Oxidative stress and enhanced sympathetic vasoconstriction in contracting muscles of nitrate-tolerant rats and humans

Journal of Physiology

Volumn 590, Issue 2, 2012, Pages 395-407

  Fadel, Paul J ^a   Farias Iii, Martin ^a   Gallagher, Kevin M ^a   Wang, Zhongyun ^a   Thomas, Gail D ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHIDIUM; GLYCERYL TRINITRATE; ISOPROSTANE DERIVATIVE; REACTIVE OXYGEN METABOLITE;

ADRENERGIC STIMULATION; ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG TOLERANCE; EVOKED RESPONSE; FLUORESCENCE ANALYSIS; FOREARM; HAND GRIP; HINDLIMB; HUMAN; HUMAN EXPERIMENT; LOWER BODY NEGATIVE PRESSURE; MALE; MUSCLE CONTRACTION; MUSCLE EXERCISE; NERVOUS SYSTEM CONDUCTANCE; NONHUMAN; NORMAL HUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT; REFLEX; REST; SKELETAL MUSCLE; SYMPATHETIC NERVE; VASOCONSTRICTION;

ADULT; ANIMALS; BIOLOGICAL MARKERS; F2-ISOPROSTANES; HUMANS; MALE; MODELS, ANIMAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NITRATES; NITROGLYCERIN; OXIDATIVE STRESS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REGIONAL BLOOD FLOW; SYMPATHETIC NERVOUS SYSTEM; VASOCONSTRICTION; VASODILATOR AGENTS;

EID: 84862907947     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.218917     Document Type: Article

References (56)

1. Armitage ME, Wingler K, Schmidt HH & La M (2009). Translating the oxidative stress hypothesis into the clinic: NOX versus NOS. J Mol Med 87, 1071-1076.
2. Bailey DM, McEneny J, Mathieu-Costello O, Henry RR, James PE, McCord JM, Pietri S, Young IS & Richardson RS (2010). Sedentary aging increases resting and exercise-induced intramuscular free radical formation. J Appl Physiol 109, 449-456.
3. Chavoshan B, Sander M, Sybert TE, Hansen J, Victor RG & Thomas GD (2002). Nitric oxide-dependent modulation of sympathetic neural control of oxygenation in exercising human skeletal muscle. J Physiol 540, 377-386.
4. Chen Z, Zhang J & Stamler JS (2002). Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci U S A 99, 8306-8311.
5. Christiansen I, Iversen HK & Olesen J (2000). Headache characteristics during the development of tolerance to nitrates: pathophysiological implications. Cephalalgia 20, 437-444.
6. Cracowski JL, Durand T & Bessard G (2002). Isoprostanes as a biomarker of lipid peroxidation in humans: physiology, pharmacology and clinical implications. Trends Pharmacol Sci 23, 360-366.
7. Dalla Libera L, Ravara B, Gobbo V, Danieli Betto D, Germinario E, Angelini A & Vescovo G (2005). Skeletal muscle myofibrillar protein oxidation in heart failure and the protective effect of Carvedilol. J Mol Cell Cardiol 38, 803-807.
8. Dinenno FA & Joyner MJ (2004). Combined NO and PG inhibition augments α-adrenergic vasoconstriction in contracting human skeletal muscle. Am J Physiol Heart Circ Physiol 287, H2576-H2584.
9. Dinenno FA, Masuki S & Joyner MJ (2005). Impaired modulation of sympathetic α-adrenergic vasoconstriction in contracting forearm muscle of ageing men. J Physiol 567, 311-321.
10. Donato AJ, Eskurza I, Silver AE, Levy AS, Pierce GL, Gates PE & Seals DR (2007). Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-κB. Circ Res 100, 1659-1666.
11. Fadel PJ, Keller DM, Watanabe H, Raven PB & Thomas GD (2004). Noninvasive assessment of sympathetic vasoconstriction in human and rodent skeletal muscle using near-infrared spectroscopy and Doppler ultrasound. J Appl Physiol 96, 1323-1330.
12. Fleckenstein JL, Watumull D, Bertocci LA, Parkey RW & Peshock RM (1992). Finger-specific flexor recruitment in humans: depiction by exercise-enhanced MRI. J Appl Physiol 72, 1974-1977.
13. Forstermann U (2010). Nitric oxide and oxidative stress in vascular disease. Pflugers Arch 459, 923-939.
14. Frame MD, Fox RJ, Kim D, Mohan A, Berk BC & Yan C (2002). Diminished arteriolar responses in nitrate tolerance involve ROS and angiotensin II. Am J Physiol Heart Circ Physiol 282, H2377-H2385.
15. Gori T & Parker JD (2002). Nitrate tolerance: a unifying hypothesis. Circulation 106, 2510-2513.
16. Griendling KK, Minieri CA, Ollerenshaw JD & Alexander RW (1994). Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74, 1141-1148.
17. Hansen J, Thomas GD, Harris SA, Parsons WJ & Victor RG (1996). Differential sympathetic neural control of oxygenation in resting and exercising human skeletal muscle. J Clin Invest 98, 584-596.
18. 2α metabolite excretion rate and day to day variation in healthy humans. Prostaglandins Leukot Essent Fatty Acids 65, 99-102.
19. Hink U, Daiber A, Kayhan N, Trischler J, Kraatz C, Oelze M, Mollnau H, Wenzel P, Vahl CF, Ho KK, Weiner H & Munzel T (2007). Oxidative inhibition of the mitochondrial aldehyde dehydrogenase promotes nitroglycerin tolerance in human blood vessels. J Am Coll Cardiol 50, 2226-2232.
20. Hink U, Oelze M, Kolb P, Bachschmid M, Zou MH, Daiber A, Mollnau H, August M, Baldus S, Tsilimingas N, Walter U, Ullrich V & Munzel T (2003). Role for peroxynitrite in the inhibition of prostacyclin synthase in nitrate tolerance. J Am Coll Cardiol 42, 1826-1834.
21. Jurt U, Gori T, Ravandi A, Babaei S, Zeman P & Parker JD (2001). Differential effects of pentaerythritol tetranitrate and nitroglycerin on the development of tolerance and evidence of lipid peroxidation: a humanin vivostudy. J Am Coll Cardiol 38, 854-859.
22. Kirby BS, Crecelius AR, Voyles WF & Dinenno FA (2011). Modulation of postjunctional α-adrenergic vasoconstriction during exercise and exogenous ATP infusions in ageing humans. J Physiol 589, 2641-2653.
23. Koch DW, Leuenberger UA & Proctor DN (2003). Augmented leg vasoconstriction in dynamically exercising older men during acute sympathetic stimulation. J Physiol 551, 337-344.
24. 2α in human platelets during administration of organic nitrates. J Am Coll Cardiol 40, 820-825.
25. Milne GL, Sanchez SC, Musiek ES & Morrow JD (2007). Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat Protoc 2, 221-226.
26. Montuschi P, Barnes PJ & Roberts LJ 2nd (2004). Isoprostanes: markers and mediators of oxidative stress. FASEB J 18, 1791-1800.
27. Morrow JD (2005). Quantification of isoprostanes as indices of oxidant stress and the risk of atherosclerosis in humans. Arterioscler Thromb Vasc Biol 25, 279-286.
28. Morrow JD & Roberts LJ 2nd (2002). Mass spectrometric quantification of F2-isoprostanes as indicators of oxidant stress. Methods Mol Biol 186, 57-66.
29. Mulsch A, Bauersachs J, Schafer A, Stasch JP, Kast R & Busse R (1997). Effect of YC-1, an NO-independent, superoxide-sensitive stimulator of soluble guanylyl cyclase, on smooth muscle responsiveness to nitrovasodilators. Br J Pharmacol 120, 681-689.
30. Munzel T, Daiber A & Gori T (2011). Nitrate therapy: new aspects concerning molecular action and tolerance. Circulation 123, 2132-2144.
31. Munzel T, Giaid A, Kurz S, Stewart DJ & Harrison DG (1995a). Evidence for a role of endothelin 1 and protein kinase C in nitroglycerin tolerance. Proc Natl Acad Sci U S A 92, 5244-5248.
32. Munzel T, Hink U, Yigit H, Macharzina R, Harrison DG & Mulsch A (1999). Role of superoxide dismutase inin vivoandin vitronitrate tolerance. Br J Pharmacol 127, 1224-1230.
33. Munzel T, Li H, Mollnau H, Hink U, Matheis E, Hartmann M, Oelze M, Skatchkov M, Warnholtz A, Duncker L, Meinertz T & Forstermann U (2000). Effects of long-term nitroglycerin treatment on endothelial nitric oxide synthase (NOS III) gene expression, NOS III-mediated superoxide production, and vascular NO bioavailability. Circ Res 86, E7-E12.
34. Munzel T, Sayegh H, Freeman BA, Tarpey MM & Harrison DG (1995b). Evidence for enhanced vascular superoxide anion production in nitrate tolerance. A novel mechanism underlying tolerance and cross-tolerance. J Clin Invest 95, 187-194.
35. Murrant CL & Reid MB (2001). Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55, 236-248.
36. Ohyanagi M, Nishigaki K & Faber JE (1992). Interaction between microvascular α1- and α2-adrenoceptors and endothelium-derived relaxing factor. Circ Res 71, 188-200.
37. Parker BA, Smithmyer SL, Jarvis SS, Ridout SJ, Pawelczyk JA & Proctor DN (2007). Evidence for reduced sympatholysis in leg resistance vasculature of healthy older women. Am J Physiol Heart Circ Physiol 292, H1148-H1156.
38. Parker JD, Farrell B, Fenton T, Cohanim M & Parker JO (1991). Counter-regulatory responses to continuous and intermittent therapy with nitroglycerin. Circulation 84, 2336-2345.
39. Powers SK & Jackson MJ (2006). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88, 1243-1276.
40. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK & Harrison DG (1996). Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 97, 1916-1923.
41. Remensnyder JP, Mitchell JH & Sarnoff SJ (1962). Functional sympatholysis during muscular activity. Observations on influence of carotid sinus on oxygen uptake. Circ Res 11, 370-380.
42. Roberts LJ 2nd & Morrow JD (2002). Products of the isoprostane pathway: unique bioactive compounds and markers of lipid peroxidation. Cell Mol Life Sci 59, 808-820.
43. Supinski G, Nethery D, Stofan D & DiMarco A (1999). Extracellular calcium modulates generation of reactive oxygen species by the contracting diaphragm. J Appl Physiol 87, 2177-2185.
44. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M, Ullrich V, Mulsch A, Schulz E, Keaney JF Jr, Stamler JS & Munzel T (2004). Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest 113, 482-489.
45. Thomas GD, Sander M, Lau KS, Huang PL, Stull JT & Victor RG (1998). Impaired metabolic modulation of α-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci U S A 95, 15090-15095.
46. Thomas GD & Victor RG (1998). Nitric oxide mediates contraction-induced attenuation of sympathetic vasoconstriction in rat skeletal muscle. J Physiol 506, 817-826.
47. Thomas GD, Zhang W & Victor RG (2001). Impaired modulation of sympathetic vasoconstriction in contracting skeletal muscle of rats with chronic myocardial infarctions: role of oxidative stress. Circ Res 88, 816-823.
48. Tsutsui H, Ide T, Hayashidani S, Suematsu N, Shiomi T, Wen J, Nakamura K, Ichikawa K, Utsumi H & Takeshita A (2001). Enhanced generation of reactive oxygen species in the limb skeletal muscles from a murine infarct model of heart failure. Circulation 104, 134-136.
49. Vallbo AB, Hagbarth KE, Torebjork HE & Wallin BG (1979). Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 59, 919-957.
50. Vissing SF, Scherrer U & Victor RG (1994). Increase of sympathetic discharge to skeletal muscle but not to skin during mild lower body negative pressure in humans. J Physiol 481, 233-241.
51. Vongpatanasin W, Wang Z, Arbique D, Arbique G, Adams-Huet B, Mitchell JH, Victor RG & Thomas GD (2011). Functional sympatholysis is impaired in hypertensive humans. J Physiol 589, 1209-1220.
52. Wang Z, Ciabattoni G, Creminon C, Lawson J, Fitzgerald GA, Patrono C & Maclouf J (1995). Immunological characterization of urinary 8-epi-prostaglandin F2α excretion in man. J Pharmacol Exp Ther 275, 94-100.
53. Warnholtz A, Mollnau H, Heitzer T, Kontush A, Moller-Bertram T, Lavall D, Giaid A, Beisiegel U, Marklund SL, Walter U, Meinertz T & Munzel T (2002). Adverse effects of nitroglycerin treatment on endothelial function, vascular nitrotyrosine levels and cGMP-dependent protein kinase activity in hyperlipidemic Watanabe rabbits. J Am Coll Cardiol 40, 1356-1363.
54. Wray DW, Nishiyama SK, Donato AJ, Sander M, Wagner PD & Richardson RS (2007). Endothelin-1-mediated vasoconstriction at rest and during dynamic exercise in healthy humans. Am J Physiol Heart Circ Physiol 293, H2550-H2556.
55. Zanzinger J, Czachurski J & Seller H (1998). Impaired modulation of sympathetic excitability by nitric oxide after long-term administration of organic nitrates in pigs. Circulation 97, 2352-2358.
56. Zhao W, Swanson SA, Ye J, Li X, Shelton JM, Zhang W & Thomas GD (2006). Reactive oxygen species impair sympathetic vasoregulation in skeletal muscle in angiotensin II-dependent hypertension. Hypertension 48, 637-643.