Modulation by dietary fat and carbohydrate of IRS1 association with type 2 diabetes traits in two populations of different ancestries

Ju-Sheng Zheng, Donna K Arnett, Laurence D Parnell, Caren E Smith, Duo Li, Ingrid B Borecki, Katherine L Tucker, José M Ordovás, Chao-Qiang Lai, Ju-Sheng Zheng, Donna K Arnett, Laurence D Parnell, Caren E Smith, Duo Li, Ingrid B Borecki, Katherine L Tucker, José M Ordovás, Chao-Qiang Lai

Abstract

Objective: Insulin receptor substrate 1 (IRS1) is central to insulin signaling pathways. This study aimed to examine the association of IRS1 variants with insulin resistance (IR) and related phenotypes, as well as potential modification by diet.

Research design and methods: Two IRS1 variants (rs7578326 and rs2943641) identified by genome-wide association studies as related to type 2 diabetes were tested for their associations with IR and related traits and interaction with diet in the Genetics of Lipid Lowering Drugs and Diet Network (GOLDN) study (n = 820) and the Boston Puerto Rican Health Study (BPRHS) (n = 844).

Results: Meta-analysis indicated that rs7578326 G-allele carriers and rs2943641 T-allele carriers had a lower risk of IR, type 2 diabetes, and metabolic syndrome (MetS). Significant interactions on IR and MetS were found for these two variants and their haplotypes with diet. In GOLDN, rs7578326 G-allele carriers and rs2943641 T-allele carriers and their haplotype G-T carriers had a significantly lower risk of IR and MetS than noncarriers only when the dietary saturated fatty acid-to-carbohydrate ratio was low (≤ 0.24). In both GOLDN (P = 0.0008) and BPRHS (P = 0.011), rs7578326 G-allele carriers had a lower risk of MetS than noncarriers only when dietary monounsaturated fatty acids were lower than the median intake of each population.

Conclusions: IRS1 variants are associated with IR and related traits and are modulated by diet in two populations of different ancestries. These findings suggest that IRS1 variants have important functions in various metabolic disorders and that dietary factors could modify these associations.

Figures

Figure 1
Figure 1
Interaction of IRS1 variant with dietary MUFA on insulin resistance in the GOLDN and BPRHS populations. Dietary MUFA interacted significantly (P = 0.024) with IRS1 variant rs7578326 on insulin resistance in GOLDN and marginally significantly (P = 0.07) in BPRHS. In both populations, G-allele carriers of rs7578326 had significantly lower HOMA-IR than noncarriers only when dietary MUFA intake was low (≤median intake of each population), but not when MUFA intake was high. P values in GOLDN were adjusted for age, sex, waist circumference, study center, smoking status, alcohol drinking, type 2 diabetes, physical activity, and family relationships. P values in the BPRHS were adjusted for age, sex, waist circumference, smoking status, alcohol drinking, type 2 diabetes, physical activity, and population structure. Number inside the bar indicates the number of subjects in that group. Values are means ± SEM.

References

    1. Centers for Disease Control and Prevention. National Diabetes Fact Sheet: United States 2011 Atlanta, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services, 2011
    1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010;87:4–14
    1. Grundy SM, Cleeman JI, Daniels SR, et al. American Heart Association. National Heart, Lung, and Blood Institute Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005;112:2735–2752
    1. Hindorff LA, Sethupathy P, Junkins HA, et al. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA 2009;106:9362–9367
    1. Voight BF, Scott LJ, Steinthorsdottir V, et al. MAGIC investigators. GIANT Consortium Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat Genet 2010;42:579–589
    1. Cornelis MC, Hu FB. Gene-environment interactions in the development of type 2 diabetes: recent progress and continuing challenges. Annu Rev Nutr 2012;32:245–259
    1. Rung J, Cauchi S, Albrechtsen A, et al. Genetic variant near IRS1 is associated with type 2 diabetes, insulin resistance and hyperinsulinemia. Nat Genet 2009;41:1110–1115
    1. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002;296:1655–1657
    1. Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab 2009;296:E581–E591
    1. Thirone AC, Huang C, Klip A. Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 2006;17:72–78
    1. Yamauchi T, Tobe K, Tamemoto H, et al. Insulin signalling and insulin actions in the muscles and livers of insulin-resistant, insulin receptor substrate 1-deficient mice. Mol Cell Biol 1996;16:3074–3084
    1. Kaburagi Y, Satoh S, Tamemoto H, et al. Role of insulin receptor substrate-1 and pp60 in the regulation of insulin-induced glucose transport and GLUT4 translocation in primary adipocytes. J Biol Chem 1997;272:25839–25844
    1. Qi Q, Bray GA, Smith SR, Hu FB, Sacks FM, Qi L. Insulin receptor substrate 1 gene variation modifies insulin resistance response to weight-loss diets in a 2-year randomized trial: the Preventing Overweight Using Novel Dietary Strategies (POUNDS LOST) trial. Circulation 2011;124:563–571
    1. Ericson U, Rukh G, Stojkovic I, et al. Sex-specific interactions between the IRS1 polymorphism and intakes of carbohydrates and fat on incident type 2 diabetes. Am J Clin Nutr 2013;97:208–216
    1. Lorenzo C, Okoloise M, Williams K, Stern MP, Haffner SM, San Antonio Heart Study The metabolic syndrome as predictor of type 2 diabetes: the San Antonio heart study. Diabetes Care 2003;26:3153–3159
    1. Wilson PWF, D’Agostino RB, Parise H, Sullivan L, Meigs JB. Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation 2005;112:3066–3072
    1. Shen J, Arnett DK, Peacock JM, et al. Interleukin1beta genetic polymorphisms interact with polyunsaturated fatty acids to modulate risk of the metabolic syndrome. J Nutr 2007;137:1846–1851
    1. Ordovas JM, Shen J. Gene-environment interactions and susceptibility to metabolic syndrome and other chronic diseases. J Periodontol 2008;79(Suppl):1508–1513
    1. Corella D, Arnett DK, Tsai MY, et al. The -256T>C polymorphism in the apolipoprotein A-II gene promoter is associated with body mass index and food intake in the genetics of lipid lowering drugs and diet network study. Clin Chem 2007;53:1144–1152
    1. Subar AF, Thompson FE, Kipnis V, et al. Comparative validation of the Block, Willett, and National Cancer Institute food frequency questionnaires : the Eating at America’s Table Study. Am J Epidemiol 2001;154:1089–1099
    1. Thompson FE, Subar AF, Brown CC, et al. Cognitive research enhances accuracy of food frequency questionnaire reports: results of an experimental validation study. J Am Diet Assoc 2002;102:212–225
    1. Salmerón J, Manson JE, Stampfer MJ, Colditz GA, Wing AL, Willett WC. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women. JAMA 1997;277:472–477
    1. Tucker KL, Mattei J, Noel SE, et al. The Boston Puerto Rican Health Study, a longitudinal cohort study on health disparities in Puerto Rican adults: challenges and opportunities. BMC Public Health 2010;10:107.
    1. Lai CQ, Tucker KL, Choudhry S, et al. Population admixture associated with disease prevalence in the Boston Puerto Rican health study. Hum Genet 2009;125:199–209
    1. Tucker KL, Bianchi LA, Maras J, Bermudez OI. Adaptation of a food frequency questionnaire to assess diets of Puerto Rican and non-Hispanic adults. Am J Epidemiol 1998;148:507–518
    1. van Rompay MI, McKeown NM, Castaneda-Sceppa C, Falcón LM, Ordovás JM, Tucker KL. Acculturation and sociocultural influences on dietary intake and health status among Puerto Rican adults in Massachusetts. J Acad Nutr Diet 2012;112:64–74
    1. Tsai MY, Hanson NQ, Straka RJ, et al. Effect of influenza vaccine on markers of inflammation and lipid profile. J Lab Clin Med 2005;145:323–327
    1. Box GEP, Cox DR. An analysis of transformations. J R Stat Soc Series B Stat Methodol 1964;26:211–252
    1. Pérez MS, Tellechea ML, Aranguren F, et al. The rs1801278 G>A polymorphism of IRS-1 is associated with metabolic syndrome in healthy nondiabetic men. Modulation by cigarette smoking status. Diabetes Res Clin Pract 2011;93:e95–e97
    1. Jellema A, Zeegers MPA, Feskens EJM, Dagnelie PC, Mensink RP. Gly972Arg variant in the insulin receptor substrate-1 gene and association with type 2 diabetes: a meta-analysis of 27 studies. Diabetologia 2003;46:990–995
    1. Baroni MG, Leonetti F, Sentinelli F, et al. The G972R variant of the insulin receptor substrate-1 (IRS-1) gene is associated with insulin resistance in “uncomplicated” obese subjects evaluated by hyperinsulinemic-euglycemic clamp. J Endocrinol Invest 2004;27:754–759
    1. Kilpeläinen TO, Zillikens MC, Stančákova A, et al. Genetic variation near IRS1 associates with reduced adiposity and an impaired metabolic profile. Nat Genet 2011;43:753–760
    1. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 2010;375:2267–2277
    1. Willett W, Manson J, Liu S. Glycemic index, glycemic load, and risk of type 2 diabetes. Am J Clin Nutr 2002;76:274S–280S

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj