Decreased NO signaling leads to enhanced vasoconstrictor responsiveness in skeletal muscle arterioles of the ZDF rat prior to overt diabetes and hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 4, 2008, Pages

  Lesniewski, Lisa A ^a   Donato, Anthony J ^a   Behnke, Bradley J ^a,b   Woodman, Christopher R ^a,c   Laughlin, M Harold ^c   Ray, Chester A ^d   Delp, Michael D ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

Endothelin 1; Nitric oxide; Norepinephrine; Type 2 diabetes; Vasoconstriction

Indexed keywords

ENDOTHELIN 1; NITRIC OXIDE; NORADRENALIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD VESSEL REACTIVITY; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; HYPERTENSION; MALE; MUSCLE BLOOD FLOW; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SOLEUS MUSCLE; VASOCONSTRICTION; ZUCKER DIABETIC FATTY RAT;

ANIMALS; ARTERIOLES; BLOOD GLUCOSE; BLOOD PRESSURE; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENDOTHELIN-1; ENZYME INHIBITORS; HYPERTENSION; INSULIN; ISOPROTERENOL; MALE; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NOREPINEPHRINE; POTASSIUM CHLORIDE; PREDIABETIC STATE; RATS; RATS, ZUCKER; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TIME FACTORS; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATOR AGENTS;

EID: 41749087596     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00692.2007     Document Type: Article

References (57)

1. Anonymous. Diabetes mellitus: a major risk factor for cardiovascular disease. A joint editorial statement by the American Diabetes Association; The National Heart, Lung, and Blood Institute; The Juvenile Diabetes Foundation International; The National Institute of Diabetes and Digestive and Kidney Diseases; and The American Heart Association. Circulation 100: 1132-1133, 1999.
2. Baron AD. Insulin resistance and vascular function. J Diabetes Complications 16: 92-102, 2002.
3. Baron AD, Clark MG. Role of blood flow in the regulation of muscle glucose uptake. Annu Rev Nutr 17: 487-499, 1997.
4. Bohlen HG, Lash JM. Endothelial-dependent vasodilation is preserved in non-insulin-dependent Zucker fatty diabetic rats. Am J Physiol Heart Circ Physiol 268: H2366-H2374, 1995.
5. Bonora E, Muggeo M. Postprandial blood glucose as a risk factor for cardiovascular disease in Type II diabetes: the epidemiological evidence. Diabetologia 44: 2107-2114, 2001.
6. Bray GA. The Zucker-fatty rat: a review. Fed Proc 36: 148-153, 1977.
7. Clark MG, Wallis MG, Barrett EJ, Vincent MA, Richards SM, Clerk LH, Rattigan S. Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 284: E241-E258, 2003.
8. Corsetti JP, Sparks JD, Peterson RG, Smith RL, Sparks CE. Effect of dietary fat on the development of non-insulin dependent diabetes mellitus in obese Zucker diabetic fatty male and female rats. Atherosclerosis 148: 231-241, 2000.
9. Cox RH, Kikta DC. Age-related changes in thoracic aorta of obese Zucker rats. Am J Physiol Heart Circ Physiol 262: H1548-H1556, 1992.
10. Delp MD, Duan C. Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80: 261-270, 1996.
11. Delp MD, Manning RO, Bruckner JV, Armstrong RB. Distribution of cardiac output during diurnal changes of activity in rats. Am J Physiol Heart Circ Physiol 261: H1487-H1493, 1991.
12. Delp MD, O'Leary DS. Integrative control of the skeletal muscle microcirculation in the maintenance of arterial pressure during exercise. J Appl Physiol 97: 1112-1118, 2004.
13. Donatelli M, Colletti I, Bucalo ML, Russo V, Verga S. Plasma endothelin levels in NIDDM patients with macroangiopathy. Diabetes Res 25: 159-164, 1994.
14. Donato AJ, Lesniewski LA, Delp MD. Ageing and exercise training alter adrenergic vasomotor responses of rat skeletal muscle arterioles. J Physiol 579: 115-125, 2007.
15. Engelgau MM, Geiss LS, Saaddine JB, Boyle JP, Benjamin SM, Gregg EW, Tierney EF, Rios-Burrows N, Mokdad AH, Ford ES, Imperatore G, Narayan KM. The evolving diabetes burden in the United States. Ann Intern Med 140: 945-950, 2004.
16. Esler M, Rumantir M, Wiesner G, Kaye D, Hastings J, Lambert G. Sympathetic nervous system and insulin resistance: from obesity to diabetes. Am J Hypertens 14: 304S-309S, 2001.
17. Etgen GJ, Oldham BA. Profiling of Zucker diabetic fatty rats in their progression to the overt diabetic state. Metabolism 49: 684-688, 2000.
18. Finegood DT, McArthur MD, Kojwang D, Thomas MJ, Topp BG, Leonard T, Buckingham RE. Beta-cell mass dynamics in Zucker diabetic fatty rats. Rosiglitazone prevents the rise in net cell death. Diabetes 50: 1021-1029, 2001.
19. Frisbee JC. Enhanced arteriolar α-adrenergic constriction impairs dilator responses and skeletal muscle perfusion in obese Zucker rats. J Appl Physiol 97: 764-772, 2004.
20. Frisbee JC. Impaired skeletal muscle perfusion in obese Zucker rats. Am J Physiol Regul Integr Comp Physiol 285: R1124-R1134, 2003.
21. Frisbee JC. Reduced nitric oxide bioavailability contributes to skeletal muscle microvessel rarefaction in the metabolic syndrome. Am J Physiol Regul Integr Comp Physiol 289: R307-R316, 2005.
22. Frisbee JC. Remodeling of the skeletal muscle microcirculation increases resistance to perfusion in obese Zucker rats. Am J Physiol Heart Circ Physiol 285: H104-H111, 2003.
23. Frisbee JC. Vascular adrenergic tone and structural narrowing constrain reactive hyperemia in skeletal muscle of obese Zucker rats. Am J Physiol Heart Circ Physiol 290: H2066-H2074, 2006.
24. Frisbee JC, Maier KG, Stepp DW. Oxidant stress-induced increase in myogenic activation of skeletal muscle resistance arteries in obese Zucker rats. Am J Physiol Heart Circ Physiol 283: H2160-H2168, 2002.
25. Garnett KE, Chapman P, Chambers JA, Waddell ID, Boam DS. Differential gene expression between Zucker Fatty rats and Zucker Diabetic Fatty rats: a potential role for the immediate-early gene Egr-1 in regulation of beta cell proliferation. J Mol Endocrinol 35: 13-25, 2005.
26. Granger HJ, Goodman AH, Granger DN. Role of resistance and exchange vessels in local microvascular control of skeletal muscle oxygenation in the dog. Circ Res 38: 379-385, 1976.
27. Haffner SM. Epidemiology of insulin resistance and its relation to coronary artery disease. Am J Cardiol 84: 11J-14J, 1999.
28. Haffner SM, Stern MP, Hazuda HP, Mitchell BD, Patterson JK. Cardiovascular risk factors in confirmed prediabetic individuals. Does the clock for coronary heart disease start ticking before the onset of clinical diabetes? JAMA 263: 2893-2898, 1990.
29. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, Wiedmeyer HM, Byrd-Holt DD. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in US adults. The Third National Health and Nutrition Examination Survey, 1988-1994. Diabetes Care 21: 518-524, 1998.
30. Isomaa B, Henricsson M, Almgren P, Tuomi T, Taskinen MR, Groop L. The metabolic syndrome influences the risk of chronic complications in patients with type II diabetes. Diabetologia 44: 1148-1154, 2001.
31. Jasperse JL, Woodman CR, Price EM, Hasser EM, Laughlin MH. Hindlimb unweighting decreases ecNOS gene expression and endothelium-dependent dilation in rat soleus feed arteries. J Appl Physiol 87: 1476-1482, 1999.
32. Kawaguchi M, Koshimura K, Murakami Y, Tsumori M, Gonda T, Kato Y. Antihypertensive effect of insulin via nitric oxide production in the Zucker diabetic fatty rat, an animal model for non-insulin-dependent diabetes mellitus. Eur J Endocrinol 140: 341-349, 1999.
33. Kawano H, Motoyama T, Hirashima O, Hirai N, Miyao Y, Sakamoto T, Kugiyama K, Ogawa H, Yasue H. Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. J Am Coll Cardiol 34: 146-154, 1999.
34. Lash JM, Sherman WM, Hamlin RL. Capillary basement membrane thickness and capillary density in sedentary and trained obese Zucker rats. Diabetes 38: 854-860, 1989.
35. Li H, Chai Q, Gutterman DD, Liu Y. Elevated glucose impairs cAMP-mediated dilation by reducing Kv channel activity in rat small coronary smooth muscle cells. Am J Physiol Heart Circ Physiol 285: H1213-H1219, 2003.
36. Lindbom L, Arfors KE. Mechanisms and site of control for variation in the number of perfused capillaries in skeletal muscle. Int J Microcirc Clin Exp 4: 19-30, 1985.
37. McCurdy MR, Colleran PN, Muller-Delp J, Delp MD. Effects of fiber composition and hindlimb unloading on the vasodilator properties of skeletal muscle arterioles. J Appl Physiol 89: 398-405, 2000.
38. Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD, Delp MD. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282: H1843-H1854, 2002.
39. Muller-Delp JM, Spier SA, Ramsey MW, Delp MD. Aging impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283: H1662-H1672, 2002.
40. Naik JS, Xiang L, Hester RL. Enhanced role for RhoA-associated kinase in adrenergic-mediated vasoconstriction in gracilis arteries from obese Zucker rats. Am J Physiol Regul Integr Comp Physiol 290: R154-R161, 2006.
41. Oltman CL, Richou LL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Progression of coronary and mesenteric vascular dysfunction in Zucker obese and Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 291: H1780-H1787, 2006.
42. Peterson R, Shaw W, Neel M, Little L, Eichberg J. Zucker diabetic fatty rat as a model for non-insulin dependent diabetes mellitus. ILAR J 32, 1990.
43. Pieper GM, Meier DA, Hager SR. Endothelial dysfunction in a model of hyperglycemia and hyperinsulinemia. Am J Physiol Heart Circ Physiol 269: H845-H850, 1995.
44. Schlaich MP, Ahlers BA, Parnell MM, Kaye DM. β-Adrenoceptor- mediated, nitric-oxide-dependent vasodilatation is abnormal in early hypertension: restoration by L-arginine. J Hypertens 22: 1917-1925, 2004.
45. Schmidt RE, Dorsey DA, Beaudet LN, Peterson RG. Analysis of the Zucker Diabetic Fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. Am J Pathol 163: 21-28, 2003.
46. Schroeder CA Jr, Chen YL, Messina EJ. Inhibition of NO synthesis or endothelium removal reveals a vasoconstrictor effect of insulin on isolated arterioles. Am J Physiol Heart Circ Physiol 276: H815-H820, 1999.
47. Serne EH, Stehouwer CD, ter Maaten JC, ter Wee PM, Rauwerda JA, Donker AJ, Gans RO. Microvascular function relates to insulin sensitivity and blood pressure in normal subjects. Circulation 99: 896-902, 1999.
48. Sexl V, Mancusi G, Raberger G, Schutz W. Age-related changes in vascular reactivity in genetically diabetic rats. Pharmacology 50: 238-246, 1995.
49. Sparks JD, Phung TL, Bolognino M, Cianci J, Khurana R, Peterson RG, Sowden MP, Corsetti JP, Sparks CE. Lipoprotein alterations in 10-and 20-week-old Zucker diabetic fatty rats: hyperinsulinemic versus insulinopenic hyperglycemia. Metabolism 47: 1315-1324, 1998.
50. Sparks JD, Shaw WN, Corsetti JP, Bolognino M, Pesek JF, Sparks CE. Insulin-treated Zucker diabetic fatty rats retain the hypertriglyceridemia associated with obesity. Metabolism 49: 1424-1430, 2000.
51. Sreenan S, Keck S, Fuller T, Cockburn B, Burant CF. Effects of troglitazone on substrate storage and utilization in insulin-resistant rats. Am J Physiol Endocrinol Metab 276: E1119-E1129, 1999.
52. Stepp DW, Frisbee JC. Augmented adrenergic vasoconstriction in hypertensive diabetic obese Zucker rats. Am J Physiol Heart Circ Physiol 282: H816-H820, 2002.
53. Sweeney TE, Sarelius IH. Arteriolar control of capillary cell flow in striated muscle. Circ Res 64: 112-120, 1989.
54. Tooke JE. Microvasculature in diabetes. Cardiovasc Res 32: 764-771, 1996.
55. Wiernsperger N. Vascular defects in the aetiology of peripheral insulin resistance in diabetes. A critical review of hypotheses and facts. Diabetes Metab Rev 10: 287-307, 1994.
56. Yan C, Kim D, Aizawa T, Berk BC. Functional interplay between angiotensin II and nitric oxide: cyclic GMP as a key mediator. Arterioscler Thromb Vasc Biol 23: 26-36, 2003.
57. Yue TL, Bao W, Gu JL, Cui J, Tao L, Ma XL, Ohlstein EH, Jucker BM. Rosiglitazone treatment in Zucker diabetic Fatty rats is associated with ameliorated cardiac insulin resistance and protection from ischemia/reperfusion- induced myocardial injury. Diabetes 54: 554-562, 2005.