Google Scholar 

  • Shen Y., Li D. K., Wu J., Zhang Z. and Gao E. 2006 Joint effects of the CYP1A1 MspI, ERalpha PvuII, and ERalpha XbaI polymorphisms on the risk of breast cancer: results from a population-based case-control study in Shanghai, China. Cancer Epidemiol. Biomarkers Prev. 15, 342–347.

    Article  PubMed  CAS  Google Scholar 

  • Singh V., Rastogi N., Sinha A., Kumar A., Mathur N. and Singh M. P. 2007 A study on the association of cytochrome-P450 1A1 polymorphism and breast cancer risk in north Indian women. Breast Cancer Res. Treat. 101, 73–81.

    Article  PubMed  CAS  Google Scholar 

  • Sohail A., Kanwal N., Ali M., Sadia S., Masood A. I., Ali F et al. 2013 Effects of glutathione-S-transferase polymorphisms on the risk of breast cancer: a population-based case-control study in Pakistan. Environ. Toxicol. Pharmacol. 35, 143–153.

    Article  PubMed  CAS  Google Scholar 

  • Song C. G., Hu Z., Yuan W. T., Di G. H., Shen Z. Z., Huang W. and Shao Z. M. 2006 Prevalence of Val158Met polymorphism in COMT gene on non-BRCA1/2 hereditary breast cancer. Zhonghua Wai Ke Za Zhi. 44, 1310–1313. Chinese.

  • Song Z., Shao C., Feng C., Lu Y., Gao Y. and Dong C. 2016 Association of glutathione S-transferase T1, M1, and P1 polymorphisms in the breast cancer risk: a meta-analysis. Ther. Clin. Risk Manag. 12, 763–769.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spurdle A. B., Chang J. H., Byrnes G. B., Chen X., Dite G. S., McCredie M. R. et al. 2007 A systematic approach to analysing gene-gene interactions: polymorphisms at the microsomal epoxide hydrolase EPHX and glutathione S-transferase GSTM1, GSTT1, and GSTP1 loci and breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 16, 769–774.

    Article  PubMed  CAS  Google Scholar 

  • Syamala V. S., Sreeja L., Syamala V., Raveendran P. B., Balakrishnan R., Kuttan R. and Ankathil R. 2008 Influence of germline polymorphisms of GSTT1, GSTM1, and GSTP1 in familial versus sporadic breast cancer susceptibility and survival. Fam. Cancer. 7, 213–220.

    Article  PubMed  CAS  Google Scholar 

  • Syamala V. S., Syamala V., Sheeja V. R., Kuttan R., Balakrishnan R. and Ankathil R. 2010 Possible risk modification by polymorphisms of estrogen metabolizing genes in familial breast cancer susceptibility in an Indian population. Cancer Invest. 28, 304–311.

    Article  PubMed  CAS  Google Scholar 

  • Taioli E., Bradlow H. L., Garbers S. V., Sepkovic D. W., Osborne M. P., Trachman J. et al. 1999 Role of estradiol metabolism and CYP1A1 polymorphisms in breast cancer risk. Cancer Detect. Prev. 23, 232–237.

    Article  PubMed  CAS  Google Scholar 

  • Tan W., Qi J., **ng D. Y., Miao X. P., Pan K. F., Zhang L. and Lin D. X. 2003 Relation between single nucleotide polymorphism in estrogen-metabolizing genes COMT, CYP17 and breast cancer risk among Chinese women. Zhonghua Zhong Liu Za Zhi. 25, 453–456. [Article in Chinese]

  • Thompson P. A., Shields P. G., Freudenheim J. L., Stone A., Vena J. E., Marshall J. R. et al. 1998 Genetic polymorphisms in catechol-O-methyltransferase, menopausal status, and breast cancer risk. Cancer Res. 58, 2107–2110.

    PubMed  CAS  Google Scholar 

  • Valentine J. C., Pigott T. D. and Rothstein H. R. 2010 How many studies do you need? J. Edu. Behav. Statistics. 35, 215–247.

  • Van der Hel O. L., Peeters P. H., Hein D. W., Doll M. A., Grobbee D. E., Kromhout D., and Bueno de Mesquita H. B. 2003 NAT2 slow acetylation and GSTM1 null genotypes may increase postmenopausal breast cancer risk in long-term smoking women. Pharmacogenetics 13, 399–407.

    Article  PubMed  Google Scholar 

  • Wan G. X., Cao Y. W., Li W. Q., Li Y. C. and Li F. 2014 The Catechol-o-methyltransferase Val158Met polymorphism contributes to the risk of breast cancer in the Chinese population: an updated meta-analysis. J. Breast Cancer 17, 149–156.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X. and Huang Z. H. 2015 Predictive potential role of glutathione S-transferase polymorphisms in the prognosis of breast cancer. Genet. Mol. Res. 14, 10236–10241.

    Article  PubMed  CAS  Google Scholar 

  • Wang Q., Li H., Tao P., Wang Y. P., Yuan P., Yang C. X. et al. 2011 Soy isoflavones, CYP1A1, CYP1B1, and COMT polymorphisms, and breast cancer: a case-control study in southwestern China. DNA Cell Biol. 30, 585–595.

    Article  PubMed  CAS  Google Scholar 

  • Wedrén S., Rudqvist T. R., Granath F., Weiderpass E., Ingelman-Sundberg M., Persson I., and Magnusson C. 2003 Catechol-o-methyltransferase gene polymorphism and post-menopausal breast cancer risk. Carcinogenesis 24, 681–687.

    Article  PubMed  CAS  Google Scholar 

  • Wen W., Cai Q., Shu X. O., Cheng J. R., Parl F., Pierce L. et al. 2005 Cytochrome P450 1B1 and catechol-o-methyltransferase genetic polymorphisms and breast cancer risk in Chinese women: results from the shanghai breast cancer study and a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 14, 329–335.

    Article  PubMed  CAS  Google Scholar 

  • Wu F. Y., Lee Y. J., Chen D. R. and Kuo H. W. 2002 Association of   DNA-protein crosslinks and breast cancer. Mutat. Res. 501, 69–78.

    Article  PubMed  CAS  Google Scholar 

  • Wu A. H., Tseng C. C., Van Den Berg D. and Yu M. C. 2003 Tea intake, COMT genotype, and breast cancer in Asian-American women. Cancer Res. 63, 7526–7529.

    PubMed  CAS  Google Scholar 

  • Wu S. H., Tsai S. M., Hou M. F., Lin H. S., Hou L. A., Ma H. et al. 2006 Interaction of genetic polymorphisms in cytochrome P450 2E1 and glutathione S-transferase M1 to breast cancer in Taiwanese woman without smoking and drinking habits. Breast Cancer Res. Treat. 100, 93–98.

    Article  PubMed  CAS  Google Scholar 

  • **ong P., Bondy M. L., Li D., Shen H., Wang L. E., Singletary S. E. et al. 2001 Sensitivity to benzo(a)pyrene diol-epoxide associated with risk of breast cancer in young women and modulation by glutathione S-transferase polymorphisms: a case-control study. Cancer Res. 61, 8465–8469.

    PubMed  CAS  Google Scholar 

  • Yadav S, Singhal N. K, Singh V, Rastogi N, Srivastava P. K and Singh M. P. 2009 Association of single nucleotide polymorphisms in CYP1B1 and COMT genes with breast cancer susceptibility in Indian women. Dis. Markers. 27, 203–210.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yao L., Yu X. and Yu L. 2010 Lack of significant association between CYP1A1 T3801C polymorphism and breast cancer risk: a meta-analysis involving 25,087 subjects. Breast Cancer Res. Treat. 122, 503–507.

    Article  PubMed  CAS  Google Scholar 

  • Yim D. S., Parkb S. K., Yoo K. Y., Yoon K. S., Chung H. H., Kang H. L. et al. 2001 Relationship between the Val158Met polymorphism of catechol O-methyl transferase and breast cancer. Pharmacogenetics 11, 279–286.

    Article  PubMed  CAS  Google Scholar 

  • Yu K. D., Di G. H., Fan L., Wu J., Hu Z., Shen Z. Z. et al. 2009 A functional polymorphism in the promoter region of GSTM1 implies a complex role for GSTM1 in breast cancer. FASEB J. 23, 2274–2287.

    Article  PubMed  CAS  Google Scholar 

  • Zakiullah A., Khisroon M., Saeed M., Khan A., Khuda F., Ali S et al. 2015 Genetic susceptibility to oral cancer due to combined effects of GSTT1, GSTM1 and CYP1A1 gene variants in tobacco addicted patients of Pashtun ethnicity of Khyber Pakhtunkhwa province of Pakistan. Asian Pac. J. Cancer Prev. 16, 1145–1150.

    Article  PubMed  CAS  Google Scholar 

  • Zgheib N. K., Shamseddine A. A., Geryess E., Tfayli A., Bazarbachi A., Salem Z. et al. 2013 Genetic polymorphisms of CYP2E1, GST, and NAT2 enzymes are not associated with risk of breast cancer in a sample of Lebanese women. Mutat. Res. 747–748, 40–47.

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y., Wise J. P., Holford T. R., **e H., Boyle P., Zahm S. H et al. 2004 Serum polychlorinated biphenyls, cytochrome P-450 1A1 polymorphisms, and risk of breast cancer in Connecticut women. Am. J. Epidemiol. 160, 1177–1183.

  • Zheng T., Holford T. R., Zahm S. H., Owens P. H., Boyle P., Zhang Y. et al. 2002 Cigarette smoking, glutathione-s-transferase M1 and t1 genetic polymorphisms, and breast cancer risk (United States). Cancer Causes Control 13, 637–645.

    Article  PubMed  Google Scholar 

  • Zhu J., Chang P., Bondy M. L., Sahin A. A., Singletary S. E., Takahashi S. et al. 2003 Detection of 2-amino-1-methyl-6-phenylimidazo[4,5-b]-pyridine-DNA adducts in normal breast tissues and risk of breast cancer. Cancer Epidemiol. Biomarkers. Prev. 12, 830–837.

    PubMed  CAS  Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group no. RG-1435-066.

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Authors and Affiliations

  1. Center of Excellence in Biotechnology Research, King Saud University, Riyadh, 111451, Saudi Arabia

    Tajamul Hussain

  2. Department of Biochemistry, College of Science, King Saud University, Riyadh, 111451, Saudi Arabia

    Salman Alrokayan

  3. Sandor Lifesciences Pvt. Ltd., Banjara Hills, Road No: 3, Hyderabad, 500 034, India

    Upadhyay Upasna & Shaik Mohammad Naushad

  4. School of Chemical and Biotechnology, SASTRA University, Tirumalaisamudram, Thanjavur, 613 401, India

    Manickam Pavithrakumari & Jaganathan Jayapriya

  5. Department of Clinical Pharmacology and Therapeutics, Nizam’s Institute of Medical Sciences, Hyderabad, 500 082, India

    Vijay Kumar Kutala

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  1. Tajamul Hussain
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Hussain, T., Alrokayan, S., Upasna, U. et al. Meta-analysis of genetic polymorphisms in xenobiotic metabolizing enzymes and their association with breast cancer risk. J Genet 97, 523–537 (2018). https://doi.org/10.1007/s12041-018-0946-4

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  • DOI: https://doi.org/10.1007/s12041-018-0946-4

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