The effect of cigarette smoke and arsenic exposure on urothelial
carcinoma risk is modified by glutathione S-transferase M1 gene null
genotype
Chi-Jung Chung1,2, Chao-Yuan Huang3, Yeong-Shiau Pu3, Horng-Sheng Shiue4,
Chien-Tien Su5, Yu-Mei Hsueh6,7
1Department of Health Risk Management, College of Public Health, China Medical
University, Taichung, Taiwan
2 Department of Medical Research, China Medical University Hospital, Taichung,
Taiwan.
3 Department of Urology, National Taiwan University Hospital, Taipei, Taiwan. 4 Department of Chinese Medicine, Chang Gung Memorial Hospital, Taipei, Taiwan. 5 Department of Family Medicine, Taipei Medical University Hospital, Taipei,
Taiwan.
6 Department of Public Health, School of Medicine, College of Medicine, Taipei
Medical University, Taipei, Taiwan.
7 School of Public Health, College of Public Health and Nutrition, Taipei Medical
University, Taipei, Taiwan.
Address correspondence to Yu-Mei Hsueh, PhD,
Department of Public Health, School of Medicine, College of Medicine, Taipei Medical University, No. 250 Wu-Hsing Street, Taipei 110, Taiwan.
E-mail: ymhsueh@tmu.edu.tw TEL: 886-2-27361661 ext. 6513 FAX: 886-2-27384831
Running title: Null genotype of GST, smoking, arsenic and UC
Conflict of interest
We disclosed all financial and interpersonal relationships that could be viewed as presenting a potential conflict of interest.
The sources of support
The study was supported by grants from the National Science Council of the ROC (NSC 86-2314-B-038-038, NSC 87-2314-B-038-029, NSC-88-2314-B-038-112, NSC-89-2314-B038-049, SC-89-2320-B038-013, NSC-90-2320-B-038-021, NSC91-3112-B-038-0019, NSC92-3112-B-038-001, NSC93-3112-B-038-001, NSC94-2314-B-038-023, NSC-95-2314-B-038-007, NSC- 96-2314-B038-003, NSC 97-2314-B-038 -015 -MY3 (1-3), NSC 97-2314-B-97-2314-B-038-015 -MY3 (2-3), NSC 97-2314-B-97-2314-B-038 -015 -MY3 (3-3), NSC 100-2314-B-038-026).
ABSTRACT
Inter-individual variation in the metabolism of xenobiotics, caused by factors such as cigarette smoking or inorganic arsenic exposure, is hypothesized to be a
susceptibility factor for urothelial carcinoma (UC). Therefore, our study aimed to evaluate the role of gene-environment interaction in the carcinogenesis of UC. A hospital-based case-control study was conducted. Urinary arsenic profiles were measured using high-performance liquid chromatography-hydride generator-atomic absorption spectrometry. Genotyping was performed using a polymerase chain reaction-restriction fragment length polymorphism technique. Information about cigarette smoking exposure was acquired from a lifestyle questionnaire. Multivariate logistic regression was applied to estimate the UC risk associated with certain risk factors. We found that UC patients had higher urinary levels of total arsenic, higher percentages of inorganic arsenic (InAs%) and monomethylarsonic acid (MMA%) and lower percentages of dimethylarsinic acid (DMA%) compared to controls. Subjects carrying the GSTM1 null genotype had significantly increased UC risk. However, no association was observed between gene polymorphisms of CYP1A1, EPHX1,
SULT1A1 and GSTT1 and UC risk after adjustment for age and sex. Significant gene-environment interactions among urinary arsenic profile, cigarette smoking, and GSTM1 wild/null polymorphism and UC risk were observed after adjustment for potential risk factors. Overall, gene-environmental interactions simultaneously played an important role in UC carcinogenesis. In the future, large-scale studies should be conducted using tag-SNPs of xenobiotic-metabolism-related enzymes for gene determination.
Key words: Arsenic; Cigarette smoking; GSTM1; Polymorphism; Urothelial Carcinoma.
INTRODUCTION
Bladder cancer is the most common type of urothelial carcinoma (UC), which originates exclusively from the urothelium present throughout the urinary tract. It was documented that 2,003 new cases of bladder cancer were diagnosed and 756 deaths occurred in Taiwan in 2009 (Department of Health, the Executive Yuan). One of the most important risk factors for bladder cancer is inorganic arsenic in drinking water (Styblo et al., 2002). A significant association between inorganic arsenic and bladder cancer existed whether in an arseniasis endemic area or non-obvious arsenic exposure area in Taiwan (Pu et al., 2007; Huang et al., 2008). In addition, cigarette smoking is also a well-known risk factor for bladder cancer and accounts for up to 50% of all new cases (Strope and Montie, 2008). Generally, cigarette smoke contains more than 60 carcinogenic compounds, which might induce proliferation of the bladder
epithelium and induce carcinogenesis (Zaridze et al., 1991). Only a small proportion of people exposed to cigarette smoke or inorganic arsenic ultimately develop UC. The differential susceptibility might be due to polymorphisms in genes encoding
biotransformation enzymes, which are associated with the metabolism of compounds in cigarette smoke or transform a procarcinogen into either a carcinogen or
intermediate compound (Zhang et al., 2011). Among these genes are those encoding a number of xenobiotic metabolizing enzymes, including Phase I enzymes (cytochrome P450 1A1 (CYP1A1), microsomal epoxide hydrolase 1 (EPHX1)) and Phase II enzymes (glutathione-S-transferase T1 (GSTT1), GSTM1 and sulfotransferases 1A1 (SULT1A1)). The most widely studied SNP, in which single nucleotide
polymorphisms (SNPs) are associated with changes in catalytic activity include CYP1A1 Msp I polymorphism (rs 4646903), SULT1A1 Arg213His (rs 9282861), EPHX1 His139Arg (rs 2234922), null genotypes of GSTT1 and GSTM1, (Hassett et al., 1994; Mo et al., 2009; Ginsberg et al., 2010; Chen et al., 2011). There is a growing body of evidence from human health risk assessments which have found a links to SNPs of CYP1A1, GSTT1, GSTM1, EPHX1, and SULT1A1 (Autrup, 2000; Wang et al., 2002; Zheng et al., 2003; Park et al., 2005; Dong et al., 2008). However, the conclusions were still controversial and needed to be explored further.
Inorganic arsenic metabolism in the human body has generally been considered a detoxification pathway through methylation (Styblo et al., 2002). Methylation of inorganic arsenic (InAs: As3++ As5+) to monomethylarsenic acid (MMA+5) and
S-adenosylmethionine (SAM) serving as the methyl donor (Marafante et al., 1984). Increasingly, epidemiology studies suggest that subjects with poor arsenic
methylation capability, including higher InAs% or MMA% or lower DMA% had an
increased risk of cancers, including UC and bladder cancer, skin lesions and vascular diseases (Pu et al., 2007; Wang et al., 2007; Leonardi et al., 2012). The related enzymes CYP1A1, SULT1A1, EPHX1, GSTT1, and GSTM1 are needed to catalyze metabolism of both cigarette smoke and inorganic arsenic. Polymorphisms of these enzymes are potential sources of inter-individual variability in internal dose of
cigarette smoking or inorganic arsenic metabolism and thus may affect the risk of UC incidence.
Although previous studies concentrated on the significance of genetic
polymorphism in these xenobiotic metabolism genes and UC risk, the lack of urinary arsenic profile data limited the ability to determine the relationships among gene susceptibility, urinary arsenic and UC risk. Therefore, we conducted a hospital-based case-control study to evaluate whether the gene polymorphisms of CYP1A1,
SULT1A1, EPHX1, GSTT1, and GSTM1 modified the risk of UC by affecting urinary arsenic metabolites or exposure of cigarette smoke.
METHODS
Study participants. A detailed protocol of recruitment in this present study has
been previously described (Pu et al., 2007). Briefly, we conducted a hospital-based, case-control study and collected 191 UC cases and 364 age- and sex-matched healthy participants as controls from September 2007 to October 2011. All subjects were recruited from the National Taiwan University Hospital and the Taipei Municipal Wan Fang Hospital. All UC cases diagnosed by histological confirmation were
outpatients at the Department of Urology. Matched controls were recruited from those receiving adult health examinations or senior citizen health examinations at the Department of Family Medicine. All study subjects provided informed
consent before a questionnaire interview and biological specimen collection. The Research Ethics Committee of the National Taiwan University Hospital in Taipei of Taiwan approved the study and the study was performed in accordance with the World Medical Association Declaration of Helsinki.
Questionnaire interview. Structural questionnaires were administered through
socioeconomic characteristics, lifestyle factors (such as cigarette smoking and environmental smoke exposure), as well as personal and family medical history.
Biological specimen collection. Spot urine samples were collected at the time of
recruitment and immediately transferred to a -20°C freezer and stored until the analysis of arsenic species. Concurrently, we used ethylene-diamine-tetraacetic acid (EDTA) vacuumed syringes to collect peripheral blood samples and extracted DNA for the identification of enzyme gene polymorphisms.
Urinary arsenic species assessment. Urinary arsenic profiles of As3+, DMA5+,
MMA5+ and As5+ were analyzed by high-performance liquid chromatography
equipped with a hydride generator and atomic absorption spectrometer (HPLC-HG-AAS). The analysis protocol for determination of the arsenic species has been described in a previous study (Hsueh et al., 1998). Recovery rates of the four arsenic species were calculated using the following formula: ([(sample spiked standard solution concentration) - sample concentration] / standard solution
concentration)×100. The recovery rates of As3+, DMA5+, MMA5+, and As5+ were from
93.8 to 102.2 %, with detection limits of 0.02, 0.08, 0.05 and 0.07 μg/L, respectively. For quality control of the measurements, we purchased freeze-dried SRM 2670 urine from the National Institute of Standards and Technology (NIST, Gaithersburg, MD, USA),which contained 480 ± 100 μg/L arsenic and the urine control was analyzed along with the urine specimens of study subjects. The detected value of arsenic in the SRM 2670 standard was 507 ± 17 μg/L (n = 4). To ensure the stability of urinary arsenic profiles, the detection of arsenic species was performed within 6 months after collection (Chen et al., 2002).
Genotyping of SNPs in CYP1A1, SULT1A1, EPHX1, GSTT1, and GSTM1.
Genomic DNA was extracted using proteinase K digestion following phenol and chloroform extraction. SNPs in CYP1A1 MspI site, SULT1A1 His213Arg, and EPHX1 His139Arg was performed by a polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) method (Wang et al., 2002; 2003). Multiplex PCR with some modifications for GSTM1 and GSTT1 null genotype was performed according to the Lin et al. method (Lin et al., 1998). All PCR products were obtained in a total volume of 30 μL, consisting of an 80 ng sample DNA, 10× PCR buffer, 2.5 mM dNTP, 2 μM of each primer and 2 U Taq polymerase. Detailed sequences of individual primers, annealing temperature, restricted enzyme, and fragment size of CYP1A1, SULT1A1, EPHX1, GSTT1 and GSTM1 are presented in
Table 1. Genotypes were analyzed by electrophoresis on 2% and 3% agarose gels for GSTT1 and GSTM1 genotypes as well as for CYP1A1, SULT1A1, and EPHX1 genotypes, respectively. For quality control, a random 5% of the samples were repeated with a concordance of 100%.
Statistical analysis. Hardy-Weinberg equilibrium was fitted by the goodness of 2
test. The SNPs of CYP1A1, SULT1A1, and EPHX1 were divided into three classes, wild-type homozygotes (WW), variant heterozygotes (WV) and variant homozygotes (VV). Other SNPs of GSTT1 and GSTM1 were divided into two classes, null and non-null genotypes. Cigarette smoking status included never, former and current. Former smokers and current smokers were defined as those who had quit cigarette smoking and those who were still smoking at the time of the recruitment, respectively. All urinary arsenic profiles were normalized by urinary creatinine (μg/g creatinine or mg/g creatinine). Urinary total arsenic (μg/g creatinine) was defined as the sum of As3+, As5+, MMA5+ and DMA5+. The relative proportion of each arsenic species (InAs
%, MMA% and DMA%) was calculated by dividing the concentration of each species by the total arsenic concentration. Multivariate logistic regression models were used to estimate the odds ratios (ORs) and 95% confidence intervals (CIs) to determine the association between genotypes of CYP1A1, SULT1A1, EPHX1, GSTT1 and GSTM1 and the risk of UC after adjustment for age, sex, and educational level. Finally, we
used the additive model (synergy index) to evaluate the combined effects of cigarette smoking status and various urinary arsenic profiles on UC risk (Hosmer and Lemeshow, 1992). All analyses were conducted using Statistical
Analysis Software (SAS) statistical package (SAS, version 8.0, Cary, NC, USA).
RESULTS
The distributions of sociodemographic characteristics and cigarette smoking status, as well as urinary arsenic profiles are shown in Table 2. The mean age of all subjects at recruitment was 62.6 years. Most subjects (70%) were male. Healthy controls had higher educational levels than UC patients. On average, half of the UC patients were never smokers. The ORs for UC were 1.21 (95% CI, 0.68-2.17) and 2.52 (95% CI, 1.56-4.06) in subjects who were former smokers and current smokers compared with those who were non-smokers, respectively. The urinary total arsenic level, InAs%, and MMA% were significantly higher and the DMA% was significantly lower in UC patients than in healthy controls. After adjusting for age and sex, cases with
increasing total arsenic, InAs%, and MMA% or decreasing DMA% had a
significantly higher risk of UC than healthy controls in a significant dose-response relationship.
The distribution of genotypes of CYP1A1, SULT1A1, EPHX1, GSTT1 and
GSTM1 and OR of UC are shown in Table 3. Subjects with null genotype of GSTM1 had significantly higher UC risk than those with non-null genotype, and their OR for UC was 1.50 (95% CI, 1.05-2.15) after adjustment for age and sex. For other gene polymorphisms, no association was seen between gene polymorphisms of CYP1A1, SULT1A1, EPHX1, and GSTT1 and OR of UC. The genotype frequency of
SULT1A1 was not fitted with Hardy-Weinberg equilibrium; therefore, we did not analyze further. In addition, we did not find any relationships among these
polymorphisms and urinary arsenic profiles (data not shown).
The associations between cigarette smoking habit, duration or amount or cumulative cigarette smoking and OR of UC stratified by GSTM1 gene
polymorphism are shown in Table 4. For subjects with null genotype of GSTM1, we found a significantly higher UC risk in current smokers than in non-smokers.
However, this phenomenon was not shown for those with the non-null genotype of GSTM1. Similar results were observed once we evaluated the index of duration of cigarette smoking.
Multivariate-adjusted ORs of a combination of cigarette smoking habits and urinary arsenic profiles on UC risk stratified by gene polymorphisms of GSTM1 are shown in Table 5. For ever smokers carrying the GSTM1 null genotype, and with high urinary total arsenics, or high InAs%, or high MMA%, or low DMA% had significantly higher UC risk than never smokers with low urinary total arsenics, or low InAs%, or low MMA%, or high DMA%. However, similar significant UC risk was not observed for those carrying the GSTM1 non-null genotype, besides the combination of ever smokers and low DMA%. Finally, all synergy indices of cigarette smoking habits
and urinary arsenic profiles on UC risk were not statistically significant. DISCUSSION
To our knowledge, this is the first study to simultaneously evaluate the
relationships between gene polymorphisms of CYP1A1, SULT1A1, EPHX1, GSTT1, and GSTM1, urinary arsenic profiles, cigarette smoking exposure and UC risk. Furthermore, we explored the interactions among GSTM1 gene polymorphism,
urinary arsenic profiles and cigarette smoking exposure on UC risk. In this study, people with null genotype of GSTM1 were significantly associated with increased UC risk. In addition, people who carried the null genotype of GSTM1 gene polymorphism and ever exposed to cigarette smoking had the highest UC risk when they were exposed to higher levels of urinary total arsenic.
Inorganic arsenic is commonly found in groundwater and surface waters and a small percentage of arsenic is found in many foods, such as agricultural rice, cereals, edible oil, and fish (Chiang et al., 2010; Tsai and Jiang, 2011; Chu and Jiang, 2011). Also, a small percentage of arsenic can be acquired from
occupational exposure (Brown and Ross, 2002). Although the International Agency for Research on Cancer (IARC) has shown that arsenic in drinking water is carcinogenic to humans, the exact source of arsenic exposure for participants in this study is unknown. Previous studies indicated that inorganic arsenic exposure was associated with increased UC risk (Huang, et al., 2008; Chen, et al., 2010). In addition, cigarette smoking has been identified as a risk factor of UC (Strope and Montie, 2008). There has also been shown to be a significantly interaction between cigarette smoking and arsenic on the risk for bladder cancer (Pu et al., 2007; Wang, et al., 2012) Furthermore, Chen et al. found a significant interaction between environmental tobacco smoking exposure and arsenic methylation capability on the risk of bladder cancer (Chen, et al., 2005).
Human cytosolic GSTs are mainly coded for at seven loci: Alpha, Kappa, Mu, Pi, Sigma, Theta and Zeta. These enzymes could detoxify xenobiotics by catalyzing the conjugation reactions of reactive intermediates with cytosolic glutathione and by preventing alterations to DNA against many environmental chemicals including inorganic arsenic as well as be involved in activating polycyclic aromatic
hydrocarbons (PAHs) and N-nitroso compounds, which are major carcinogens from cigarette smoking (Board et al., 2000; Moore et al., 2005; Schilter et al., 1993; Zhao et al., 2012). Previous studies demonstrated that a homozygous deletion, or null genotype, at either the GSTM1 (or the GSTT1) locus could lead to functional loss of the enzyme (Gronau et al., 2003). Thus, it might be hypothesized to be implicated in the susceptibility to several cancers, including oral, bladder, breast, and prostate etc. (Park et al., 2003; Cengiz et al., 2007; Mo et al., 2009; Zhang et al., 2011). Similarly, the present study results show that people with the null genotype of GSTM1 MspI
polymorphism had significantly increased OR of UC which is in accordance with previous findings of other investigators (Engel et al., 2002; Cengiz et al., 2007; Song et al., 2009). In contrast, there are some studies which showed no associations
between GSTM1 MspI polymorphism and UC (Srivastava et al., 2005; Lesseur et al., 2012). Furthermore, the frequency of the null genotype of GSTM1 MspI
polymorphism in our control group was about 54%, which was similar with other studies in China or in Taiwan (Hsu et al., 2008; Song et al., 2009).
At present, there are still limited studies which elucidate the interaction between
the null genotype of GSTM1 and cigarette smoking or between the null genotype of GSTM1 and inorganic arsenic on UC risk. Lesseur et al. recently showed a slight interaction of GSTM1 gene-arsenic in the high arsenic exposure group by using the index of toenail arsenic level (Lesseur et al., 2012). In contrast, a case-control study from Bangladesh suggested no evidence of effect of GSTM1 polymorphisms on the relation between arsenic exposure and skin lesions, but they adopted the concentration of arsenic in drinking water and the outcome was skin lesions (McCarty et al., 2007). On the other hand, previous efforts showed that the GSTM1 polymorphism has been associated with the distribution of arsenic metabolites, including InAs%, DMA% and DMA5+/MMA5+ (Chiou et al., 1997; Marcos et al., 2006; Steinmaus et al., 2007;
Agusa et al., 2010). It might be implied that the GSTM1 polymorphism might
accelerate the methylation of inorganic arsenic. In the present study results, we found a significantly high UC risk for ever smoker carrying the GSTM1 null genotype with high urinary total arsenic. Furthermore, for people carrying the GSTM1 null
genotype, ever smokers with high urinary total arsenic, or high InAs%, or high MMA %, or low DMA% had significantly increased UC risk. Individuals with high
urinary total arsenic, or high InAs%, or high MMA%, or low DMA% possess poor arsenic methylation capability. Hence, the results indicated that individuals carrying the GSTM1 null genotype, poor arsenic methylation capability and exposure to cigarette smoking had increased UC risk. However, we could not find
any link between the GSTM1 null genotype and urinary arsenic profile; it might be due to the small sample size of our study. But, our study has the advantage of using an internal dose in individuals to detect arsenic exposure levels exactly, even in
geographic areas without obvious arsenic exposure.
EPHX1 is a key enzyme involved in the first step of metabolism by hydrolysis of highly reactive epoxide intermediates and exhibits the functions of detoxification and
activation similar to some CYP enzymes. Results from global gene expression analyses of cells co-treatment with arsenite and B[a]P showed that CYP1A1 and NQO1 genes are in some cases additively and in others synergistically deregulated by the mixtures (Kann et al., 2005). The variant types of CYP1A1, EPHX1, and GSTT1 was 40%, 11%, and 54% of the healthy controls analyzed in the present study , respectively, and those were in the range of 30-40%, 14%, and 40-55% of previous studies for Japanese, Korean, and Chinese population (Hamajima et al., 2002; Wang et al., 2003; Yeh et al., 2006; Hsu et al., 2008). In addition, the variant genotype frequency of SULT1A1 Arg213His polymorphism was 7%, which was in accordance with that of the Chung et al. study (Chung et al., 2009). However, this polymorphism site was not fitting the Hardy-Weinberg equilibrium in this study. A recent meta-analysis study reported the association of the CYP1A1 MspI polymorphism with lung cancer and an apparent interaction between the CYP1A1 polymorphism and cigarette smoking (Ji et al., 2012). However, we could not observe the association between CYP1A1 MspI polymorphism with UC and this result is accordance with that of Srivastava et al (Srivastava et al., 2008). EPHX1 His139Arg, and GSTT1 wild/null polymorphisms had no relevance to bladder cancers in the present study which was consistent with the results of other studies in Taiwan, New Hampshire, or north Indian subjects (Chen et al., 2004; Srivastava et al., 2005; Hsu et al., 2008; Lesseur et al., 2012).
The present study had some limitations that need to be discuss ed when interpreting results. First, we just evaluated one single spot level of urinary arsenic species and the accuracy may be in doubt. But the values might be reliable under the assumption that all participants had no change in lifestyle. In addition , the case-control study design does not approve the determination of the causality of the observed association between urinary arsenic profiles and UC. W
e cannot exclude the possibility that the association between an increases in urinary arsenic profiles and UC might be the result of and not the cause of increased UC risk . Finally, the sample size of the present study was small; therefore, the significant findings should be interpreted with caution.
In summary, this study shows that the GSTM1 wild/null polymorphism was significantly associated with increased UC risk. High urinary total arsenic
concentration, high InAs%, high MMA%, and low DMA% as well as ever smoker status may also be responsible for an increased OR of UC. In addition, apparent
gene-environment interactions, such as urinary arsenic profile and GSTM1 wild/null polymorphism or cigarette smoking and GSTM1 wild/null polymorphism played an important role in UC carcinogenesis. Large-scale studies using tag-SNPs for genotype determination are recommended for future research.
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