Japanese Journal of Clinical Oncology Advance Access originally published online on February 12, 2008
Japanese Journal of Clinical Oncology 2008 38(3):186-191; doi:10.1093/jjco/hym176
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© The Author (2008). Published by Oxford University Press. All rights reserved
DNA Repair Gene hOGG1 Codon 326 and XRCC1 Codon 399 Polymorphisms and Bladder Cancer Risk in a Japanese Population
1 Department of Public Health, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
2 Department of Urology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
For reprints and all correspondence: Yoshiki Kuroda, Department of Public Health, Faculty of Medicine, University of Miyazaki, 5200 Kihara Kiyotake, Miyazaki, 889-1692 Japan. E-mail: ykuroda{at}med.miyazaki-u.ac.jp
Received September 22, 2007; accepted December 18, 2007
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Abstract |
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 TOP Abstract INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Background: Bladder cancer is the most common urologic malignancy in the USA. Tobacco smoking generates oxidative DNA damage and induces bladder cancer. Base excision repair (BER) is a very important mechanism for repairing oxidative DNA damage. There are many enzymes involved in BER. Human oxoguanine glycosylase 1 (hOGG1) and X-ray repair cross-complementing 1 (XRCC1) are enzyme genes of BER. Actually, the hOGG1 codon 326 polymorphism was associated with the risk of lung oesophagus and stomach cancer. On the other hand, among several XRCC1 gene polymorphisms, codon 399 polymorphism was reported to reduce the risk of bladder cancer and raise the risk of lung cancer.
Methods: We examined the association between the genetic polymorphisms of hOGG1 codon 326 and XRCC1 codon 399 and bladder cancer risk. In this study, we recruited 251 bladder cancer cases and 251 healthy controls to evaluate the effect of hOGG1 codon 326 and XRCC1 codon 399 polymorphisms on bladder cancer. We detected genotypes by the polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) method.
Results: The frequencies of the hOGG1 codon 326 genotypes Cys/Cys was significantly higher in the cases than in the controls. Adjusted odds ratio (OR) was 1.85 (95% CI: 1.12–3.03; p = 0.02) compared with Ser/Ser, and was 2.05 (95% CI: 1.36–3.08; p = 0.01) compared with Ser/Ser + Ser/Cys. In addition, when evaluated with smoking status, the adjusted OR (Cys/Cys versus Ser/Ser + Ser/Cys) ran up to 2.78 (95% CI: 1.39–5.60; p < 0.01) among non-smokers. For the XRCC1 polymorphism, the Gln/Gln of XRCC1 codon 399 genotype was statistically higher in the controls than in the cases though compared with Alg/Alg + Alg/Gln. The adjusted OR was 0.45 (95% CI: 0.21–0.99; p = 0.05), and was lifted up to 0.37 (95% CI: 0.14–0.98; p = 0.05) among smokers.
Conclusion: It is indicated that the hOGG1 codon 326 and XRCC1 codon 399 polymorphisms are risk factors of bladder cancer.
Key Words: hOGG1 • XRCC1 • polymorphism • bladder cancer
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INTRODUCTION |
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TOPAbstractINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Bladder cancer is strongly associated with smoking and occupational and environmental exposures to carcinogens. Tobacco smoking is estimated to be the main identifying risk factor for this cancer, which is responsible for 40–50% and 30% of all bladder cancer cases (1,2). Actually, tobacco smoke contains high quantities of chemical carcinogens, such as polycyclic aromatic hydrocarbons, aromatic amines, N-nitroso compounds and reactive oxygen species (ROS). These chemical carcinogens can form bulky adducts after activation by specific enzymes (3), and can induce a variety of oxidative damage (3–5). This damage results in single base changes, and leads to cancer (6,7). This damage, however, can be reversed and removed by base excision repair (BER) mechanisms (8–10) to protect human from carcinogenesis. The human oxoguanine glycosylase 1 (hOGG1) and X-ray repair cross-complementing 1 (XRCC1) genes are key genes in BER pathway.
hOGG1 and XRCC1 genes may play a key role in maintaining genome integrity and preventing cancer development. The human 8-oxoguanine glycosylase 1 (hOGG1) encoded by the hOGG1 gene can directly remove 8-hydroxy-2-deoxyguanine (8-OHdG) from damaged DNA as a part of BER pathway (11,12). The XRCC1 is a multi-domain protein, which repair single-strand breaks in DNA (13,14). Genetic variations in DNA repair genes are thought to modulate DNA repair capacity and are suggested to be related with cancer risk. Therefore, the polymorphisms of these genes alter the repair function that leads to carcinogenesis. For example, the hOGG1 gene has codon 326 polymorphism, and Cys326 has lower ability to prevent mutagenesis by 8-OHdG than Ser326 in vivo in human cells (12). And for the XRCC1, it has codon 399 polymorphism, and was associated with higher levels of aflatoxin B1-DNA adducts and higher bleomycin sensitivity (15,16) There were some reports about the relation between hOGG1 codon 326 and XRCC1 codon 399 polymorphisms and risk for several cancers. The hOGG1 codon 326 polymorphism was associated with the risk of lung (17), oesophagus (18) and stomach cancer (19). On the other hand, XRCC1 codon 399 polymorphism was reported to reduce the risk of bladder cancer (20) and raise the risk of lung cancer (21,22). But the results about these polymorphisms were controversial, and additional studies are needed. Besides, there are no reports concerning bladder cancer among the Japanese. We planned to investigate the effects of hOGG1 codon 326 and XRCC1 codon 399 polymorphisms on bladder cancer risk in a Japanese population with the interaction of smoking as a measure of ROS exposure.
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SUBJECTS AND METHODS |
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Subjects
Both the case and control groups included in this study are described in Table 1. The cases were 251 bladder cancer patients who were recruited from Kitakyushu City and Miyazaki City in Japan through the University of Occupational and Environmental Health (UOEH) Hospital and the University of Miyazaki Hospital. The patients were diagnosed with transitional cell carcinoma during the period of September 1992–January 2002. None of the cases had a history of any cancer except bladder cancer. The controls were 251 individuals who were selected from individuals who had visited the two university hospitals and local medical clinics in Kitakyushu City between September 1993 and September 2001. They were checked physically, including blood and urine tests. Individuals with any cancer history were excluded from the controls. Controls were frequency matched to cases based on just sex, but age and smoking status distribution were not significantly different between the cases and controls (Table 1).
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All participants were administered a questionnaire by a trained interviewer covering medical, occupational and smoking status. There was no subject who had any exposure to carcinogens, heavy metals or radiation in their occupational history. Smoking status was summarized as smoker or non-smoker. Smokers included current smokers and ex-smokers. Non-smokers had never smoked. All cases and controls were given a detailed explanation of the nature of the study, and informed consent was obtained. The ethics committees of University of Miyazaki approved this study.
Genotype Analysis
Genomic DNA was extracted from peripheral blood leukocytes by proteinase K digestion and phenol/chloroform extraction. The genotypes of hOGG1 codon 326 and XRCC1 codon 399 were determined by polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP), as described previously (19,23). The primers used for hOGG1 codon 326 (19) were sense primer (5'-CTGTTCAGTGCC GACCTGCGCCGA-3') and antisense primer (5'-ATCTTG TTGTGCAAACTGAC-3'). The primers used for XRCC1 codon 399 (23) were sense primer (5'-GGACTGTCACC GCATGCGTCGG-3') and antisense primer (5'-GGCTGG GACCACCTGTGTT-3'). The PCR mixture and condition were same for two polymorphisms. The PCR reaction mixture (50 µl) contained 10 pmol of each primer, 2.0 mM MgCl2, 200 mM each dNTP, 1 unit of Taq DNA polymerase (Takara Ex Taq) and 100–300 ng of genomic DNA. The reaction mixture was preincubated for 5 min at 94°C. After that, the PCR condition was 94°C for 60 s and 55°C for 60 s, followed by 72°C for 60 s for 35 cycles. The PCR products for hOGG1 codon 326 were digested with restriction enzyme MobI (New England Biolabs, Beverly, MA) at 37°C for 12 h. The products for XRCC1 codon 399 were digested by the restriction enzyme MspI (at 37°C for 12 h). DNA fragments of the two polymorphisms were electrophorezed through a 2% agarose gel and stained with ethidium bromide. The genotypes of hOGG1 and XRCC1 were determined by the length of the digested products. The Ser/Ser genotype of hOGG1 codon 326 had 224 and 23 bp fragments, Cys/Cys had a 247 bp fragment, and Ser/Cys had 247, 224 and 23 bp fragments. On the other hand, Arg/Arg of XRCC1 codon 399 had 115 and 34 bp fragments, Gln/Gln had a 149 bp fragment, and Arg/Gln had 149, 115 and 34 bp fragments.
Statistical Analysis
The differences in the distribution between the cases and controls were tested using 
2, and Mann–Whitney tests, where appropriate. Hardy–Weinberg equilibrium test among the controls was conducted using the observed genotype frequencies and 2-test. The odds ratio (OR) and 95% confidence intervals (95% CI) were adjusted for age and smoking status by multiple logistic regression analysis with the SPSS for Windows Medical Pack (SPSS, Chicago, IL, USA).
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RESULTS |
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The frequencies of the hOGG1 codon 326 and XRCC1 codon 399 genotypes associated with bladder cancer are shown in Table 2. The distribution in the controls of hOGG1 codon 326 and XRCC1 codon 399 were consistent with the Hardy–Weinberg equilibrium (hOGG1: P = 0.25; XRCC1: P = 0.25).
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The frequency of the hOGG1 codon 326 Cys/Cys genotype was statistically significantly higher in the bladder cancer cases (33.1%) than in the controls (19.5%). The OR of Cys/Cys adjusted by age, gender and smoking status was 1.85 (95% CI: 1.12–3.03; P = 0.02) compared with Ser/Ser, and 2.05 (95% CI: 1.36–3.08; P = 0.01) compared with Ser/Ser + Ser/Cys. On the other hand, the distribution of the XRCC1 codon 399 genotypes in the cases was almost identical to that in the controls synthetically, but compared with Arg/Arg + Arg/Gln, the adjusted OR was 0.45 (95% CI: 0.21–0.99; P = 0.05).
In addition, we evaluated the relationship between the genotypes of hOGG1 codon 326 and XRCC1 codon 399 and bladder cancer risk separated by smoking status (Table 3). Among the non-smokers, the frequency of the hOGG1 codon 326 Cys/Cys genotype was statistically significantly higher in the bladder cancer cases compared with the controls. The adjusted OR was 2.53 (95% CI: 1.05–6.09; P = 0.04) compared with Ser/Ser genotype, 2.78 (95% CI: 1.39–5.60; P < 0.01). Among the smokers, the frequencies of Cys/Cys genotype were significantly higher in cases than in controls compared with Ser/Ser + Ser/Cys. The adjusted OR was 1.72 (95% CI: 1.03–2.86; P = 0.04).
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On the other hand, in the XRCC1 codon 399 polymorphism, the distribution of the genotype of XRCC1 codon 399 was not statistically different between the cases and controls in either the smokers or non-smokers totally. However, comparing the Gln/Gln genotype to Arg/Arg + Arg/Gln, the Gln/Gln genotype was significantly lower in the cases (4.0%) than in the controls (8.4%). The adjusted OR was 0.45 (95% CI: 0.21–0.99; P = 0.05), and dropped down to 0.37 (95% CI: 0.14–0.98; P = 0.05) (Table 3).
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DISCUSSION |
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TOPAbstractINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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DNA repair enzyme gene polymorphism that may alter the function or efficiency of damaged DNA repair may contribute to an increase in the risk for several cancers. The typical damage is oxidative DNA damage. Among the many types of oxidative DNA damages, 8-OHdG is one of the most mutagenic lesions with a propensity to miss-repair, and which has caused GC
TA substitution (24–26). The enzyme hOGG1 encoded by the hOGG1 gene can directly remove 8-OHdG from damaged DNA as a part of the BER pathway (11,12). Several studies have suggested that the hOGG1 polymorphism was associated with increased risk for lung, oesophageal and gastric cancer (17–19). One of the other BER genes for oxidative damage is the XRCC1. The XRCC1 is a multi-domain protein that interacts with at least three other proteins (poly-ADP-ribose polymerase, DNA ligase III, and DNA polymerase β) to repair single-strand breaks in DNA (13,14). There are three polymorphisms in the XRCC1, those at codon 194, codon 280 and codon 399 (27). The polymorphism at codon 399 (Arg to Gln) was associated with cancer risks in several epidemiologic studies (28–30). Two prior studies suggested that the Gln/Gln genotype of the XRCC1 was inversely associated with bladder cancer risk (20,30). However, some reports offered conflicting evidence (29,31,32). There have been no reports about the relation between hOGG1 and XRCC1 polymorphisms and bladder cancer risk in the Japanese population. Therefore, we investigated the relationship between hOGG1 and XRCC1 polymorphisms and bladder cancer risk.
The distributions of the hOGG1 codon 326 and XRCC1 codon 399 polymorphisms were different depending on ethnic groups (17,19,33). The distribution of the hOGG1 codon 326 genotype in our study was similar to other Japanese reports (19). And the distribution of the XRCC1 codon 399 genotype of our study was also similar to other Japanese reports (34,35). Our study indicated that the Cys/Cys genotype of hOGG1 was a risk factor for bladder cancer (adjusted OR = 1.85, 95% CI: 1.12–3.03; P = 0.02), and additionally we found that bladder cancer risk with the Cys/Cys genotype was increased among the non-smokers (adjusted OR = 2.53, 95% CI: 1.05–6.09; P = 0.04). Comparing non-smokers with smokers, we are interested in the decline of the adjusted OR in smokers (Cys/Cys versus Ser/Ser + Ser/Cys). We think that genetic differences could tend to be more important at the exposure to low doses of a carcinogen (such as a low level of cigarette smoking). Amos et al. (36), Khoury et al. (37) and Wang et al. (38) also reported that genetic differences in cancer risk might be smaller at high loads of carcinogen exposure.
This was the second report to evaluate the relation between the hOGG1 codon 326 polymorphism and bladder cancer risk, and the first report in Japanese population. The first one reported for Koreans (39) was same as ours. However, including ours, these are the only two reports about bladder cancer risk with the hOGG1 codon 326 polymorphism. Further study is needed to evaluate the influence of the hOGG1 polymorphism sufficiently.
On the other hand, the Gln/Gln genotype of XRCC1 was not associated with bladder cancer risk (adjusted OR = 0.48, 95% CI: 0.22–1.06; P = 0.07) in overall evaluation. However, comparing Gln/Gln with Arg/Arg + Arg/Gln, we could indicate that the Gln/Gln genotype had a protective effect against bladder cancer (adjusted OR = 0.45, 95% CI 0.21–0.99; P = 0.05) and (adjusted OR = 0.37, 95% CI: 0.14–0.98; P = 0.05) among smokers. Several case-control studies about the relationship between XRCC1 codon 399 polymorphism and bladder cancer risk have been published. The Gln/Gln genotype had a protective effect against bladder cancer (20,30). But other reports could not indicate the same (29,31,32). Shen et al. (20) indicated that the XRCC1 codon 399 polymorphism had a protective effect against bladder cancer among smokers. That result was consistent with ours. Lunn et al. (15) reported that the Gln allele carrier had a significantly increased DNA adducts level, and they suggest that the Arg399Gln amino acid change may alter the phenotype of the XRCC1 protein, resulting in deficient DNA repair. The effects of the XRCC1 codon 399 polymorphism have been evaluated in many studies with many kinds of cancer (22,29,40). The relations between XRCC1 polymorphism and cancer risk are controversial. Different races and sample sizes could be the reason for this discrepancy. Our sample size was similar to other reports of bladder cancer, but our distributions of the XRCC1 codon 399 polymorphism were not similar to those of other racial studies (20,30–32). We admit that our sample size is not sufficiently large. We, therefore, need additional evaluations of the effects of the XRCC1 polymorphism with a larger study population.
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CONCLUSION |
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TOPAbstractINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Our data show a significant relationship between bladder cancer and genetic polymorphism of hOGG1 codon 326 and XRCC1 codon 399. These findings may be helpful for studying the risk for, and identifying individuals susceptible to, bladder cancer. This is the first report on the relationship between the hOGG1 codon 236 and XRCC1 codon 399 polymorphisms and bladder cancer risk in Japanese.
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Acknowledgments |
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This work was supported by the Faculty of Medicine, University of Miyazaki, and the UOEH. Special thanks to the staff and patients of the two facilities.
Conflict of interest statement
None declared.
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References |
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