Local nitric oxide synthase inhibition reduces skeletal muscle glucose uptake but not capillary blood flow during in situ muscle contraction in rats

Diabetes

Volumn 56, Issue 12, 2007, Pages 2885-2892

  Ross, Renee M ^a   Wadley, Glenn D ^b   Clark, Michael G ^a   Rattigan, Stephen ^a   McConell, Glenn K ^b  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY BLOOD FLOW; ARTICLE; BLOOD PRESSURE; CAPILLARY FLOW; CARDIOVASCULAR RESPONSE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVATION; ENZYME INHIBITION; EPIGASTRIC ARTERY; FEMORAL ARTERY; GLUCOSE TRANSPORT; HEART RATE; LEG MUSCLE; MALE; MUSCLE BLOOD FLOW; MUSCLE EXCITATION; MUSCLE FORCE; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; WISTAR RAT;

ANIMALS; BLOOD FLOW VELOCITY; CAPILLARIES; ENZYME INHIBITORS; GLUCOSE; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, WISTAR;

EID: 36849093422     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db07-0745     Document Type: Article

References (49)

1. Richter EA, Derave W, Wojtaszewski JF: Glucose, exercise and insulin: emerging concepts. J Physiol 535:313-322, 2001
2. Kennedy JW, Hirshman MF, Gervino EV, Ocel JV, Forse RA, Hoenig SJ, Aronson D, Goodyear LJ, Horton ES: Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 48:1192-1197, 1999
3. Kingwell B, Formosa M, Muhlmann M, Bradley S, McConell G: Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 51:2572-2580, 2002
4. Bradley SJ, Kingwell BA, McConell GK: Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes 48:1815-1821, 1999 [Erratum in Diabetes 48:2480, 1999]
5. Rattigan S, Clark MG, Barrett EJ: Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46:1381-1388, 1997
6. 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
7. Etgen GJ Jr, Fryburg DA, Gibbs EM: Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway. Diabetes 46:1915-1919, 1997
8. Balon TW, Nadler JL: Evidence that nitric oxide increases glucose transport in skeletal muscle. J Appl Physiol 82:359-363, 1997
9. Higaki Y, Hirshman MF, Fujii N, Goodyear LJ: Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 50:241-247, 2001
10. Roberts CK, Barnard RJ, Scheck SH, Balon TW: Exercise-stimulated glucose transport in skeletal muscle is nitric oxide dependent. Am J Physiol 273:E220-E225, 1997
11. Rottman J, Bracy D, Malabanan C, Yue Z, Clanton J, Wasserman D: Contrasting effects of exercise and NOS inhibition on tissue-specific fatty acid and glucose uptake in mice. Am J Physiol Endocrinol Metab 283:E116-E123, 2002
12. Stephens TJ, Canny BJ, Snow RJ, McConell GK: 5′-aminoimidazole-4- carboxyamide-ribonucleoside-activated glucose transport is not prevented by nitric oxide synthase inhibition in rat isolated skeletal muscle. Clin Exp Pharmacol Physiol 31:419-423, 2004
13. McConell GK, Kingwell BA: Does nitric oxide regulate skeletal muscle glucose uptake during exercise? Exerc Sport Sci Rev 34:36-41, 2006
14. Dawson D, Vincent MA, Barrett EJ, Kaul S, Clark A, Leong-Poi H, Lindner JR: Vascular recruitment in skeletal muscle during exercise and hyperinsulinemia assessed by contrast ultrasound. Am J Physiol Endocrinol Metab 282:E714-E720, 2002
15. Mahajan H, Richards SM, Rattigan S, Clark MG: Local methacholine but not bradykinin potentiates insulin-mediated glucose uptake in muscle in vivo by augmenting capillary recruitment. Diabetologia 47:2226-2234, 2004
16. Lindner JR, Wei K: Contrast echocardiography. Curr Probl Cardiol 27:454-519, 2002
17. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S: Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97:473-483, 1998
18. Wei K, Le E, Bin JP, Coggins M, Thorpe J, Kaul S: Quantification of renal blood flow with contrast-enhanced ultrasound. J Am Coll Cardiol 37:1135-1140, 2001
19. Chen ZP, McConell GK, Michell BJ, Snow RJ, Canny BJ, Kemp BE: AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol Endocrinol Metab 279:E1202-E1206, 2000
20. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE: AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443:285-289, 1999
21. Wadley GD, Lee-Young RS, Canny BJ, Wasuntarawat C, Chen ZP, Hargreaves M, Kemp BE, McConell GK: Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am J Physiol Endocrinol Metab 290:E694-E702, 2006
22. Young ME, Leighton B: Evidence for altered sensitivity of the nitric oxide/cGMP signalling cascade in insulin-resistant skeletal muscle. Biochem J 329:73-79, 1998
23. Roberts CK, Barnard RJ, Jasman A, Balon TW: Acute exercise increases nitric oxide synthase activity in skeletal muscle. Am J Physiol 277:E390-E394, 1999
24. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ: Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47:1369-1373, 1998
25. Chen Z-P, Stephens TJ, Murthy S, Canny BJ, Hargreaves M, Witters LA, Kemp BE, McConell GK: Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes 52:2205-2212, 2003
26. Richter EA, Nielsen JN, Jorgensen SB, Frosig C, Birk JB, Wojtaszewski JF: Exercise signalling to glucose transport in skeletal muscle. Proc Nutr Soc 63:211-216, 2004
27. Zou MH, Hou XY, Shi CM, Kirkpatick S, Liu F, Goldman MH, Cohen RA: Activation of 5′-AMP-activated kinase is mediated through c-Src and phosphoinositide 3-kinase activity during hypoxia-reoxygenation of bovine aortic endothelial cells: role of peroxynitrite. J Biol Chem 278:34003-34010, 2003
28. Park SH, Gammon SR, Knippers JD, Paulsen SR, Rubink DS, Winder WW: Phosphorylation-activity relationships of AMPK and acetyl-CoA carboxylase in muscle. J Appl Physiol 92:2475-2482, 2002
29. Lee-Young RS, Palmer MJ, Linden KC, LePlastrier K, Canny BJ, Hargreaves M, Wadley GD, Kemp BE, McConell GK: Carbohydrate ingestion does not alter skeletal muscle AMPK signaling during exercise in humans. Am J Physiol Endocrinol Metab 291:E566-E573, 2006
30. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, Katz A: Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575:251-262, 2006
31. Musi N, Hayashi T, Fujii N, Hirshman MF, Witters LA, Goodyear LJ: AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle. Am J Physiol Endocrinol Metab 280:E677-E684, 2001
32. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ: A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7:1085-1094, 2001
33. McConell GK, Lee-Young RS, Chen ZP, Stepto NK, Huynh NN, Stephens TJ, Canny BJ, Kemp BE: Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen. J Physiol 568:665-676, 2005
34. Jorgensen SB, Viollet B, Andreelli F, Frosig C, Birk JB, Schjerling P, Vaulont S, Richter EA, Wojtaszewski JF: Knockout of the alpha2 but not alpha1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4- carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. J Biol Chem 279:1070-1079, 2004
35. Fujii N, Hirshman MF, Kane EM, Ho RC, Peter LE, Seifert MM, Goodyear LJ: AMP-activated protein kinase alpha2 activity is not essential for contraction- and hyperosmolarity-induced glucose transport in skeletal muscle. J Biol Chem 280:39033-39041, 2005
36. Wojtaszewski JF, MacDonald C, Nielsen JN, Hellsten Y, Hardie D, Kemp BE, Kiens B, Richter EA: Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab 284:E813-E822, 2003
37. Lau KS, Grange RW, Isotani E, Sarelius IH, Kamm KE, Huang PL, Stull JT: nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle. Physiol Genomics 2:21-27, 2000
38. Krogh A: August Krogh-Nobel Lecture: A contribution to the physiology of the capillaries. In Nobel Lectures, Physiology or Medicine 1901-1921. Amsterdam, Elsevier Publishing Company, 1967, p. 1-8
39. Lindbom L, Tuma RF, Arfors KE: Influence of oxygen on perfused capillary density and capillary red cell velocity in rabbit skeletal muscle. Microvasc Res 19:197-208, 1980
40. Kindig CA, Richardson TE, Poole DC: Skeletal muscle capillary hemodynamics from rest to contractions: implications for oxygen transfer. J Appl Physiol 92:2513-2520, 2002
41. 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
42. 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
43. 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
44. Rattigan S, Bradley EA, Richards SM, Clark MG: Muscle metabolism and control of capillary blood flow: insulin and exercise. Essays Biochem 42:133-144, 2006
45. Rattigan S, Clark MG, Barrett EJ: Acute vasoconstriction-induced insulin resistance in rat muscle in vivo. Diabetes 48:564-569, 1999
46. Wheatley CM, Rattigan S, Richards SM, Barrett EJ, Clark MG: Skeletal muscle contraction stimulates capillary recruitment and glucose uptake in insulin-resistant obese Zucker rats. Am J Physiol Endocrinol Metab 287:E804-E809, 2004
47. 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
48. Frandsen U, Bangsbo J, Sander M, Hoffner L, Betak A, Saltin B, Hellsten Y: Exercise-induced hyperaemia and leg oxygen uptake are not altered during effective inhibition of nitric oxide synthase with N(G)-nitro-L-arginine methyl ester in humans. J Physiol 531:257-264, 2001
49. 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