Endurance exercise attenuates ventilator-induced diaphragm dysfunction

Journal of Applied Physiology

Volumn 112, Issue 3, 2012, Pages 501-510

  Smuder, Ashley J ^a   Min, Kisuk ^a   Hudson, Matthew B ^a   Kavazis, Andreas N ^b   Kwon, Oh Sung ^a   Nelson, W Bradley ^a   Powers, Scott K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Muscle atrophy; Proteolysis; Respiratory muscle weakness

Indexed keywords

ANTIOXIDANT; HEAT SHOCK PROTEIN 72; PEPTIDE HYDROLASE; PPARGC1A PROTEIN, RAT; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL VENTILATION; BODY WEIGHT; CELL RESPIRATION; DIAPHRAGM; ENDURANCE; FEMALE; GENETICS; METABOLISM; MITOCHONDRION; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCLE FIBRIL; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN DEGRADATION; RAT; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; BODY WEIGHT; CELL RESPIRATION; DIAPHRAGM; FEMALE; HSP72 HEAT-SHOCK PROTEINS; MITOCHONDRIA; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOFIBRILS; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PEPTIDE HYDROLASES; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATION, ARTIFICIAL; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84856923834     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01086.2011     Document Type: Article

References (50)

1. Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, Oliveira PJ, Duarte JA. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am J Physiol Heart Circ Physiol 289: H722-H731, 2005. (Pubitemid 41129389)
2. Bader N, Grune T. Protein oxidation and proteolysis. Biol Chem 387: 1351-1355, 2006. (Pubitemid 44691414)
3. Betters JL, Criswell DS, Shanely RA, Van Gammeren D, Falk D, Deruisseau KC, Deering M, Yimlamai T, Powers SK. Trolox attenuates mechanical ventilation-induced diaphragmatic dysfunction and proteolysis. Am J Respir Crit Care Med 170: 1179-1184, 2004. (Pubitemid 39577375)
4. Criswell D, Powers S, Dodd S, Lawler J, Edwards W, Renshler K, Grinton S. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc 25: 1135-1140, 1993. (Pubitemid 23298826)
5. Deruisseau KC, Kavazis AN, Powers SK. Selective downregulation of ubiquitin conjugation cascade mRNA occurs in the senescent rat soleus muscle. Exp Gerontol 40: 526-531, 2005. (Pubitemid 40884506)
6. DeRuisseau KC, Shanely RA, Akunuri N, Hamilton MT, Van Gammeren D, Zergeroglu AM, McKenzie M, Powers SK. Diaphragm unloading via controlled mechanical ventilation alters the gene expression profile. Am J Respir Crit Care Med 172: 1267-1275, 2005. (Pubitemid 43076565)
7. Esteban A, Frutos F, Tobin MJ, Alia I, Solsona JF, Valverdu I, Fernandez R, de la Cal MA, Benito S, Tomas R, Carriedo D, Macias S, Blanco J. A comparison of four methods of weaning patients from mechanical ventilation Spanish Lung Failure Collaborative Group. N Engl J Med 332: 345-350, 1995.
8. Estrabrook R. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol 10: 41-47, 1967.
9. Futier E, Constantin JM, Combaret L, Mosoni L, Roszyk L, Sapin V, Attaix D, Jung B, Jaber S, Bazin JE. Pressure support ventilation attenuates ventilator-induced protein modifications in the diaphragm. Crit Care 12: R116, 2008.
10. Gayan-Ramirez G, Testelmans D, Maes K, Racz GZ, Cadot P, Zador E, Wuytack F, Decramer M. Intermittent spontaneous breathing protects the rat diaphragm from mechanical ventilation effects. Crit Care Med 33: 2804-2809, 2005. (Pubitemid 41816415)
11. Grune T, Merker K, Sandig G, Davies KJ. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem Biophys Res Commun 305: 709-718, 2003. (Pubitemid 36579287)
12. Kandarian SC, Stevenson EJ. Molecular events in skeletal muscle during disuse atrophy. Exerc Sport Sci Rev 30: 111-116, 2002. (Pubitemid 34787297)
13. Kavazis AN, Alvarez S, Talbert E, Lee Y, Powers SK. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol Heart Circ Physiol 297: H144-H152, 2009.
14. Kavazis AN, McClung JM, Hood DA, Powers SK. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol Heart Circ Physiol 294: H928-H935, 2008. (Pubitemid 351253305)
15. Kavazis AN, Smuder AJ, Min K, Tumer N, Powers SK. Short-term exercise training protects against doxorubicin-induced cardiac mitochondrial damage independent of HSP72. Am J Physiol Heart Circ Physiol 299: H1515-H1524, 2010.
16. Kavazis AN, Talbert EE, Smuder AJ, Hudson MB, Nelson WB, Powers SK. Mechanical ventilation induces diaphragmatic mitochondrial dysfunction and increased oxidant production. Free Radic Biol Med 46: 842-850, 2009.
17. Laghi F, Cattapan SE, Jubran A, Parthasarathy S, Warshawsky P, Choi YS, Tobin MJ. Is weaning failure caused by low-frequency fatigue of the diaphragm? Am J Respir Crit Care Med 167: 120-127, 2003. (Pubitemid 36076069)
18. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, Rubinstein NA, Powers SK, Shrager JB. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358: 1327-1335, 2008. (Pubitemid 351468409)
19. Locke M, Tanguay RM, Klabunde RE, Ianuzzo CD. Enhanced postischemic myocardial recovery following exercise induction of HSP 72. Am J Physiol Heart Circ Physiol 269: H320-H325, 1995.
20. Lubos E, Loscalzo J, Handy DE. Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 15: 1957-1997, 2011.
21. Makinen MW, Lee CP. Biochemical studies of skeletal muscle mitochondria. I. Microanalysis of cytochrome content, oxidative and phosphorylative activities of mammalian skeletal muscle mitochondria. Arch Biochem Biophys 126: 75-82, 1968.
22. Martin AD, Smith BK, Davenport PD, Harman E, Gonzalez-Rothi RJ, Baz M, Layon AJ, Banner MJ, Caruso LJ, Deoghare H, Huang TT, Gabrielli A. Inspiratory muscle strength training improves weaning outcome in failure to wean patients: a randomized trial. Crit Care 15: R84, 2011.
23. McClung JM, Kavazis AN, DeRuisseau KC, Falk DJ, Deering MA, Lee Y, Sugiura T, Powers SK. Caspase-3 regulation of diaphragm myonuclear domain during mechanical ventilation-induced atrophy. Am J Respir Crit Care Med 175: 150-159, 2007. (Pubitemid 46115086)
24. McClung JM, Van Gammeren D, Whidden MA, Falk DJ, Kavazis AN, Hudson MB, Gayan-Ramirez G, Decramer M, DeRuisseau KC, Powers SK. Apocynin attenuates diaphragm oxidative stress and protease activation during prolonged mechanical ventilation. Crit Care Med 37: 1373-1379, 2009.
25. Messer JI, Jackman MR, Willis WT. Pyruvate and citric acid cycle carbon requirements in isolated skeletal muscle mitochondria. Am J Physiol Cell Physiol 286: C565-C572, 2004. (Pubitemid 38292662)
26. Naito H, Powers SK, Demirel HA, Aoki J. Exercise training increases heat shock protein in skeletal muscles of old rats. Med Sci Sports Exerc 33: 729-734, 2001. (Pubitemid 32336632)
27. Naito H, Powers SK, Demirel HA, Sugiura T, Dodd SL, Aoki J. Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats. J Appl Physiol 88: 359-363, 2000. (Pubitemid 30053868)
28. Nathens AB, Neff MJ, Jurkovich GJ, Klotz P, Farver K, Ruzinski JT, Radella F, Garcia I, Maier RV. Randomized, prospective trial of antioxidant supplementation in critically ill surgical patients. Ann Surg 236: 814-822, 2002. (Pubitemid 35403237)
29. Petrof BJ, Jaber S, Matecki S. Ventilator-induced diaphragmatic dysfunction. Curr Opin Crit Care 16: 19-25.
30. Powers SK, Criswell D, Lawler J, Ji LL, Martin D, Herb RA, Dudley G. Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 266: R375-R380, 1994.
31. Powers SK, Criswell D, Lieu FK, Dodd S, Silverman H. Exerciseinduced cellular alterations in the diaphragm. Am J Physiol Regul Integr Comp Physiol 263: R1093-R1098, 1992.
32. Powers SK, Hudson MB, Nelson WB, Talbert EE, Min K, Szeto HH, Kavazis AN, Smuder AJ. Mitochondria-targeted antioxidants protect against mechanical-ventilation-induced diaphragm weakness. Crit Care Med 39: 1749-1759, 2011.
33. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
34. Powers SK, Locke, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 33: 386-392, 2001. (Pubitemid 32209657)
35. Powers SK, Shanely RA, Coombes JS, Koesterer TJ, McKenzie M, Van Gammeren D, Cicale M, Dodd SL. Mechanical ventilation results in progressive contractile dysfunction in the diaphragm. J Appl Physiol 92: 1851-1858, 2002. (Pubitemid 34666410)
36. Powers SK, Talbert EE, Adhihetty PJ. Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol 589: 2129-2138, 2011.
37. Quintanilha AT. Effects of physical exercise and/or vitamin E on tissue oxidative metabolism. Biochem Soc Trans 12: 403-404, 1984. (Pubitemid 14114755)
38. Radell PJ, Remahl S, Nichols DG, Eriksson LI. Effects of prolonged mechanical ventilation and inactivity on piglet diaphragm function. Intensive Care Med 28: 358-364, 2002. (Pubitemid 34230660)
39. Sassoon CS, Zhu E, Caiozzo VJ. Assist-control mechanical ventilation attenuates ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 170: 626-632, 2004. (Pubitemid 39202204)
40. Senf SM, Dodd SL, McClung JM, Judge AR. Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 22: 3836-3845, 2008.
41. Shanely RA, Coombes JS, Zergeroglu AM, Webb AI, Powers SK. Short-duration mechanical ventilation enhances diaphragmatic fatigue resistance but impairs force production. Chest 123: 195-201, 2003. (Pubitemid 36126732)
42. Shanely RA, Zergeroglu MA, Lennon SL, Sugiura T, Yimlamai T, Enns D, Belcastro A, Powers SK. Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am J Respir Crit Care Med 166: 1369-1374, 2002. (Pubitemid 35292704)
43. Smuder AJ, Kavazis AN, Hudson MB, Nelson WB, Powers SK. Oxidation enhances myofibrillar protein degradation via calpain and caspase-3. Free Radic Biol Med 49: 1152-1160.
44. Smuder AJ, Kavazis AN, Min K, Powers SK. Exercise protects against doxorubicin-induced oxidative stress and proteolysis in skeletal muscle. J Appl Physiol 110: 935-942.
45. Staib JL, Tumer N, Powers SK. Increased temperature and protein oxidation lead to HSP72 mRNA and protein accumulation in the in vivo exercised rat heart. Exp Physiol 94: 71-80, 2009.
46. Vincent HK, Powers SK, Demirel HA, Coombes JS, Naito H. Exercise training protects against contraction-induced lipid peroxidation in the diaphragm. Eur J Appl Physiol Occup Physiol 79: 268-273, 1999. (Pubitemid 29057272)
47. Vincent HK, Powers SK, Stewart DJ, Demirel HA, Shanely RA, Naito H. Short-term exercise training improves diaphragm antioxidant capacity and endurance. Eur J Appl Physiol 81: 67-74, 2000. (Pubitemid 30008861)
48. Whidden MA, McClung JM, Falk DJ, Hudson MB, Smuder AJ, Nelson WB, Powers SK. Xanthine oxidase contributes to mechanical ventilation-induced diaphragmatic oxidative stress and contractile dysfunction. J Appl Physiol 106: 385-394, 2009.
49. Whidden MA, Smuder AJ, Wu M, Hudson MB, Nelson WB, Powers SK. Oxidative stress is required for mechanical ventilationinduced protease activation in the diaphragm. J Appl Physiol 108: 1376-1382.
50. Zergeroglu MA, McKenzie MJ, Shanely RA, Van Gammeren D, DeRuisseau KC, Powers SK. Mechanical ventilation-induced oxidative stress in the diaphragm. J Appl Physiol 95: 1116-1124, 2003. (Pubitemid 37034008)