Acute effects of hydrogen peroxide on skeletal muscle microvascular oxygenation from rest to contractions

Journal of Applied Physiology

Volumn 110, Issue 5, 2011, Pages 1290-1298

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

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Blood flow; Exercise; Force; Oxygen uptake; Reactive oxygen species

Indexed keywords

HYDROGEN PEROXIDE; OXYGEN;

ANIMAL; ARTICLE; DRUG EFFECT; MALE; METABOLISM; MICROCIRCULATION; MICROVASCULATURE; MUSCLE CONTRACTION; OXYGEN CONSUMPTION; PHYSIOLOGY; RAT; REST; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ANIMALS; HYDROGEN PEROXIDE; MALE; MICROCIRCULATION; MICROVESSELS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; OXYGEN; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY; REST;

EID: 79956143884     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01489.2010     Document Type: Article

References (64)

1. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88: 287-332, 2008.
2. Altman PL, Dittmer DS. Biology Data Book. Bethesda, MD: FASEB, 1974.
3. 2 generation. Am J Physiol Cell Physiol 290: C844-C851, 2006.
4. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol 509: 565-575, 1998. (Pubitemid 28287013)
5. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of nitric oxide on single skeletal muscle fibres from the mouse. J Physiol 509: 577-586, 1998. (Pubitemid 28287014)
6. 2 gradients across biomembranes. FEBS Lett 475: 121-126, 2000. (Pubitemid 30365063)
7. Arbogast S, Reid MB. Oxidant activity in skeletal muscle fibers is influenced by temperature, CO2 level, and muscle-derived nitric oxide. Am J Physiol Regul Integr Comp Physiol 287: R698-R705, 2004. (Pubitemid 39280453)
8. Ardanaz N, Pagano PJ. Hydrogen peroxide as a paracrine vascular mediator: regulation and signaling leading to dysfunction. Exp Biol Med (Maywood) 231: 237-251, 2006. (Pubitemid 43334308)
9. Bailey JK, Kindig CA, Behnke BJ, Musch TI, Schmid-Schoenbein GW, Poole DC. Spinotrapezius muscle microcirculatory function: effects of surgical exteriorization. Am J Physiol Heart Circ Physiol 279: H3131-H3137, 2000. (Pubitemid 32005905)
10. Behnke BJ, Kindig CA, Musch TI, Koga S, Poole DC. Dynamics of microvascular oxygen pressure across the rest-exercise transition in rat skeletal muscle. Respir Physiol 126: 53-63, 2001. (Pubitemid 32318524)
11. Behnke BJ, Kindig CA, Musch TI, Sexton WL, Poole DC. Effects of prior contractions on muscle microvascular oxygen pressure at onset of subsequent contractions. J Physiol 539: 927-934, 2002. (Pubitemid 35175441)
12. 2-induced endothelial dysfunction. Free Radic Biol Med 41: 810-817, 2006. (Pubitemid 44163414)
13. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345: 50-54, 1994.
14. Copp SW, Ferreira LF, Herspring KF, Hirai DM, Snyder BS, Poole DC, Musch TI. The effects of antioxidants on microvascular oxygenation and blood flow in skeletal muscle of young rats. Exp Physiol 94: 961-971, 2009.
15. Cosentino F, Katusic ZS. Tetrahydrobiopterin and dysfunction of endothelial nitric oxide synthase in coronary arteries. Circulation 91: 139-144, 1995.
16. Cseko″ C, Bagi Z, Koller A. Biphasic effect of hydrogen peroxide on skeletal muscle arteriolar tone via activation of endothelial and smooth muscle signaling pathways. J Appl Physiol 97: 1130-1137, 2004. (Pubitemid 39121443)
17. Delliaux S, Brerro-Saby C, Steinberg JG, Jammes Y. Reactive oxygen species activate the group IV muscle afferents in resting and exercising muscle in rats. Pfl̈gers Arch 459: 143-150, 2009.
18. Delp MD, Duan C. Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80: 261-270, 1996. (Pubitemid 26034871)
19. Eddy L, Arduini A, Hochstein P. Reduction of ferrylmyoglobin in rat diaphragm. Am J Physiol Cell Physiol 259: C995-C997, 1990.
20. Ferreira LF, Reid MB. Muscle-derived ROS and thiol regulation in muscle fatigue. J Appl Physiol 104: 853-860, 2008. (Pubitemid 351468816)
21. Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry 49: 835-842, 2010.
22. Gao YJ, Zhang Y, Hirota S, Janssen LJ, Lee RM. Vascular relaxation response to hydrogen peroxide is impaired in hypertension. Br J Pharmacol 142: 143-149, 2004. (Pubitemid 38698203)
23. Herspring KF, Ferreira LF, Copp SW, Snyder BS, Poole DC, Musch TI. Effects of antioxidants on contracting spinotrapezius muscle microvascular oxygenation and blood flow in aged rats. J Appl Physiol 105: 1889-1896, 2008.
24. Hirai DM, Copp SW, Ferreira LF, Musch TI, Poole DC. Nitric oxide bioavailability modulates the dynamics of microvascular oxygen exchange during recovery from contractions. Acta Physiol (Oxf) 200: 159-169, 2010.
25. Hirai DM, Copp SW, Herspring KF, Ferreira LF, Poole DC, Musch TI. Aging impacts microvascular oxygen pressures during recovery from contractions in rat skeletal muscle. Respir Physiol Neurobiol 169: 315-322, 2009.
26. 2 in regulating tissue respiration in dog muscle working in situ. J Appl Physiol 73: 728-736, 1992.
27. Hu Z, Chen J, Wei Q, Xia Y. Bidirectional actions of hydrogen peroxide on endothelial nitric-oxide synthase phosphorylation and function: cocommitment and interplay of Akt and AMPK. J Biol Chem 283: 25256-25263, 2008.
28. Ishise S, Pegram BL, Yamamoto J, Kitamura Y, Frohlich ED. Reference sample microsphere method: cardiac output and blood flows in conscious rat. Am J Physiol Heart Circ Physiol 239: H443-H449, 1980.
29. Kindig CA, McDonough P, Erickson HH, Poole DC. Effect of L-NAME on oxygen uptake kinetics during heavy-intensity exercise in the horse. J Appl Physiol 91: 891-896, 2001. (Pubitemid 32681124)
30. Leek BT, Mudaliar SR, Henry R, Mathieu-Costello O, Richardson RS. Effect of acute exercise on citrate synthase activity in untrained and trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 280: R441-R447, 2001.
31. 2 kinetics in heavy submaximal exercise by hyperoxia and prior high-intensity exercise. J Appl Physiol 83: 1318-1325, 1997. (Pubitemid 27433101)
32. Marvar PJ, Hammer LW, Boegehold MA. Hydrogen peroxide-dependent arteriolar dilation in contracting muscle of rats fed normal and high salt diets. Microcirculation 14: 779-791, 2007. (Pubitemid 350138983)
33. Masuoka N, Sugiyama H, Ishibashi N, Wang DH, Masuoka T, Kodama H, Nakano T. Characterization of acatalasemic erythrocytes treated with low and high dose hydrogen peroxide. Hemolysis and aggregation. J Biol Chem 281: 21728-21734, 2006. (Pubitemid 44181876)
34. Matoba T, Shimokawa H, Nakashima M, Hirakawa Y, Mukai Y, Hirano K, Kanaide H, Takeshita A. Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest 106: 1521-1530, 2000. (Pubitemid 32040953)
35. Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD. Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92: e31-e40, 2003.
36. 2+ sensitivity in fatiguing mouse skeletal muscle at 37°C. J Physiol 564: 189-199, 2005. (Pubitemid 40542197)
37. Murphy RM, Dutka TL, Lamb GD. Hydroxyl radical and glutathione interactions alter calcium sensitivity and maximum force of the contractile apparatus in rat skeletal muscle fibres. J Physiol 586: 2203-2216, 2008. (Pubitemid 351540511)
38. 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 262: H411-H419, 1992.
39. Nagababu E, Chrest FJ, Rifkind JM. Hydrogen-peroxide-induced heme degradation in red blood cells: the protective roles of catalase and glutathione peroxidase. Biochim Biophys Acta 1620: 211-217, 2003. (Pubitemid 36197913)
40. Neumann CA, Cao J, Manevich Y. Peroxiredoxin 1 and its role in cell signaling. Cell Cycle 8: 4072-4078, 2009.
41. 2+ content after fatigue. J Appl Physiol 93: 1999-2008, 2002. (Pubitemid 35390356)
42. Oter O, Ribou AC. Quenching of long lifetime emitting fluorophores with paramagnetic molecules. J Fluoresc 19: 389-397, 2009.
43. Phillips SA, Hatoum OA, Gutterman DD. The mechanism of flowinduced dilation in human adipose arterioles involves hydrogen peroxide during CAD. Am J Physiol Heart Circ Physiol 292: H93-H100, 2007. (Pubitemid 46105166)
44. Poole DC, Behnke BJ, McDonough P, McAllister RM, Wilson DF. Measurement of muscle microvascular oxygen pressures: compartmentalization of phosphorescent probe. Microcirculation 11: 317-326, 2004. (Pubitemid 39619082)
45. 2 measured in vivo. J Appl Physiol 79: 2050-2057, 1995. (Pubitemid 26010578)
46. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
47. Prochniewicz E, Lowe DA, Spakowicz DJ, Higgins L, O'Conor K, Thompson LV, Ferrington DA, Thomas DD. Functional, structural, and chemical changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers. Am J Physiol Cell Physiol 294: C613-C626, 2008. (Pubitemid 351264413)
48. Reid MB. Invited Review: redox modulation of skeletal muscle contraction: what we know and what we don't. J Appl Physiol 90: 724-731, 2001. (Pubitemid 32118935)
49. Reid MB, Khawli FA, Moody MR. Reactive oxygen in skeletal muscle. III. Contractility of unfatigued muscle. J Appl Physiol 75: 1081-1087, 1993. (Pubitemid 23289594)
50. Rumsey WL, Vanderkooi JM, Wilson DF. Imaging of phosphorescence: a novel method for measuring oxygen distribution in perfused tissue. Science 241: 1649-1651, 1988.
51. Shimokawa H. Hydrogen peroxide as an endothelium-derived hyperpolarizing factor. Pfl̈gers Arch 459: 915-922, 2010.
52. Sims NR, Anderson MF, Hobbs LM, Kong JY, Phillips S, Powell JA, Zaidan E. Impairment of brain mitochondrial function by hydrogen peroxide. Brain Res Mol Brain Res 77: 176-184, 2000. (Pubitemid 30317345)
53. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM. Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587: 3885-3897, 2009.
54. Skulachev VP. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys 29: 169-202, 1996. (Pubitemid 26280789)
55. 2+ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat. Am J Physiol Cell Physiol 296: C1015-C1023, 2009.
56. Thomas SR, Witting PK, Drummond GR. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 10: 1713-1765, 2008.
57. Tonkonogi M, Walsh B, Svensson M, Sahlin K. Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress. J Physiol 528: 379-388, 2000.
58. Trott DW, Seawright JW, Luttrell MJ, Woodman CR. NAD(P)H oxidase-derived reactive oxygen species contribute to age-related impairments of endothelium-dependent dilation in rat soleus feed arteries. J Appl Physiol (January 13, 2011). doi:10.1152/japplphysiol.01037.2010.
59. Vasilaki A, Mansouri A, Remmen H, van der Meulen JH, Larkin L, Richardson AG, McArdle A, Faulkner JA, Jackson MJ. Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell 5: 109-117, 2006. (Pubitemid 44056502)
60. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, Muoio DM, Lowell BB. Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275: 16258-16266, 2000. (Pubitemid 30366939)
61. Vinogradov SA, Fernandez-Searra MA, Dugan BW, Wilson DF. Frequency domain instrument for measuring phosphorescence lifetime distributions in heterogeneous samples. Rev Sci Instrum 72: 3396-3406, 2001. (Pubitemid 33606977)
62. Wang HJ, Pan YX, Wang WZ, Zucker IH, Wang W. NADPH oxidasederived reactive oxygen species in skeletal muscle modulates the exercise pressor reflex. J Appl Physiol 107: 450-459, 2009.
63. Zhou X, Bohlen HG, Miller SJ, Unthank JL. NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo. Am J Physiol Heart Circ Physiol 295: H1008-H1016, 2008.
64. Zhou X, Bohlen HG, Unthank JL, Miller SJ. Abnormal nitric oxide production in aged rat mesenteric arteries is mediated by NAD(P)H oxidase-derived peroxide. Am J Physiol Heart Circ Physiol 297: H2227-H2233, 2009.