Biphasic stress response in the soleus during reloading after hind limb unloading

Medicine and Science in Sports and Exercise

Volumn 44, Issue 4, 2012, Pages 600-609

  Lawler, John M ^a   Kwak, Hyo Bum ^a   Kim, Jong Hee ^a   Lee, Yang ^a   Hord, Jeffrey M ^a   Martinez, Daniel A ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

heat shock proteins; muscle atrophy; Nf b; nnos; oxidative stress; spaceflight

Indexed keywords

3 NITROTYROSINE; 3-NITROTYROSINE; DNA BINDING PROTEIN; DRUG DERIVATIVE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR; HSPB1 PROTEIN, RAT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN LIKE GROWTH FACTOR 1, RAT; INSULIN-LIKE GROWTH FACTOR-1, RAT; NOS2 PROTEIN, RAT; SERINE; SOMATOMEDIN C; TRANSCRIPTION FACTOR; TYROSINE;

ANIMAL; ARTICLE; HISTOLOGY; IMMOBILIZATION; MALE; METABOLISM; MUSCLE ATROPHY; ORGAN SIZE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; DNA-BINDING PROTEINS; HINDLIMB SUSPENSION; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; INSULIN-LIKE GROWTH FACTOR I; MALE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; ORGAN SIZE; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SERINE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TYROSINE;

EID: 84858701892     PISSN: 01959131     EISSN: 15300315     Source Type: Journal    
DOI: 10.1249/MSS.0b013e31823ab37a     Document Type: Article

References (46)

1. Arbogast S, Smith J, Matuszczak Y, et al. Bowman-Birk inhibitor concentrate prevents atrophy, weakness, and oxidative stress in soleus muscle of hindlimb-unloaded mice. J Appl Physiol. 2007; 102:956-64. (Pubitemid 46377018)
2. Barrera G, Pizzimenti S, Laurora S, Briatore F, Toaldo C, Dianzani MU. 4-Hydroxynonenal and cell cycle. Biofactors. 2005;24: 151-7. (Pubitemid 41750538)
3. Blanchard-Fillion B, Prou D, Polydoro M, et al. Metabolism of 3-nitrotyrosine induces apoptotic death in dopaminergic cells. J Neurosci. 2006;26:6124-30.
4. Booth FW, Criswell DS. Molecular events underlying skeletal muscle atrophy and the development of effective countermeasures. Int J Sports Med. 1997;14:S265-9.
5. Buck M, Chojkier M. Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants. EMBO J. 1996;15:1753-65. (Pubitemid 26119211)
6. Cai D, Frantz JD, Tawa NE Jr, et al. IKKA/NF-JB activation causes severe muscle wasting in mice. Cell. 2004;119:285-98. (Pubitemid 39360909)
7. Fitts RH, Riley DR, Widrick JJ. Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J Appl Physiol. 2000;89:823-39. (Pubitemid 30637134)
8. Gius D, Botero A, Shah S, Curry HA. Intracellular oxidation/reduction status in the regulation of transcription factors NF-JB and AP-1. Toxicol Lett. 1999;106:93-106. (Pubitemid 29257819)
9. Gomez-Cabrera MC, Domenech E, Vina J. Moderate exercise as an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med. 2008;44:126-31.
10. Gupte AA, Bomhoff GL, Geiger, PC. Age-related differences in skeletal muscle insulin signaling: the role of stress kinase and heat shock proteins. J Appl Physiol. 2008;105:839-48.
11. Hambrecht R, Adams V, Gielen S, et al. Exercise intolerance in patients with chronic heart failure and increased expression of inducible nitric oxide synthase in the skeletal muscle. J Am Coll Cardiol. 1999;33:174-9. (Pubitemid 29064089)
12. Hindle AG, Lawler JM, Campbell KL, Horning M. Muscle aging and oxidative stress in wild-caught shrews. Comp Biochem Physiol B Biochem Mol Biol. 2010;155:427-34.
13. Huey KA. Regulation of HSP25 expression and phosphorylation in functionally overloaded rat plantaris and soleus muscles. J Appl Physiol. 2006;100:451-6. (Pubitemid 43671594)
14. Hunter RB, Stevenson E, Koncarevic A, Mitchell-Felton H, Essig DA, Kandarian SC. Activation of an alternative NF-JB pathway in skeletal muscle during disuse atrophy. FASEB J. 2002;16:529-38. (Pubitemid 34273236)
15. Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J. Acute exercise activates nuclear factor (NF)-JB signaling pathway in rat skeletal muscle. FASEB J. 2004;18:1499-506. (Pubitemid 39336631)
16. Kaminski HJ, Andrade FH. Nitric oxide: biologic effects on muscle and role in muscle diseases. Neuromuscul Disord. 2001;11:517-24. (Pubitemid 32761793)
17. Kasper CE. Sarcolemmal disruption in reloaded atrophic skeletal muscle. J Appl Physiol. 1995;79:607-14.
18. Koh TJ. Do small heat shock proteins protect skeletal muscle from injury? Exerc Sport Sci Rev. 2002;30(3):117-21. (Pubitemid 34787298)
19. Koh TJ, Escobedo J. Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions. Am J Physiol. 2004;286:C713-22. (Pubitemid 38292678)
20. Kondo H, Nakagaki I, Sasaki S, Hori S, Itokawa Y. Mechanism of oxidative stress in skeletal muscle atrophied by immobilization. Am J Physiol. 1993;265:E839-44. (Pubitemid 24030395)
21. Kumar A, Boriek AM. Mechanical stress activates the nuclear factor-JB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J. 2003;17:386-96. (Pubitemid 36292954)
22. Lawler JM, Kwak HB, Kim JH, Suk MH. Exercise training upregulates MnSOD while reducing pro-oxidant signaling in the aging rat left ventricle. Am J Physiol. 2009;296:R1496-502.
23. Lawler JM, Powers SK, Visser T, Van Dijk H, Kordus MJ, Ji LL. Acute exercise and skeletal muscle antioxidant and metabolic enzymes: effects of fiber type and age. Am J Physiol. 1993;265: R1344-50.
24. Lawler JM, Song W, Demaree SR. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med. 2003;35:9-16. (Pubitemid 36782333)
25. Lawler JM, Song W, Kwak HB. Differential response of heat shock proteins to hindlimb unloading and reloading in the soleus. Muscle Nerve. 2006;33:200-7. (Pubitemid 43208676)
26. Mearow KM, Dodge ME, Rahimtula M, Yegappan C. Stressmediated signaling in PC12 cells-the role of the small heat shock protein, HSP27, and Akt in protecting cells from heat stress and nerve growth factor withdrawal. J Neurochem. 2002;83:452-62. (Pubitemid 35191410)
27. Naito H, Powers SK, Demirel HA, Sugiura T, Dodd SL, Aoki J. Heat stress attenuates skeletal muscle atrophy in hindlimbunweighted rats. J Appl Physiol. 2000;88:359-63. (Pubitemid 30053868)
28. Piette J, Piret B, Bonizzi G, et al. Multiple redox regulation in NFJB transcription factor activation. Biol Chem. 1997;378:1237-45. (Pubitemid 27507539)
29. Pizza FX, Hernandez IJ, Tidball JG. Nitric oxide synthase inhibition reduces muscle inflammation and necrosis in modified muscle use. J Leukoc Biol. 1998;64:427-33. (Pubitemid 28455387)
30. Powers SK, Hudson MB, Nelson WB, et al. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med. 2011;39:1749-59.
31. Powers SK, Kavazis AN, DeRuisseau KC. Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol. 2005;288: R337-44. (Pubitemid 40129594)
32. Rane MJ, Pan Y, Singh S, et al. Heat shock protein 27 controls apoptosis by regulating Akt activation. J Biol Chem. 2003;278: 27828-35. (Pubitemid 36899975)
33. Reid MB. Response of the ubiquitin-proteasome pathway to changes in muscle activity. Am J Physiol. 2005;288:R1423-31. (Pubitemid 40720691)
34. Renard P, Ernest I, Houbion A, et al. Development of a sensitive multi-well colorimetric assay for active NFJB. Nucleic Acids Res. 2001;29:E21.
35. Riley DA, Bain JL, Thompson JL, et al. Disproportionate loss of thin filaments in human soleus muscle after 17-day bed rest. Muscle Nerve. 1998;21:1280-9. (Pubitemid 28406710)
36. Safdar A, Hamadeh MJ, Kaczor JJ, Raha S, Debeer J, Tarnopolsky MA. Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLoS One. 2010;5:e10778.
37. Selsby JT, Dodd SL. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol. 2005; 289:R134-9. (Pubitemid 40874968)
38. Senf SM, Dodd SL, McClung JM, Judge AR. HSP70 overexpression inhibits NF-JB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J. 2008;22:3836-45.
39. Smith LW, Smith JD, Criswell DS. Involvement of nitric oxide synthase in skeletal muscle adaptation to chronic overload. J Appl Physiol. 2002;92:2005-11. (Pubitemid 34666428)
40. Seo Y, Lee K, Park K, Bae K, Choi I. A proteomic assessment of muscle contractile alterations during unloading and reloading. J Biochem. 2006;39:71-80. (Pubitemid 43258848)
41. Soltow QA, Betters JL, Sellman JE, Lira VA, Long JH, Criswell DS. Ibuprofen inhibits skeletal muscle hypertrophy in rats. Med Sci Sports Exerc. 2006;38(5):840-6.
42. Song W, Kwak HB, Lawler JM. Exercise training attenuates ageinduced changes in apoptotic signaling in rat skeletal muscle. Antioxid Redox Signal. 2006;8:517-28. (Pubitemid 43741321)
43. Suzuki N, Motohashi N, Uezumi A, et al. NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J Clin Invest. 2007;117:2468-76. (Pubitemid 47494348)
44. Vaziri ND, Ding Y, Sangha DS, Purdy RE. Upregulation of NOS by simulated microgravity, potential cause of orthostatic intolerance. J Appl Physiol. 2000;89:338-44. (Pubitemid 30482597)
45. Xu X, Chen CN, Arriaga EA, Thompson LV. Asymmetric superoxide release inside and outside the mitochondria in skeletal muscle under conditions of aging and disuse. J Appl Physiol. 2010; 109:1133-9.
46. Zergeroglu MA, McKenzie MJ, Shanely RA, Van Gammeren D, DeRuisseau KC, Powers SK. Mechanical ventilation-induced oxidative stress in the diaphragm. J Appl Physiol. 2003;95:1116-24. (Pubitemid 37034008)