Role of insulin resistance in endothelial dysfunction (original) (raw)
DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14(3):173–94. ArticlePubMedCAS Google Scholar
Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, et al. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci U S A. 2007;104(31):12587–94. ArticlePubMedCAS Google Scholar
Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, et al. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation. 2006;113(6):898–918. ArticlePubMed Google Scholar
Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr Rev. 2007;28(5):463–91. ArticlePubMedCAS Google Scholar
Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S, et al. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes. 2004;53(6):1418–23. ArticlePubMedCAS Google Scholar
Baron AD, Laakso M, Brechtel G, Edelman SV. Mechanism of insulin resistance in insulin-dependent diabetes mellitus: a major role for reduced skeletal muscle blood flow. J Clin Endocrinol Metab. 1991;73(3):637–43. ArticlePubMedCAS Google Scholar
Natali A, Taddei S, Quinones Galvan A, Camastra S, Baldi S, Frascerra S, et al. Insulin sensitivity, vascular reactivity, and clamp-induced vasodilatation in essential hypertension. Circulation. 1997;96(3):849–55. ArticlePubMedCAS Google Scholar
Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation. 2006;113(15):1888–904. ArticlePubMed Google Scholar
Barac A, Campia U, Panza JA. Methods for evaluating endothelial function in humans. Hypertension. 2007;49(4):748–60. ArticlePubMedCAS Google Scholar
Zeng G, Quon MJ. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells. J Clin Invest. 1996;98(4):894–8. ArticlePubMedCAS Google Scholar
Dudzinski DM, Michel T. Life history of eNOS: partners and pathways. Cardiovasc Res. 2007;75(2):247–60. ArticlePubMedCAS Google Scholar
Herman AG, Moncada S. Therapeutic potential of nitric oxide donors in the prevention and treatment of atherosclerosis. Eur Heart J. 2005;26(19):1945–55. ArticlePubMedCAS Google Scholar
Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003;23(2):168–75. ArticlePubMedCAS Google Scholar
Muris DM, Houben AJ, Schram MT, Stehouwer CD. Microvascular dysfunction is associated with a higher incidence of type 2 diabetes mellitus–brief report: a systematic review and meta-analysis. Arterioscler Thromb Vasc Biol. 2012.
Hamburg NM, Keyes MJ, Larson MG, Vasan RS, Schnabel R, Pryde MM, et al. Cross-sectional relations of digital vascular function to cardiovascular risk factors in the Framingham Heart Study. Circulation. 2008;117(19):2467–74. ArticlePubMed Google Scholar
Bonetti PO, Pumper GM, Higano ST, Holmes Jr DR, Kuvin JT, Lerman A. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol. 2004;44(11):2137–41. ArticlePubMed Google Scholar
Prior JO, Quinones MJ, Hernandez-Pampaloni M, Facta AD, Schindler TH, Sayre JW, et al. Coronary circulatory dysfunction in insulin resistance, impaired glucose tolerance, and type 2 diabetes mellitus. Circulation. 2005;111(18):2291–8. ArticlePubMedCAS Google Scholar
Muniyappa R, Hall G, Kolodziej TL, Karne RJ, Crandon SK, Quon MJ. Cocoa consumption for 2 wk enhances insulin-mediated vasodilatation without improving blood pressure or insulin resistance in essential hypertension. Am J Clin Nutr. 2008;88(6):1685–96. ArticlePubMedCAS Google Scholar
Ketel IJ, Stehouwer CD, Serne EH, Korsen TJ, Hompes PG, Smulders YM, et al. Obese but not normal-weight women with polycystic ovary syndrome are characterized by metabolic and microvascular insulin resistance. J Clin Endocrinol Metab. 2008;93(9):3365–72. ArticlePubMedCAS Google Scholar
Semple RK, Sleigh A, Murgatroyd PR, Adams CA, Bluck L, Jackson S, et al. Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J Clin Invest. 2009;119(2):315–22. PubMedCAS Google Scholar
Lteif A, Vaishnava P, Baron AD, Mather KJ. Endothelin limits insulin action in obese/insulin-resistant humans. Diabetes. 2007;56(3):728–34. ArticlePubMedCAS Google Scholar
Vincent MA, Montagnani M, Quon MJ. Molecular and physiologic actions of insulin related to production of nitric oxide in vascular endothelium. Curr Diab Rep. 2003;3(4):279–88. ArticlePubMed Google Scholar
Potenza MA, Marasciulo FL, Chieppa DM, Brigiani GS, Formoso G, Quon MJ, et al. Insulin resistance in spontaneously hypertensive rats is associated with endothelial dysfunction characterized by imbalance between NO and ET-1 production. Am J Physiol Heart Circ Physiol. 2005;289(2):H813–22. ArticlePubMedCAS Google Scholar
Montagnani M, Golovchenko I, Kim I, Koh GY, Goalstone ML, Mundhekar AN, et al. Inhibition of phosphatidylinositol 3-kinase enhances mitogenic actions of insulin in endothelial cells. J Biol Chem. 2002;277(3):1794–9. ArticlePubMedCAS Google Scholar
Mukai Y, Wang CY, Rikitake Y, Liao JK. Phosphatidylinositol 3-kinase/protein kinase Akt negatively regulates plasminogen activator inhibitor type 1 expression in vascular endothelial cells. Am J Physiol Heart Circ Physiol. 2007;292(4):H1937–42. ArticlePubMedCAS Google Scholar
Jiang ZY, Lin YW, Clemont A, Feener EP, Hein KD, Igarashi M, et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest. 1999;104(4):447–57. ArticlePubMedCAS Google Scholar
Vicent D, Ilany J, Kondo T, Naruse K, Fisher SJ, Kisanuki YY, et al. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest. 2003;111(9):1373–80. PubMedCAS Google Scholar
Duncan ER, Crossey PA, Walker S, Anilkumar N, Poston L, Douglas G, et al. Effect of endothelium-specific insulin resistance on endothelial function in vivo. Diabetes. 2008;57(12):3307–14. ArticlePubMedCAS Google Scholar
Wheatcroft SB, Shah AM, Li JM, Duncan E, Noronha BT, Crossey PA, et al. Preserved glucoregulation but attenuation of the vascular actions of insulin in mice heterozygous for knockout of the insulin receptor. Diabetes. 2004;53(10):2645–52. ArticlePubMedCAS Google Scholar
Kubota T, Kubota N, Moroi M, Terauchi Y, Kobayashi T, Kamata K, et al. Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury. Circulation. 2003;107(24):3073–80. ArticlePubMedCAS Google Scholar
Fernandez-Hernando C, Ackah E, Yu J, Suarez Y, Murata T, Iwakiri Y, et al. Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 2007;6(6):446–57. ArticlePubMedCAS Google Scholar
Perticone F, Sciacqua A, Scozzafava A, Ventura G, Laratta E, Pujia A, et al. Impaired endothelial function in never-treated hypertensive subjects carrying the Arg972 polymorphism in the insulin receptor substrate-1 gene. J Clin Endocrinol Metab. 2004;89(7):3606–9. ArticlePubMedCAS Google Scholar
Federici M, Pandolfi A, De Filippis EA, Pellegrini G, Menghini R, Lauro D, et al. G972R IRS-1 variant impairs insulin regulation of endothelial nitric oxide synthase in cultured human endothelial cells. Circulation. 2004;109(3):399–405. ArticlePubMedCAS Google Scholar
Okon EB, Chung AW, Rauniyar P, Padilla E, Tejerina T, McManus BM, et al. Compromised arterial function in human type 2 diabetic patients. Diabetes. 2005;54(8):2415–23. ArticlePubMedCAS Google Scholar
Lerman A, Edwards BS, Hallett JW, Heublein DM, Sandberg SM, Burnett Jr JC. Circulating and tissue endothelin immunoreactivity in advanced atherosclerosis. N Engl J Med. 1991;325(14):997–1001. ArticlePubMedCAS Google Scholar
Shemyakin A, Bohm F, Wagner H, Efendic S, Bavenholm P, Pernow J. Enhanced endothelium-dependent vasodilatation by dual endothelin receptor blockade in individuals with insulin resistance. J Cardiovasc Pharmacol. 2006;47(3):385–90. PubMedCAS Google Scholar
Mather KJ, Mirzamohammadi B, Lteif A, Steinberg HO, Baron AD. Endothelin contributes to basal vascular tone and endothelial dysfunction in human obesity and type 2 diabetes. Diabetes. 2002;51(12):3517–23. ArticlePubMedCAS Google Scholar
Cardillo C, Campia U, Kilcoyne CM, Bryant MB, Panza JA. Improved endothelium-dependent vasodilation after blockade of endothelin receptors in patients with essential hypertension. Circulation. 2002;105(4):452–6. ArticlePubMedCAS Google Scholar
Cardillo C, Campia U, Iantorno M, Panza JA. Enhanced vascular activity of endogenous endothelin-1 in obese hypertensive patients. Hypertension. 2004;43(1):36–40. ArticlePubMedCAS Google Scholar
Cardillo C, Campia U, Bryant MB, Panza JA. Increased activity of endogenous endothelin in patients with type II diabetes mellitus. Circulation. 2002;106(14):1783–7. ArticlePubMedCAS Google Scholar
Cardillo C, Nambi SS, Kilcoyne CM, Choucair WK, Katz A, Quon MJ, et al. Insulin stimulates both endothelin and nitric oxide activity in the human forearm. Circulation. 1999;100(8):820–5. ArticlePubMedCAS Google Scholar
Ahlborg G, Lindstrom J. Insulin sensitivity and big ET-1 conversion to ET-1 after ETA- or ETB-receptor blockade in humans. J Appl Physiol. 2002;93(6):2112–21. PubMedCAS Google Scholar
Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest. 1996;97(11):2601–10. ArticlePubMedCAS Google Scholar
Balletshofer BM, Rittig K, Enderle MD, Volk A, Maerker E, Jacob S, et al. Endothelial dysfunction is detectable in young normotensive first-degree relatives of subjects with type 2 diabetes in association with insulin resistance. Circulation. 2000;101(15):1780–4. ArticlePubMedCAS Google Scholar
Han KA, Patel Y, Lteif AA, Chisholm R, Mather KJ. Contributions of dysglycaemia, obesity, and insulin resistance to impaired endothelium-dependent vasodilation in humans. Diabetes Metab Res Rev. 2011;27(4):354–61. ArticlePubMedCAS Google Scholar
Caballero AE, Arora S, Saouaf R, Lim SC, Smakowski P, Park JY, et al. Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes. 1999;48(9):1856–62. ArticlePubMedCAS Google Scholar
Lteif AA, Han K, Mather KJ. Obesity, insulin resistance, and the metabolic syndrome: determinants of endothelial dysfunction in whites and blacks. Circulation. 2005;112(1):32–8. ArticlePubMedCAS Google Scholar
Title LM, Lonn E, Charbonneau F, Fung M, Mather KJ, Verma S, et al. Relationship between brachial artery flow-mediated dilatation, hyperemic shear stress, and the metabolic syndrome. Vasc Med. 2008;13(4):263–70. ArticlePubMed Google Scholar
Lind L. Endothelium-dependent vasodilation, insulin resistance and the metabolic syndrome in an elderly cohort: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study. Atherosclerosis. 2008;196(2):795–802. ArticlePubMedCAS Google Scholar
Wendelhag I, Fagerberg B, Hulthe J, Bokemark L, Wikstrand J. Endothelium-dependent flow-mediated vasodilatation, insulin resistance and the metabolic syndrome in 60-year-old men. J Intern Med. 2002;252(4):305–13. ArticlePubMedCAS Google Scholar
Petrie JR, Ueda S, Webb DJ, Elliott HL, Connell JM. Endothelial nitric oxide production and insulin sensitivity. A physiological link with implications for pathogenesis of cardiovascular disease. Circulation. 1996;93(7):1331–3. ArticlePubMedCAS Google Scholar
Tack CJ, Ong MK, Lutterman JA, Smits P. Insulin-induced vasodilatation and endothelial function in obesity/insulin resistance. Effects of troglitazone. Diabetologia. 1998;41(5):569–76. ArticlePubMedCAS Google Scholar
Hogikyan RV, Galecki AT, Pitt B, Halter JB, Greene DA, Supiano MA. Specific impairment of endothelium-dependent vasodilation in subjects with type 2 diabetes independent of obesity. J Clin Endocrinol Metab. 1998;83(6):1946–52. ArticlePubMedCAS Google Scholar
Jaap AJ, Shore AC, Tooke JE. Relationship of insulin resistance to microvascular dysfunction in subjects with fasting hyperglycaemia. Diabetologia. 1997;40(2):238–43. ArticlePubMedCAS Google Scholar
Watts GF, O’Brien SF, Silvester W, Millar JA. Impaired endothelium-dependent and independent dilatation of forearm resistance arteries in men with diet-treated non-insulin-dependent diabetes: role of dyslipidaemia. Clin Sci (Lond). 1996;91(5):567–73. CAS Google Scholar
Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol. 1996;27(3):567–74. ArticlePubMedCAS Google Scholar
Sola S, Mir MQ, Cheema FA, Khan-Merchant N, Menon RG, Parthasarathy S, et al. Irbesartan and lipoic acid improve endothelial function and reduce markers of inflammation in the metabolic syndrome: results of the Irbesartan and Lipoic Acid in Endothelial Dysfunction (ISLAND) study. Circulation. 2005;111(3):343–8. ArticlePubMedCAS Google Scholar
Heitzer T, Finckh B, Albers S, Krohn K, Kohlschutter A, Meinertz T. Beneficial effects of alpha-lipoic acid and ascorbic acid on endothelium-dependent, nitric oxide-mediated vasodilation in diabetic patients: relation to parameters of oxidative stress. Free Radic Biol Med. 2001;31(1):53–61. ArticlePubMedCAS Google Scholar
Chen H, Karne RJ, Hall G, Campia U, Panza JA, Cannon 3rd RO, et al. High-dose oral vitamin C partially replenishes vitamin C levels in patients with Type 2 diabetes and low vitamin C levels but does not improve endothelial dysfunction or insulin resistance. Am J Physiol Heart Circ Physiol. 2006;290(1):H137–45. ArticlePubMedCAS Google Scholar
Perticone F, Ceravolo R, Candigliota M, Ventura G, Iacopino S, Sinopoli F, et al. Obesity and body fat distribution induce endothelial dysfunction by oxidative stress: protective effect of vitamin C. Diabetes. 2001;50(1):159–65. ArticlePubMedCAS Google Scholar
Lekakis JP, Anastasiou EA, Papamichael CM, Stamatelopoulos KS, Dagre AG, Alevizaki MC, et al. Short-term oral ascorbic acid improves endothelium-dependent vasodilatation in women with a history of gestational diabetes mellitus. Diabetes Care. 2000;23(9):1432–4. ArticlePubMedCAS Google Scholar
Darko D, Dornhorst A, Kelly FJ, Ritter JM, Chowienczyk PJ. Lack of effect of oral vitamin C on blood pressure, oxidative stress and endothelial function in Type II diabetes. Clin Sci (Lond). 2002;103(4):339–44. CAS Google Scholar
Regensteiner JG, Popylisen S, Bauer TA, Lindenfeld J, Gill E, Smith S, et al. Oral L-arginine and vitamins E and C improve endothelial function in women with type 2 diabetes. Vasc Med. 2003;8(3):169–75. ArticlePubMed Google Scholar
Beckman JA, Goldfine AB, Gordon MB, Garrett LA, Keaney Jr JF, Creager MA. Oral antioxidant therapy improves endothelial function in Type 1 but not Type 2 diabetes mellitus. Am J Physiol Heart Circ Physiol. 2003;285(6):H2392–8. PubMedCAS Google Scholar
Pena AS, Wiltshire E, Gent R, Piotto L, Hirte C, Couper J. Folic acid does not improve endothelial function in obese children and adolescents. Diabetes Care. 2007;30(8):2122–7. ArticlePubMedCAS Google Scholar
Title LM, Ur E, Giddens K, McQueen MJ, Nassar BA. Folic acid improves endothelial dysfunction in type 2 diabetes–an effect independent of homocysteine-lowering. Vasc Med. 2006;11(2):101–9. ArticlePubMed Google Scholar
Heitzer T, Krohn K, Albers S, Meinertz T. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia. 2000;43(11):1435–8. ArticlePubMedCAS Google Scholar
Nystrom T, Nygren A, Sjoholm A. Tetrahydrobiopterin increases insulin sensitivity in patients with type 2 diabetes and coronary heart disease. Am J Physiol Endocrinol Metab. 2004;287(5):E919–25. ArticlePubMedCAS Google Scholar
Grassi D, Necozione S, Lippi C, Croce G, Valeri L, Pasqualetti P, et al. Cocoa reduces blood pressure and insulin resistance and improves endothelium-dependent vasodilation in hypertensives. Hypertension. 2005;46(2):398–405. ArticlePubMedCAS Google Scholar
Hamdy O, Ledbury S, Mullooly C, Jarema C, Porter S, Ovalle K, et al. Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome. Diabetes Care. 2003;26(7):2119–25. ArticlePubMed Google Scholar
Maeda S, Jesmin S, Iemitsu M, Otsuki T, Matsuo T, Ohkawara K, et al. Weight loss reduces plasma endothelin-1 concentration in obese men. Exp Biol Med (Maywood). 2006;231(6):1044–7. CAS Google Scholar
Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol. 2000;20(6):1595–9. ArticlePubMedCAS Google Scholar
Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, et al. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation. 2003;107(25):3152–8. ArticlePubMedCAS Google Scholar
Davis BJ, Xie Z, Viollet B, Zou MH. Activation of the AMP-activated kinase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes. 2006;55(2):496–505. ArticlePubMedCAS Google Scholar
Diamanti-Kandarakis E, Alexandraki K, Protogerou A, Piperi C, Papamichael C, Aessopos A, et al. Metformin administration improves endothelial function in women with polycystic ovary syndrome. Eur J Endocrinol. 2005;152(5):749–56. ArticlePubMedCAS Google Scholar
Natali A, Baldeweg S, Toschi E, Capaldo B, Barbaro D, Gastaldelli A, et al. Vascular effects of improving metabolic control with metformin or rosiglitazone in type 2 diabetes. Diabetes Care. 2004;27(6):1349–57. ArticlePubMedCAS Google Scholar
UKPDS. Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group. Lancet. 1998;352(9131):854–65. Article Google Scholar
Eddy D, Schlessinger L, Kahn R, Peskin B, Schiebinger R. Relationship of insulin resistance and related metabolic variables to coronary artery disease: a mathematical analysis. Diabetes Care. 2009;32(2):361–6. ArticlePubMedCAS Google Scholar