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DOI: 10.1055/s-2002-19710
Effect of a Nitric Oxide Donor on Microcirculation of Acutely Denervated Skeletal Muscle during Reperfusion
Publication History
Publication Date:
24 January 2002 (online)
ABSTRACT
The authors have shown that exogenous nitric oxide (NO) protects innervated skeletal muscle against reperfusion injury. This study further evaluated the effects of exogenous NO donor on denervated skeletal muscle. Forty-eight denervated rat cremaster muscles underwent 3 hr of ischemia, followed by 90 min of reperfusion, and received systemic infusion of 100 nmol/min s-nitroso-n-acetylcysteine (SNAC) or an equal amount of phosphate-buffered saline (PBS). Results showed that the average diameter in 10 to 20 μm arterioles was between 107 percent and 123 percent of baseline in the SNAC group, and between 55 percent and 84 percent in the PBS group during 90 min of reperfusion. These values in 21 to 40 μm and 41 to 70 μm arteries were between 100 percent and 110 percent in the SNAC group, and between 70 percent and 90 percent in the PBS group from 20 to 90 min of reperfusion. Compared to the PBS group, the SNAC group had a statistically significantly greater vessel diameter in both 10 to 20 μm (p<0.001) and 21 to 40 μm arterioles (p<0.01) during 90 min of reperfusion, and in 41 to 70 μm arteries (p<0.02) from 20 to 90 min of reperfusion. The overall blood flow of the muscle in the SNAC group increased from 37 percent of baseline at 10 min to 108 percent at 40 min of reperfusion, and remained above baseline thereafter. In contrast, this value in the PBS group was only between 27 percent and 68 percent of baseline during 90 min of reperfusion. The blood flow was statistically significantly (p<0.03) greater in the SNAC group than in the PBS group from 40 to 90 min of reperfusion. Among the conclusions were: (1) NO donor SNAC improves the microcirculation of denervated skeletal muscle during early reperfusion; and (2) this protection against reperfusion injury is independent of innervation in skeletal muscle.
KEYWORD
Muscle - nitric oxide - microcirculation - ischemia - denervation
REFERENCES
- 1 Chen L E, Seaber A V, Urbaniak J R. The effect of denervation of skeletal muscle: rat cremaster model. J Orthop Res . 1991; 9 266
- 2 Chen L E, Seaber A V, Urbaniak J R. Combined effect of acute denervation and ischemia on the microcirculation of skeletal muscle. J Orthop Res . 1992; 10 112
- 3 Wang W Z, Anderson G L, Firrell J C. Arteriole constriction following ischemia denervated skeletal muscle. J Reconstr Microsurg . 1995; 11 99
- 4 Gazdag A, Chen L E, Hagen P. Effect of denervation on endothelium-derived raalaxing factor-dependent relaxation in the rat cremaster muscle. Microsurgery . 1993; 14 494
- 5 Sternberg W C, Makhoul R G, Adelman B. Nitric oxide-mediated, endothelium-dependent vasodilation is selectively attenuated in the postischemic extremities. Surgery . 1993; 114 960
- 6 Wang W Z, Anderson G, Fleming J T. Lack of nitric oxide contributes to vasospasm during ischemia/reperfusion injury. Plast Reconstr Surg . 1997; 99 1099
- 7 Liu K, Chen L E, Seaber A V. S-nitroso-n-acetylcysteine protects skeletal muscle against reperfusion injury. Microsurgery . 1998; 19 299
- 8 Chen L E, Seaber A V, Nasser R M. Effects of S-nitroso-n-acetylctsteine on contractile function of reperfused skeletal muscle. Am J Physiol . 1998; 274 R822
- 9 Engelman D T, Watanabe M, Engelman R M. Constitutive nitric oxide release is impaired after ischemia and reperfusion. J Thorac Cardiovasc Surg . 1995; 110 1047
- 10 Meldrum D G, Stephenson L L, Zamboni W A. Effects of LNAME and L-arginine on ischemia-reperfusion injury in rat skeletal muscle. Plast Reconstr Surg . 1999; 103 935
- 11 Lovett III E J, Fink B F, Bernard A. Analysis of nitric oxide activity in prevention of reperfusion injury. Ann Plast Surg . 2001; 46 269
- 12 Cordeiro P G, Santamaria E, Hu Q Y. Use of a nitric oxide precursor to protect pig myocutaneous flaps from ischemia-reperfusion injury. Plast Reconstr Surg . 1998; 102 2040
- 13 Pudupakkam S, Harris K A, Jamieson W G. Ischemic tolerance in skeletal muscle: role of nitric oxide. Am J Physiol . 1998; 275 H94
- 14 Wang W Z, Anderson G L, Guo S Z. Initiation of microvascular protection by nitric oxide in late preconditioning. J Reconstr Microsurg . 2000; 16 621
- 15 Huk I, Brovkovych V, Nanobashvili J. Prostaglandin E1 reduces ischemia/reperfusion injury by normalizing nitric oxide and superoxide release. Shock . 2000; 14 234
- 16 Nakamura K, Yokoyama K, Itoman M. Changes in nitric oxide, superoxide, and blood circulation in muscles over time after warm ischaemic reperfusion in rabbit rectus femoris muscle. Scand J Plast Reconstr Surg Hand Surg . 2001; 35 13
- 17 Stamler J S. S-nitrosothiols: correlation of biological chemistry with physiological actions. In: Weissman BA, Allon N, Shapira S (eds): Biochemical, Pharmacological, and Clinical Aspects of Nitric Oxide New York: Plenum Press 1995: 67-78
- 18 Kashiba M, Kasahara E, Chien K C. Fates and vascular action of S-nitrosoglutathione and related compounds in the circulation. Arch Biochem Biophys . 1999; 363 213
- 19 Hogg N. Biological chemistry and clinical potential of Snitrosothiols. Free Radic Biol Med . 2000; 28 1478
- 20 Ceron P I, Cremonez D C, Bendhack L M. The relaxation induced by S-nitroso-glutathione and S-nitroso-N- acetylcysteine in rat aorta is not related to nitric oxide production. J Pharmacol Exp Ther . 2001; 298 686
- 21 Mathews W R, Kerr S W. Biological activity of S-nitrosothiols: the role of nitric oxide. J Pharmacol Exp Ther . 1993; 267 1529
- 22 Janero D R. Nitric oxide (NO)-related pharmaceuticals: contemporary approaches to therapeutic no modulation. Free Radical Biol Med . 2001; 28 1495
- 23 Singh R J, Hogg N, Joseph J. Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem . 1996; 271 18596
- 24 Nikitovic D, Holmgren A. S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem . 1996; 271 19180
- 25 Aleryani S, Milo E, Rose Y. Superoxide-mediated decomposition of biological S-nitrosothiols. J Biol Chem . 1998; 273 6041
- 26 Liu L, Hausladen A, Zeng M. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature . 2001; 410 490
- 27 Arstall M A, Bailey C, Gross W L. Reversible Snitrosation of creatine kinase by nitric oxide in adult rat ventricular myocytes. J Mol Cell Cardiol . 1998; 30 979
- 28 Al-Mustafa A H, Sies H, Stahl W. Sulfur-to-nitrogen transnitrosation: transfer of nitric oxide from S-nitroso compounds to diethanolamine and the role of intermediate sulfur- to-sulfur transnitrosation. Toxicology . 2001; 163 127
- 29 Konorev E A, Joseph J, Tarpey M M. The mechanism of cardioprotection by S-nitrosoglutathione monoethyl ester in rat isolated heart during cardioplegic ischaemic arrest. Br J Pharmacol . 1996; 119 511
- 30 Hoshida S, Yamashita N, Igarashi J. A nitric oxide donor reverses myocardial injury in rabbits with acute hypercholesterolemia. J Pharmacol Exp Ther . 1996; 278 741
- 31 Lehr H A, Guhlmann A, Nolte D. Leukotrienes as mediators in ischemia-reperfusion injury in a microcirculation model in the hamster. J Clin Invest . 1991; 87 2036
- 32 Kurose I, Wolf R, Grisham M B. Modulation of ischemia/reperfusion-induced microvascular dysfunction by nitric oxide. Circ Res . 1994; 74 376
- 33 Kretzschmar M, Klein U, Palutke M. Reduction of ischemia-reperfusion syndrome after abdominal aortic aneurysmectomy by N-acetylcysteine but not mannitol. Acta Anaesthesiol Scand . 1996; 40 657
- 34 Knuckey N W, Palm D, Primiano M. N-acetylcysteine enhances hippocampal neuronal survival after transient forebrain ischemia in rats. Stroke . 1995; 26 305
- 35 Liu C J, Ueda M, Kosaka S. A newly developed solution enhances thirty-hour preservation in a canine lung transplantation model. J Thorac Cardiovasc Surg . 1996; 112 569
- 36 Delp M D, Laughlin M H. Regulation of skeletal muscle perfusion during exercise. Acta Physiol Scand . 1998; 162 411
- 37 Guyton A C, Hall J E. The Textbook of Medical Physiology, 9th edition Philadelpia: W. B. Saunders Co., 1996: 73-86
- 38 Honig C R, Frierson J L, Patterson J L. Comparison of neural controls of resistance and capillary density in resting muscle. Am J Physiol . 1970; 218 937
- 39 Joyner M J, Nauss L A, Warner M A. Sympathetic modulation of blood flow and O2 uptake in rhythmically contracting human forearm muscle. Am J Physiol . 1992; 263 H1078
- 40 Chen L E, Gu Y D, Wu M M. Effects of ischemia on the histology and muscular force of striated muscle in rabbit. Acta Academiae Med Primae Shanghai . 1985; 12 167
- 41 Harris K, Walker P M, Mickle D AG. Metabolic response of skeletal muscle to ischemia. Am J Physiol . 1986; 250 H213
- 42 Lash J M. Regulation of skeletal muscle blood flow during contractions. Proc Soc Exper Biol Med . 1996; 211 218
- 43 Rowell L B, O'Leary D S. Reflex control of the circulation during execise: chemoreflexes and mechanoreflexes. J Appl Physiol . 1990; 69 407
- 44 Urbaniak J R, Seaber A V, Chen L E. Assessment of ischemia and reperfusion injury. Clin Orthop . 1997; 334 30
- 45 Victor R G, Bertocci L A, Pryor S L. Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J Clin Invest . 1988; 82 1301
- 46 Habler H J, Wasner G, Janig W. Attenuation of neurogenic vasoconstriction by nitric oxide in hindlimb microvascular beds of the rat in vivo. Hypertension . 1997; 30 957
- 47 Cocks T M, Angus J A. Endothelium-dependent relaxation of coronary arteries by noradrenaline and serotonin. Nature . 1983; 305 627
- 48 Thorin E, Atkinson J. Modulation by the endothelium of sympathetic vasoconstriction in an in vitro preparation of the rat tail artery. Br J Pharmacol . 1994; 111 351
- 49 Nase P, Boegehold M A. Nitric oxide modulates arteriolar responses to increased sympathetic nerve activity. Am J Physiol . 1996; 271 H860
- 50 Klitzman B. Microvascular determinants of blood flow. J Reconstr Microsurg . 1987; 4 77