Effects of neuronal nitric oxide synthase inhibition on resting and exercising hindlimb muscle blood flow in the rat

Journal of Physiology

Volumn 588, Issue 8, 2010, Pages 1321-1331

  Copp, Steven W ^a   Hirai, Daniel M ^a   Schwagerl, Peter J ^a   Musch, Timothy I ^a   Poole, David C ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; S METHYLTHIOCITRULLINE; ACETYLCHOLINE;

ADRENAL BLOOD FLOW; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; KIDNEY BLOOD FLOW; LEG BLOOD FLOW; LIVER BLOOD FLOW; MALE; MUSCLE BLOOD FLOW; MUSCLE CELL; MUSCLE FIBER MEMBRANE CONDUCTANCE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REST; SPRAGUE DAWLEY RAT; TREADMILL EXERCISE; ADULT; HEART RATE; HINDLIMB MUSCLE; HYPEREMIA; HYPOTENSION; MEAN ARTERIAL PRESSURE; SPLANCHNIC BLOOD FLOW; VASCULAR RESISTANCE; YOUNG ADULT;

ANIMALS; BLOOD PRESSURE; CITRULLINE; ENZYME INHIBITORS; HEART RATE; HINDLIMB; MALE; MODELS, ANIMAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE I; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; REST; THIOUREA;

EID: 77953226218     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.183723     Document Type: Article

References (45)

1. Buckwalter JB, Taylor JC, Hamann JJ, Clifford PS. Role of nitric oxide in exercise sympatholysis. J Appl Physiol 2004, 97:417-423.
2. Clifford PS, Hellsten Y. Vasodilatory mechanisms in contracting skeletal muscle. J Appl Physiol 2004, 97:393-403.
3. Copp SW, Hirai DM, Hageman KS, Poole DC, Musch TI. Nitric oxide synthase inhibition during treadmill exercise reveals fibre-type specific vascular control in the rat hindlimb. Am J Physiol Regul Integr Comp Physiol 2010, 298:R478-R485.
4. Delp MD, Duan C. Composition and size of type I, IIA, IID/X, and IIB fibres and citrate synthase activity of rat muscle. J Appl Physiol 1996, 80:261-270.
5. Dinenno FA, Joyner MJ. Blunted sympathetic vasoconstriction in contracting skeletal muscle of healthy humans: is nitric oxide obligatory. J Physiol 2003, 553:281-292.
6. Dinenno FA, Joyner MJ. Combined NO and PG inhibition augments α-adrenergic vasoconstriction in contracting human skeletal muscle. Am J Physiol Heart Circ Physiol 2004, 287:H2576-H2584.
7. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
8. Fadel PJ, Zhao W, Thomas GD. Impaired vasomodulation is associated with reduced neuronal nitric oxide synthase in skeletal muscle of ovariectomized rats. J Physiol 2003, 549:243-253.
9. Furfine ES, Harmon MF, Paith JE, Knowles RG, Salter M, Kiff RJ, Duffy C, Hazelwood R, Oplinger JA, Garvey EP. Potent and selective inhibition of human nitric oxide synthases. Selective inhibition of neuronal nitric oxide synthase by S-methyl-L-thiocitrulline and S-ethyl-L-thiocitrulline. J Biol Chem 1994, 269:26677-26683.
10. Grange RW, Isotani E, Lau KS, Kamm KE, Huang PL, Stull JT. Nitric oxide contributes to vascular smooth muscle relaxation in contracting fast-twitch muscles. Physiol Genomics 2001, 5:35-44.
11. Hirai T, Musch TI, Morgan DA, Kregel KC, Claassen DE, Pickar JG, Lewis SJ, Kenney MJ. Differential sympathetic nerve responses to nitric oxide synthase inhibition in anaesthetized rats. Am J Physiol Regul Integr Comp Physiol 1995, 269:R807-R813.
12. Hirai T, Visneski MD, Kearns KJ, Zelis R, Musch TI. Effects of NO synthase inhibition on the muscular blood flow response to treadmill exercise in rats. J Appl Physiol 1994, 77:1288-1293.
13. Hirschfield W, Moody MR, O'Brien WE, Gregg AR, Bryan RM, Reid MB. Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS. Am J Physiol Regul Integr Comp Physiol 2000, 278:R95-R100.
14. Huang A, Sun D, Shesely EG, Levee EM, Koller A, Kaley G. Neuronal NOS-dependent dilation to flow in coronary arteries of male eNOS-KO mice. Am J Physiol Heart Circ Physiol 2002, 282:H429-H436.
15. Ichihara A, Inscho EW, Imig JD, Navar LG. Neuronal nitric oxide synthase modulates rat renal microvascular function. Am J Physiol Renal Physiol 1998, 274:F516-F524.
16. Ikenaga H, Fallet RW, Carmines PK. Basal nitric oxide production curtails arteriolar vasoconstrictor responses to ANG II in rat kidney. Am J Physiol Renal Physiol 1996, 271:F365-F373.
17. Jankord R, McAllister RM, Ganjam VK, Laughlin MH. Chronic inhibition of nitric oxide synthase augments the ACTH response to exercise. Am J Physiol Regul Integr Comp Physiol 2009, 296:R728-R734.
18. Jansson L, Carlsson PO, Bodin B, Andersson A, Kallskog O. Neuronal nitric oxide synthase and splanchnic blood flow in anaesthetized rats. Acta Physiol Scand 2005, 183:257-262.
19. Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, Creager MA. Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 1993, 88:2510-2516.
20. Joyner MJ, Dietz NM. Nitric oxide and vasodilation in human limbs. J Appl Physiol 1997, 83:1785-1796.
21. Kavdia M, Popel AS. Contribution of nNOS- and eNOS-derived NO to microvascular smooth muscle NO exposure. J Appl Physiol 2004, 97:293-301.
22. Kobzik L, Reid MB, Bredt DS, Stamler JS. Nitric oxide in skeletal muscle. Nature 1994, 372:546-548.
23. Komers R, Oyama TT, Chapman JG, Allison KM, Anderson S. Effects of systemic inhibition of neuronal nitric oxide synthase in diabetic rats. Hypertension 2000, 35:655-661.
24. Kubo SH, Rector TS, Bank AJ, Williams RE, Heifetz SM. Endothelium-dependent vasodilation is attenuated in patients with heart failure. Circulation 1991, 84:1589-1596.
25. Kwon O, Hong SM, Ramesh G. Diminished NO generation by injured endothelium and loss of macula densa nNOS may contribute to sustained acute kidney injury after ischemia-reperfusion. Am J Physiol Renal Physiol 2009, 296:F25-F33.
26. Lai Y, Thomas GD, Yue Y, Yang HT, Li D, Long C, Judge L, Bostick B, Chamberlain JS, Terjung RL, Duan D. Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 2009, 119:624-635.
27. 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 2000, 2:21-27.
28. McNaughton L, Puttagunta L, Martinez-Cuesta MA, Kneteman N, Mayers I, Moqbel R, Hamid Q, Radomski MW. Distribution of nitric oxide synthase in normal and cirrhotic human liver. Proc Natl Acad Sci U S A 2002, 99:17161-17166.
29. Musch TI, Bruno A, Bradford GE, Vayonis A, Moore RL. Measurements of metabolic rate in rats: a comparison of techniques. J Appl Physiol 1988, 65:964-970.
30. Musch TI, McAllister RM, Symons JD, Stebbins CL, Hirai T, Hageman KS, Poole DC. Effects of nitric oxide synthase inhibition on vascular conductance during high speed treadmill exercise in rats. Exp Physiol 2001, 86:749-757.
31. Musch TI, Terrell JA. Skeletal muscle blood flow abnormalities in rats with a chronic myocardial infarction: rest and exercise. Am J Physiol Heart Circ Physiol 1992, 262:H411-H419.
32. Radegran G, Hellsten Y. Adenosine and nitric oxide in exercise-induced human skeletal muscle vasodilatation. Acta Physiol Scand 2000, 168:575-591.
33. Roberts CK, Barnard RJ, Jasman A, Balon TW. Acute exercise increases nitric oxide synthase activity in skeletal muscle. Am J Physiol Endocrinol Metab 1999, 277:E390-E394.
34. Rockey DC, Chung JJ. Reduced nitric oxide production by endothelial cells in cirrhotic rat liver: endothelial dysfunction in portal hypertension. Gastroenterology 1998, 114:344-351.
35. Rowell L. Human Cardiovascular Control 1993, Oxford University Press, Inc., New York
36. Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, Thomas GD, Victor RG. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 2000, 97:13818-13823.
37. Schrage WG, Eisenach JH, Joyner MJ. Ageing reduces nitric-oxide- and prostaglandin-mediated vasodilatation in exercising humans. J Physiol 2007, 579:227-236.
38. Seddon M, Melikian N, Dworakowski R, Shabeeh H, Jiang B, Byrne J, Casadei B, Chowienczyk P, Shah AM. Effects of neuronal nitric oxide synthase on human coronary artery diameter and blood flow in vivo. Circulation 2009, 119:2656-2662.
39. Seddon MD, Chowienczyk PJ, Brett SE, Casadei B, Shah AM. Neuronal nitric oxide synthase regulates basal microvascular tone in humans in vivo. Circulation 2008, 117:1991-1996.
40. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev 2001, 81:209-237.
41. Talukder MA, Fujiki T, Morikawa K, Motoishi M, Kubota H, Morishita T, Tsutsui M, Takeshita A, Shimokawa H. Up-regulated neuronal nitric oxide synthase compensates coronary flow response to bradykinin in endothelial nitric oxide synthase-deficient mice. J Cardiovasc Pharmacol 2004, 44:437-445.
42. Thomas GD, Sander M, Lau KS, Huang PL, Stull JT, Victor RG. Impaired metabolic modulation of α-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci U S A 1998, 95:15090-15095.
43. Thomas GD, Shaul PW, Yuhanna IS, Froehner SC, Adams ME. Vasomodulation by skeletal muscle-derived nitric oxide requires α-syntrophin-mediated sarcolemmal localization of neuronal nitric oxide synthase. Circ Res 2003, 92:554-560.
44. Wakefield ID, March JE, Kemp PA, Valentin JP, Bennett T, Gardiner SM. Comparative regional haemodynamic effects of the nitric oxide synthase inhibitors, S-methyl-L-thiocitrulline and L-NAME, in conscious rats. Br J Pharmacol 2003, 139:1235-1243.
45. Wei CL, Khoo HE, Lee KH, Hon WM. Differential expression and localization of nitric oxide synthases in cirrhotic livers of bile duct-ligated rats. Nitric Oxide 2002, 7:91-102.