Figures
Abstract
Background
The SULT1A1 Arg213His (rs9282861) polymorphism is reported to be associated with many kinds of cancer risk. However, the findings are conflicting. For better understanding this SNP site and cancer risk, we summarized available data and performed this meta-analysis.
Methods
Data were collected from the following electronic databases: PubMed, Web of Knowledge and CNKI. The association was assessed by odd ratio (OR) and the corresponding 95% confidence interval (95% CI).
Results
A total of 53 studies including 16733 cancer patients and 23334 controls based on the search criteria were analyzed. Overall, we found SULT1A1 Arg213His polymorphism can increase cancer risk under heterozygous (OR = 1.09, 95% CI = 1.01–1.18, P = 0.040), dominant (OR = 1.10, 95% CI = 1.01–1.19, P = 0.021) and allelic (OR = 1.08, 95% CI = 1.02–1.16, P = 0.015) models. In subgroup analyses, significant associations were observed in upper aero digestive tract (UADT) cancer (heterozygous model: OR = 1.62, 95% CI = 1.11–2.35, P = 0.012; dominant model: OR = 1.63, 95% CI = 1.13–2.35, P = 0.009; allelic model: OR = 1.52, 95% CI = 1.10–2.11, P = 0.012) and Indians (recessive model: OR = 1.93, 95% CI = 1.22–3.07, P = 0.005) subgroups. Hospital based study also showed marginally significant association. In the breast cancer subgroup, ethnicity and publication year revealed by meta-regression analysis and one study found by sensitivity analysis were the main sources of heterogeneity. The association between SULT1A1 Arg213His and breast cancer risk was not significant. No publication bias was detected.
Conclusions
The present meta-analysis suggests that SULT1A1 Arg213His polymorphism plays an important role in carcinogenesis, which may be a genetic factor affecting individual susceptibility to UADT cancer. SULT1A1 Arg213His didn't show any association with breast cancer, but the possible risk in Asian population needs further investigation.
Citation: Xiao J, Zheng Y, Zhou Y, Zhang P, Wang J, Shen F, et al. (2014) Sulfotransferase SULT1A1 Arg213His Polymorphism with Cancer Risk: A Meta-Analysis of 53 Case-Control Studies. PLoS ONE 9(9): e106774. https://doi.org/10.1371/journal.pone.0106774
Editor: Qing-Yi Wei, Duke Cancer Institute, United States of America
Received: March 10, 2014; Accepted: July 30, 2014; Published: September 16, 2014
Copyright: © 2014 Xiao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All data are included within the paper and its Supporting Information files.
Funding: This work was supported by the grants from the National Natural Science Foundation of China (Grant numbers 81071957 and 81000938), (http://www.nsfc.gov.cn/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Sulfotransferase (SULT) enzymes catalyze the sulfate conjugation of a broad range of substrates and play an important role in metabolism of endogenous and exogenous compounds including thyroid and steroid hormones, neurotransmitters, drugs and procarcinogens [1], [2]. There are many isoforms of the SULTs supergene family, each with different amino acid sequence identity and substrate specificity [3]. SULT1A1 is an important member of the sulfotransferase family involving in the pathogenic process of various cancers [3]–[5].
The SULT1A1 gene is located on chromosome 16p12.1–p11.2 [6]. Previous study indicated that exon 7 of the SULT1A1 gene contained a G to A transition at codon 213 (rs9282861) that causes an Arg to His amino acid substitution [4]. Some studies have shown that this genetic polymorphism leads to a decrease in enzymatic activity of SULT1A1 and the sulfonation efficiency thus associating with susceptibility to several cancers [7], [8]. Although the specific role of SULT1A1 Arg213His polymorphism in carcinogenesis has been investigated in numerous case-control studies, the results have been inconclusive, even conflictive. In order to give a comprehensive and precise result, we performed this meta-analysis study to analyze the association between this polymorphism and cancer risk.
Materials and Methods
Identification of eligible studies
The meta-analysis was conducted following the criteria of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Checklist S1). In this study, we did an exhaustive literature search on studies that examined the association of the SULT1A1 gene polymorphisms with cancer risks. All eligible studies were identified by searching the following databases: PubMed, Web of Knowledge and China National Knowledge Infrastructure (CNKI, http://www.cnki.net/). The following terms were utilized: “sulfotransferase, SULT or SULT1A1”, “polymorphism, variation, variant or mutation” and “cancer or carcinoma”. In the CNKI database, we searched with these corresponding key words in Chinese characters. Included studies should meet the following criteria: (1) evaluating the association between SULT1A1 Arg213His polymorphism and cancer risk; (2) study designed as case-control; (3) sufficient data available to estimate an odd ratio (OR) with its 95% confidence interval (95% CI).
Data extraction
Two investigators extracted data independently and reached consensus on the following characteristics of the selected studies: first author's name, the year of publication, ethnicity of the study population, matching criteria, number of participants, genotype distribution and control source.
Statistical analysis
Hardy-Weinberg equilibrium was assessed by Chi-square test. Crude odd ratio (OR) and 95% confidence interval (CI) were used to estimate the association between SULT1A1 polymorphism and cancer susceptibility under the dominant model (Arg/His+His/His vs. Arg/Arg), recessive model (His/His vs. Arg/Arg+Arg/His), homozygous model (His/His vs. Arg/Arg), heterozygous model (His/Arg vs. Arg/Arg) and allelic model (His vs. Arg). The heterogeneity among the studies was evaluated by Q-test and I2 value ranging from 0% to 100% to describe the percentage of between-study variation caused by heterogeneity. P value for the Q-test less than 0.10 indicates existing heterogeneity among studies. And then the pooled OR was measured by a random effect model (the DerSimonian-Laird method). Otherwise, a fixed effect model (the Mantel-Haenszel method) was chosen.
Subgroup analyses were performed according to cancer type (breast cancer, colorectal cancer, urothelial cancer, prostate cancer, lung cancer, upper aero digestive tract (UADT) cancer, ovarian cancer and gastric cancer), ethnicity (Caucasian, East Asian, Indian and African) and source of controls (hospital based and population based). When heterogeneity was detected, a multivariable meta-regression analysis including cancer type, ethnicity, control source and year of publication to explore potential source of heterogeneity and sensitivity analysis were performed.
The potential publication bias was estimated using Egger's linear regression test by visual inspection of the funnel plot. P<0.05 was considered statistically significant, and all P values were two-sided. Analyses were performed using the software Review Manager 5.3 (Cochrane Collaboration), R software (www.r-project.org) and STATA 12.0 software (StataCrop).
Results
Characteristics of eligible studies
The flow diagram of literature search was given in Figure 1. A total of 91 studies focusing the association between the SULT1A1 Arg213His polymorphism and cancer risks were identified. 25 of them were ruled out because of unavailable data or repeated data. Thus, the allele and genotype frequencies of the SULT1A1 Arg213His polymorphism were extracted from 66 articles. However, 18 articles didn't meet with Hardy-Weinberg equilibrium and were abandoned (Excluded list S1). As a result, 53 studies of 48 articles, involving 16733 cases and 23334 controls were included in the pooled analyses [9]–[56].
The characteristics of studies included in the current meta-analysis are shown in Table 1. Among these studies, 13 were conducted for breast cancer, 10 for colorectal cancer, 7 for urothelial cancer, 5 for prostate cancer, 5 for lung cancer, 5 for UADT (upper aero digestive tract) cancer, 3 for ovarian cancer, 2 for gastric cancer and 1 for myeloid leukemia, multiple myeloma, and endometrial cancer, respectively. By ethnics, there were 27 studies of Caucasians, 11 studies of East Asians, 4 studies of Indians, 2 studies of Africans and 9 studies of mixed ethnics. By source of controls, 16 studies were population-based, 17 studies were hospital-based and 20 studies were not clear.
Overall Analysis
Table 2 showed the results of overall analysis and the subgroup analysis. The analyses on the full data set indicated a significant association of the SULT1A1 Arg213His polymorphism with cancer risk: heterozygous (OR = 1.09, 95% CI = 1.01–1.19, P = 0.035), homozygous (OR = 1.20, 95% CI = 1.04–1.39, P = 0.014), dominant (OR = 1.12, 95% CI = 1.03–1.22, P = 0.008) (Figure S1), recessive (OR = 1.16, 95% CI = 1.02–1.32, P = 0.027) and allelic model (OR = 1.11, 95% CI = 1.04–1.20, P = 0.003), with high heterogeneity among studies (I2 = 63.1%, 62.6%, 68.5%, 58.3% and 73.7%, respectively, all P<0.001)(Table 3).
Subgroup Analyses
We analyzed the association in cancer type subgroup. SULT1A1 Arg213His polymorphism can increase cancer risks in the following cancer types: breast cancer (homozygous model: OR = 1.37, 95% CI = 1.01–1.87, P = 0.045; dominant model: OR = 1.18, 95% CI = 1.00–1.40, P = 0.050 and allelic model: OR = 1.15, 95% CI = 1.00–1.32, P = 0.044); UADT cancer (heterozygous model: OR = 1.62, 95% CI = 1.11–2.35, P = 0.012; dominant model: OR = 1.63, 95% CI = 1.13–2.35, P = 0.009 and allelic model: OR = 1.52, 95% CI = 1.10–2.11, P = 0.012). Forest plots of breast cancer risk and UADT cancer risk were shown in Figure 2 and Figure 3 separately.
Analyzed by ethnicity, a moderately increased risk was observed in Caucasians (homozygous model: OR = 1.20, 95% CI = 1.01–1.43, P = 0.035 and allelic model: OR = 1.10, 95% CI = 1.01–1.19, P = 0.019) and Indians (recessive model: OR = 1.93, 95% CI = 1.22–3.07, P = 0.005). No significant association was found in other ethnicities in any model.
By control source, significant association was observed in hospital based study, but not the population based study.
Meta-regression analysis
To find potential source of heterogeneity, multivariable meta-regression analyses were conducted in total group and subgroups including cancer type, ethnicity, control source and publication year. In the breast cancer subgroup, ethnicity (heterozygous model, P = 0.027; recessive model, P = 0.020) and publication year (heterozygous model, P = 0.019; recessive model, P = 0.012) are significant sources of heterogeneity (Table S1). Other variables don't affect heterogeneity.
Sensitivity analysis
The sensitivity analysis was constructed by repeating the meta-analysis sequentially removing each study. In the recessive model, two studies [26], [57] were found to affect the pooled OR and the heterogeneity when removed. The study conducted by Khvostova was focused on breast cancer and Sun's study was focused on colorectal cancer among Caucasians, so further sensitivity analyses were conducted in total data set and breast cancer, colorectal cancer and Caucasian subgroups after removing the two studies (Table 4 and Table S2). In total group, the heterogeneity was significantly decreased (I2 = 58.2, 42.2, 63.5, 33.1 and 66.4, respectively). In the subgroup sensitivity analyses, removing the two studies can significantly decrease the heterogeneity among studies, most I2 values less than 50%. And this polymorphism didn't show any obvious correlation with breast cancer risk (Figure 4). At last, we conducted the sensitivity analyses on the remaining studies and the result was stable.
Publication bias
Funnel plots and Egger's test were carried out to assess publication bias. The shapes of funnel plots indicated no obvious asymmetry (Figure 5). Egger's test found no publication bias in the heterozygous (P = 0.074); homozygous (P = 0.146); dominant (P = 0.076); recessive (P = 0.282) and allelic model (P = 0.081).
(A) heterozygous model (B) homozygous model (C) dominant model (D) recessive model The horizontal line in the funnel plot indicates the fixed-effects summary estimate, whereas the sloping lines indicate the expected 95% confidence intervals for a given SE.
Discussion
SULT1A1 enzyme encoded by SULT1A1 gene plays an important role in xenobiotic metabolism. The Arg213His polymorphism, the most widely studied polymorphism within SULT1A1 gene, can reduce enzyme activity and thermostability, and consequently results in an individual's susceptibility to cancer [7], [8].
There have been a few meta-analyses focusing on this mutation and cancer risk [58]–[60]. However, most of these analyses were conducted before the year 2012 and a new meta-analysis is needed to give a comprehensive conclusion due to the increasing data of case-control studies.
This present meta-analysis, including 16733 cases and 23334 controls from 53 case-control studies, explored the association between the SULT1A1 Arg213His polymorphism and cancer risk. This is the largest scale meta-analysis so far. Our results suggested that the SULT1A1 Arg213His was associated with UADT cancer risk. As the upper aero digestive tract is exposed to numerous potential carcinogens such as phenolic xenobiotics, polycyclic aromatic hydrocarbons and heterocyclic aromatic amines contained in cigarette smoking, environmental pollutants and some food, this result manifests that the mutation within SULT1A1 causes the low SULT1A1 activity and is associated with high susceptibility to cancers related with environment.
In the sensitivity analyses, the study conducted by Khvostova influences the pooled estimates and the heterogeneity most in breast cancer subgroup. And after removing this study, the significant association between SULT1A1 Arg213His and breast cancer risk became null (Figure 2 and Figure 4). We further checked data from Khvostova and observed the percentage of wild homozygous genotype in Khvostova's study was obviously lower than that in other studies thus causing great heterogeneity. At last a robust result was achieved and failed to reveal significant association in breast cancer subgroup. This result is similar to Wang, Lee and Jiang [61]–[63], but they found a positive association of this polymorphism with breast cancer susceptibility among Asians. While in our meta-analysis, we only recruited one paper focused on breast cancer among Asians because other papers on Asians deviate from HWE and were excluded. This is a limitation of this meta-analysis and more independent case-control studies conducted on Asians are needed to conclude a more comprehensive result.
In the ethnic subgroup analysis, we found that the genotype distributions of the SNP site are different in ethnic groups. When calculating the percentage of alleles in every ethnic, we found that His allele in Asians (9.58%) is significantly less than in Caucasians (35.2%). Different ethnicities may have different genetic backgrounds, thus causing different genotype frequencies in Asian and other ethnic groups which may influence cancer susceptibility.
Li and Kotnis have conducted meta-analyses focused on environment-related cancers, such as tobacco-related cancers and found cancer risk could be modulated by interaction between genetic variants and environmental factors [58], [59]. As exposed environmental factors are different according to cancer types, for example smoking leads to lung cancer, while the intake of meat influences breast cancer and colorectal cancer [64], [65] and our analysis took many kinds of cancer into account, we decided not to include environmental factors. Moreover, the definitions of exposed environmental factors were not consistent in the studies, which could cause great heterogeneity. Our estimates were based on crude OR values, not adjusted OR values, which may yield inaccurate calculation.
There were several sources bringing in heterogeneity, such as study design, age and sex distribution, and ethnicity. Meta-regression analysis was conducted to find source of heterogeneity. In the breast cancer subgroup, publication year could cause great heterogeneity and further attention was paid to years. We found all the recruited studies were carried out before 2005 or after 2010, and there were no studies between 2006 and 2009. The His allele was 29.6% in the studies before 2005 and 33.0% after 2010, which was significantly different (P = 0.02). This may be caused by the different study population, and needs more case-control studies to illustrate.
In conclusion, our meta-analysis suggests that the SULT1A1 Arg213His polymorphism may contribute UADT cancer risk. As the result was calculated through sampling statics and statistical difference is not the same as clinical difference, the result can be used for clinical reference, not for clinical diagnosis of cancer. Further detailed investigation with larger number of worldwide participants is needed to clarify the role of this polymorphism in cancer risk.
Supporting Information
Figure S1.
Forest plot on the association between SULT1A1 Arg213His polymorphism and overall cancer risk in dominant model.
https://doi.org/10.1371/journal.pone.0106774.s001
(TIF)
Table S1.
The P-value of meta-regression in overall and breast cancer groups.
https://doi.org/10.1371/journal.pone.0106774.s002
(DOCX)
Table S2.
Heterogeneity test after omitting studies of Khvostova and Sun.
https://doi.org/10.1371/journal.pone.0106774.s003
(DOCX)
Excluded list S1.
Excluded studies list with reasons.
https://doi.org/10.1371/journal.pone.0106774.s005
(XLS)
Author Contributions
Conceived and designed the experiments: XLY MHW WPW. Performed the experiments: JJX YBZ YHZ PZ. Analyzed the data: YBZ LXF. Contributed reagents/materials/analysis tools: JJX JGW FYS. Wrote the paper: JJX YBZ VKK.
References
- 1. Coughtrie MW (2002) Sulfation through the looking glass–recent advances in sulfotransferase research for the curious. Pharmacogenomics J 2: 297–308.
- 2. Richard K, Hume R, Kaptein E, Stanley EL, Visser TJ, et al. (2001) Sulfation of thyroid hormone and dopamine during human development: ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain. Journal of Clinical Endocrinology and Metabolism 86: 2734–2742.
- 3. Glatt H (2000) Sulfotransferases in the bioactivation of xenobiotics. Chemico-biological interactions 129: 141–170.
- 4. Raftogianis RB, Wood TC, Otterness DM, Van Loon JA, Weinshilboum RM (1997) Phenol sulfotransferase pharmacogenetics in humans: association of common SULT1A1 alleles with TS PST phenotype. Biochem Biophys Res Commun 239: 298–304.
- 5. Glatt H (1997) Sulfation and sulfotransferases 4: bioactivation of mutagens via sulfation. FASEB J 11: 314–321.
- 6. Dooley TP, Huang Z (1996) Genomic organization and DNA sequences of two human phenol sulfotransferase genes (STP1 and STP2) on the short arm of chromosome 16. Biochem Biophys Res Commun 228: 134–140.
- 7. Nagar S, Walther S, Blanchard RL (2006) Sulfotransferase (SULT) 1A1 polymorphic variants *1, *2, and *3 are associated with altered enzymatic activity, cellular phenotype, and protein degradation. Mol Pharmacol 69: 2084–2092.
- 8. Ozawa S, Tang YM, Yamazoe Y, Kato R, Lang NP, et al. (1998) Genetic polymorphisms in human liver phenol sulfotransferases involved in the bioactivation of N-hydroxy derivatives of carcinogenic arylamines and heterocyclic amines. Chem Biol Interact 109: 237–248.
- 9. Arslan S, Silig Y, Pinarbasi H (2009) An investigation of the relationship between SULT1A1 Arg(213)His polymorphism and lung cancer susceptibility in a Turkish population. Cell Biochem Funct 27: 211–215.
- 10. Arslan S, Silig Y, Pinarbasi H (2011) Sulfotransferase 1A1 Arg(213)His polymorphism and prostate cancer risk. Exp Ther Med 2: 1159–1162.
- 11. Bamber DE, Fryer AA, Strange RC, Elder JB, Deakin M, et al. (2001) Phenol sulphotransferase SULT1A1*1 genotype is associated with reduced risk of colorectal cancer. Pharmacogenetics 11: 679–685.
- 12. Boccia S, Cadoni G, La Torre G, Arzani D, Volante M, et al. (2006) A case-control study investigating the role of sulfotransferase 1A1 polymorphism in head and neck cancer. J Cancer Res Clin Oncol 132: 466–472.
- 13. Boccia S, Sayed-Tabatabaei FA, Persiani R, Gianfagna F, Rausei S, et al. (2007) 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 7: 206.
- 14. Chacko P, Rajan B, Mathew BS, Joseph T, Pillai MR (2004) CYP17 and SULT1A1 gene polymorphisms in Indian breast cancer. Breast Cancer 11: 380–388.
- 15. Chen K, Fan C-H, Jin M-J, Song L, Xu H, et al. (2006) A case-control study on the association between the genetic polymorphism of sulfotransferase 1A1, diet and susceptibility of colorectal cancer. Zhonghua Zhongliu Zazhi 28: 670–673.
- 16. Cheng TC, Chen ST, Huang CS, Fu YP, Yu JC, 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.
- 17. Cleary SP, Cotterchio M, Shi E, Gallinger S, Harper P (2010) Cigarette smoking, genetic variants in carcinogen-metabolizing enzymes, and colorectal cancer risk. Am J Epidemiol 172: 1000–1014.
- 18. Cui X, Lu X, Hiura M, Omori H, Miyazaki W, et al. (2013) Association of genotypes of carcinogen-metabolizing enzymes and smoking status with bladder cancer in a Japanese population. Environ Health Prev Med 18: 136–142.
- 19. Eichholzer M, Rohrmann S, Barbir A, Hermann S, Teucher B, et al. (2012) Polymorphisms in heterocyclic aromatic amines metabolism-related genes are associated with colorectal adenoma risk. Int J Mol Epidemiol Genet 3: 96–106.
- 20. Hirata H, Hinoda Y, Okayama N, Suehiro Y, Kawamoto K, et al. (2008) CYP1A1, SULT1A1, and SULT1E1 polymorphisms are risk factors for endometrial cancer susceptibility. Cancer 112: 1964–1973.
- 21. Holt SK, Rossing MA, Malone KE, Schwartz SM, Weiss NS, et al. (2007) Ovarian cancer risk and polymorphisms involved in estrogen catabolism. Cancer Epidemiology Biomarkers & Prevention 16: 481–489.
- 22. 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.
- 23. Hung RJ, Boffetta P, Brennan P, Malaveille C, Hautefeuille A, et al. (2004) GST, NAT, SULT1A1, CYP1B1 genetic polymorphisms, interactions with environmental exposures and bladder cancer risk in a high-risk population. Int J Cancer 110: 598–604.
- 24. Ihsan R, Chauhan PS, Mishra AK, Yadav DS, Kaushal M, et al. (2011) Multiple analytical approaches reveal distinct gene-environment interactions in smokers and non smokers in lung cancer. PLoS One 6: e29431.
- 25. Jerevall PL, Al-Imadi A, Bergman M, Stal O, Wingren S (2005) Sulfotransferase1A1 and risk of postmenopausal breast cancer. Anticancer Res 25: 2515–2517.
- 26. Khvostova EP, Pustylnyak VO, Gulyaeva LF (2012) Genetic polymorphism of estrogen metabolizing enzymes in Siberian women with breast cancer. Genet Test Mol Biomarkers 16: 167–173.
- 27. Koike H, Nakazato H, Ohtake N, Matsui H, Okugi H, et al. (2008) Further evidence for null association of phenol sulfotransferase SULT1A1 polymorphism with prostate cancer risk: a case-control study of familial prostate cancer in a Japanese population. Int Urol Nephrol 40: 947–951.
- 28.
Kotnis A, Namkung J, Kannan S, Jayakrupakar N, Park T, et al.. (2012) Multiple Pathway-Based Genetic Variations Associated with Tobacco Related Multiple Primary Neoplasms. PLoS One 7.
- 29. Langsenlehner U, Krippl P, Renner W, Yazdani-Biuki B, Eder T, et al. (2004) Genetic variants of the sulfotransferase 1A1 and breast cancer risk. Breast Cancer Res Treat 87: 19–22.
- 30. Liang G, Miao X, Zhou Y, Tan W, Lin D (2004) A functional polymorphism in the SULT1A1 gene (G638A) is associated with risk of lung cancer in relation to tobacco smoking. Carcinogenesis 25: 773–778.
- 31. Lilla C, Risch A, Kropp S, Chang-Claude J (2005) SULT1A1 genotype, active and passive smoking, and breast cancer risk by age 50 years in a German case-control study. Breast Cancer Res 7: R229–237.
- 32. Lilla C, Risch A, Verla-Tebit E, Hoffmeister M, Brenner H, et al. (2007) SULT1A1 genotype and susceptibility to colorectal cancer. Int J Cancer 120: 201–206.
- 33. Nowell S, Coles B, Sinha R, MacLeod S, Ratnasinghe DL, et al. (2002) Analysis of total meat intake and exposure to individual heterocyclic amines in a case-control study of colorectal cancer: contribution of metabolic variation to risk. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis 506: 175–185.
- 34. Nowell S, Ratnasinghe DL, Ambrosone CB, Williams S, Teague-Ross T, et al. (2004) Association of SULT1A1 phenotype and genotype with prostate cancer risk in African-Americans and Caucasians. Cancer Epidemiol Biomarkers Prev 13: 270–276.
- 35. Ozawa S, Katoh T, Inatomi H, Imai H, Kuroda Y, et al. (2002) Association of genotypes of carcinogen-activating enzymes, phenol sulfotransferase SULT1A1 (ST1A3) and arylamine N-acetyltransferase NAT2, with urothelial cancer in a Japanese population. Int J Cancer 102: 418–421.
- 36. Pereira WO, Paiva AS, Queiroz JW, Toma L, Dietrich CP, et al. (2005) Genetic polymorphism in the sulfotransferase SULT1A1 gene in cancer. Cancer Genet Cytogenet 160: 55–60.
- 37. Roupret M, Cancel-Tassin G, Comperat E, Fromont G, Sibony M, et al. (2007) Phenol sulfotransferase SULT1A1*2 allele and enhanced risk of upper urinary tract urothelial cell carcinoma. Cancer Epidemiol Biomarkers Prev 16: 2500–2503.
- 38. Sachse C, Smith G, Wilkie MJV, Barrett JH, Waxman R, et al. (2002) A pharmacogenetic study to investigate the role of dietary carcinogens in the etiology of colorectal cancer. Carcinogenesis 23: 1839–1849.
- 39. Santos SS, Koifman RJ, Ferreira RM, Diniz LF, Brennan P, et al. (2012) SULT1A1 genetic polymorphisms and the association between smoking and oral cancer in a case-control study in Brazil. Front Oncol 2: 183.
- 40. Sellers TA, Schildkraut JM, Pankratz VS, Vierkant RA, Fredericksen ZS, et al. (2005) Estrogen bioactivation, genetic polymorphisms, and ovarian cancer. Cancer Epidemiology Biomarkers & Prevention 14: 2536–2543.
- 41. Serrano D, Lazzeroni M, Zambon CF, Macis D, Maisonneuve P, et al. (2011) Efficacy of tamoxifen based on cytochrome P450 2D6, CYP2C19 and SULT1A1 genotype in the Italian Tamoxifen Prevention Trial. Pharmacogenomics J 11: 100–107.
- 42. Seth P, Lunetta KL, Bell DW, Gray H, Nasser SM, et al. (2000) Phenol sulfotransferases: hormonal regulation, polymorphism, and age of onset of breast cancer. Cancer Res 60: 6859–6863.
- 43. Sillanpaa P, Kataja V, Eskelinen M, Kosma VM, Uusitupa M, et al. (2005) Sulfotransferase 1A1 genotype as a potential modifier of breast cancer risk among premenopausal women. Pharmacogenet Genomics 15: 749–752.
- 44. Steiner M, Bastian M, Schulz WA, Pulte T, Franke KH, et al. (2000) Phenol sulphotransferase SULT1A1 polymorphism in prostate cancer: lack of association. Arch Toxicol 74: 222–225.
- 45. Sun X-F, Ahmadi A, Arbman G, Wallin A, Asklid D, et al. (2005) Polymorphisms in sulfotransferase 1A1 and glutathione S-transferase P1 genes in relation to colorectal cancer risk and patients' survival. World Journal of Gastroenterology 11: 6875–6879.
- 46. Syamala VS, Syamala V, Sheeja VR, Kuttan R, Balakrishnan R, et al. (2010) Possible Risk Modification by Polymorphisms of Estrogen Metabolizing Genes in Familial Breast Cancer Susceptibility in an Indian Population. Cancer Invest 28: 304–311.
- 47. Tamaki Y, Arai T, Sugimura H, Sasaki T, Honda M, et al. (2011) Association between cancer risk and drug-metabolizing enzyme gene (CYP2A6, CYP2A13, CYP4B1, SULT1A1, GSTM1, and GSTT1) polymorphisms in cases of lung cancer in Japan. Drug Metab Pharmacokinet 26: 516–522.
- 48. Tang DL, Rundle A, Mooney L, Cho S, Schnabel F, et al. (2003) Sulfotransferase 1A1 (SULT1A1) polymorphism, PAH-DNA adduct levels in breast tissue and breast cancer risk in a case-control study. Breast Cancer Res Treat 78: 217–222.
- 49. Tsukino H, Kuroda Y, Nakao H, Imai H, Inatomi H, et al. (2004) Cytochrome P450 (CYP) 1A2, sulfotransferase (SULT) 1A1, and N-acetyltransferase (NAT) 2 polymorphisms and susceptibility to urothelial cancer. J Cancer Res Clin Oncol 130: 99–106.
- 50. Wang Y, Spitz MR, Tsou AM, Zhang K, Makan N, et al. (2002) Sulfotransferase (SULT) 1A1 polymorphism as a predisposition factor for lung cancer: a case-control analysis. Lung Cancer 35: 137–142.
- 51. Wang YH, Juang GD, Hwang TI, Shen CH, Shao KY, et al. (2008) Genetic polymorphism of sulfotransferase 1A1, cigarette smoking, hazardous chemical exposure and urothelial cancer risk in a Taiwanese population. Int J Urol 15: 1029–1034.
- 52. Wong CF, Liyou N, Leggett B, Young J, Johnson A, et al. (2002) Association of the SULT1A1 R213H polymorphism with colorectal cancer. Clin Exp Pharmacol Physiol 29: 754–758.
- 53. Wu MT, Wang YT, Ho CK, Wu DC, Lee YC, et al. (2003) SULT1A1 polymorphism and esophageal cancer in males. Int J Cancer 103: 101–104.
- 54. Zheng LZ, Wang YF, Schabath MB, Grossman HB, Wu XF (2003) Sulfotransferase 1A1 (SULT1A1) polymorphism and bladder cancer risk: a case-control study. Cancer Lett 202: 61–69.
- 55. Zheng W, Xie DW, Cerhan JR, Sellers TA, Wen WQ, et al. (2001) Sulfotransferase 1A1 polymorphism, endogenous estrogen exposure, well-done meat intake, and breast cancer risk. Cancer Epidemiology Biomarkers & Prevention 10: 89–94.
- 56. Feng X, Zhu S, Wang L, Duan M, Zhang J, et al. (2006) Relationship between SULT1A1 gene polymorphisms and susceptibility to esophageal cancer. CHINESE JOURNAL OF DISEASE CONTROL & PREVENTION 10: 373–376.
- 57. Sun XF, Ahmadi A, Arbman G, Wallin A, Asklid D, et al. (2005) Polymorphisms in sulfotransferase 1A1 and glutathione S-transferase P1 genes in relation to colorectal cancer risk and patients' survival. World J Gastroenterol 11: 6875–6879.
- 58. Li K, Ren YW, Wan Y, Yin ZH, Wu W, et al. (2012) SULT1A1 Arg213His polymorphism and susceptibility of environment-related cancers: a meta analysis of 5,915 cases and 7,900 controls. Mol Biol Rep 39: 2597–2605.
- 59. Kotnis A, Kannan S, Sarin R, Mulherkar R (2008) Case-control study and meta-analysis of SULT1A1 Arg213His polymorphism for gene, ethnicity and environment interaction for cancer risk. Br J Cancer 99: 1340–1347.
- 60. Sun Y, Zang Z, Xu X, Zhang Z, Zhong L, et al. (2011) The association of SULT1A1 codon 213 polymorphism and breast cancer susceptibility: meta-analysis from 16 studies involving 23,445 subjects. Breast Cancer Res Treat 125: 215–219.
- 61. Wang Z, Fu Y, Tang C, Lu S, Chu WM (2010) SULT1A1 R213H polymorphism and breast cancer risk: a meta-analysis based on 8,454 cases and 11,800 controls. Breast Cancer Res Treat 122: 193–198.
- 62. Lee H, Wang Q, Yang F, Tao P, Li H, et al. (2012) SULT1A1 Arg213His polymorphism, smoked meat, and breast cancer risk: a case-control study and meta-analysis. DNA Cell Biol 31: 688–699.
- 63. Jiang Y, Zhou L, Yan T, Shen Z, Shao Z, et al. (2010) Association of sulfotransferase SULT1A1 with breast cancer risk: a meta-analysis of case-control studies with subgroups of ethnic and menopausal statue. J Exp Clin Cancer Res 29: 101.
- 64. Kruk J, Marchlewicz M (2013) Dietary fat and physical activity in relation to breast cancer among Polish women. Asian Pac J Cancer Prev 14: 2495–2502.
- 65. Durko L, Malecka-Panas E (2014) Lifestyle Modifications and Colorectal Cancer. Curr Colorectal Cancer Rep 10: 45–54.