Impaired Exercise training-induced muscle fiber hypertrophy and Akt/mTOR pathway activation in hypoxemic patients with COPD

Journal of Applied Physiology

Volumn 118, Issue 8, 2015, Pages 1040-1049

  Costes, Frédéric ^a,b   Gosker, Harry ^c   Feasson, Léonard ^a,b   Desgeorges, Marine ^b   Kelders, Marco ^c   Castells, Josiane ^b   Schols, Annemie ^c   Freyssenet, Damien ^b  

^a UNIVERSITY HOSPITAL OF SAINT ETIENNE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

COPD; Exercise training; Hypoxia; Skeletal muscle

Indexed keywords

CITRATE SYNTHASE; LACTATE DEHYDROGENASE; MTOR PROTEIN, HUMAN; PROTEIN KINASE B; SOMATOMEDIN C; TARGET OF RAPAMYCIN KINASE;

ANIMAL; ANOXIA; CELL LINE; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMPLICATION; ENZYMOLOGY; EXERCISE; FEMALE; HUMAN; HYPERTROPHY; MALE; METABOLISM; MIDDLE AGED; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; ANOXIA; CELL LINE; CITRATE (SI)-SYNTHASE; FEMALE; HUMANS; HYPERTROPHY; INSULIN-LIKE GROWTH FACTOR I; L-LACTATE DEHYDROGENASE; MALE; MICE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; PHYSICAL CONDITIONING, HUMAN; PROTO-ONCOGENE PROTEINS C-AKT; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; TOR SERINE-THREONINE KINASES;

EID: 84928316101     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00557.2014     Document Type: Article

References (50)

1. Agle DP, Baum GL, Chester EH, Wendt M. Multidiscipline treatment of chronic pulmonary insufficiency. 1 Psychologic aspects of rehabilitation. Psychosom Med 35:41-49, 1973.
2. Altenburg WA, De Greef MH, Ten Hacken NH, Wempe JB. A better response in exercise capacity after pulmonary rehabilitation in more severe COPD patients. Respir Med 106:694-700, 2012.
3. Amirouche A, Durieux AC, Banzet S, Koulmann N, Bonnefoy R, Mouret C, Bigard X, Peinnequin A, Freyssenet D. Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150:286-294, 2009.
4. Belman MJ, Brooks LR, Ross DJ, Mohsenifar Z. Variability of breathlessness measurement in patients with chronic obstructive pulmonary disease. Chest 99:566-571, 1991.
5. Bernard S, Le Blanc P, Whittom F, Carrier G, Jobin J, Belleau R, Maltais F. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158:629-634, 1998.
6. Berthon P, Duguez S, Favier FB, Amirouche A, Feasson L, Vico L, Denis C, Freyssenet D. Regulation of ubiquitin-proteasome system, caspase enzyme activities, and extracellular proteinases in rat soleus muscle in response to unloading. Pflugers Arch 454:625-633, 2007.
7. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, De Chiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704-1708, 2001.
8. Carone M, Patessio A, Ambrosino N, Baiardi P, Balbi B, Balzano G, Cuomo V, Donner CF, Fracchia C, Nava S, Neri M, Pozzi E, Vitacca M, Spanevello A. Efficacy of pulmonary rehabilitation in chronic respiratory failure (CRF) due to chronic obstructive pulmonary disease (COPD): the Maugeri Study. Respir Med 101:2447-2453, 2007.
9. Chaudhary P, Suryakumar G, Prasad R, Singh SN, Ali S, Ilavazhagan G. Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin-proteasome pathway and calpains. Mol Cell Biochem 364:101-113, 2012.
10. Desgeorges MM, Freyssenet D, Chanon S, Castells J, Pugnière P, Béchet D, Peinnequin A, Devillard X, Defour A. Post-transcriptional regulation of autophagy in C2C12 myotubes following starvation and nutrient restoration. Int J Biochem Cell Biol 54:208-216, 2014.
11. Doucet M, Russell AP, Léger B, Debigaré R, Joanisse DR, Caron MA, Le Blanc P, Maltais F. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176:261-269, 2007.
12. Duguez S, Bihan Le MC, Gouttefangeas D, Féasson L, Freyssenet D. Myogenic and nonmyogenic cells differentially express proteinases, Hsc/Hsp70, and BAG-1 during skeletal muscle regeneration. Am J Physiol Endocrinol Metab 285:E206-E215, 2003.
13. Duguez S, Féasson L, Denis C, Freyssenet D. Mitochondrial biogenesis during skeletal muscle regeneration. Am J Physiol Endocrinol Metab 282:E802-E809, 2002.
14. Durieux AC, Amirouche A, Banzet S, Koulmann N, Bonnefoy R, Pasdeloup M, Mouret C, Bigard X, Peinnequin A, Freyssenet D. Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression. Endocrinology 148:3140-3147, 2007.
15. Eliason G, Abdel-Halim SM, Piehl-Aulin K, Kadi F. Alterations in the muscle-to-capillary interface in patients with different degrees of chronic obstructive pulmonary disease. Respir Res 11:97, 2010.
16. Etheridge T, Atherton PJ, Wilkinson D, Selby A, Rankin D, Webborn N, Smith K, Watt PW. Effects of hypoxia on muscle protein synthesis (MPS) and anabolic signaling at rest and in response to acute resistance exercise. Am J Physiol Endocrinol Metab 301:E697-E702, 2011.
17. Fabbri LM, Rabe KF. From COPD to chronic systemic inflammatory syndrome? Lancet 370:797-799, 2007.
18. Favier FB, Costes F, Defour A, Bonnefoy R, Lefai E, Bauge S, Peinnequin A, Benoit H, Freyssenet DG, Baugé S. Downregulation of Akt/mammalian target of rapamycin pathway in skeletal muscle is associated with increased REDD1 expression in response to chronic hypoxia. Am J Physiol Regul Integr Comp Physiol 298:R1659-R1666, 2010.
19. 2 peak and the capillary supply to skeletal muscle. J Appl Physiol 82:1305-1310, 1997.
20. Howald H, Pette D, Simoneau JA, Uber A, Hoppeler H, Cerretelli P. Effects of chronic hypoxia on muscle enzyme activities. Int J Sport Med 11:S10-S14, 1990.
21. Joassard OR, Amirouche A, Gallot YS, Desgeorges MM, Castells J, Durieux AC, Berthon P, Freyssenet DG. Regulation of Akt-mTOR, ubiquitin-proteasome and autophagy-lysosome pathways in response to formoterol administration in rat skeletal muscle. Int J Biochem Cell Biol 45:2444-2455, 2013.
22. Kang SG, Brown AL, Chung JH. Oxygen tension regulates the stability of insulin receptor substrate-1 (IRS-1) through caspase-mediated cleavage. J Biol Chem 282:6090-6097, 2007.
23. Kyle UG, Dupertuis YM, Raguso CA, Hans D, Pichard C. Appendicular skeletal muscle mass (ASMM) percentiles in 7489 healthy adults aged 18-98 years determined by bioelectrical impedance analysis (BIA). Clin Nutr 22:S1, 2003.
24. Lewis MI, Fournier M, Storer TW, Bhasin S, Porszasz J, Ren SG, Da X, Casaburi R. Skeletal muscle adaptations to testosterone and resistance training in men with COPD. J Appl Physiol 103:1299-1310, 2007.
25. Majmundar AJ, Skuli N, Mesquita RC, Kim MN, Yodh AG, Nguyen-McCarty M, Simon MC. O (2) regulates skeletal muscle progenitor differentiation through phosphatidylinositol 3-kinase/AKT signaling. Mol Cell Biol 32:36-49, 2012.
26. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458-471, 2007.
27. McClelland GB, Brooks GA. Changes in MCT 1, MCT 4, and LDH expression are tissue specific in rats after long-term hypobaric hypoxia. J Appl Physiol 92:1573-1584, 2002.
28. Nici L, Donner C, Wouters E, Zuwallack R, Ambrosino N, Bourbeau J, Carone M, Celli B, Engelen M, Fahy B, Garvey C, Goldstein R, Gosselink R, Lareau S, MacIntyre N, Maltais F, Morgan M, O'Donnell D, Prefault C, Reardon J, Rochester C, Schols A, Singh S, Troosters T. American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation. Am J Respir Crit Care Med 173:1390-1413, 2006.
29. Pison CM, Cano NJ, Chérion C, Caron F, Court-Fortune I, Antonini MT, Gonzalez-Bermejo J, Meziane L, Molano LC, Janssens JP, Costes F, Wuyam B, Similowski T, Melloni B, Hayot M, Augustin J, Tardif C, Lejeune H, Roth H, Pichard C. Multimodal nutritional rehabilitation improves clinical outcomes of malnourished patients with chronic respiratory failure: a randomised controlled trial. Thorax 66:953-960, 2011.
30. Plant PJ, Brooks D, Faughnan M, Bayley T, Bain J, Singer L, Correa J, Pearce D, Binnie M, Batt J. Cellular markers of muscle atrophy in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 42:461-471, 2010.
31. Puhan MA, Chandra D, Mosenifar Z, Ries A, Make B, Hansel NN, Wise RA, Sciurba F. The minimal important difference of exercise tests in severe COPD. Eur Respir J 37:784-790, 2011.
32. Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C, Rodriguez-Roisin R, Van Weel C, Zielinski J. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 176:532-555, 2007.
33. Radom-Aizik S, Kaminski N, Hayek S, Halkin H, Cooper DM, Ben-Dov I. Effects of exercise training on quadriceps muscle gene expression in chronic obstructive pulmonary disease. J Appl Physiol 102:1976-1984, 2007.
34. Ries AL, Bauldoff GS, Carlin BW, Casaburi R, Emery CF, Mahler DA, Make B, Rochester CL, Zuwallack R, Herrerias C. Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based clinical practice guidelines. Chest 131:4S-42S, 2007.
35. Ripamonti M, Viganò A, Moriggi M, Milano G, Von Segesser LK, Samaja M, Gelfi C. Cytochrome c oxidase expression in chronic and intermittent hypoxia rat gastrocnemius muscle quantitated by CE. Electrophoresis 27:3897-3903, 2006.
36. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI (3) K/Akt/mTOR and PI (3) K/Akt/GSK3 pathways. Nat Cell Biol 3:1009-1013, 2001.
37. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399-412, 2004.
38. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82:53-59, 2005.
39. Schols AM, Soeters PB, Mostert R, Pluymers RJ, Wouters EF. Physiologic effects of nutritional support and anabolic steroids in patients with chronic obstructive pulmonary disease. A placebo-controlled randomized trial. Am J Respir Crit Care Med 152:1268-1274, 1995.
40. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395-403, 2004.
41. Tzatsos A, Tsichlis PN. Energy depletion inhibits phosphatidylinositol 3-kinase/Akt signaling and induces apoptosis via AMP-activated protein kinase-dependent phosphorylation of IRS-1 at Ser-794. J Biol Chem 282:18069-18082, 2007.
42. Vallet G, Ahmaïdi S, Serres I, Fabre C, Bourgouin D, Desplan J, Varray A, Préfaut C. Comparison of two training programmes in chronic airway limitation patients: standardized versus individualized protocols. Eur Respir J 10:114-122, 1997.
43. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1-12, 2002.
44. Vincent L, Féasson L, Oyono-Enguéllé S, Banimbek V, Denis C, Guarneri C, Aufradet E, Monchanin G, Martin C, Gozal D, Dohbobga M, Wouassi D, Garet M, Thiriet P, Messonnier L. Remodeling of skeletal muscle microvasculature in sickle cell trait and alpha-thalassemia. Am J Physiol Heart Circ Physiol 298:H375-H384, 2010.
45. Vogiatzis I, Simoes DC, Stratakos G, Kourepini E, Terzis G, Manta P, Athanasopoulos D, Roussos C, Wagner PD, Zakynthinos S. Effect of pulmonary rehabilitation on muscle remodelling in cachectic patients with COPD. Eur Respir J 36:301-310, 2010.
46. Vogiatzis I, Terzis G, Stratakos G, Cherouveim E, Athanasopoulos D, Spetsioti S, Nasis I, Manta P, Roussos C, Zakynthinos S. Effect of pulmonary rehabilitation on peripheral muscle fiber remodeling in patients with COPD in GOLD stages II to IV. Chest 140:744-752, 2011.
47. Wagner PD. Possible mechanisms underlying the development of cachexia in COPD. Eur Respir J 31:492-501, 2008.
48. Wanger J, Clausen JL, Coates A, Pedersen OF, Brusasco V, Burgos F, Casaburi R, Crapo R, Enright P, Van Der Grinten CP, Gustafsson P, Hankinson J, Jensen R, Johnson D, Macintyre N, McKay R, Miller MR, Navajas D, Pellegrino R, Viegi G. Standardisation of the measurement of lung volumes. Eur Respir J 26:511-522, 2005.
49. Wüst RC, Degens H. Factors contributing to muscle wasting and dysfunction in COPD patients. Int J Chron Obstruct Pulmon Dis 2:289-300, 2007.
50. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472-483, 2007.