Local NOS inhibition impairs vascular and metabolic actions of insulin in rat hindleg muscle in vivo

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 6, 2013, Pages

  Bradley, Eloise A ^a   Richards, Stephen M ^a   Keske, Michelle A ^a   Rattigan, Stephen ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Hyperinsulinemiceuglycemic clamp; Microvascular blood flow; Muscle blood flow; Nitric oxide; Nitric oxide synthase

Indexed keywords

1 METHYLXANTHINE; INSULIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; ENZYME INHIBITION; EPIGASTRIC ARTERY; FEMORAL ARTERY FLOW; GLUCOSE TRANSPORT; HEART RATE; HINDLIMB; HYPERINSULINEMIA; IN VIVO STUDY; INSULIN METABOLISM; LEG MUSCLE; MEAN ARTERIAL PRESSURE; MICROVASCULATURE; MUSCLE BLOOD FLOW; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; VASCULAR CLAMP;

HYPERINSULINEMIC-EUGLYCEMIC CLAMP; MICROVASCULAR BLOOD FLOW; MUSCLE BLOOD FLOW; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMALS; BLOOD FLOW VELOCITY; BLOOD GLUCOSE; BLOOD PRESSURE; ENZYME INHIBITORS; FEMORAL ARTERY; HEART RATE; HINDLIMB; INSULIN; MALE; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; REGIONAL BLOOD FLOW;

EID: 84884403724     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00289.2013     Document Type: Article

References (40)

1. Baron AD, Brechtel G. Insulin differentially regulates systemic and skeletal muscle vascular resistance. Am J Physiol Endocrinol Metab 265: E61-E67, 1993.
2. Baron AD, Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G. Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J Clin Invest 96: 786-792, 1995.
3. Bradley EA, Willson KJ, Choi-Lundberg D, Clark MG, Rattigan S. Effects of central administration of insulin or L-NMMA on rat skeletal muscle microvascular perfusion. Diabetes Obes Metab 12: 900-908, 2010.
4. 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.
5. Clerk LH, Rattigan S, Clark MG. Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 51: 1138-1145, 2002.
6. Clerk LH, Vincent MA, Jahn LA, Liu Z, Lindner JR, Barrett EJ. Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 55: 1436-1442, 2006.
7. Coggins M, Lindner J, Rattigan S, Jahn L, Fasy E, Kaul S, Barrett E. Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 50: 2682-2690, 2001.
8. Duplain H, Burcelin R, Sartori C, Cook S, Egli M, Lepori M, Vollenweider P, Pedrazzini T, Nicod P, Thorens B, Scherrer U. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104: 342-345, 2001.
9. Frandsen U, Bangsbo J, Langberg H, Saltin B, Hellsten Y. Inhibition of nitric oxide synthesis by systemic N(G)-monomethyl-L-arginine administration in humans: effects on interstitial adenosine, prostacyclin and potassium concentrations in resting and contracting skeletal muscle. J Vasc Res 37: 297-302, 2000.
10. Genders AJ, Bradley EA, Rattigan S, Richards SM. cGMP phosphodiesterase inhibition improves the vascular and metabolic actions of insulin in skeletal muscle. Am J Physiol Endocrinol Metab 301: E342-E350, 2011.
11. Huang F, Villafana S, Hong E. Role of central and sympathetic nervous systems in pressor effect of L-NAME. J Cardiovasc Pharmacol 41: 68-72, 2003.
12. James DE, Jenkins AB, Kraegen EW. Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Physiol Endocrinol Metab 248: E567-E574, 1985.
13. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ. Obesity blunts microvascular recruitment in human forearm muscle after a mixed meal. Diabetes Care 32: 1672-1677, 2009.
14. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am J Physiol Endocrinol Metab 248: E353-E362, 1985.
15. Kubota T, Kubota N, Kumagai H, Yamaguchi S, Kozono H, Takahashi T, Inoue M, Itoh S, Takamoto I, Sasako T, Kumagai K, Kawai T, Hashimoto S, Kobayashi T, Sato M, Tokuyama K, Nishimura S, Tsunoda M, Ide T, Murakami K, Yamazaki T, Ezaki O, Kawamura K, Masuda H, Moroi M, Sugi K, Oike Y, Shimokawa H, Yanagihara N, Tsutsui M, Terauchi Y, Tobe K, Nagai R, Kamata K, Inoue K, Kodama T, Ueki K, Kadowaki T. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab 13: 294-307, 2011.
16. 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.
17. Montagnani M, Ravichandran LV, Chen H, Esposito DL, Quon MJ. 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, 2002.
18. Premilovac D, Bradley EA, Ng HL, Richards SM, Rattigan S, Keske MA. Muscle insulin resistance resulting from impaired microvascular insulin sensitivity in Sprague Dawley rats. Cardiovasc Res 98: 28-36, 2013.
19. Rattigan S, Barrett EJ, Clark MG. Insulin-mediated capillary recruitment in skeletal muscle: is this a mediator of insulin action on glucose metabolism? Current Diabetes Rep 3: 195-200, 2003.
20. Rattigan S, Clark MG, Barrett EJ. Acute vasoconstriction-induced insulin resistance in rat muscle in vivo. Diabetes 48: 564-569, 1999.
21. Rattigan S, Clark MG, Barrett EJ. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46: 1381-1388, 1997.
22. Ross RM, Kolka CM, Rattigan S, Clark MG. Acute blockade by endothelin-1 of haemodynamic insulin action in rats. Diabetologia 50: 443-451, 2007.
23. Scherrer U, Randin D, Vollenweider P, Vollenweider L, Nicod P. Nitric oxide release accounts for insulin's vascular effects in humans. J Clin Invest 94: 2511-2515, 1994.
24. Shankar R, Zhu JS, Ladd B, Henry D, Shen HQ, Baron AD. Central nervous system nitric oxide synthase activity regulates insulin secretion and insulin action. J Clin Invest 102: 1403-1412, 1998.
25. Shankar RR, Wu Y, Shen HQ, Zhu JS, Baron AD. Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 49: 684-687, 2000.
26. St-Pierre P, Genders AJ, Keske MA, Richards SM, Rattigan S. Loss of insulin-mediated microvascular perfusion in skeletal muscle is associated with the development of insulin resistance. Diabetes Obes Metab 12: 798-805, 2010.
27. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. Insulinmediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest 94: 1172-1179, 1994.
28. Symons JD, McMillin SL, Riehle C, Tanner J, Palionyte M, Hillas E, Jones D, Cooksey RC, Birnbaum MJ, McClain DA, Zhang QJ, Gale D, Wilson LJ, Abel ED. Contribution of insulin and Akt1 signaling to endothelial nitric oxide synthase in the regulation of endothelial function and blood pressure. Circ Res 104: 1085-1094, 2009.
29. Traystman RJ, Moore LE, Helfaer MA, Davis S, Banasiak K, Williams M, Hurn PD. Nitro-L-arginine analogues. Dose- and time-related nitric oxide synthase inhibition in brain. Stroke 26: 864-869, 1995.
30. Trovati M, Massucco P, Mattiello L, Costamagna C, Aldieri E, Cavalot F, Anfossi G, Bosia A, Ghigo D. Human vascular smooth muscle cells express a constitutive nitric oxide synthase that insulin rapidly activates, thus increasing guanosine 3=:5=-cyclic monophosphate and adenosine 3=:5=-cyclic monophosphate concentrations. Diabetologia 42: 831-839, 1999.
31. Vincent MA, Barrett EJ, Lindner JR, Clark MG, Rattigan S. Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 285: E123-E129, 2003.
32. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S, Barrett EJ. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53: 1418-1423, 2004.
33. Vincent MA, Clerk LH, Lindner JR, Price WJ, Jahn LA, Leong-Poi H, Barrett EJ. Mixed meal and light exercise each recruit muscle capillaries in healthy humans. Am J Physiol Endocrinol Metab 290: E1191-E1197, 2006.
34. Vincent MA, Dawson D, Clark AD, Lindner JR, Rattigan S, Clark MG, Barrett EJ. Skeletal muscle microvascular recruitment by physiological hyperinsulinemia precedes increases in total blood flow. Diabetes 51: 42-48, 2002.
35. Vincent MA, Montagnani M, Quon MJ. Molecular and physiologic actions of insulin related to production of nitric oxide in vascular endothelium. Curr Diabetes Rep 3: 279-288, 2003.
36. Wallis MG, Wheatley CM, Rattigan S, Barrett EJ, Clark AD, Clark MG. Insulin-mediated hemodynamic changes are impaired in muscle of zucker obese rats. Diabetes 51: 3492-3498, 2002.
37. Youd JM, Rattigan S, Clark MG. Acute impairment of insulin-mediated capillary recruitment and glucose uptake in rat skeletal muscle in vivo by TNFa. Diabetes 49: 1904-1909, 2000.
38. 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.
39. Zeng GY, 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.
40. Zhang L, Vincent MA, Richards SM, Clerk LH, Rattigan S, Clark MG, Barrett EJ. Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 53: 447-453, 2004.