Association of Toll-like Receptor 4 Gene polymorphisms with susceptibility to type 2 diabetes mellitus in the Chinese population Toll样受体4基因多态性与中国人群2型糖尿病易感性的关联研究
Background Toll‐like receptor 4 (TLR4) plays an important role in innate immunity. Activation of innate immune response and subsequent chronic low‐grade inflammation are thought to be involved in the pathogenesis of type 2 diabetes. In this study, we aimed to investigate the association of TLR4 vari...
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| Published in | Journal of diabetes Vol. 7; no. 4; pp. 485 - 492 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Blackwell Publishing Ltd
01.07.2015
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 1753-0393 1753-0407 |
| DOI | 10.1111/1753-0407.12206 |
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| Abstract | Background
Toll‐like receptor 4 (TLR4) plays an important role in innate immunity. Activation of innate immune response and subsequent chronic low‐grade inflammation are thought to be involved in the pathogenesis of type 2 diabetes. In this study, we aimed to investigate the association of TLR4 variants with type 2 diabetes in the Chinese population.
Methods
Seven tag single nucleotide polymorphisms (SNPs) of TLR4 based on HapMap Chinese data were genotyped in the Shanghai Chinese, including 3404 type 2 diabetes patients and 3401 controls. The controls were extensively phenotyped for the traits related to glucose metabolism and insulin secretion.
Results
In total participants, we identified that rs10759932 and rs1927911 were associated with type 2 diabetes (odds ratio 1.106, P = 0.009 for rs10759532, odds ratio 1.092, P = 0.013 for rs1927911). rs11536889 showed a trend association with type 2 diabetes (odds ratio 0.957, P = 0.057). This SNP was also associated with 2‐h plasma glucose (P = 0.033) and high‐density lipoprotein‐cholesterol (P = 0.031). In female participants, rs10759932, rs1927911 and rs11536889 were associated with type 2 diabetes (odds ratio 1.176, P = 0.002 for rs10759932, odds ratio 1.136, P = 0.009 for rs1927911, odds ratio 0.882, P = 0.024 for rs11536889). Besides, rs11536889 was significantly associated with 2‐h plasma glucose (P = 0.050) and HOMA‐B (P = 0.046) with adjusting for age and body mass index in female normal subjects.
Conclusions
We conclude that genetic variants of TLR4 are associated with type 2 diabetes in the Chinese population, especially in female subjects.
摘要
背景：
Toll样受体4（toll‐like receptor 4）在固有免疫中发挥重要作用。固有免疫的激活及其后续的慢性低度炎症可能也参与了2型糖尿病的发生。本研究旨在探讨中国人群中TLR4基因多态性与2型糖尿病的相关性。
方法：
研究对象来自中国上海，包括3404例2型糖尿病患者及3401例正常对照者。根据HapMap中国人数据库选取了7个TLR4的标签单核苷酸多态性（single nucleotide polymorphism，SNP），并对其在所有研究对象中进行基因分型。收集对照人群的葡萄糖代谢及胰岛素分泌相关的详细表型用于数量性状分析。
结果：
在总人群中，发现rs10759932和rs1927911均与2型糖尿病显著相关（rs10759932：OR，1.106，P = 0.009；rs1927911：OR，1.092，P = 0.013）。rs11536889与2型糖尿病有相关趋势（OR，0.957，P = 0.057），此位点与2小时血糖（P = 0.033）及高密度脂蛋白（P = 0.031）亦相关。在女性人群中，rs10759932、rs1927911及rs11536889均与2型糖尿病显著相关（rs10759932：OR，1.176，P = 0.002；rs1927911：OR，1.136，P = 0.009；rs11536889：OR，0.882，P = 0.024）。此外，在女性对照人群中，校正年龄及BMI后，rs11536889与2小时血糖（P = 0.050）及HOMA‐B（P = 0.046）显著相关。
结论：
在中国人群，尤其是女性人群中，TLR4基因变异与2型糖尿病发生风险相关。 |
|---|---|
| AbstractList | Background
Toll‐like receptor 4 (TLR4) plays an important role in innate immunity. Activation of innate immune response and subsequent chronic low‐grade inflammation are thought to be involved in the pathogenesis of type 2 diabetes. In this study, we aimed to investigate the association of TLR4 variants with type 2 diabetes in the Chinese population.
Methods
Seven tag single nucleotide polymorphisms (SNPs) of TLR4 based on HapMap Chinese data were genotyped in the Shanghai Chinese, including 3404 type 2 diabetes patients and 3401 controls. The controls were extensively phenotyped for the traits related to glucose metabolism and insulin secretion.
Results
In total participants, we identified that rs10759932 and rs1927911 were associated with type 2 diabetes (odds ratio 1.106, P = 0.009 for rs10759532, odds ratio 1.092, P = 0.013 for rs1927911). rs11536889 showed a trend association with type 2 diabetes (odds ratio 0.957, P = 0.057). This SNP was also associated with 2‐h plasma glucose (P = 0.033) and high‐density lipoprotein‐cholesterol (P = 0.031). In female participants, rs10759932, rs1927911 and rs11536889 were associated with type 2 diabetes (odds ratio 1.176, P = 0.002 for rs10759932, odds ratio 1.136, P = 0.009 for rs1927911, odds ratio 0.882, P = 0.024 for rs11536889). Besides, rs11536889 was significantly associated with 2‐h plasma glucose (P = 0.050) and HOMA‐B (P = 0.046) with adjusting for age and body mass index in female normal subjects.
Conclusions
We conclude that genetic variants of TLR4 are associated with type 2 diabetes in the Chinese population, especially in female subjects.
摘要
背景：
Toll样受体4（toll‐like receptor 4）在固有免疫中发挥重要作用。固有免疫的激活及其后续的慢性低度炎症可能也参与了2型糖尿病的发生。本研究旨在探讨中国人群中TLR4基因多态性与2型糖尿病的相关性。
方法：
研究对象来自中国上海，包括3404例2型糖尿病患者及3401例正常对照者。根据HapMap中国人数据库选取了7个TLR4的标签单核苷酸多态性（single nucleotide polymorphism，SNP），并对其在所有研究对象中进行基因分型。收集对照人群的葡萄糖代谢及胰岛素分泌相关的详细表型用于数量性状分析。
结果：
在总人群中，发现rs10759932和rs1927911均与2型糖尿病显著相关（rs10759932：OR，1.106，P = 0.009；rs1927911：OR，1.092，P = 0.013）。rs11536889与2型糖尿病有相关趋势（OR，0.957，P = 0.057），此位点与2小时血糖（P = 0.033）及高密度脂蛋白（P = 0.031）亦相关。在女性人群中，rs10759932、rs1927911及rs11536889均与2型糖尿病显著相关（rs10759932：OR，1.176，P = 0.002；rs1927911：OR，1.136，P = 0.009；rs11536889：OR，0.882，P = 0.024）。此外，在女性对照人群中，校正年龄及BMI后，rs11536889与2小时血糖（P = 0.050）及HOMA‐B（P = 0.046）显著相关。
结论：
在中国人群，尤其是女性人群中，TLR4基因变异与2型糖尿病发生风险相关。 |
| Author | Jia, Weiping Jiang, Feng Sun, Xue Yan, Jing Peng, Danfeng Chen, Miao Zhang, Rong Tang, Shanshan Luo, Yi Hu, Cheng |
| Author_xml | – sequence: 1 givenname: Danfeng surname: Peng fullname: Peng, Danfeng organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 2 givenname: Feng surname: Jiang fullname: Jiang, Feng organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 3 givenname: Rong surname: Zhang fullname: Zhang, Rong organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 4 givenname: Shanshan surname: Tang fullname: Tang, Shanshan organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 5 givenname: Miao surname: Chen fullname: Chen, Miao organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 6 givenname: Jing surname: Yan fullname: Yan, Jing organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 7 givenname: Xue surname: Sun fullname: Sun, Xue organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 8 givenname: Yi surname: Luo fullname: Luo, Yi organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 9 givenname: Cheng surname: Hu fullname: Hu, Cheng email: wpjia@sjtu.edu.cnalfredhc@sjtu.edu.cn organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China – sequence: 10 givenname: Weiping surname: Jia fullname: Jia, Weiping email: wpjia@sjtu.edu.cnalfredhc@sjtu.edu.cn organization: Shanghai Diabetes Institute, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Center for Diabetes, Shanghai Key Clinic Center for Metabolic Diseases, Department of Endocrinology and Metabolism, Shanghai Jiao Tong University Affiliated Sixth People's Hospital, Shanghai, China |
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| References | Devaraj S, Tobias P, Jialal I. Knockout of toll-like receptor-4 attenuates the pro-inflammatory state of diabetes. Cytokine. 2011; 55: 441-445. Amyot J, Semache M, Ferdaoussi M, Fontes G, Poitout V. Lipopolysaccharides impair insulin gene expression in isolated islets of Langerhans via Toll-Like Receptor-4 and NF-kappaB signalling. PLoS One. 2012; 7: e36200. Hoshino K, Takeuchi O, Kawai T et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol. 1999; 162: 3749-3752. Bagarolli RA, Saad MJ, Saad ST. Toll-like receptor 4 and inducible nitric oxide synthase gene polymorphisms are associated with Type 2 diabetes. J Diabetes Complications. 2010; 24: 192-198. Yang SH, Dou KF, Song WJ. Prevalence of diabetes among men and women in China. N Engl J Med. 2010; 362: 2425-2426, author reply 6. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28: 412-419. Zu L, He J, Jiang H, Xu C, Pu S, Xu G. Bacterial endotoxin stimulates adipose lipolysis via toll-like receptor 4 and extracellular signal-regulated kinase pathway. J Biol Chem. 2009; 284: 5915-5926. Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr. 2006; 83: 461S-465. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat Immunol. 2010; 11: 373-384. Jia WP, Pang C, Chen L et al. Epidemiological characteristics of diabetes mellitus and impaired glucose regulation in a Chinese adult population: The Shanghai Diabetes Studies, a cross-sectional 3-year follow-up study in Shanghai urban communities. Diabetologia. 2007; 50: 286-292. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. The c-Jun N-terminal kinase mediates the induction of oxidative stress and insulin resistance by palmitate and toll-like receptor 2 and 4 ligands in 3T3-L1 adipocytes. Horm Metab Res. 2009; 41: 523-530. Liu F, Lu W, Qian Q, Qi W, Hu J, Feng B. Frequency of TLR 2, 4, and 9 gene polymorphisms in Chinese population and their susceptibility to type 2 diabetes and coronary artery disease. J Biomed Biotechnol. 2012; 2012: 373945. Ahmad R, Al-Mass A, Atizado V et al. Elevated expression of the toll like receptors 2 and 4 in obese individuals: Its significance for obesity-induced inflammation. J Inflamm. 2012; 9: 48. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest. 2006; 116: 1793-1801. Cai H, Cai J, Tao G. Association of toll-like receptor 4 polymorphisms with type 2 diabetes mellitus. APMIS. 2013; 121: 605-611. Saberi M, Woods NB, de Luca C et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 2009; 10: 419-429. Kumagai Y, Akira S. Identification and functions of pattern-recognition receptors. J Allergy Clin Immunol. 2010; 125: 985-992. Fu XD, Sun XQ, Wang HY, Guo JF, Zhang GZ, Xu QH. Genetic polymorphisms of the TLR4 gene and their association with susceptibility to type 2 diabetes mellitus in the Chinese population. Genet Mol Res. 2013; 12: 3813-3820. Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care. 2010; 33: 861-868. Leung TF, Tang NL, Wong GW, Fok TF. CD14 and toll-like receptors: Potential contribution of genetic factors and mechanisms to inflammation and allergy. Curr Drug Targets Inflamm Allergy. 2005; 4: 169-175. Jiang ZS, Wang SX, Jia HX, Wang J, Liu YT. Association of toll-like receptor 4 polymorphisms with type 2 diabetes mellitus. Inflammation. 2013; 36: 251-257. Hu C, Wang C, Zhang R et al. Association of genetic variants of NOS1AP with type 2 diabetes in a Chinese population. Diabetologia. 2010; 53: 290-298. Pal D, Dasgupta S, Kundu R et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med. 2012; 18: 1279-1285. Okamura Y, Watari M, Jerud ES et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001; 276: 10229-10233. Weyrich P, Staiger H, Stancakova A et al. The D299G/T399I Toll-like receptor 4 variant associates with body and liver fat: Results from the TULIP and METSIM Studies. PLoS One. 2010; 5: e13980. Cook DN, Pisetsky DS, Schwartz DA. Toll-like receptors in the pathogenesis of human disease. Nat Immunol. 2004; 5: 975-979. Pickup JC, Crook MA. Is type II diabetes mellitus a disease of the innate immune system? Diabetologia. 1998; 41: 1241-1248. Manolakis AC, Kapsoritakis AN, Tiaka EK et al. TLR4 gene polymorphisms: Evidence for protection against type 2 diabetes but not for diabetes-associated ischaemic heart disease. Eur J Endocrinol. 2011; 165: 261-267. 2010; 11 2010; 33 1985; 28 2010; 53 2009; 41 2012; 2012 2010; 125 1999; 162 2011; 55 2010; 362 2004; 5 2012; 18 2007; 50 2013; 121 1998; 41 2006; 116 2001; 276 2013; 36 2009; 10 2006; 83 2010; 24 2013; 12 2005; 4 2009; 284 2012; 7 2010; 5 2011; 165 2012; 9 |
| References_xml | – reference: Hu C, Wang C, Zhang R et al. Association of genetic variants of NOS1AP with type 2 diabetes in a Chinese population. Diabetologia. 2010; 53: 290-298. – reference: Cook DN, Pisetsky DS, Schwartz DA. Toll-like receptors in the pathogenesis of human disease. Nat Immunol. 2004; 5: 975-979. – reference: Amyot J, Semache M, Ferdaoussi M, Fontes G, Poitout V. Lipopolysaccharides impair insulin gene expression in isolated islets of Langerhans via Toll-Like Receptor-4 and NF-kappaB signalling. PLoS One. 2012; 7: e36200. – reference: Leung TF, Tang NL, Wong GW, Fok TF. CD14 and toll-like receptors: Potential contribution of genetic factors and mechanisms to inflammation and allergy. Curr Drug Targets Inflamm Allergy. 2005; 4: 169-175. – reference: Zu L, He J, Jiang H, Xu C, Pu S, Xu G. Bacterial endotoxin stimulates adipose lipolysis via toll-like receptor 4 and extracellular signal-regulated kinase pathway. J Biol Chem. 2009; 284: 5915-5926. – reference: Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat Immunol. 2010; 11: 373-384. – reference: Pickup JC, Crook MA. Is type II diabetes mellitus a disease of the innate immune system? Diabetologia. 1998; 41: 1241-1248. – reference: Jia WP, Pang C, Chen L et al. Epidemiological characteristics of diabetes mellitus and impaired glucose regulation in a Chinese adult population: The Shanghai Diabetes Studies, a cross-sectional 3-year follow-up study in Shanghai urban communities. Diabetologia. 2007; 50: 286-292. – reference: Liu F, Lu W, Qian Q, Qi W, Hu J, Feng B. Frequency of TLR 2, 4, and 9 gene polymorphisms in Chinese population and their susceptibility to type 2 diabetes and coronary artery disease. J Biomed Biotechnol. 2012; 2012: 373945. – reference: Hoshino K, Takeuchi O, Kawai T et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol. 1999; 162: 3749-3752. – reference: Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. The c-Jun N-terminal kinase mediates the induction of oxidative stress and insulin resistance by palmitate and toll-like receptor 2 and 4 ligands in 3T3-L1 adipocytes. Horm Metab Res. 2009; 41: 523-530. – reference: Yang SH, Dou KF, Song WJ. Prevalence of diabetes among men and women in China. N Engl J Med. 2010; 362: 2425-2426, author reply 6. – reference: Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr. 2006; 83: 461S-465. – reference: Kumagai Y, Akira S. Identification and functions of pattern-recognition receptors. J Allergy Clin Immunol. 2010; 125: 985-992. – reference: Pal D, Dasgupta S, Kundu R et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med. 2012; 18: 1279-1285. – reference: Manolakis AC, Kapsoritakis AN, Tiaka EK et al. TLR4 gene polymorphisms: Evidence for protection against type 2 diabetes but not for diabetes-associated ischaemic heart disease. Eur J Endocrinol. 2011; 165: 261-267. – reference: Ahmad R, Al-Mass A, Atizado V et al. Elevated expression of the toll like receptors 2 and 4 in obese individuals: Its significance for obesity-induced inflammation. J Inflamm. 2012; 9: 48. – reference: Jiang ZS, Wang SX, Jia HX, Wang J, Liu YT. Association of toll-like receptor 4 polymorphisms with type 2 diabetes mellitus. Inflammation. 2013; 36: 251-257. – reference: Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care. 2010; 33: 861-868. – reference: Devaraj S, Tobias P, Jialal I. Knockout of toll-like receptor-4 attenuates the pro-inflammatory state of diabetes. Cytokine. 2011; 55: 441-445. – reference: Fu XD, Sun XQ, Wang HY, Guo JF, Zhang GZ, Xu QH. Genetic polymorphisms of the TLR4 gene and their association with susceptibility to type 2 diabetes mellitus in the Chinese population. Genet Mol Res. 2013; 12: 3813-3820. – reference: Weyrich P, Staiger H, Stancakova A et al. The D299G/T399I Toll-like receptor 4 variant associates with body and liver fat: Results from the TULIP and METSIM Studies. PLoS One. 2010; 5: e13980. – reference: Saberi M, Woods NB, de Luca C et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 2009; 10: 419-429. – reference: Bagarolli RA, Saad MJ, Saad ST. Toll-like receptor 4 and inducible nitric oxide synthase gene polymorphisms are associated with Type 2 diabetes. J Diabetes Complications. 2010; 24: 192-198. – reference: Cai H, Cai J, Tao G. Association of toll-like receptor 4 polymorphisms with type 2 diabetes mellitus. APMIS. 2013; 121: 605-611. – reference: Okamura Y, Watari M, Jerud ES et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001; 276: 10229-10233. – reference: Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28: 412-419. – reference: Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. 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Toll‐like receptor 4 (TLR4) plays an important role in innate immunity. Activation of innate immune response and subsequent chronic low‐grade... |
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| SubjectTerms | genetic polymorphisms toll-like receptor 4 type 2 diabetes mellitus 关键词：基因多态性，toll样受体4，2型糖尿病 |
| Title | Association of Toll-like Receptor 4 Gene polymorphisms with susceptibility to type 2 diabetes mellitus in the Chinese population Toll样受体4基因多态性与中国人群2型糖尿病易感性的关联研究 |
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