Antioxidant treatments do not improve force recovery after fatiguing stimulation of mouse skeletal muscle fibres

Journal of Physiology

Volumn 593, Issue 2, 2015, Pages 457-472

  Cheng, Arthur J ^a   Bruton, Joseph D ^a   Lanner, Johanna T ^a   Westerblad, Håkan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CALCIUM ION; GKT 137831; GP91DS TAT; MALONALDEHYDE; MYOSIN; N(G) NITROARGININE METHYL ESTER; OXIDOREDUCTASE INHIBITOR; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SS 31; UNCLASSIFIED DRUG; ANTIOXIDANT; CALCIUM; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL STIMULATION; CONTROLLED STUDY; DRUG MECHANISM; FAST MUSCLE; FEMALE; FLEXOR DIGITORUM BREVIS MUSCLE; LIPID PEROXIDATION; MECHANICAL STRESS; MOUSE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE FIBRIL; MUSCLE FUNCTION; MUSCLE STRENGTH; MUSCLE TETANIC CONTRACTION; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; OXIDATIVE STRESS; PROLONGED LOW FREQUENCY FORCE DEPRESSION; REST; SKELETAL MUSCLE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CONVALESCENCE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIOXIDANTS; CALCIUM; FEMALE; MICE; MICE, INBRED C57BL; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; NADPH OXIDASE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN SPECIES; RECOVERY OF FUNCTION;

EID: 84921030936     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.279398     Document Type: Article

References (55)

1. Allen DG, Lamb GD & Westerblad H (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88, 287-332.
2. Allman BL & Rice CL (2001). Incomplete recovery of voluntary isometric force after fatigue is not affected by old age. Muscle Nerve 24, 1156-1167.
3. Altenhöfer S, Radermacher KA, Kleikers PW, Wingler K & Schmidt HH (2014). Evolution of NADPH oxidase inhibitors: selectivity and mechanisms for target engagement. Antioxid Redox Signal, doi:10.1089/ars.2013.5814
4. Andersson DC, Fauconnier J, Yamada T, Lacampagne A, Zhang SJ, Katz A & Westerblad H (2011). Mitochondrial production of reactive oxygen species contributes to the β-adrenergic stimulation of mouse cardiomyocytes. J Physiol 589, 1791-1801.
5. Andrade FH, Reid MB, Allen DG & Westerblad H (1998). Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol 509, 565-575.
6. Andrade FH, Reid MB & Westerblad H (2001). Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J 15, 309-311.
7. 2+ in mitochondrial myopathy. Human Mol Genet 18, 278-288.
8. Balon TW & Nadler JL (1994). Nitric oxide release is present from incubated skeletal muscle preparations. J Appl Physiol 77, 2519-2521.
9. Balon TW & Nadler JL (1996). Nitric oxide mediates skeletal glucose transport. Am J Physiol Endocrinol Metab 270, E1058-E1059.
10. Boncompagni S, Rossi AE, Micaroni M, Beznoussenko GV, Polishchuk RS, Dirksen RT & Protasi F (2009). Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol Biol Cell 20, 1058-1067.
11. 2+ in living cells. Adv Exp Med Biol 740, 27-43.
12. 2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice. J Physiol 588, 4275-4288.
13. oC. J Appl Physiol 85, 478-483.
14. Bruton JD, Place N, Yamada T, Silva JP, Andrade FH, Dahlstedt AJ, Zhang SJ, Katz A, Larsson NG & Westerblad H (2008). Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J Physiol 586, 175-184.
15. 2+] in the development of low frequency fatigue in mouse single muscle fibres. J Physiol 491, 813-824.
16. Csányi G, Cifuentes-Pagano E, Al Ghouleh I, Ranayhossaini D, Egaña L, Lopes L, Jackson H, Kelley E & Pagano P (2011). Nox2 B-loop peptide, Nox2ds, specifically inhibits the NADPH oxidase Nox2. Free Radic Biol Med 51, 1116-1125.
17. Dahlstedt AJ, Katz A, Tavi P & Westerblad H (2003). Creatine kinase injection restores contractile function in creatine-kinase-deficient mouse skeletal muscle fibres. J Physiol 547, 395-403.
18. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
19. Edwards RH, Hill DK, Jones DA & Merton PA (1977). Fatigue of long duration in human skeletal muscle after exercise. J Physiol 272, 769-778.
20. Grimby L & Hannerz J (1977). Firing rate and recruitment order of toe extensor motor units in different modes of voluntary conraction. J Physiol 264, 865-879.
21. Hearn AS, Tu C, Nick HS & Silverman DN (1999). Characterization of the product-inhibited complex in catalysis by human manganese superoxide dismutase. J Biol Chem 274, 24457-24460.
22. Hernandez A, Cheng A & Westerblad H (2012). Antioxidants and skeletal muscle performance: "Common knowledge " vs. experimental evidence. Front Physiol 3, 46.
23. Hill CA, Thompson MW, Ruell PA, Thom JM & White MJ (2001). Sarcoplasmic reticulum function and muscle contractile character following fatiguing exercise in humans. J Physiol 531, 871-878.
24. Hirschfield W, Moody MR, O'Brien WE, Gregg AR, Bryan RM, Jr. & Reid MB (2000). Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS. Am J Physiol Regul Integr Comp Physiol 278, R95-R100.
25. Jiang J, Chen X, Serizawa N, Szyndralewiez C, Page P, Schröder K, Brandes R, Devaraj S & Török N (2012). Liver fibrosis and hepatocyte apoptosis are attenuated by GKT137831, a novel NOX4/NOX1 inhibitor in vivo. Free Radic Biol Med 53, 289-296.
26. Kang L, Lustig M, Bonner J, Lee-Young R, Mayes W, James F, Lin C-T, Perry C, Anderson E, Neufer P & Wasserman D (2012). Mitochondrial antioxidative capacity regulates muscle glucose uptake in the conscious mouse: effect of exercise and diet. J Appl Physiol 113, 1173-1183.
27. Keeton RB & Binder-Macleod SA (2006). Low-frequency fatigue. Phys Ther 86, 1146-1150.
28. Kobzik L, Reid MB, Bredt DS & Stamler JS (1994). Nitric oxide in skeletal muscle. Nature 372, 546-548.
29. Lamb GD & Westerblad H (2011). Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J Physiol 589, 2119-2127.
30. Lundberg JO & Weitzberg E (2010). NO-synthase independent NO generation in mammals. Biochem Biophys Res Commun 396, 39-45.
31. Marsden CD, Meadows JC & Merton PA (1971). Isolated single motor units in human muscle and their rate of discharge during maximal voluntary effort. J Physiol 217, 12P-13P.
32. Michaelson LP, Shi G, Ward CW & Rodney GG (2010). Mitochondrial redox potential during contraction in single intact muscle fibers. Muscle Nerve 42, 522-529.
33. 2+ sensitivity in fast-twitch muscle fibres of rats and humans. J Physiol 590, 1443-1463.
34. Murphy RM, Dutka TL & Lamb GD (2008). 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.
35. 2+ in fatigued single intact mouse muscle fibres. J Physiol 592, 2003-2012.
36. Pal R, Basu Thakur P, Li S, Minard C & Rodney GG (2013). Real-time imaging of NADPH oxidase activity in living cells using a novel fluorescent protein reporter. PLoS One 8, e63989.
37. Paulsen G, Cumming KT, Holden G, Hallen J, Ronnestad BR, Sveen O, Skaug A, Paur I, Bastani NE, Ostgaard HN et al. (2014). Vitamin C and E supplementation hampers cellular adaptation to endurance training in humans: a double-blind, randomised, controlled trial. J Physiol 592, 1887-1901.
38. Place N, Yamada T, Zhang SJ, Westerblad H & Bruton JD (2009). High temperature does not alter fatigability in intact mouse skeletal muscle fibres. J Physiol 587, 4717-4724.
39. Powers SK & Jackson MJ (2008). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88, 1243-1276.
40. Powers SK, Ji LL, Kavazis AN & Jackson MJ (2011). Reactive oxygen species: impact on skeletal muscle. Compr Physiol 1, 941-969.
41. Reid MB, Stokic DS, Koch SM, Khawli FA & Leis AA (1994). N-acetylcysteine inhibits muscle fatigue in humans. J Clin Invest 94, 2468-2474.
42. Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR & Blüher M (2009). Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106, 8665-8670.
43. Sakellariou GK, Jackson MJ & Vasilaki A (2014). Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases. Free Radic Res 48, 12-29.
44. Sakellariou GK, Vasilaki A, Palomero J, Kayani A, Zibrik L, McArdle A & Jackson MJ (2013). Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity. Antioxid Redox Signal 18, 603-621.
45. Sandström ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H & Katz A (2006). Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575, 251-262.
46. Siegel MP, Kruse SE, Percival JM, Goh J, White CC, Hopkins HC, Kavanagh TJ, Szeto HH, Rabinovitch PS & Marcinek DJ (2013). Mitochondrial-targeted peptide rapidly improves mitochondrial energetics and skeletal muscle performance in aged mice. Aging Cell 12, 763-771.
47. Szeto HH, Liu S, Soong Y, Wu D, Darrah SF, Cheng FY, Zhao Z, Ganger M, Tow CY & Seshan SV (2011). Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury. J Am Soc Nephrol 22, 1041-1052.
48. Szeto H & Schiller P (2011). Novel therapies targeting inner mitochondrial membrane - from discovery to clinical development. Pharm Res 28, 2669-2679.
49. Thomas GD & Victor RG (1998). Nitric oxide mediates contraction-induced attenuation of sympathetic vasoconstriction in rat skeletal muscle. J Physiol 506, 817-826.
50. Wei L, Salahura G, Boncompagni S, Kasischke KA, Protasi F, Sheu SS & Dirksen RT (2011). Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease. FASEB J 25, 3068-3078.
51. i and force in skeletal muscle. Acta Physiol Scand 156, 407-416.
52. Westerblad H & Allen DG (2011). Emerging roles of ROS/RNS in muscle function and fatigue. Antioxid Redox Signal 15, 2487-2499.
53. Westerblad H, Duty S & Allen DG (1993). Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscle. J Appl Physiol 75, 382-388.
54. Wright DC, Geiger PC, Han DH, Jones TE & Holloszy JO (2007). Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1α and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282, 18793-18799.
55. Zong M, Bruton JD, Grundtman C, Yang H, Li JH, Alexanderson H, Palmblad K, Andersson U, Harris HE, Lundberg IE & Westerblad H (2012). TLR4 as receptor for HMGB1 induced muscle dysfunction in myositis. Ann Rheum Dis 72, 1390-1399.