A transient antioxidant stress response accompanies the onset of disuse atrophy in human skeletal muscle

Journal of Applied Physiology

Volumn 107, Issue 2, 2009, Pages 549-557

  Dalla Libera, Luciano ^a   Ravara, Barbara ^a   Gobbo, Valerio ^a   Tarricone, Elena ^a   Vitadello, Maurizio ^a   Biolo, Gianni ^b   Vescovo, Giorgio ^c   Gorza, Luisa ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c SAN BORTOLO HOSPITAL   (Italy)

Author keywords

Bed rest; Glucose related protein 75; Heme oxygenase 1; Hindlimb suspension; Protein carbonylation

Indexed keywords

GLUCOSE REGULATED PROTEIN; GLUCOSE REGULATED PROTEIN 75; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; HUMAN; HUMAN TISSUE; MUSCLE ATROPHY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE;

ADULT; ANIMALS; ANTIOXIDANTS; BED REST; BIOPSY; HEME OXYGENASE-1; HINDLIMB SUSPENSION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MALE; MEMBRANE PROTEINS; MUSCULAR ATROPHY; OXIDATIVE STRESS; PROTEIN CARBONYLATION; QUADRICEPS MUSCLE; RATS; RATS, WISTAR; TIME FACTORS; YOUNG ADULT;

EID: 68249153286     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00280.2009     Document Type: Article

References (51)

1. Adams GR, Caiozzo VJ, Baldwin KM. Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol 95: 2185-2201, 2003.
2. Allen DL, Linderman JK, Roy RR, Bigbeee AJ, Grindeland RE, Mukku V, Egerton VR. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol Cell Physiol 273: C579-C587, 1997.
3. Arbogast S, Smith J, Matuszczak Y, Hardin BJ, Moylan JS, Smith JD, Ware J, Kennedy AR, Reid MB. Bowman-Birk inhibitor concentrate prevents atrophy, weakness, and oxidative stress in soleus muscle of hindlimb-unloaded mice. J Appl Physiol 102: 956-964, 2007.
4. Barker T, Traber MG. From animals to humans: evidence linking oxidative stress as a causative factor in muscle atrophy. J Physiol 583: 221-222, 2007.
5. Berg HE, Larsson L, Tesch PA. Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol 82: 182-188, 1997.
6. Biolo G, Agostini F, Simunic B, Sturma M, Torelli L, Preiser JC, Deby-Dupont G, Magni P, Strollo F, di Prampero P, Guarnieri G, Mekjavic IB, Pis?ot R, Narici M. Positive energy balance is associated to accelerated muscle atrophy and increased erythrocyte glutathione turnover during 5 wk of bed rest. Am J Clin Nutr 88: 950-958, 2008.
7. Blottner D, Salanova M, Püttmann B, Schiffl G, Felsenberg D, Buehring B, Rittweger J. Human skeletal muscle structure and function preserved by vibration muscle exercise following 55 days of bed rest. Eur J Appl Physiol 97: 261-271, 2006.
8. Crowe AV, McArdle A, McArdle F, Patweel DM, Bell GM, Kemp GJ, Bone JM, Griffiths RD, Jackson MJ. Markers of oxidative stress in the skeletal muscle of patients on haemodialysis. Nephrol Dial Transplant 22: 1177-1183, 2007.
9. Dalla Libera L, Ravara B, Gobbo V, Danieli Betto D, Germinario E, Angelini A, Vescovo G. Skeletal muscle myofibrillar protein oxidation in heart failure and the protective effect of Carvedilol. J Mol Cell Cardiol 38: 803-807, 2005.
10. Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase-derived oxidative stress. Hypertension 50: 636-642, 2007.
11. de Boer MD, Seynnes OR, di Prampero PE, Pišot R, Mekjavic IB, Biolo G, Narici MV. Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur J Appl Physiol 104: 401-407, 2008.
12. 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.
13. Furukawa-Hibi Y, Yoshida-Araki K, Ohta T, Ikeda K, Motoyama N. FOXO forkhead transcription factors induce G(2)-M checkpoint in response to oxidative stress. J Biol Chem 277: 26729-26732, 2002.
14. Gjøvaag TF, Dahl HA. Effect of training and detraining on the expression of heat shock proteins in m. triceps brachii of untrained males and females. Eur J Appl Physiol 98: 310-322, 2006.
15. Gorza L. Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies. J Histochem Cytochem 38: 257-265, 1990.
16. Gorza L, Menabò R, Di Lisa F, Vitadello M. Troponin T cross-linking in human apoptotic cardiomyocytes. Am J Pathol 150: 2087-2098, 1997.
17. Hofer T, Marzetti E, Xu J, Seo AY, Gulec S, Knutson MD, Leeuwenburgh C, Dupont-Versteegden EE. Increased iron content and RNA oxidative damage in skeletal muscle with aging and disuse atrophy. Exp Gerontol 43: 563-570, 2008.
18. Hunter RB, Mitchell-Felton H, Essig DA, Kandarian SC. Expression of endoplasmic reticulum stress proteins during skeletal muscle disuse atrophy. Am J Physiol Cell Physiol 281: C1285-C1290, 2001.
19. Jaspers SR, Tischler ME. Atrophy and growth failure of rat hindlimb muscles in tail-cast suspension. J Appl Physiol 57: 1472-1479, 1984.
20. Kaul SC, Deocaris CC, Wadhwa R. Three faces of mortalin: a housekeeper, guardian and killer. Exp Gerontol 42: 263-274, 2007.
21. Koesterer TJ, Dodd SL, Powers S. Increased antioxidant capacity does not attenuate muscle atrophy caused by unweighting. J Appl Physiol 93: 1959-1965, 2002.
22. Kondo H, Miura M, Itokawa Y. Oxidative stress in skeletal muscle atrophied by immobilization. Acta Physiol Scand 142: 527-528, 1991.
23. Kondo H, Miura M, Itokawa Y. Antioxidant enzyme systems in skeletal muscle atrophied by immobilization. Pflügers Arch 422: 404-406, 1993.
24. Larsson L, Li X, Berg HE, Frontera WR. Effects of removal of weight-bearing function on contractility and myosin isoform composition in single human skeletal muscle cells. Pflügers Arch 432: 320-328, 1996.
25. 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.
26. Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J Mol Med 86: 1113-1126, 2008.
27. Liu Y, Liu W, Song XD, Zuo J. Effect of GRP75/mthsp70/PBP74/ mortalin overexpression on intracellular ATP level, mitochondrial membrane potential and ROS accumulation following glucose deprivation in PC12 cells. Mol Cell Biochem 268: 45-51, 2005.
28. Margaritis I, Rousseau AS, Marini JF, Chopard A. Does antioxidant system adaptive response alleviate related oxidative damage with long term bed rest? Clin Biochem 42: 371-379, 2009.
29. Marin-Corral J, Minguella J, Ramírez-Sarmiento AL, Hussain SNA, Gea J, Barreiro E. Oxidized proteins and superoxide anion production in the diaphragm of severe COPD patients. Eur Respir J 33: 1309-1319, 2009.
30. Mitsumoto A, Takeuchi A, Okawa K, Nakagawa Y. A subset of newly synthesized polypeptides in mitochondria from human endothelial cells exposed to hydroperoxide stress. Free Radic Biol Med 32: 22-37, 2002.
31. Motterlini R. Heme oxygenase-1: a key step in counteracting cellular dysfunction. Cell Mol Biol 51: 343-346, 2005.
32. Naito H, Powers SK, Demirel HA, Sugiura T, Dodd SL, Aoki J. Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighed rats. J Appl Physiol 88: 359-363, 2000.
33. Oishi Y, Ogata T, Yamamoto KI, Terada M, Ohira T, Ohira Y, Taniguchi K, Roy RR. Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiol (Oxf) 192: 381-395, 2008.
34. Pavy-Le Traon A, Heer M, Narici MV, Rittweger J, Vernikos J. From space to Earth: advances in human physiology from 20 years of bed rest studies (1986 -2006). Eur J Appl Physiol 101: 143-194, 2007.
35. Pizzo P, Scapin S, Vitadello M, Florean C, Gorza L. Grp94 acts as a mediator of curcumin-induced anti-oxidant defence in myogenic cells. J Cell Mol Med. In press.
36. Powers SK, Kavazis AN, McClung JM. Oxidative stress and disuse muscle atrophy. J Appl Physiol 102: 2389-2397, 2007.
37. Ryter SW, Alam J, Choi AMK. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650, 2006.
38. Sacheck JM, Hyatt JPK, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155, 2007.
39. Salanova M, Schiffl G, Rittweger J, Felsenberg D, Blottner D. Ryanodine receptor type-1 (RyR1) expression and protein S-nitrosylation pattern in human soleus myofibres following bed rest and exercise countermeasure. Histochem Cell Biol 130: 105-118, 2008.
40. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T. Three myosin heavy chain isoforms in type 2 skeletal muscle fibers. J Muscle Res Cell Motil 10: 197-205, 1989.
41. Senf SH, Dodd SL, McClung JM, Judge AR. Hsp70 overexpression inhibits NF-κB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 22: 3836-3845, 2008.
42. Serrano L, Perez M, Lucia A, Chicharro JL, Quiroz-Rothe E, Rivero JLL. Immunolabelling, histochemistry and in situ hybridisation in human skeletal muscle fibres to detect myosin heavy chain expression at the protein and mRNA level. J Anat 199: 329-337, 2001.
43. Smerdu V, Karsch-Mizrachi I, Campione M, Leinwand L, Schiaffino S. Type IIx myosin heavy chain transcripts are expressed in type IIb fibers of human skeletal muscle. Am J Physiol Cell Physiol 267: C1723-C1728, 1994.
44. Stein TP. Space flight and oxidative stress. Nutrition 18: 867-871, 2002.
45. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551: 33-48, 2003.
46. Tarricone E, Scapin C, Vitadello M, Esposito F, Margonato V, Milano G, Samaja M, Gorza L. Cellular distribution of Hsp70 expression in rat skeletal muscles. Effects of moderate exercise training and chronic hypoxia. Cell Stress Chaperones 13: 483-495, 2008.
47. van der Velden J. Functional significance of myofilament protein oxidation. Eur Heart J 27: 764-765, 2006.
48. Venojärvi M, Aunola S, Puhke R, Marniemi J, Hämälä inen H, Halonen JP, Lindström J, Rastas M, Hällsten K, Nuutila P, Hänninen O, Atalay M. Exercise training with dietary counselling increases mitochondrial chaperone expression in middle-aged subjects with impaired glucose tolerance. BMC Endocr Disord 8: 3, 2009.
49. Vescovo G, Dalla Libera L, Serafini F, Leprotti C, Facchin M, Volterrani M, Ceconi C, Ambrosio GB. Improved exercise tolerance after losartan and enalapril in heart failure: correlation with changes in skeletal muscle myosin heavy chain composition. Circulation 98: 1742-1749, 1998.
50. Vescovo G, Ravara B, Dalla Libera L. Skeletal muscle myofibrillar protein oxidation and exercise capacity in heart failure. Basic Res Cardiol 103: 285-290, 2008.
51. Waterlow JC. Protein turnover in the whole animal. Invest Cell Pathol 3: 107-119, 1980.