Interaction between the NOS3 gene and obesity as a determinant of risk of type 2 diabetes: The atherosclerosis risk in communities study

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Bressler, Jan ^a   Pankow, James S ^b   Coresh, Josef ^c   Boerwinkle, Eric ^a,d  

^a UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGED; DIABETES MELLITUS, TYPE 2; FEMALE; GENOTYPE; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE III; OBESITY; PROSPECTIVE STUDIES; RISK FACTORS;

EID: 84894288562     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079466     Document Type: Article

References (73)

1. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339: 229-234. (Pubitemid 28350165)
2. Stern MP, Haffner SM (1986) Body fat distribution and hyperinsulinemia as risk factors for diabetes and cardiovascular disease. Arteriosclerosis 6: 123-130. (Pubitemid 16024120)
3. Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376. (Pubitemid 11169009)
4. Rees DD, Palmer RM, Moncada S (1989) Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci U S A 86: 3375-3378. (Pubitemid 19129614)
5. Marsden PA, Heng HH, Scherer SW, Stewart RJ, Hall AV, et al. (1993) Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem 268: 17478-17488. (Pubitemid 23236991)
6. Yoshimura M, Yasue H, Nakayama M, Shimasaki Y, Sumida H, et al. (1998) A missense Glu298Asp variant in the endothelial nitric oxide synthase gene is associated with coronary spasm in the Japanese. Hum Genet 103: 65-69. (Pubitemid 28398388)
7. Hibi K, Ishigami T, Tamura K, Mizushima S, Nyui N, et al. (1998) Endothelial nitric oxide synthase gene polymorphism and acute myocardial infarction. Hypertension 32: 521-526. (Pubitemid 28429143)
8. Casas JP, Bautista LE, Humphries SE, Hingorani AD (2004) Endothelial nitric oxide synthase genotype and ischemic heart disease: meta-analysis of 26 studies involving 23028 subjects. Circulation 109: 1359-1365. (Pubitemid 38387821)
9. Shimasaki Y, Yasue H, Yoshimura M, Nakayama M, Kugiyama K, et al. (1998) Association of the missense Glu298Asp variant of the endothelial nitric oxide synthase gene with myocardial infarction. J Am Coll Cardiol 31: 1506-1510. (Pubitemid 28273291)
10. Hingorani AD, Liang CF, Fatibene J, Lyon A, Monteith S, et al. (1999) A common variant of the endothelial nitric oxide synthase (Glu298->Asp) is a major risk factor for coronary artery disease in the UK. Circulation 100: 1515-1520. (Pubitemid 29461463)
11. Casas JP, Cavalleri GL, Bautista LE, Smeeth L, Humphries SE, et al. (2006) Endothelial nitric oxide synthase gene polymorphisms and cardiovascular disease: a HuGE review. Am J Epidemiol 164: 921-935. (Pubitemid 44729832)
12. Berger K, Stogbauer F, Stoll M, Wellmann J, Huge A, et al. (2007) The glu298asp polymorphism in the nitric oxide synthase 3 gene is associated with the risk of ischemic stroke in two large independent case-control studies. Hum Genet 121: 169-178. (Pubitemid 46404451)
13. Miyamoto Y, Saito Y, Kajiyama N, Yoshimura M, Shimasaki Y, et al. (1998) Endothelial nitric oxide synthase gene is positively associated with essential hypertension. Hypertension 32: 3-8. (Pubitemid 28324117)
14. Pereira TV, Rudnicki M, Cheung BM, Baum L, Yamada Y, et al. (2007) Three endothelial nitric oxide (NOS3) gene polymorphisms in hypertensive and normotensive individuals: meta-analysis of 53 studies reveals evidence of publication bias. J Hypertens 25: 1763-1774. (Pubitemid 47356613)
15. Misono M, Maeda S, Iemitsu M, Nakata Y, Otsuki T, et al. (2009) Combination of polymorphisms in the beta2-adrenergic receptor and nitric oxide synthase 3 genes increases the risk for hypertension. J Hypertens 27: 1377-1383.
16. Monti LD, Barlassina C, Citterio L, Galluccio E, Berzuini C, et al. (2003) Endothelial nitric oxide synthase polymorphisms are associated with type 2 diabetes and the insulin resistance syndrome. Diabetes 52: 1270-1275. (Pubitemid 36523367)
17. Rahimi Z, Nourozi-Rad R, Rahimi Z, Parsian A (2012) Strong interaction between T allele of endothelial nitric oxide synthase with B1 allele of cholesteryl ester transfer protein TaqIB highly elevates the risk of coronary artery disease and type 2 diabetes mellitus. Hum Genomics 6: 20.
18. Tso AW, Tan KC, Wat NM, Janus ED, Lam TH, et al. (2006) Endothelial nitric oxide synthase G894T (Glu298Asp) polymorphism was predictive of glycemic status in a 5-year prospective study of Chinese subjects with impaired glucose tolerance. Metabolism 55: 1155-1158. (Pubitemid 44215934)
19. Shin Shin Y, Baek SH, Chang KY, Park CW, Yang CW, et al. (2004) Relations between eNOS Glu298Asp polymorphism and progression of diabetic nephropathy. Diabetes Res Clin Pract 65: 257-265. (Pubitemid 39141182)
20. Thameem F, Puppala S, Arar NH, Stern MP, Blangero J, et al. (2008) Endothelial nitric oxide synthase (eNOS) gene polymorphisms and their association with type 2 diabetes-related traits in Mexican Americans. Diab Vasc Dis Res 5: 109-113. (Pubitemid 351839282)
21. Awata T, Neda T, Iizuka H, Kurihara S, Ohkubo T, et al. (2004) Endothelial nitric oxide synthase gene is associated with diabetic macular edema in type 2 diabetes. Diabetes Care 27: 2184-2190. (Pubitemid 39167183)
22. Hu CJ, Wang CH, Lee JH, Hsieh CM, Cheng CC, et al. (2007) Association between polymorphisms of ACE, B2AR, ANP and ENOS and cardiovascular diseases: a community-based study in the Matsu area. Clin Chem Lab Med 45: 20-25. (Pubitemid 46155554)
23. Ukkola O, Erkkila PH, Savolainen MJ, Kesaniemi YA (2001) Lack of association between polymorphisms of catalase, copper-zinc superoxide dismutase (SOD), extracellular SOD and endothelial nitric oxide synthase genes and macroangiopathy in patients with type 2 diabetes mellitus. J Intern Med 249: 451-459. (Pubitemid 34208949)
24. Liu Y, Burdon KP, Langefeld CD, Beck SR, Wagenknecht LE, et al. (2005) T-786C polymorphism of the endothelial nitric oxide synthase gene is associated with albuminuria in the diabetes heart study. J Am Soc Nephrol 16: 1085-1090. (Pubitemid 41710319)
25. Ohtoshi K, Yamasaki Y, Gorogawa S, Hayaishi-Okano R, Node K, et al. (2002) Association of (-)786T-C mutation of endothelial nitric oxide synthase gene with insulin resistance. Diabetologia 45: 1594-1601. (Pubitemid 35352054)
26. Santos KG, Crispim D, Canani LH, Ferrugem PT, Gross JL, et al. (2011) Association of eNOS gene polymorphisms with renal disease in Caucasians with type 2 diabetes. Diabetes Res Clin Pract 91: 353-362.
27. Santos KG, Crispim D, Canani LH, Ferrugem PT, Gross JL, et al. (2012) Relationship of endothelial nitric oxide synthase (eNOS) gene polymorphisms with diabetic retinopathy in Caucasians with type 2 diabetes. Ophthalmic Genet 33: 23-27.
28. Abhary S, Hewitt AW, Burdon KP, Craig JE (2009) A systematic meta-analysis of genetic association studies for diabetic retinopathy. Diabetes 58: 2137-2147.
29. Tesauro M, Thompson WC, Rogliani P, Qi L, Chaudhary PP, et al. (2000) Intracellular processing of endothelial nitric oxide synthase isoforms associated with differences in severity of cardiopulmonary diseases: cleavage of proteins with aspartate vs. glutamate at position 298. Proc Natl Acad Sci U S A 97: 2832-2835. (Pubitemid 30159257)
30. Persu A, Stoenoiu MS, Messiaen T, Davila S, Robino C, et al. (2002) Modifier effect of ENOS in autosomal dominant polycystic kidney disease. Hum Mol Genet 11: 229-241. (Pubitemid 34173352)
31. Bang H, Edwards AM, Bomback AS, Ballantyne CM, Brillon D, et al. (2009) Development and validation of a patient self-assessment score for diabetes risk. Ann Intern Med 151: 775-783.
32. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, et al. (1996) Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 97: 2601-2610.
33. The ARIC investigators. (1989) The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. Am J Epidemiol 129: 687-702.
34. Obesity: preventing and managing the global epidemic. (2000) Report of a WHO consultation. World Health Organ Tech Rep Ser 894: i-xii, 1-253.
35. Siedel J, Hagele EO, Ziegenhorn J, Wahlefeld AW (1983) Reagent for the enzymatic determination of serum total cholesterol with improved lipolytic efficiency. Clin Chem 29: 1075-1080. (Pubitemid 13106884)
36. Warnick GR, Benderson J, Albers JJ (1982) Dextran sulfate-Mg2+ precipitation procedure for quantitation of high-density-lipoprotein cholesterol. Clin Chem 28: 1379-1388. (Pubitemid 12125081)
37. Cohen J (1960) A coefficient of agreement for nominal scales. Educational and Psychological Measurement 20: 37-46.
38. Gauderman W, Morrison J (2006) QUANTO 1.1: A computer program for power and sample size calculations for genetic epidemiology studies. Available: http://hydra.usc.edu/gxe/Accessed 2013 October 15.
39. International HapMap Consortium, Frazer KA, Ballinger DG, Cox DR, Hinds DA, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
40. Podolsky RH, Barbeau P, Kang HS, Zhu H, Treiber FA, et al. (2007) Candidate genes and growth curves for adiposity in African- and European-American youth. Int J Obes (Lond) 31: 1491-1499. (Pubitemid 47482665)
41. Hink U, Li H, Mollnau H, Oelze M, Matheis E, et al. (2001) Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88: E14-22.
42. Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, et al. (1993) Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 88: 2510-2516. (Pubitemid 23360174)
43. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM (2000) Endothelial dysfunction in diabetes. Br J Pharmacol 130: 963-974. (Pubitemid 30453529)
44. McVeigh GE, Brennan GM, Johnston GD, McDermott BJ, McGrath LT, et al. (1992) Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 35: 771-776.
45. Kahn BB, Flier JS (2000) Obesity and insulin resistance. J Clin Invest 106: 473-481. (Pubitemid 30666380)
46. Caballero AE (2003) Endothelial dysfunction in obesity and insulin resistance: a road to diabetes and heart disease. Obes Res 11: 1278-1289.
47. Rask-Madsen C, King GL (2007) Mechanisms of Disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 3: 46-56. (Pubitemid 46006612)
48. Kershaw EE, Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89: 2548-2556. (Pubitemid 38766330)
49. Meier U, Gressner AM (2004) Endocrine regulation of energy metabolism: review of pathobiochemical and clinical chemical aspects of leptin, ghrelin, adiponectin, and resistin. Clin Chem 50: 1511-1525. (Pubitemid 39121218)
50. Huang PL (2009) eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 20: 295-302.
51. Haffner SM (2003) Pre-diabetes, insulin resistance, inflammation and CVD risk. Diabetes Res Clin Pract 61 Suppl 1: S9-S18.
52. Caballero AE, Arora S, Saouaf R, Lim SC, Smakowski P, et al. (1999) Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes 48: 1856-1862. (Pubitemid 29415208)
53. Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, et al. (2000) Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo : a specific vascular action of insulin. Circulation 101: 676-681. (Pubitemid 30094740)
54. Montagnani M, Chen H, Barr VA, Quon MJ (2001) Insulin-stimulated activation of eNOS is independent of Ca2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 276: 30392-30398.
55. Montagnani M, Ravichandran LV, Chen H, Esposito DL, Quon MJ (2002) Insulin receptor substrate-1 and phosphoinositide-dependent kinase-1 are required for insulin-stimulated production of nitric oxide in endothelial cells. Mol Endocrinol 16: 1931-1942. (Pubitemid 34828099)
56. Fleming I, Busse R (1999) Signal transduction of eNOS activation. Cardiovasc Res 43: 532-541. (Pubitemid 29369252)
57. Zeng G, Nystrom FH, Ravichandran LV, Cong LN, Kirby M, et al. (2000) Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101: 1539-1545. (Pubitemid 30180890)
58. Zou MH, Cohen R, Ullrich V (2004) Peroxynitrite and vascular endothelial dysfunction in diabetes mellitus. Endothelium 11: 89-97. (Pubitemid 39207182)
59. Balkestein EJ, van Aggel-Leijssen DP, van Baak MA, Struijker-Boudier HA, Van Bortel LM (1999) The effect of weight loss with or without exercise training on large artery compliance in healthy obese men. J Hypertens 17: 1831-1835. (Pubitemid 30345318)
60. Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, et al. (2002) Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation 105: 804-809. (Pubitemid 34174919)
61. Hamdy O, Ledbury S, Mullooly C, Jarema C, Porter S, et al. (2003) Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome. Diabetes Care 26: 2119-2125. (Pubitemid 41184262)
62. Sciacqua A, Candigliota M, Ceravolo R, Scozzafava A, Sinopoli F, et al. (2003) Weight loss in combination with physical activity improves endothelial dysfunction in human obesity. Diabetes Care 26: 1673-1678. (Pubitemid 36929102)
63. Rittig K, Hieronimus A, Thamer C, Machann J, Peter A, et al. (2010) Reducing visceral adipose tissue mass is essential for improving endothelial function in type 2 diabetes prone individuals. Atherosclerosis 212: 575-579.
64. Cook S, Hugli O, Egli M, Menard B, Thalmann S, et al. (2004) Partial gene deletion of endothelial nitric oxide synthase predisposes to exaggerated high-fat diet-induced insulin resistance and arterial hypertension. Diabetes 53: 2067-2072. (Pubitemid 38970756)
65. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, et al. (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 93: 13176-13181. (Pubitemid 26382789)
66. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, et al. (2006) Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 38: 320-323.
67. Cornelis MC, Qi L, Kraft P, Hu FB (2009) TCF7L2, dietary carbohydrate, and risk of type 2 diabetes in US women. Am J Clin Nutr 89: 1256-1262.
68. Deeb SS, Fajas L, Nemoto M, Pihlajamaki J, Mykkanen L, et al. (1998) A Pro12Ala substitution in PPARgamma2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat Genet 20: 284-287. (Pubitemid 28507675)
69. Memisoglu A, Hu FB, Hankinson SE, Liu S, Meigs JB, et al. (2003) Prospective study of the association between the proline to alanine codon 12 polymorphism in the PPARgamma gene and type 2 diabetes. Diabetes Care 26: 2915-2917. (Pubitemid 37205568)
70. Lamri A, Abi Khalil C, Jaziri R, Velho G, Lantieri O, et al. (2012) Dietary fat intake and polymorphisms at the PPARG locus modulate BMI and type 2 diabetes risk in the D.E.S.I.R. prospective study. Int J Obes (Lond) 36: 218-224.
71. Gudmundsson J, Sulem P, Steinthorsdottir V, Bergthorsson JT, Thorleifsson G, et al. (2007) Two variants on chromosome 17 confer prostate cancer risk, and the one in TCF2 protects against type 2 diabetes. Nat Genet 39: 977-983. (Pubitemid 47185170)
72. Brito EC, Lyssenko V, Renstrom F, Berglund G, Nilsson PM, et al. (2009) Previously associated type 2 diabetes variants may interact with physical activity to modify the risk of impaired glucose regulation and type 2 diabetes: a study of 16,003 Swedish adults. Diabetes 58: 1411-1418.
73. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, et al. (2010) Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet 11: 446-450.