Role of intrinsic aerobic capacity and ventilator-induced diaphragm dysfunction

Journal of Applied Physiology

Volumn 118, Issue 7, 2015, Pages 849-857

  Sollanek, Kurt J ^a   Smuder, Ashley J ^a   Wiggs, Michael P ^a   Morton, Aaron B ^a   Koch, Lauren G ^b   Britton, Steven L ^b   Powers, Scott K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Mitochondria; Muscle atrophy; Oxidative stress; Reactive oxygen species

Indexed keywords

ANIMAL; ANIMAL EXPERIMENT; DIAPHRAGM; EXERCISE TOLERANCE; FITNESS; MUSCULAR DISEASES; PATHOPHYSIOLOGY; PROCEDURES; RAT; VENTILATOR-INDUCED LUNG INJURY;

ANIMALS; DIAPHRAGM; EXERCISE TOLERANCE; MUSCULAR DISEASES; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL FITNESS; RATS; VENTILATOR-INDUCED LUNG INJURY;

EID: 84928187410     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00797.2014     Document Type: Article

References (49)

1. 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.
2. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ, Skinner JS. American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc 41: 1510-1530, 2009.
3. Dasta JF, McLaughlin TP, Mody SH, Piech CT. Daily cost of an intensive care unit day: the contribution of mechanical ventilation. Crit Care Med 33: 1266-1271, 2005.
4. Esteban A, et al. Evolution of mechanical ventilation in response to clinical research. Am J Respir Crit Care Med 177: 170-177, 2008.
5. Esteban A, Frutos F, Tobin MJ, Alia I, Solsona JF, Valverdu I, Fernandez R, de la Cal MA, Benito S, Tomas R, et al. A comparison of four methods of weaning patients from mechanical ventilation. Spanish Lung Failure Collaborative Group. N Engl J Med 332: 345-350, 1995.
6. Hollander J, Bejma J, Ookawara T, Ohno H, Ji LL. Superoxide dismutase gene expression in skeletal muscle: fiber-specific effect of age. Mech Ageing Dev 116: 33-45, 2000.
7. Ichinoseki-Sekine N, Yoshihara T, Kakigi R, Sugiura T, Powers SK, Naito H. Heat stress protects against mechanical ventilation-induced diaphragmatic atrophy. J Appl Physiol 117: 518-524, 2014.
8. 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.
9. Koch LG, Britton SL. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 5: 45-52, 2001.
10. Koch LG, Britton SL, Wisloff U. A rat model system to study complex disease risks, fitness, aging, and longevity. Trends Cardiovasc Med 22: 29-34, 2012.
11. Koch LG, Meredith TA, Fraker TD, Metting PJ, Britton SL. Heritability of treadmill running endurance in rats. Am J Physiol Regul Integr Comp Physiol 275: R1455-R1460, 1998.
12. Koch LG, Pollott GE, Britton SL. Selectively bred rat model system for low and high response to exercise training. Physiol Genomics 45: 606-614, 2013.
13. Lessard SJ, Rivas DA, Alves-Wagner AB, Hirshman MF, Gallagher IJ, Constantin-Teodosiu D, Atkins R, Greenhaff PL, Qi NR, Gustafsson T, Fielding RA, Timmons JA, Britton SL, Koch LG, Goodyear LJ. Resistance to aerobic exercise training causes metabolic dysfunction and reveals novel exercise-regulated signaling networks. Diabetes 62: 2717-2727, 2013.
14. Lessard SJ, Rivas DA, Stephenson EJ, Yaspelkis BB 3rd, Koch LG, Britton SL, Hawley JA. Exercise training reverses impaired skeletal muscle metabolism induced by artificial selection for low aerobic capacity. Am J Physiol Regul Integr Comp Physiol 300: R175-R182, 2011.
15. 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.
16. 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.
17. Maglara AA, Vasilaki A, Jackson MJ, McArdle A. Damage to developing mouse skeletal muscle myotubes in culture: protective effect of heat shock proteins. J Physiol 548: 837-846, 2003.
18. 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.
19. Marton O, Koltai E, Takeda M, Koch LG, Britton SL, Davies KJ, Boldogh I, Radak Z. Mitochondrial biogenesis-associated factors underlie the magnitude of response to aerobic endurance training in rats. Pflugers Arch. In press.
20. McClung JM, Kavazis AN, Whidden MA, DeRuisseau KC, Falk DJ, Criswell DS, Powers SK. Antioxidant administration attenuates mechanical ventilation-induced rat diaphragm muscle atrophy independent of protein kinase B (PKB Akt) signalling. J Physiol 585: 203-215, 2007.
21. Morton JP, Kayani AC, McArdle A, Drust B. The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Med 39: 643-662, 2009.
22. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med 346: 793-801, 2002.
23. 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.
24. 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.
25. Powers SK, Criswell D, Lawler J, Martin D, Ji LL, Herb RA, Dudley G. Regional training-induced alterations in diaphragmatic oxidative and antioxidant enzymes. Respir Physiol 95: 227-237, 1994.
26. Powers SK, Criswell D, Lieu FK, Dodd S, Silverman H. Diaphragmatic fiber type specific adaptation to endurance exercise. Respir Physiol 89: 195-207, 1992.
27. 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.
28. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
29. Powers SK, MLA, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 33: 386-392, 2001.
30. Powers SK, Shanely RA. Exercise-induced changes in diaphragmatic bioenergetic and antioxidant capacity. Exerc Sport Sci Rev 30: 69-74, 2002.
31. 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.
32. Powers SK, Wiggs MP, Sollanek KJ, Smuder AJ. Ventilator-induced diaphragm dysfunction: cause and effect. Am J Physiol Regul Integr Comp Physiol 305: R464-R477, 2013.
33. Ren YY, Overmyer KA, Qi NR, Treutelaar MK, Heckenkamp L, Kalahar M, Koch LG, Britton SL, Burant CF, Li JZ. Genetic analysis of a rat model of aerobic capacity and metabolic fitness. PLoS One 8: e77588, 2013.
34. Rivas DA, Lessard SJ, Saito M, Friedhuber AM, Koch LG, Britton SL, Yaspelkis BB, 3rd Hawley JA. Low intrinsic running capacity is associated with reduced skeletal muscle substrate oxidation and lower mitochondrial content in white skeletal muscle. Am J Physiol Regul Integr Comp Physiol 300: R835-R843, 2011.
35. Seifert EL, Bastianelli M, Aguer C, Moffat C, Estey C, Koch LG, Britton SL, Harper ME. Intrinsic aerobic capacity correlates with greater inherent mitochondrial oxidative and H2O2 emission capacities without major shifts in myosin heavy chain isoform. J Appl Physiol 113: 1624-1634, 2012.
36. Selsby JT, Dodd SL. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol Regul Integr Comp Physiol 289: R134-R139, 2005.
37. 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.
38. Smuder AJ, Hudson MB, Nelson WB, Kavazis AN, Powers SK. Nuclear factor-kappaB signaling contributes to mechanical ventilation-induced diaphragm weakness. Crit Care Med 40: 927-934, 2012.
39. Smuder AJ, Min K, Hudson MB, Kavazis AN, Kwon OS, Nelson WB, Powers SK. Endurance exercise attenuates ventilator-induced diaphragm dysfunction. J Appl Physiol 112: 501-510, 2012.
40. Stephenson EJ, Stepto NK, Koch LG, Britton SL, Hawley JA. Divergent skeletal muscle respiratory capacities in rats artificially selected for high and low running ability: a role for Nor1? J Appl Physiol 113: 1403-1412, 2012.
41. Talbert EE, Smuder AJ, Min K, Kwon OS, Szeto HH, Powers SK. Immobilization-induced activation of key proteolytic systems in skeletal muscles is prevented by a mitochondria-targeted antioxidant. J Appl Physiol 115: 529-538, 2013.
42. Tamaki N. Effect of growth on muscle capillarity and fiber type composition in rat diaphragm. Eur J Appl Physiol Occup Physiol 54: 24-29, 1985.
43. Tweedie C, Romestaing C, Burelle Y, Safdar A, Tarnopolsky MA, Seadon S, Britton SL, Koch LG, Hepple RT. Lower oxidative DNA damage despite greater ROS production in muscles from rats selectively bred for high running capacity. Am J Physiol Regul Integr Comp Physiol 300: R544-R553, 2011.
44. Vassilakopoulos T, Petrof BJ. Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 169: 336-341, 2004.
45. 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.
46. 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.
47. 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, 2010.
48. Wisloff U, Najjar SM, Ellingsen O, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei K, Lee SJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307: 418-420, 2005.
49. Xiao R, Ferry AL, Dupont-Versteegden EE. Cell death-resistance of differentiated myotubes is associated with enhanced anti-apoptotic mechanisms compared to myoblasts. Apoptosis 16: 221-234, 2011.