Polymorphisms in genes coding for enzymes metabolizing smoking-derived substances and the risk of periodontitis
Jeong-Sook Kim
Department of Periodontology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorJong Y. Park
Department of Interdisciplinary Oncology, H. Lee Moffitt Cancer Center & Research Institute, University of South Florida, Tampa, FL 33647, USA
Search for more papers by this authorWon-Yoon Chung
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorMin-Ah Choi
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Brain Korea 21 Project for Medical Science, Yonsei University, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorKyoo-Sung Cho
Department of Periodontology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorKwang-Kyun Park
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Brain Korea 21 Project for Medical Science, Yonsei University, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorJeong-Sook Kim
Department of Periodontology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorJong Y. Park
Department of Interdisciplinary Oncology, H. Lee Moffitt Cancer Center & Research Institute, University of South Florida, Tampa, FL 33647, USA
Search for more papers by this authorWon-Yoon Chung
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorMin-Ah Choi
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Brain Korea 21 Project for Medical Science, Yonsei University, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorKyoo-Sung Cho
Department of Periodontology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorKwang-Kyun Park
Department of Oral Biology, Yonsei University College of Dentistry, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Brain Korea 21 Project for Medical Science, Yonsei University, 134 Shinchon-Dong, Seodaemoon-Ku, Seoul 120-752, South Korea
Search for more papers by this authorAbstract
Objectives: Although the direct cause for periodontitis is oral bacterial infection, its progression depends upon genetic and environmental factors. Smoking, one of the environmental factors, is a risk factor for the development and severity of periodontitis. Therefore, individual susceptibility to periodontitis may be influenced by the polymorphisms of genes coding for enzymes metabolizing tobacco-derived substances. The object of this study is to investigate roles of genetic polymorphisms of these metabolizing enzymes in the risk for periodontitis.
Material and Methods: We investigated three important enzymes: cytochrome P450 (CYP) 1A1, CYP2E1 and glutathione S-transferase (GST) M1, involved in the metabolic activation and detoxification of tobacco-derived substances. The prevalence of the polymorphisms of these genes was examined in 115 patients with periodontitis as well as in 126 control subjects.
Results: Significantly increased risk for periodontitis was observed for subjects with the polymorphic CYP1A1 m2 allele (odds ratio (OR)=2.3, 95% confidence interval (CI)=1.2–4.4). A significant risk increase for periodontitis associated with the GSTM1 allele was observed (OR=2.1, 95% CI=1.3–3.6). However, no association was observed between the CYP2E1 Pst1 polymorphism and risk for periodontitis (OR=1.3, 95% CI=0.6–2.5).
Conclusion: These results suggest that the GSTM1 and CYP1A1 polymorphisms may play an important role in risk for periodontitis.
References
- Ausubel, F. M., Brent, R., Kingston, R., Moore, D. D., Seidman, J. G. & Smith, J. A. (1988) Current Protocols in Molecular Biology, Vol. 1. New York: John Wiley and Sons.
- Beck, J. D. & Slade, G. D. (1996) Epidemiology of periodontal diseases. Current Opinion in Periodontology 3, 3–9.
- Berglundh, T., Donati, M., Hahn-Zoric, M., Hanson, L. A. & Padyukov, L. (2003) Association of the –1087 IL 10 gene polymorphism with severe chronic periodontitis in Swedish Caucasians. Journal of Clinical Periodontology 30, 249–254.
- Bolt, H. M., Roos, P. H. & Thier, R. (2003) The cytochrome P-450 isoenzyme CYP2E1 in the biological processing of industrial chemicals: consequences for occupational and environmental medicine. International Archives of Occupational Environmental Health 76, 174–185.
- Burgan, S. W. (1997) The role of tobacco use in periodontal diseases: a literature review. General Dentistry 45, 449–460.
- Craandijk, J., Van Krugten, M. V., Verweij, C. L., Van Der Velden, U. & Loos, B. G. (2002) Tumor necrosis factor-alpha gene polymorphisms in relation to periodontitis. Journal of Clinical Periodontology 29, 28–34.
- Deakin, M., Elder, J., Hendrickse, C., Peckham, D., Baldwin, D., Pantin, C., Wild, N., Leopard, P., Bell, D. A., Jones, P., Duncan, H., Brannigan, K., Alldersea, J., Fryer, A. A. & Strange, R. C. (1996) Glutathione S-transferase GSTT1 genotypes and susceptibility to cancer: studies of interactions with GSTM1 in lung, oral, gastric and colorectal cancers. Carcinogenesis 17, 881–884.
- Galbraith, G. M., Hendley, T. M., Sanders, J. J., Palesch, Y. & Pandey, J. P. (1999) Polymorphic cytokine genotypes as markers of disease severity in adult periodontitis. Journal of Clinical Periodontology 26, 705–709.DOI: 10.1034/j.1600-051X.1999.t01-1-261101.x
- Gonzales, J. R., Michel, J., Diete, A., Herrmann, J. M., Bodeker, R. H. & Meyle, J. (2002) Analysis of genetic polymorphisms at the interleukin-10 loci in aggressive and chronic periodontitis. Journal of Clinical Periodontology 29, 816–822.DOI: 10.1034/j.1600-051X.2002.290905.x
- Greenstein, G. & Hart, T. C. (2002) A critical assessment of interleukin-1 (IL-1) genotyping when used in a genetic susceptibility test for severe chronic periodontitis. Journal of Periodontology 73, 231–247.
- Guengerich, F. P., Kim, D. H. & Iwasaki, M. (1991) Role of human cytochrome P-450 IIE1 in the oxidation of many low molecular weight cancer suspects. Chemical Research in Toxicology 4, 168–179.
- Haber, J., Wattles, J., Crowley, M., Mandell, R., Joshipura, K. & Kent, R. L. (1993) Evidence of cigarette smoking as a major risk factor for periodontitis. Journal of Periodontology 64, 16–23.
- Hayashi, S., Watanabe, J. & Kawajiri, K. (1991) Genetic polymorphisms in the 5′-flanking region change transcriptional regulation of the human cytochrome P450IIE1 gene. Journal of Biochemistry (Tokyo) 110, 559–565.
- Hirvonen, A., Husgafvel-Pursiainen, K., Karjalainen, A., Anttila, S. & Vainio, H. (1992) Point-mutational MspI and Ile-Val polymorphisms closely linked in the CYP1A1 gene: lack of association with susceptibility to lung cancer in a Finnish study population. Cancer Epidemiology, Biomarkers & Prevention 1, 485–489.
- Holla, L. I., Buckova, D., Fassmann, A., Benes, P. & Znojil, V. (2002a) Plasminogen-activator-inhibitor-1 promoter polymorphism as a risk factor for adult periodontitis in non-smokers. Genes and Immunity 3, 292–294.DOI: 10.1038/sj.gene.6363874
- Holla, L. I., Fassmann, A., Benes, P., Halabala, T. & Znojil, V. (2002b) 5 polymorphisms in the transforming growth factor-beta 1 gene (TGF-beta 1) in adult periodontitis. Journal of Clinical Periodontology 29, 336–341.DOI: 10.1034/j.1600-051X.2002.290409.x
- Hung, H. C., Chuang, J., Chien, Y. C., Chern, H. D., Chiang, C. P., Kuo, Y. S., Hildesheim, A. & Chen, C. J. (1997) Genetic polymorphisms of CYP2E1, GSTM1, and GSTT1; environmental factors and risk of oral cancer. Cancer Epidemiology, Biomarkers & Prevention 6, 901–905.
- Kadlubar, F. F. & Hammons, G. J. (1987) Cytochrome P450 in metabolism of chemical carcinogens. In: Mammalian Cytochromes P-450, eds. F. P. Guengerich, Vol. 2, pp. 81–130. Boca Raton, FL: CRC Press.
- Kang, B. Y., Choi, Y. K., Choi, W. H., Kim, K. T., Choi, S. S., Kim, K. & Ha, N. J. (2003) Two polymorphisms of interleukin-4 gene in Korean adult periodontitis. Archives of Pharmacal Research 26, 482–486.
-
Katoh, T.,
Kaneko, S.,
Kohshi, K.,
Munaka, M.,
Kitagawa, K.,
Kunugita, N.,
Ikemura, K. &
Kawamoto, T. (1999) Genetic polymorphisms of tobacco- and alcohol-related metabolizing enzymes and oral cavity cancer.
International Journal of Cancer
83, 606–609.DOI: 10.1002/(SICI)1097-0215(19991126)83:5<606::AID-IJC6>3.3.CO;2-G
10.1002/(SICI)1097-0215(19991126)83:5<606::AID-IJC6>3.0.CO;2-P CAS PubMed Web of Science® Google Scholar
- Kobayashi, T., Westerdaal, N. A., Miyazaki, A., Van Der Pol, W. L., Suzuki, T., Yoshie, H., Van De Winkel, J. G. & Hara, K. (1997) Relevance of immunoglobulin G Fc receptor polymorphism to recurrence of adult periodontitis in Japanese patients. Infection and Immunity 65, 3556–3560.
- Kocher, T., Sawaf, H., Fanghanel, J., Timm, R. & Meisel, P. (2002) Association between bone loss in periodontal disease and polymorphism of N-acetyltransferase (NAT2). Journal of Clinical Periodontology 29, 21–27.DOI: 10.1034/j.1600-051x.2002.290104.x
- Kornman, K. S. & De Giovine, F. S. (1998) Genetic variations in cytokine expression: a risk factor for severity of adult periodontitis. Annals of Periodontology 3, 327–338.
- Laine, M. L., Farre, M. A., Crusius, J. B., Van Winkelhoff, A. J. & Pena, A. S. (2000) The mouthwash: a non-invasive sampling method to study cytokine gene polymorphisms. Journal of Periodontology 71, 1315–1318.
- Laine, M. L., Farre, M. A., Gonzalez, G., Van Dijk, L. J., Ham, A. J., Winkel, E. G., Crusius, J. B., Vandenbroucke, J. P., Van Winkelhoff, A. J. & Pena, A. S. (2001) Polymorphisms of the interleukin-1 gene family, oral microbial pathogens, and smoking in adult periodontitis. Journal of Dental Research 80, 1695–1699.
- Loos, B. G., Leppers-Van de Straat, F. G., Van de Winkel, J. G. & Van der Velden, U. (2003) Fcgamma receptor polymorphisms in relation to periodontitis. Journal of Clinical Periodontology 30, 595–602.
- Meisel, P., Siegemund, A., Grimm, R., Herrmann, F. H., John, U., Schiwahn, C. & Kocher, T. (2003) The interleukin-1 polymorphism, smoking, and the risk of periodontal disease in the population-based SHIP study. Journal of Dental Research 82, 189–193.
- Meisel, P., Timm, R., Sawaf, H., Fanghanel, J., Siegmund, W. & Kocher, T. (2000) Polymorphism of the N-acetyltransferase (NAT2), smoking and the potential risk of periodontal disease. Archives of Toxicology 74, 343–348.DOI: 10.1007/s002040000136
- Nakachi, K., Imai, K., Hayashi, S. & Kawajiri, K. (1993) Polymorphisms of the CYP1A1 and glutathione S-transferase genes associated with susceptibility to lung cancer in relation to cigarette dose in a Japanese population. Cancer Research 53, 2994–2999.
- Offenbacher, S. (1996) Periodontal diseases: pathogenesis. Annals of Periodontology 1, 821–878.
- Park, J. Y., Muscat, J. E., Kaur, T., Schantz, S. P., Stern, J. C., Richie, J. P. Jr. & Lazarus, P. (2000) Comparison of GSTM polymorphisms and risk for oral cancer between African-Americans and Caucasians. Pharmacogenetics 10, 123–131.DOI: 10.1097/00008571-200003000-00004
- Park, J. Y., Muscat, J. E., Ren, Q., Schantz, S. P., Harwick, R. D., Stern, J. C., Pike, V., Richie, J. P. Jr. & Lazarus, P. (1997) CYP1A1 and GSTM1 polymorphisms and oral cancer risk. Cancer Epidemiology, Biomarkers & Prevention 6, 791–797.
- Parkhill, J. M., Hennig, B. J., Chapple, I. L., Heasman, P. A. & Taylor, J. J. (2000) Association of interleukin-1 gene polymorphisms with early-onset periodontitis. Journal of Clinical Periodontology 27, 682–689.DOI: 10.1034/j.1600-051x.2000.027009682.x
- Persson, I., Johansson, I., Bergling, H., Dahl, M. L., Seidegard, J., Rylander, R., Rannug, A., Hogberg, J. & Sundberg, M. I. (1993) Genetic polymorphism of cytochrome P4502E1 in a Swedish population. Relationship to incidence of lung cancer. FEBS Letters 319, 207–211.DOI: 10.1016/0014-5793(93)80547-8
- Sanger, F., Nicklen, S. & Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the USA 74, 5463–5467.
- Sato, M., Sato, T., Izumo, T. & Amagasa, T. (1999) Genetic polymorphism of drug-metabolizing enzymes and susceptibility to oral cancer. Carcinogenesis 20, 1927–1931.
- Sato, M., Sato, T., Izumo, T. & Amagasa, T. (2000) Genetically high susceptibility to oral squamous cell carcinoma in terms of combined genotyping of CYP1A1 and GSTM1 genes. Oral Oncology 36, 267–271.DOI: 10.1016/S1368-8375(99)00090-1
- Scarel-Caminaga, R. M., Trevilatto, P. C., Souza, A. P., Brito, R. B. & Line, S. R. (2002) Investigation of an IL-2 polymorphism in patients with different levels of chronic periodontitis. Journal of Clinical Periodontology 29, 587–591.DOI: 10.1034/j.1600-051X.2002.290701.x
- Scarel-Caminaga, R. M., Trevilatto, P. C., Souza, A. P., Brito, R. B. Jr. & Line, S. R. (2003) Investigation of IL4 gene polymorphism in individuals with different levels of chronic periodontitis in a Brazilian population. Journal of Clinical Periodontology 30, 341–345.
- Schenkein, H. A., Gunsolley, J. C., Koertge, T. C., Schenkein, J. G. & Tew, J. G. (1995) Smoking and its effects on early-onset periodontitis. Journal of American Dental Association 126, 1107–1113.
- Sikdar, N., Mahmud, S. A., Paul, R. R. & Roy, B. (2003) Polymorphism in CYP1A1 and CYP2E1 genes and susceptibility to leukoplakia in Indian tobacco users. Cancer Letters 195, 33–42.DOI: 10.1016/S0304-3835(03)00156-3
- Soga, Y., Nishimura, F., Ohyama, H., Maeda, H., Takashiba, S. & Murayama, Y. (2003) Tumor necrosis factor-alpha gene (TNF-alpha) −1031/–863, –857 single-nucleotide polymorphisms (SNPs) are associated with severe adult periodontitis in Japanese. Journal of Clinical Periodontology 30, 524–531.DOI: 10.1034/j.1600-051X.2003.00287.x
- Sun, J. L., Meng, H. X., Cao, C. F., Tachi, Y., Shinohara, M., Ueda, M., Imai, H. & Ohura, K. (2002) Relationship between vitamin D receptor gene polymorphism and periodontitis. Journal of Periodontal Research 37, 263–267.DOI: 10.1034/j.1600-0765.2002.01605.x
- Tachi, Y., Shimpuku, H., Nosaka, Y., Kawamura, T., Shinohara, M., Ueda, M., Imai, H. & Ohura, K. (2003) Vitamin D receptor gene polymorphism is associated with chronic periodontitis. Life Science 73, 3313–3321.DOI: 10.1016/j.lfs.2003.03.001
- Tanimoto, K., Hayashi, S. I., Yoshiga, K. & Ichikawa, T. (1999) Polymorphisms of the CYP1A1 and GSTM1 gene involved in oral squamous cell carcinoma in association with a cigarette dose. Oral Oncology 35, 191–196.DOI: 10.1016/S1368-8375(98)00094-3
- Trevilatto, P. C., Scarel-Caminaga, R. M., De Brito, R. B. Jr., De Souza, A. P. & Line, S. R. (2003) Polymorphism at position -174 of IL-6 gene is associated with susceptibility to chronic periodontitis in a Caucasian Brazilian population. Journal of Clinical Periodontology 30, 438–442.
- Walker, S. J., Van Dyke, T. E., Rich, S., Kornman, K. S., Di Giovine, F. S. & Hart, T. C. (2000) Genetic polymorphisms of the IL-1alpha and IL-1beta genes in African-American LJP patients and an African-American control population. Journal of Periodontology 71, 723–728.
- Yamazaki, K., Tabeta, K., Nakajima, T., Ohsawa, Y., Ueki, K., Itoh, H. & Yoshie, H. (2001) Interleukin-10 gene promoter polymorphism in Japanese patients with adult and early-onset periodontitis. Journal of Clinical Periodontology 28, 828–832.DOI: 10.1034/j.1600-051x.2001.028009828.x
- Yoshihara, A., Sugita, N., Yamamoto, K., Kobayashi, T., Miyazaki, H. & Yoshi, H. (2001) Analysis of vitamin D and Fcgamma receptor polymorphisms in Japanese patients with generalized early-onset periodontitis. Journal of Dental Research 80, 2051–2054.