Accelerated endothelial dysfunction in mild prediabetic insulin resistance: The early role of reactive oxygen species

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 5, 2007, Pages

  Duncan, Edward R ^a   Walker, Simon J ^a   Ezzat, Vivienne A ^a   Wheatcroft, Stephen B ^b   Li, Jian Mei ^c   Shah, Ajay M ^a   Kearney, Mark T ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Endothelial function; Enos; Insulin resistance; Superoxide

Indexed keywords

ACETYLCHOLINE; GLUCOSE; HYDROETHIDINE; INSULIN; MESSENGER RNA; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOAVAILABILITY; CARDIOVASCULAR RISK; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; DETERIORATION; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; EXPERIMENTAL MOUSE; FLUORESCENCE; GLUCOSE HOMEOSTASIS; GLYCEMIC CONTROL; IMPAIRED GLUCOSE TOLERANCE; INSULIN RESISTANCE; MALE; MICROVASCULARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; UPREGULATION; VASODILATATION; WILD TYPE;

ACETYLCHOLINE; ANIMALS; AORTA, THORACIC; BLOOD GLUCOSE; BLOOD PRESSURE; ENDOTHELIUM, VASCULAR; INSULIN; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; NITROPRUSSIDE; PHENYLEPHRINE; PREDIABETIC STATE; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STATISTICS, NONPARAMETRIC; VASOCONSTRICTION;

EID: 36148946364     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00299.2007     Document Type: Article

References (59)

1. Barua RS, Ambrose JA, Eales-Reynolds LJ, DeVoe MC, Zervas JG, Saha DC. Dysfunctional endothelial nitric oxide biosynthesis in healthy smokers with impaired endothelium-dependent vasodilatation. Circulation 104: 1905-1910, 2001.
2. Barua RS, Ambrose JA, Srivastava S, DeVoe MC, Eales-Reynolds LJ. Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase: an in vitro demonstration in human coronary artery endothelial cells. Circulation 107: 2342-2347, 2003.
3. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2: 559-569, 1998.
4. Bugiardini R, Manfrini O, Pizzi C, Fontana F, Morgagni G. Endothelial function predicts future development of coronary artery disease: a study of women with chest pain and normal coronary angiograms. Circulation 109: 2518-2523, 2004.
5. Buttery LD, Chester AH, Springall DR, Borland JA, Michel T, Yacoub MH, Polak JM. Explanted vein grafts with an intact endothelium demonstrate reduced focal expression of endothelial nitric oxide synthase specific to atherosclerotic sites. J Pathol 179: 197-203, 1996.
6. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87: 840-844, 2000.
7. Carmiel-Haggai M, Cederbaum AI, Nieto N. A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J 19: 136-138, 2005.
8. Cubbon RM, Wheatcroft SB, Grant PJ, Gale CP, Barth JH, Sapsford RJ, Ajjan R, Kearney MT, Hall AS. Temporal trends in mortality of patients with diabetes mellitus suffering acute myocardial infarction: a comparison of over 3000 patients between 1995 and 2003. Eur Heart J 28: 540-545, 2007.
9. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, Pratipanawatr T, DeFronzo RA, Kahn CR, Mandarino LJ. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105: 311-320, 2000.
10. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
11. Du X, Edelstein D, Obici S, Higham N, Zou MH, Brownlee M. Insulin resistance reduces arterial prostacyclin synthase and eNOS activities by increasing endothelial fatty acid oxidation. J Clin Invest 116: 1071-1081, 2006.
12. Fitzgerald SM, Kemp-Harper BK, Tare M, Parkington HC. Role of endothelium-derived hyperpolarizing factor in endothelial dysfunction during diabetes. Clin Exp Pharmacol Physiol 32: 482-487, 2005.
13. Fornengo P, Bosio A, Epifani G, Pallisco O, Mancuso A, Pascale C. Prevalence of silent myocardial ischaemia in new-onset middle-aged Type 2 diabetic patients without other cardiovascular risk factors. Diabet Med 23: 775-779, 2006.
14. Freidenberg GR, Henry RR, Klein HH, Reichart DR, Olefsky JM. Decreased kinase activity of insulin receptors from adipocytes of noninsulin-dependent diabetic subjects. J Clin Invest 79: 240-250, 1987.
15. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114: 1752-1761, 2004.
16. Gokce N, Keaney JF Jr, Hunter LM, Watkins MT, Nedeljkovic ZS, Menzoian JO, Vita JA. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease. J Am Coll Cardiol 41: 1769-1775, 2003.
17. Guzik TJ, West NE, Black E, McDonald D, Ratnatunga C, Pillai R, Channon KM. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res 86: E85-E90, 2000.
18. Haffner SM, D'Agostino R Jr, Mykkanen L, Tracy R, Howard B, Rewers M, Selby J, Savage PJ, Saad MF. Insulin sensitivity in subjects with type 2 diabetes Relationship to cardiovascular risk factors: the Insulin Resistance Atherosclerosis Study. Diabetes Care 22: 562-568, 1999.
19. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. 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, 1998.
20. Haffner SM, Mykkanen L, Festa A, Burke JP, Stern MP. Insulinresistant prediabetic subjects have more atherogenic risk factors than insulin-sensitive prediabetic subjects: implications for preventing coronary heart disease during the prediabetic state. Circulation 101: 975-980, 2000.
21. Hanley AJ, Williams K, Stern MP, Haffner SM. Homeostasis model assessment of insulin resistance in relation to the incidence of cardiovascular disease: the San Antonio Heart Study. Diabetes Care 25: 1177-1184, 2002.
22. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944-948, 2006.
23. Hu G, Jousilahti P, Qiao Q, Katoh S, Tuomilehto J. Sex differences in cardiovascular and total mortality among diabetic and non-diabetic individuals with or without history of myocardial infarction. Diabetologia 48: 856-861, 2005.
24. James PT, Rigby N, Leach R. The obesity epidemic, metabolic syndrome and future prevention strategies. Eur J Cardiovasc Prev Rehabil 11: 3-8, 2004.
25. Kanazawa K, Kawashima S, Mikami S, Miwa Y, Hirata K, Suematsu M, Hayashi Y, Itoh H, Yokoyama M. Endothelial constitutive nitric oxide synthase protein and mRNA increased in rabbit atherosclerotic aorta despite impaired endothelium-dependent vascular relaxation. Am J Pathol 148: 1949-1956, 1996.
26. Katakam PV, Tulbert CD, Snipes JA, Erdos B, Miller AW, Busija DW. Impaired insulin-induced vasodilation in small coronary arteries of Zucker obese rats is mediated by reactive oxygen species. Am J Physiol Heart Circ Physiol 288: H854-H860, 2005.
27. Kido Y, Burks DJ, Withers D, Bruning JC, Kahn CR, White MF, Accili D. Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J Clin Invest 105: 199-205, 2000.
28. Krauss S, Zhang CY, Scorrano L, Dalgaard LT, St. Pierre J, Grey ST, Lowell BB. Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction. J Clin Invest 112: 1831-1842, 2003.
29. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA, Tarpey M, Fukai T, Harrison DG. Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 103: 1282-1288, 2001.
30. Li G, Barrett EJ, Wang H, Chai W, Liu Z. Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells. Endocrinology 146: 4690-4696, 2005.
31. Li H, Wallerath T, Munzel T, Forstermann U. Regulation of endothelial-type NO synthase expression in pathophysiology and in response to drugs. Nitric Oxide 7: 149-164, 2002.
32. Li JM, Mullen AM, Shah AM. Phenotypic properties and characteristics of superoxide production by mouse coronary microvascular endothelial cells. J Mol Cell Cardiol 33: 1119-1131, 2001.
33. Li JM, Shah AM. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287: R1014-R1030, 2004.
34. Li JM, Wheatcroft S, Fan LM, Kearney MT, Shah AM. Opposing roles of p47phox in basal versus angiotensin II-stimulated alterations in vascular O2- production, vascular tone, and mitogen-activated protein kinase activation. Circulation 109: 1307-1313, 2004.
35. 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 28: 412-419, 1985.
36. Matz RL, Schott C, Stoclet JC, Andriantsitohaina R. Age-related endothelial dysfunction with respect to nitric oxide, endothelium-derived hyperpolarizing factor and cyclooxygenase products. Physiol Res 49: 11-18, 2000.
37. Montagnani M, Chen H, Barr VA, Quon MJ. Insulin-stimulated activation of eNOS is independent of Ca2 but requires phosphorylation by Akt at Ser(1179). J Biol Chem 276: 30392-30398, 2001.
38. Noronha BT, Li JM, Wheatcroft SB, Shah AM, Kearney MT. Inducible nitric oxide synthase has divergent effects on vascular and metabolic function in obesity. Diabetes 54: 1082-1089, 2005.
39. Oemar BS, Tschudi MR, Godoy N, Brovkovich V, Malinski T, Luscher TF. Reduced endothelial nitric oxide synthase expression and production in human atherosclerosis. Circulation 97: 2494-2498, 1998.
40. Pannirselvam M, Simon V, Verma S, Anderson T, Triggle CR. Chronic oral supplementation with sepiapterin prevents endothelial dysfunction and oxidative stress in small mesenteric arteries from diabetic (db/db) mice. Br J Pharmacol 140: 701-706, 2003.
41. Peterson TE, Poppa V, Ueba H, Wu A, Yan C, Berk BC. Opposing effects of reactive oxygen species and cholesterol on endothelial nitric oxide synthase and endothelial cell caveolae. Circ Res 85: 29-37, 1999.
42. Reaven G. Insulin resistance, type 2 diabetes mellitus, and cardiovascular disease: the end of the beginning. Circulation 112: 3030-3032, 2005.
43. Rudich A, Kozlovsky N, Potashnik R, Bashan N. Oxidant stress reduces insulin responsiveness in 3T3-L1 adipocytes. Am J Physiol Endocrinol Metab 272: E935-E940, 1997.
44. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 101: 1899-1906, 2000.
45. Scotland RS, Madhani M, Chauhan S, Moncada S, Andresen J, Nilsson H, Hobbs AJ, Ahluwalia A. Investigation of vascular responses in endothelial nitric oxide synthase/cyclooxygenase-1 double-knockout mice: key role for endothelium-derived hyperpolarizing factor in the regulation of blood pressure in vivo. Circulation 111: 796-803, 2005.
46. Shinozaki K, Nishio Y, Okamura T, Yoshida Y, Maegawa H, Kojima H, Masada M, Toda N, Kikkawa R, Kashiwagi A. Oral administration of tetrahydrobiopterin prevents endothelial dysfunction and vascular oxidative stress in the aortas of insulin-resistant rats. Circ Res 87: 566-573, 2000.
47. Sinaiko AR, Steinberger J, Moran A, Prineas RJ, Vessby B, Basu S, Tracy R, Jacobs DR Jr. Relation of body mass index and insulin resistance to cardiovascular risk factors, inflammatory factors, and oxidative stress during adolescence. Circulation 111: 1985-1991, 2005.
48. Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR Jr, Lerman A. Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation 101: 948-954, 2000.
49. Vicent D, Ilany J, Kondo T, Naruse K, Fisher SJ, Kisanuki YY, Bursell S, Yanagisawa M, King GL, Kahn CR. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest 111: 1373-1380, 2003.
50. Vinayaga MR, Bobby Z, Selvaraj N, Sridhar MG. Vitamin E protects the insulin sensitivity and redox balance in rat L6 muscle cells exposed to oxidative stress. Clin Chim Acta 367: 132-136, 2006.
51. Vita JA, Treasure CB, Nabel EG, McLenachan JM, Fish RD, Yeung AC, Vekshtein VI, Selwyn AP, Ganz P. Coronary vasomotor response to acetylcholine relates to risk factors for coronary artery disease. Circulation 81: 491-497, 1990.
52. Walrand S, Valeix S, Rodriguez C, Ligot P, Chassagne J, Vasson MP. Flow cytometry study of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin Chim Acta 331: 103-110, 2003.
53. Wheatcroft SB, Kearney MT, Shah AM, Grieve DJ, Williams IL, Miell JP, Crossey PA. Vascular endothelial function and blood pressure homeostasis in mice overexpressing IGF binding protein-1. Diabetes 52: 2075-2082, 2003.
54. Wheatcroft SB, Shah AM, Li JM, Duncan E, Noronha BT, Crossey PA, Kearney MT. Preserved glucoregulation but attenuation of the vascular actions of insulin in mice heterozygous for knockout of the insulin receptor. Diabetes 53: 2645-2652, 2004.
55. Wheatcroft SB, Williams IL, Shah AM, Kearney MT. Pathophysiological implications of insulin resistance on vascular endothelial function. Diabet Med 20: 255-268, 2003.
56. Wigand JP, Blackard WG. Downregulation of insulin receptors in obese man. Diabetes 28: 287-291, 1979.
57. Wilson PW, D'Agostino RB, Parise H, Sullivan L, Meigs JB. Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation 112: 3066-3072, 2005.
58. Zeng G, Nystrom FH, Ravichandran LV, Cong LN, Kirby M, Mostowski H, Quon MJ. 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, 2000.
59. Zeng G, Quon MJ. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells J Clin Invest 98: 894-898, 1996.