Association between polymorphism in uncoupling proteins and type 2 diabetes in a northwestern Colombian population
Keywords:
Diabetes mellitus/genetics, insulin resistance, obesity, polymorphism, genotype, haplotypes
Abstract
Introduction. The uncoupling proteins belong to the family of anion transporting proteins which uncouple the ATP production from the mitochondrial respiration, cause proton leakage through the inner mitochondrial membrane, and release energy as heat. Although uncoupling protein function has not been well established, specific polymorphisms in these proteins have been associated with type 2 diabetes mellitus, obesity and insulin resistance.Objective. The association was assessed between the polymorphisms in uncoupling protein genes 1, 2 and 3 genes and type 2 diabetes mellitus.
Materials and methods. In a northwestern Colombian population, 545 diabetes cases and 449 controls were investigated for presence of 14 polymorphisms in uncoupling protein genes (3826A/G, ID 45, 2723T/A, 1957G/A, 866G/A, and 55C/T) by PCR and PCR-RFLP. Single associations were evaluated by chi-square test, and bayesian logistic regression analysis was done including as covariates the individual admixture estimates obtained by 54 informative markers for European, African and Amerind ancestry.
Results. Association between type 2 diabetes mellitus and the polymorphisms 3826A (OR=0.78; 95%CI=0.63-0.97; p=0.02) and 55C (OR=1.41; 95%CI=1.04-1.92; p=0.03) and the haplotype D45, 866G, 1957G, 2723T, and 55C (OR=1.26; 95%CI=1.02-1.56; p=0.03) were found. These associations remained after adjustment using individual genetic admixture estimates.
Conclusion. Some alleles of uncoupling protein genes 1, 2 and 3, and their haplotypes confer risk to type 2 diabetes in a northwestern Colombian population.
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References
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2. McCarthy MI. Progress in defining the molecular basis of type 2 diabetes mellitus through susceptibility-gene identification. Hum Mol Genet. 2004;13:33-41.
3. Tusie Luna MT. Genes and type 2 diabetes mellitus. Arch Med Res. 2005;36:210-22.
4. Sokolova IM, Sokolov EP. Evolution of mitochondrial uncoupling proteins: novel invertebrate UCP homologues suggest early evolutionary divergence of the UCP family. FEBS Lett. 2005;579:313-7.
5. Li Y, Maedler K, Shu L, Haataja L. UCP-2 and UCP-3 proteins are differentially regulated in pancreatic beta-cells. PLoS ONE. 2008;3:e1397.
6. Nedergaard J, Cannon B. The ‘novel’ ‘uncoupling’ proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol. 2003;88:65-84.
7. Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, et al. The biology of mitochondrial uncoupling proteins. Diabetes. 2004;53 (Suppl.1):S130-5.
8. Pawade T, Ho PW, Kwok KH, Chu AC, Ho SL, Ramsden DB. Uncoupling proteins: targets of endocrine disruptors? Mol Cell Endocrinol. 2005;244:79-86.
9. Sale MM, Hsu FC, Palmer ND, Gordon CJ, Keene KL, Borgerink HM, et al. The uncoupling protein 1 gene, UCP1, is expressed in mammalian islet cells and associated with acute insulin response to glucose in African American families from the IRAS Family Study. BMC Endocr Disord. 2007;7:1.
10. Chan CB, Saleh MC, Koshkin V, Wheeler MB. Uncoupling protein 2 and islet function. Diabetes 2004;53 (Suppl.1):S136-42.
11. Hsu YH, Niu T, Song Y, Tinker L, Kuller LH, Liu S. Genetic variants in the UCP2-UCP3 gene cluster and risk of diabetes in the Women’s Health Initiative Observational Study. Diabetes. 2008;57:1101-7.
12. Gable DR, Stephens JW, Cooper JA, Miller GJ, Humphries SE. Variation in the UCP2-UCP3 gene cluster predicts the development of type 2 diabetes in healthy middle-aged men. Diabetes. 2006;55:1504-11.
13. Shin HD, Kim KS, Cha MH, Yoon Y. The effects of UCP-1 polymorphisms on obesity phenotypes among Korean female subjects. Biochem Biophys Res Commun. 2005;335:624-30.
14. Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962;14:353-62.
15. Chakraborty R, Ferrell RE, Stern MP, Haffner SM, Hazuda HP, Rosenthal M. Relationship of prevalence of non-insulin-dependent diabetes mellitus to Amerindian admixture in the Mexican Americans of San Antonio, Texas. Genet Epidemiol. 1986;3:435-54.
16. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, et al. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults. The Third National Health and Nutrition Examination Survey, 1988-1994. Diabetes Care. 1998;21:518-24.
17. Williams RC, Long JC, Hanson RL, Sievers ML, Knowler WC. Individual estimates of European genetic admixture associated with lower body-mass index, plasma glucose, and prevalence of type 2 diabetes in Pima Indians. Am J Hum Genet. 2000;66:527-38.
18. Sandoval C, De la Hoz A, Yunis E. Estructura genética de la población colombiana. Revista Facultad de Medicina Universidad Nacional de Colombia. 1993;41:3-14.
19. Bedoya G, Montoya P, García J, Soto I, Bourgeois S, Carvajal L, et al. Admixture dynamics in Hispanics: a shift in the nuclear genetic ancestry of a South American population isolate. Proc Natl Acad Sci USA. 2006;103:7234-9.
20. Gower BA, Fernández JR, Beasley TM, Shriver MD, Goran MI. Using genetic admixture to explain racial differences in insulin-related phenotypes. Diabetes. 2003;52:1047-51.
21. Hoggart CJ, Parra EJ, Shriver MD, Bonilla C, Kittles RA, Clayton DG, et al. Control of confounding of genetic associations in stratified populations. Am J Hum Genet. 2003;72:1492-504.
22. Parra EJ, Hoggart CJ, Bonilla C, Dios S, Norris JM, Marshall JA, et al. Relation of type 2 diabetes to individual admixture and candidate gene polymorphisms in the Hispanic American population of San Luis Valley, Colorado. J Med Genet. 2004;41:e116.
23. The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus Diabetes Care. 2002;25.
24. Bedoya G, García J, Montoya P, Rojas W, Amézquita ME, Soto I, et al. Análisis de isonimia entre poblaciones del noroeste de Colombia. Biomédica. 2006;26:538-45.
25. Shriver MD, Smith MW, Jin L, Marcini A, Akey JM, Deka R, et al. Ethnic-affiliation estimation by use of population-specific DNA markers. Am J Hum Genet. 1997;60:957-64.
26. Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995;86.
27. Schneider S, Roessli D, Excoffier L. Arlequin: A software for population genetics data analysis. Versión 2000. Ginebra: Laboratorio de Genética y Biometría, Departamento de Antropología, Universidad de Ginebra; 2000.
28. McKeigue PM, Carpenter JR, Parra EJ, Shriver MD. Estimation of admixture and detection of linkage in admixed populations by a Bayesian approach: application to African-American populations. Ann Hum Genet. 2000;64:171-86.
29. Nagai N, Sakane N, Ueno LM, Hamada T, Moritani T. The -3826 A-->G variant of the uncoupling protein-1 gene diminishes postprandial thermogenesis after a high fat meal in healthy boys. J Clin Endocrinol Metab. 2003;88:5661-7.
30. Forga L, Corbalan M, Marti A, Fuentes C, Martínez-González MA, Martínez A. Influencia del polimorfismo -3826 A Æ G en el gen de la UCP1 sobre los componentes del síndrome metabólico. An Sist Sanit Navar. 2003;26:231-6.
31. Heilbronn LK, Kind KL, Pancewicz E, Morris AM, Noakes M, Clifton PM. Association of -3826 G variant in uncoupling protein-1 with increased BMI in overweight Australian women. Diabetologia. 2000;43:242-4.
32. Kim KS, Cho DY, Kim YJ, Choi SM, Kim JY, Shin SU, et al. The finding of new genetic polymorphism of UCP-1 A-1766G and its effects on body fat accumulation. Biochim Biophys Acta. 2005;1741:149-55.
33. Salopuro T, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, et al. Common variants in beta2- and beta3-adrenergic receptor genes and uncoupling protein 1 as predictors of the risk for type 2 diabetes and body weight changes. The Finnish Diabetes Prevention Study. Clin Genet. 2004;66:365-7.
34. Esterbauer H, Oberkofler H, Liu YM, Breban D, Hell E, Krempler F, et al. Uncoupling protein-1 mRNA expression in obese human subjects: the role of sequence variations at the uncoupling protein-1 gene locus. J Lipid Res. 1998;39:834-44.
35. Nakazaki M, Kakei M, Ishihara H, Koriyama N, Hashiguchi H, Aso K, et al. Association of upregulated activity of K(ATP) channels with impaired insulin secretion in UCP1-expressing insulinoma cells. J Physiol. 2002;540:781-9.
36. Bernal-Mizrachi C, Weng S, Li B, Nolte LA, Feng C, Coleman T, et al. Respiratory uncoupling lowers blood pressure through a leptin-dependent mechanism in genetically obese mice. Arterioscler Thromb Vasc Biol. 2002;22:961-8.
37. Carroll AM, Porter RK. Starvation-sensitive UCP 3 protein expression in thymus and spleen mitochondria. Biochim Biophys Acta. 2004;1700:145-50.
38. Lengacher S, Magistretti PJ, Pellerin L. Quantitative rt-PCR analysis of uncoupling protein isoforms in mouse brain cortex: methodological optimization and comparison of expression with brown adipose tissue and skeletal muscle. J Cereb Blood Flow Metab. 2004;24:780-8.
39. Moulin K, Arnaud E, Nibbelink M, Viguerie-Bascands N, Penicaud L, Casteilla L. Cloning of BUG demonstrates the existence of a brown preadipocyte distinct from a white one. Int J Obes Relat Metab Disord. 2001;25:1431-41.
40. Villarroya F, Iglesias R, Giralt M. PPARs in the control of uncoupling proteins gene expression. PPAR Res. 2007;2007:74364.
41. Meirhaeghe A, Amouyel P, Helbecque N, Cottel D, Otabe S, Froguel P, et al. An uncoupling protein 3 gene polymorphism associated with a lower risk of developing type II diabetes and with atherogenic lipid profile in a French cohort. Diabetologia. 2000;43:1424-8.
42. Damcott CM, Feingold E, Moffett SP, Barmada MM, Marshall JA, Hamman RF, et al. Genetic variation in uncoupling protein 3 is associated with dietary intake and body composition in females. Metabolism. 2004;53:458-64.
43. Schrauwen P, Xia J, Walder K, Snitker S, Ravussin E. A novel polymorphism in the proximal UCP3 promoter region: effect on skeletal muscle UCP3 mRNA expression and obesity in male non-diabetic Pima Indians. Int J Obes Relat Metab Disord. 1999;23:1242-5.
44. Krook A, Digby J, O’Rahilly S, Zierath JR, Wallberg-Henriksson H. Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients. Diabetes. 1998;47:1528-31.
45. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, et al. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature. 2000;406:415-8.
46. Choi CS, Fillmore JJ, Kim JK, Liu ZX, Kim S, Collier EF, et al. Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest. 2007;117:1995-2003.
47. Esterbauer H, Schneitler C, Oberkofler H, Ebenbichler C, Paulweber B, Sandhofer F, et al. A common polymorphism in the promoter of UCP2 is associated with decreased risk of obesity in middle-aged humans. Nat Genet. 2001;28:178-83.
48. Ochoa MC, Santos JL, Azcona C, Moreno-Aliaga MJ, Martínez-González MA, Martínez JA, et al. Association between obesity and insulin resistance with UCP2-UCP3 gene variants in Spanish children and adolescents. Mol Genet Metab. 2007;92:351-8.
49. Aschner P, King H, Triana de Torrado M, Rodríguez BM. Glucose intolerance in Colombia. A population-based survey in an urban community. Diabetes Care. 1993;16:90-3.
50. Mejía S, Vélez A, Buriticá O, Arango M, Del-Río J. La política farmacéutica nacional en Colombia y la reforma de la seguridad social: acceso y uso racional de medicamentos. Cad Saude Publica. 2002;18:1025-39.
51. Qi L, Hu FB, Hu G. Genes, environment, and interactions in prevention of type 2 diabetes: a focus on physical activity and lifestyle changes. Curr Mol Med. 2008;8:519-32.
52. Colditz GA, Willett WC, Rotnitzky A, Manson JE. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med. 1995;122:481-6.
53. Leahy JL. Pathogenesis of type 2 diabetes mellitus. Arch Med Res. 2005;36:197-209.
54. Rothman KJ, Greenland S. Modern Epidemiology. Second edition. Filadelfia, EU: Lippincott-Raven; 1998.
55. Cheurfa N, Dubois-Laforgue D, Ferrarezi DA, Reis AF, Brenner GM, Bouche C, et al. The common -866G>A variant in the promoter of UCP2 is associated with decreased risk of coronary artery disease in type 2 diabetic men. Diabetes. 2008;57:1063-8.
2. McCarthy MI. Progress in defining the molecular basis of type 2 diabetes mellitus through susceptibility-gene identification. Hum Mol Genet. 2004;13:33-41.
3. Tusie Luna MT. Genes and type 2 diabetes mellitus. Arch Med Res. 2005;36:210-22.
4. Sokolova IM, Sokolov EP. Evolution of mitochondrial uncoupling proteins: novel invertebrate UCP homologues suggest early evolutionary divergence of the UCP family. FEBS Lett. 2005;579:313-7.
5. Li Y, Maedler K, Shu L, Haataja L. UCP-2 and UCP-3 proteins are differentially regulated in pancreatic beta-cells. PLoS ONE. 2008;3:e1397.
6. Nedergaard J, Cannon B. The ‘novel’ ‘uncoupling’ proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol. 2003;88:65-84.
7. Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, et al. The biology of mitochondrial uncoupling proteins. Diabetes. 2004;53 (Suppl.1):S130-5.
8. Pawade T, Ho PW, Kwok KH, Chu AC, Ho SL, Ramsden DB. Uncoupling proteins: targets of endocrine disruptors? Mol Cell Endocrinol. 2005;244:79-86.
9. Sale MM, Hsu FC, Palmer ND, Gordon CJ, Keene KL, Borgerink HM, et al. The uncoupling protein 1 gene, UCP1, is expressed in mammalian islet cells and associated with acute insulin response to glucose in African American families from the IRAS Family Study. BMC Endocr Disord. 2007;7:1.
10. Chan CB, Saleh MC, Koshkin V, Wheeler MB. Uncoupling protein 2 and islet function. Diabetes 2004;53 (Suppl.1):S136-42.
11. Hsu YH, Niu T, Song Y, Tinker L, Kuller LH, Liu S. Genetic variants in the UCP2-UCP3 gene cluster and risk of diabetes in the Women’s Health Initiative Observational Study. Diabetes. 2008;57:1101-7.
12. Gable DR, Stephens JW, Cooper JA, Miller GJ, Humphries SE. Variation in the UCP2-UCP3 gene cluster predicts the development of type 2 diabetes in healthy middle-aged men. Diabetes. 2006;55:1504-11.
13. Shin HD, Kim KS, Cha MH, Yoon Y. The effects of UCP-1 polymorphisms on obesity phenotypes among Korean female subjects. Biochem Biophys Res Commun. 2005;335:624-30.
14. Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962;14:353-62.
15. Chakraborty R, Ferrell RE, Stern MP, Haffner SM, Hazuda HP, Rosenthal M. Relationship of prevalence of non-insulin-dependent diabetes mellitus to Amerindian admixture in the Mexican Americans of San Antonio, Texas. Genet Epidemiol. 1986;3:435-54.
16. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, et al. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults. The Third National Health and Nutrition Examination Survey, 1988-1994. Diabetes Care. 1998;21:518-24.
17. Williams RC, Long JC, Hanson RL, Sievers ML, Knowler WC. Individual estimates of European genetic admixture associated with lower body-mass index, plasma glucose, and prevalence of type 2 diabetes in Pima Indians. Am J Hum Genet. 2000;66:527-38.
18. Sandoval C, De la Hoz A, Yunis E. Estructura genética de la población colombiana. Revista Facultad de Medicina Universidad Nacional de Colombia. 1993;41:3-14.
19. Bedoya G, Montoya P, García J, Soto I, Bourgeois S, Carvajal L, et al. Admixture dynamics in Hispanics: a shift in the nuclear genetic ancestry of a South American population isolate. Proc Natl Acad Sci USA. 2006;103:7234-9.
20. Gower BA, Fernández JR, Beasley TM, Shriver MD, Goran MI. Using genetic admixture to explain racial differences in insulin-related phenotypes. Diabetes. 2003;52:1047-51.
21. Hoggart CJ, Parra EJ, Shriver MD, Bonilla C, Kittles RA, Clayton DG, et al. Control of confounding of genetic associations in stratified populations. Am J Hum Genet. 2003;72:1492-504.
22. Parra EJ, Hoggart CJ, Bonilla C, Dios S, Norris JM, Marshall JA, et al. Relation of type 2 diabetes to individual admixture and candidate gene polymorphisms in the Hispanic American population of San Luis Valley, Colorado. J Med Genet. 2004;41:e116.
23. The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus Diabetes Care. 2002;25.
24. Bedoya G, García J, Montoya P, Rojas W, Amézquita ME, Soto I, et al. Análisis de isonimia entre poblaciones del noroeste de Colombia. Biomédica. 2006;26:538-45.
25. Shriver MD, Smith MW, Jin L, Marcini A, Akey JM, Deka R, et al. Ethnic-affiliation estimation by use of population-specific DNA markers. Am J Hum Genet. 1997;60:957-64.
26. Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995;86.
27. Schneider S, Roessli D, Excoffier L. Arlequin: A software for population genetics data analysis. Versión 2000. Ginebra: Laboratorio de Genética y Biometría, Departamento de Antropología, Universidad de Ginebra; 2000.
28. McKeigue PM, Carpenter JR, Parra EJ, Shriver MD. Estimation of admixture and detection of linkage in admixed populations by a Bayesian approach: application to African-American populations. Ann Hum Genet. 2000;64:171-86.
29. Nagai N, Sakane N, Ueno LM, Hamada T, Moritani T. The -3826 A-->G variant of the uncoupling protein-1 gene diminishes postprandial thermogenesis after a high fat meal in healthy boys. J Clin Endocrinol Metab. 2003;88:5661-7.
30. Forga L, Corbalan M, Marti A, Fuentes C, Martínez-González MA, Martínez A. Influencia del polimorfismo -3826 A Æ G en el gen de la UCP1 sobre los componentes del síndrome metabólico. An Sist Sanit Navar. 2003;26:231-6.
31. Heilbronn LK, Kind KL, Pancewicz E, Morris AM, Noakes M, Clifton PM. Association of -3826 G variant in uncoupling protein-1 with increased BMI in overweight Australian women. Diabetologia. 2000;43:242-4.
32. Kim KS, Cho DY, Kim YJ, Choi SM, Kim JY, Shin SU, et al. The finding of new genetic polymorphism of UCP-1 A-1766G and its effects on body fat accumulation. Biochim Biophys Acta. 2005;1741:149-55.
33. Salopuro T, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, et al. Common variants in beta2- and beta3-adrenergic receptor genes and uncoupling protein 1 as predictors of the risk for type 2 diabetes and body weight changes. The Finnish Diabetes Prevention Study. Clin Genet. 2004;66:365-7.
34. Esterbauer H, Oberkofler H, Liu YM, Breban D, Hell E, Krempler F, et al. Uncoupling protein-1 mRNA expression in obese human subjects: the role of sequence variations at the uncoupling protein-1 gene locus. J Lipid Res. 1998;39:834-44.
35. Nakazaki M, Kakei M, Ishihara H, Koriyama N, Hashiguchi H, Aso K, et al. Association of upregulated activity of K(ATP) channels with impaired insulin secretion in UCP1-expressing insulinoma cells. J Physiol. 2002;540:781-9.
36. Bernal-Mizrachi C, Weng S, Li B, Nolte LA, Feng C, Coleman T, et al. Respiratory uncoupling lowers blood pressure through a leptin-dependent mechanism in genetically obese mice. Arterioscler Thromb Vasc Biol. 2002;22:961-8.
37. Carroll AM, Porter RK. Starvation-sensitive UCP 3 protein expression in thymus and spleen mitochondria. Biochim Biophys Acta. 2004;1700:145-50.
38. Lengacher S, Magistretti PJ, Pellerin L. Quantitative rt-PCR analysis of uncoupling protein isoforms in mouse brain cortex: methodological optimization and comparison of expression with brown adipose tissue and skeletal muscle. J Cereb Blood Flow Metab. 2004;24:780-8.
39. Moulin K, Arnaud E, Nibbelink M, Viguerie-Bascands N, Penicaud L, Casteilla L. Cloning of BUG demonstrates the existence of a brown preadipocyte distinct from a white one. Int J Obes Relat Metab Disord. 2001;25:1431-41.
40. Villarroya F, Iglesias R, Giralt M. PPARs in the control of uncoupling proteins gene expression. PPAR Res. 2007;2007:74364.
41. Meirhaeghe A, Amouyel P, Helbecque N, Cottel D, Otabe S, Froguel P, et al. An uncoupling protein 3 gene polymorphism associated with a lower risk of developing type II diabetes and with atherogenic lipid profile in a French cohort. Diabetologia. 2000;43:1424-8.
42. Damcott CM, Feingold E, Moffett SP, Barmada MM, Marshall JA, Hamman RF, et al. Genetic variation in uncoupling protein 3 is associated with dietary intake and body composition in females. Metabolism. 2004;53:458-64.
43. Schrauwen P, Xia J, Walder K, Snitker S, Ravussin E. A novel polymorphism in the proximal UCP3 promoter region: effect on skeletal muscle UCP3 mRNA expression and obesity in male non-diabetic Pima Indians. Int J Obes Relat Metab Disord. 1999;23:1242-5.
44. Krook A, Digby J, O’Rahilly S, Zierath JR, Wallberg-Henriksson H. Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients. Diabetes. 1998;47:1528-31.
45. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, et al. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature. 2000;406:415-8.
46. Choi CS, Fillmore JJ, Kim JK, Liu ZX, Kim S, Collier EF, et al. Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest. 2007;117:1995-2003.
47. Esterbauer H, Schneitler C, Oberkofler H, Ebenbichler C, Paulweber B, Sandhofer F, et al. A common polymorphism in the promoter of UCP2 is associated with decreased risk of obesity in middle-aged humans. Nat Genet. 2001;28:178-83.
48. Ochoa MC, Santos JL, Azcona C, Moreno-Aliaga MJ, Martínez-González MA, Martínez JA, et al. Association between obesity and insulin resistance with UCP2-UCP3 gene variants in Spanish children and adolescents. Mol Genet Metab. 2007;92:351-8.
49. Aschner P, King H, Triana de Torrado M, Rodríguez BM. Glucose intolerance in Colombia. A population-based survey in an urban community. Diabetes Care. 1993;16:90-3.
50. Mejía S, Vélez A, Buriticá O, Arango M, Del-Río J. La política farmacéutica nacional en Colombia y la reforma de la seguridad social: acceso y uso racional de medicamentos. Cad Saude Publica. 2002;18:1025-39.
51. Qi L, Hu FB, Hu G. Genes, environment, and interactions in prevention of type 2 diabetes: a focus on physical activity and lifestyle changes. Curr Mol Med. 2008;8:519-32.
52. Colditz GA, Willett WC, Rotnitzky A, Manson JE. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med. 1995;122:481-6.
53. Leahy JL. Pathogenesis of type 2 diabetes mellitus. Arch Med Res. 2005;36:197-209.
54. Rothman KJ, Greenland S. Modern Epidemiology. Second edition. Filadelfia, EU: Lippincott-Raven; 1998.
55. Cheurfa N, Dubois-Laforgue D, Ferrarezi DA, Reis AF, Brenner GM, Bouche C, et al. The common -866G>A variant in the promoter of UCP2 is associated with decreased risk of coronary artery disease in type 2 diabetic men. Diabetes. 2008;57:1063-8.
How to Cite
1.
Franco-Hincapié L, Duque CE, Parra MV, Gallego N, Villegas A, Ruiz-Linares A, et al. Association between polymorphism in uncoupling proteins and type 2 diabetes in a northwestern Colombian population. biomedica [Internet]. 2009 Mar. 1 [cited 2024 May 12];29(1):108-1. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/46
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