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Journal of Muscle Research and Cell Motility

, Volume 36, Issue 6, pp 405–421 | Cite as

Skeletal muscle atrophy: disease-induced mechanisms may mask disuse atrophy

  • C. J. Malavaki
  • G. K. Sakkas
  • G. I. Mitrou
  • A. Kalyva
  • I. Stefanidis
  • K. H. Myburgh
  • C. Karatzaferi
Review Article

Abstract

Disuse atrophy is the loss of skeletal muscle mass due to inactivity or lower than ‘normal’ use. It is not only a furtive component of the ‘modern’ sedentary lifestyle but also a part of numerous pathologies, where muscle loss is linked to disease specific and/or other toxicity factors, eventually leading to wasting (cachexia). Whether disuse-or-disease induced, muscle loss leads to weakness and metabolic comorbidities with a high societal and financial cost. This review discusses the intricate network of interacting signalling pathways including Atrogin-1/MAFbx, IGF1-Akt, myostatin, glucocorticoids, NF-kB, MAPKs and caspases that seem to regulate disuse atrophy but also share common activation patterns in other states of muscle loss such as sarcopenia or cachexia. Reactive oxygen species are also important regulators of cell signalling pathways that can accelerate proteolysis and depress protein synthesis. Exercise is an effective countermeasure and antioxidants may show some benefit. We discuss how the experimental model used can crucially affect the outcome and hence our understanding of atrophy. Timing of sampling is crucial as some signalling mechanisms reach their peak early during the atrophy process to rapidly decline thereafter, while other present high levels even weeks and months after study initiation. The importance of such differences lays in future consideration of appropriate treatment targets. Apart from attempting to correct defective genes or negate their effects, technological advances in new rational ways should aim to regulate specific gene expression at precise time points for the treatment of muscle atrophy in therapeutic protocols depending on the origin of atrophy induction.

Keywords

Protein synthesis Protein degradation Ubiquitin–proteasome system Redox status Mechanical loading Atrophy countermeasures 

Notes

Acknowledgments

G.K.S, G.M, I.S., and C.K., acknowledge the support of the European Union (European Social Fund—ESF) and Greek national funds through the Operational Program “Educational and Lifelong Learning” of the National Strategic Reference Framework (NSRF)—Research Funding Program: Thales Investing in knowledge society through the European Social Fund, (MuscleFun Project-MIS 377260). K.H.M. acknowledges H2020 MCAS-RISE-645648-Muscle Stress Relief. C.M. was supported by “IKY FELLOWSHIPS OF EXCELLENCE FOR POSTGRADUATE STUDIES IN GREECE-SIEMENS PROGRAM”.

References

  1. Accili D, Arden KC (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117:421–426PubMedCrossRefGoogle Scholar
  2. A.D.A.M (2005) Medical encyclopedia muscle atrophy. A.D.A.M, AtlantaGoogle Scholar
  3. Ahmad AZ, Akhter S, Mallik N, Anwar M, Tabassum W, Ahmad FJ (2013) Application of decoy oligonucleotides as novel therapeutic strategy: a contemporary overview. Curr Drug Discov Technol 10:71–84PubMedGoogle Scholar
  4. Aloni R, Peleg D, Meyuhas O (1992) Selective translational control and nonspecific posttranscriptional regulation of ribosomal protein gene expression during development and regeneration of rat liver. Mol Cell Biol 12:2203–2212PubMedCentralPubMedCrossRefGoogle Scholar
  5. Anderson EJ, Neufer PD (2006) Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. Am J Physiol Cell Physiol 290:C844–C851. doi: 10.1152/ajpcell.00402.2005 PubMedCrossRefGoogle Scholar
  6. Annexstad EJ, Lund-Petersen I, Rasmussen M (2014) Duchenne muscular dystrophy. Tidsskr Nor Laegeforen 134:1361–1364. doi: 10.4045/tidsskr.13.0836 PubMedCrossRefGoogle Scholar
  7. Appell HJ (1990) Muscular atrophy following immobilisation. Sports Med 10:42–58PubMedCrossRefGoogle Scholar
  8. Artaza JN, Bhasin S, Mallidis C, Taylor W, Ma K, Gonzalez-Cadavid NF (2002) Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells. J Cell Physiol 190:170–179. doi: 10.1002/jcp.10044 PubMedCrossRefGoogle Scholar
  9. Barton E, Morris C (2003) Mechanisms and strategies to counteract muscle atrophy. J Gerontol 58A:923–926CrossRefGoogle Scholar
  10. Bodine SC et al (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704–1708. doi: 10.1126/science.10658741065874 PubMedCrossRefGoogle Scholar
  11. Bonaldo P, Sandri M (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6:25–39. doi: 10.1242/dmm.010389 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Booth FW, Seider MJ (1979) Early change in skeletal muscle protein synthesis after limb immobilization of rats. J Appl Physiol 47:974–977PubMedGoogle Scholar
  13. Booth FW, Roberts CK, Laye MJ (2012) Lack of exercise is a major cause of chronic diseases comprehensive. Physiology 2:1143–1211. doi: 10.1002/cphy.c110025 Google Scholar
  14. Brooks SV, Faulkner JA (1994) Skeletal muscle weakness in old age: underlying mechanisms. Med Sci Sports Exerc 26:432–439PubMedCrossRefGoogle Scholar
  15. Brooks NE, Myburgh KH (2014) Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways. Front Physiol 5:99. doi: 10.3389/fphys.2014.00099 PubMedCentralPubMedCrossRefGoogle Scholar
  16. Brooks NE, Cadena SM, Vannier E, Cloutier G, Carambula S, Myburgh KH, Roubenoff R, Castaneda-Sceppa C (2010) Effects of resistance exercise combined with essential amino acid supplementation and energy deficit on markers of skeletal muscle atrophy and regeneration during bed rest and active recovery. Muscle Nerve 42(6):927–935. doi: 10.1002/mus.21780 PubMedCentralPubMedCrossRefGoogle Scholar
  17. Brooks NE, Myburgh KH, Storey KB (2011) Myostatin levels in skeletal muscle of hibernating ground squirrels. J Exp Biol 214:2522–2527. doi: 10.1242/jeb.055764 PubMedCentralPubMedCrossRefGoogle Scholar
  18. Brunet A et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868PubMedCrossRefGoogle Scholar
  19. Campbell EL et al (2013) Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men. Biogerontology 14:247–259PubMedCrossRefGoogle Scholar
  20. Campos Y et al (2010) Ozz-E3 ubiquitin ligase targets sarcomeric embryonic myosin heavy chain during muscle development. PLoS One 5(3):e9866. doi: 10.1371/journal.pone.0009866 PubMedCentralPubMedCrossRefGoogle Scholar
  21. Carlsson P, Mahlapuu M (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250:1–23PubMedCrossRefGoogle Scholar
  22. Carrera AC (2004) TOR signaling in mammals. J Cell Sci 117:4615–4616. doi: 10.1242/jcs.01311 PubMedCrossRefGoogle Scholar
  23. Chemello F, Bean C, Cancellara P, Laveder P, Reggiani C, Lanfranchi G (2011) Microgenomic analysis in skeletal muscle: expression signatures of individual fast and slow myofibers. PLoS One 6(2):e16807. doi: 10.1371/journal.pone.0016807 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Chen YW, Gregory CM, Scarborough MT, Shi R, Walter GA, Vandenborne K (2007) Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol Genomics 31:510–520. doi: 10.1152/physiolgenomics.00115.2006 PubMedCrossRefGoogle Scholar
  25. Chen SY, Wu N, Lee YC, Zhao Y (2013) Association between muscle atrophy/weakness and health care costs and utilization among patients receiving total knee replacement surgery: a retrospective cohort study. J Pain Res 6:595–603. doi: 10.2147/JPR.S48235 PubMedCentralPubMedGoogle Scholar
  26. Childs TE, Spangenburg EE, Vyas DR, Booth FW (2003) Temporal alterations in protein signaling cascades during recovery from muscle atrophy. Am J Physiol Cell Physiol 285:C391–C398. doi: 10.1152/ajpcell.00478.2002 PubMedCrossRefGoogle Scholar
  27. Chondrogianni N, Stratford FL, Trougakos IP, Friguet B, Rivett AJ, Gonos ES (2003) Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J Biol Chem 278:28026–28037. doi: 10.1074/jbc.M301048200 PubMedCrossRefGoogle Scholar
  28. Cohen S et al (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185:1083–1095. doi: 10.1083/jcb.200901052 PubMedCentralPubMedCrossRefGoogle Scholar
  29. da Silva CA, Petermann C, Cancellier KM, Durigan JLQ, Polacow MLO (2011) IGF-1 minimizes the harmful effects of disuse on rat soleus muscle. Acta Ortop Bras 19:137–140CrossRefGoogle Scholar
  30. de Boer MD et al (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585:241–251. doi: 10.1113/jphysiol.2007.142828 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Du J et al (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115–123. doi: 10.1172/JCI18330 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Engelbrecht AM, Smith C, Neethling I, Thomas M, Ellis B, Mattheyse M, Myburgh KH (2010) Daily brief restraint stress alters signaling pathways and induces atrophy and apoptosis in rat skeletal muscle. Stress 13(2):132–141. doi: 10.3109/10253890903089834 PubMedCrossRefGoogle Scholar
  33. Fielitz J et al (2007) Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3. J Clin Investig 117:2486–2495. doi: 10.1172/JCI32827 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Finkel T (2001) Reactive oxygen species and signal transduction. IUBMB Life 52:3–6. doi: 10.1080/15216540252774694 PubMedCrossRefGoogle Scholar
  35. Flach RJ, Bennett AM (2010) MAP kinase phosphatase-1–a new player at the nexus between sarcopenia and metabolic disease. Aging (Albany NY) 2:170–176Google Scholar
  36. Foletta VC, White LJ, Larsen AE, Leger B, Russell AP (2011) The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pflug Arch 461:325–335. doi: 10.1007/s00424-010-0919-9 CrossRefGoogle Scholar
  37. Gallagher P et al (2005) Effects of 84-days of bedrest and resistance training on single muscle fibre myosin heavy chain distribution in human vastus lateralis and soleus muscles. Acta Physiol Scand 185:61–69PubMedCrossRefGoogle Scholar
  38. Gayan-Ramirez G, Vanderhoydonc F, Verhoeven G, Decramer M (1999) Acute treatment with corticosteroids decreases IGF-1 and IGF-2 expression in the rat diaphragm and gastrocnemius. Am J Respir Crit Care Med 159:283–289. doi: 10.1164/ajrccm.159.1.9803021 PubMedCrossRefGoogle Scholar
  39. Gilson H et al (2007) Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148:452–460. doi: 10.1210/en.2006-0539 PubMedCrossRefGoogle Scholar
  40. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98:14440–14445. doi: 10.1073/pnas.251541198251541198 PubMedCentralPubMedCrossRefGoogle Scholar
  41. Gonzalez-Cadavid NF et al (1998) Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci USA 95:14938–14943PubMedCentralPubMedCrossRefGoogle Scholar
  42. Goossens V, Grooten J, De Vos K, Fiers W (1995) Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 92:8115–8119PubMedCentralPubMedCrossRefGoogle Scholar
  43. Gruenewald DA, Matsumoto AM (2003) Testosterone supplementation therapy for older men: potential benefits and risks. J Am Geriatr Soc 51:101–115PubMedCrossRefGoogle Scholar
  44. Gustafsson T, Osterlund T, Flanagan JN, von Walden F, Trappe TA, Linnehan RM, Tesch PA (2010) Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 109:721–727. doi: 10.1152/japplphysiol.00110.2009 PubMedCrossRefGoogle Scholar
  45. Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS Jr (2000) NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289:2363–2366PubMedCrossRefGoogle Scholar
  46. Hasselgren PO (1999) Glucocorticoids and muscle catabolism. Curr Opin Clin Nutr Metab Care 2:201–205PubMedCrossRefGoogle Scholar
  47. Hasselgren PO, Fischer JE (1997) The ubiquitin-proteasome pathway: review of a novel intracellular mechanism of muscle protein breakdown during sepsis and other catabolic conditions. Ann Surg 225:307–316PubMedCentralPubMedCrossRefGoogle Scholar
  48. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479. doi: 10.1146/annurev.biochem.67.1.425 PubMedCrossRefGoogle Scholar
  49. Hilder TL, Tou JC, Grindeland RE, Wade CE, Graves LM (2003) Phosphorylation of insulin receptor substrate-1 serine 307 correlates with JNK activity in atrophic skeletal muscle. FEBS Lett 553:63–67PubMedCrossRefGoogle Scholar
  50. Hirose M, Kaneki M, Sugita H, Yasuhara S, Martyn JA (2000) Immobilization depresses insulin signaling in skeletal muscle. Am J Physiol Endocrinol Metab 279:E1235–E1241PubMedGoogle Scholar
  51. Hochstrasser M (1996) Protein degradation or regulation: Ub the judge. Cell 84:813–815PubMedCrossRefGoogle Scholar
  52. Holgate ST, Komaroff AL, Mangan D, Wessely S (2011) Chronic fatigue syndrome: understanding a complex illness. Nat Rev Neurosci 12:539–544. doi: 10.1038/nrn3087 PubMedCrossRefGoogle Scholar
  53. Hunter RB, Kandarian SC (2004) Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J Clin Investig 114:1504–1511. doi: 10.1172/JCI21696 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Hunter RB, Stevenson E, Koncarevic A, Mitchell-Felton H, Essig DA, Kandarian SC (2002) Activation of an alternative NF-kappaB pathway in skeletal muscle during disuse atrophy. FASEB J 16:529–538PubMedCrossRefGoogle Scholar
  55. Jackman RW, Kandarian SC (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287:C834–C843. doi: 10.1152/ajpcell.00579.2003287/4/C834 PubMedCrossRefGoogle Scholar
  56. Jagoe RT, Goldberg AL (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4:183–190PubMedCrossRefGoogle Scholar
  57. Jin J, Li X, Gygi SP, Harper JW (2007) Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447:1135–1138. doi: 10.1038/nature05902 PubMedCrossRefGoogle Scholar
  58. Jones SW, Hill RJ, Krasney PA, O’Conner B, Peirce N, Greenhaff PL (2004) Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18:1025–1027. doi: 10.1096/fj.03-1228fje PubMedGoogle Scholar
  59. Kaltsatou A et al (2015) Uremic myopathy: is oxidative stress implicated in muscle dysfunction in uremia? Front Physiol 6:102. doi: 10.3389/fphys.2015.00102 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Kawamura I et al (1999) Intratumoral injection of oligonucleotides to the NF kappa B binding site inhibits cachexia in a mouse tumor model. Gene Ther 6:91–97. doi: 10.1038/sj.gt.3300819 PubMedCrossRefGoogle Scholar
  61. Kedar V, McDonough H, Arya R, Li HH, Rockman HA, Patterson C (2004) Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc Natl Acad Sci USA 101:18135–18140. doi: 10.1073/pnas.0404341102 PubMedCentralPubMedCrossRefGoogle Scholar
  62. Kondo H, Miura M, Itokawa Y (1991) Oxidative stress in skeletal muscle atrophied by immobilization. Acta Physiol Scand 142:527–528. doi: 10.1111/j.1748-1716.1991.tb09191.x PubMedCrossRefGoogle Scholar
  63. Krawiec BJ, Frost RA, Vary TC, Jefferson LS, Lang CH (2005) Hindlimb casting decreases muscle mass in part by proteasome-dependent proteolysis but independent of protein synthesis. Am J Physiol Endocrinol Metab 289:E969–E980. doi: 10.1152/ajpregu.00126.2005 PubMedCrossRefGoogle Scholar
  64. Lagirand-Cantaloube J et al (2008) The initiation factor eIF3-f is a major target for Atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J 27:1266–1276. doi: 10.1038/emboj.2008.52 PubMedCentralPubMedCrossRefGoogle Scholar
  65. Lagirand-Cantaloube J, Cornille K, Csibi A, Batonnet-Pichon S, Leibovitch MP, Leibovitch SA (2009) Inhibition of Atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS One. doi: 10.1371/journal.pone.0004973 PubMedCentralPubMedGoogle Scholar
  66. Lawler JM, Song W (2002) Specificity of antioxidant enzyme inhibition in skeletal muscle to reactive nitrogen species donors. Biochem Biophys Res Commun 294:1093–1100. doi: 10.1016/S0006-291X(02)00602-2 PubMedCrossRefGoogle Scholar
  67. Lawler JM, Song W, Demaree SR (2003) Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35:9–16PubMedCrossRefGoogle Scholar
  68. Lee SJ, Glass DJ (2011) Treating cancer cachexia to treat cancer. Skelet Muscle 1:2. doi: 10.1186/2044-5040-1-2 PubMedCentralPubMedCrossRefGoogle Scholar
  69. Levine S et al (2011) Increased proteolysis, myosin depletion, and atrophic AKT-FOXO signaling in human diaphragm disuse. Am J Respir Crit Care Med 183:483–490. doi: 10.1164/rccm.200910-1487OC PubMedCentralPubMedCrossRefGoogle Scholar
  70. Li YP, Reid MB (2000) NF-kappaB mediates the protein loss induced by TNF-alpha in differentiated skeletal muscle myotubes. Am J Physiol Regul Integr Comp Physiol 279:R1165–R1170PubMedGoogle Scholar
  71. Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB (1998) Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J 12:871–880PubMedGoogle Scholar
  72. Li YP, Chen Y, Li AS, Reid MB (2003) Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am J Physiol Cell Physiol 285:C806–C812. doi: 10.1152/ajpcell.00129.200300129.2003 PubMedCrossRefGoogle Scholar
  73. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB (2005) TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J 19:362–370. doi: 10.1096/fj.04-2364com PubMedCentralPubMedCrossRefGoogle Scholar
  74. Lofberg E et al (2002) Effects of high doses of glucocorticoids on free amino acids, ribosomes and protein turnover in human muscle. Eur J Clin Investig 32:345–353CrossRefGoogle Scholar
  75. Malavaki CJ et al (2013) Imatinib as a key inhibitor of the platelet-derived growth factor receptor mediated expression of cell surface heparan sulfate proteoglycans and functional properties of breast cancer cells. FEBS J 280:2477–2489. doi: 10.1111/febs.12163 PubMedCrossRefGoogle Scholar
  76. Mammucari C et al (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471. doi: 10.1016/j.cmet.2007.11.001 PubMedCrossRefGoogle Scholar
  77. Mammucari C, Schiaffino S, Sandri M (2008) Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4:524–526PubMedCrossRefGoogle Scholar
  78. Masharani UB et al (2011) Insulin resistance in non-obese subjects is associated with activation of the JNK pathway and impaired insulin signaling in skeletal muscle. PLoS One. doi: 10.1371/journal.pone.0019878 PubMedCentralPubMedGoogle Scholar
  79. McFarlane C et al (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209:501–514. doi: 10.1002/jcp.20757 PubMedCrossRefGoogle Scholar
  80. Min K, Smuder AJ, Kwon OS, Kavazis AN, Szeto HH, Powers SK (2011) Mitochondrial-targeted antioxidants protect skeletal muscle against immobilization-induced muscle atrophy. J Appl Physiol 111:1459–1466. doi: 10.1152/japplphysiol.00591.2011 PubMedCentralPubMedCrossRefGoogle Scholar
  81. Moresi V et al (2010) Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143:35–45. doi: 10.1016/j.cell.2010.09.004 PubMedCentralPubMedCrossRefGoogle Scholar
  82. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13. doi: 10.1042/BJ20081386 PubMedCentralPubMedCrossRefGoogle Scholar
  83. Murphy KT, Koopman R, Naim T, Leger B, Trieu J, Ibebunjo C, Lynch GS (2010) Antibody-directed myostatin inhibition in 21-mo-old mice reveals novel roles for myostatin signaling in skeletal muscle structure and function. FASEB J 24:4433–4442. doi: 10.1096/fj.10-159608 PubMedCrossRefGoogle Scholar
  84. Nakao R et al (2009) Ubiquitin ligase Cbl-b is a negative regulator for insulin-like growth factor 1 signaling during muscle atrophy caused by unloading. Mol Cell Biol 29:4798–4811. doi: 10.1128/MCB.01347-08 PubMedCentralPubMedCrossRefGoogle Scholar
  85. Nikawa T et al (2004) Skeletal muscle gene expression in space-flown rats. FASEB J 18:522–524. doi: 10.1096/fj.03-0419fje PubMedGoogle Scholar
  86. Nordquist J, Hoglund AS, Norman H, Tang X, Dworkin B, Larsson L (2007) Transcription factors in muscle atrophy caused by blocked neuromuscular transmission and muscle unloading in rats. Mol Med 13:461–470. doi: 10.2119/2006-00066.Nordquist PubMedCentralPubMedCrossRefGoogle Scholar
  87. Nowell MM, Choi H, Rourke BC (2011) Muscle plasticity in hibernating ground squirrels (Spermophilus lateralis) is induced by seasonal, but not low-temperature, mechanisms Journal of comparative physiology B. Biochem Syst Environ Physiol 181:147–164. doi: 10.1007/s00360-010-0505-7 CrossRefGoogle Scholar
  88. Ogawa M et al (2013) The preventive effect of beta-carotene on denervation-induced soleus muscle atrophy in mice. Br J Nutr 109:1349–1358. doi: 10.1017/S0007114512003297 PubMedCrossRefGoogle Scholar
  89. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci USA 99:9213–9218. doi: 10.1073/pnas.142166599 PubMedCentralPubMedCrossRefGoogle Scholar
  90. Palus S, von Haehling S, Springer J (2014) Muscle wasting: an overview of recent developments in basic research. Int J Cardiol 176:640–644. doi: 10.1016/j.ijcard.2014.08.086 PubMedCrossRefGoogle Scholar
  91. Paschalis V et al (2007) Uniform and prolonged changes in blood oxidative stress after muscle-damaging exercise. In Vivo 21:877–883PubMedGoogle Scholar
  92. Pellegrino MA, Desaphy JF, Brocca L, Pierno S, Camerino DC, Bottinelli R (2011) Redox homeostasis, oxidative stress and disuse muscle atrophy. J Physiol 589:2147–2160. doi: 10.1113/jphysiol.2010.203232 PubMedCentralPubMedCrossRefGoogle Scholar
  93. Peterson JM, Bakkar N, Guttridge DC (2011) NF-kappaB signaling in skeletal muscle health and disease. Curr Top Dev Biol 96:85–119. doi: 10.1016/B978-0-12-385940-2.00004-8 PubMedCrossRefGoogle Scholar
  94. Powers SK (2014) Can antioxidants protect against disuse muscle atrophy? Sports Med 44(Suppl 2):S155–S165. doi: 10.1007/s40279-014-0255-x PubMedCrossRefGoogle Scholar
  95. Powers SK, Kavazis AN, McClung JM (2007) Oxidative stress and disuse muscle atrophy. J Appl Physiol 102:2389–2397. doi: 10.1152/japplphysiol.01202.2006 PubMedCrossRefGoogle Scholar
  96. Powers SK, Smuder AJ, Criswell DS (2011) Mechanistic links between oxidative stress and disuse muscle atrophy. Antioxid Redox Signal 15:2519–2528. doi: 10.1089/ars.2011.3973 PubMedCentralPubMedCrossRefGoogle Scholar
  97. Powers SK, Smuder AJ, Judge AR (2012) Oxidative stress and disuse muscle atrophy: cause or consequence? Curr Opin Clin Nutr Metab Care 15:240–245. doi: 10.1097/MCO.0b013e328352b4c2 PubMedCentralPubMedCrossRefGoogle Scholar
  98. Pupim LB, Flakoll PJ, Yu c, Ikizler TA (2005) Recombinant human growth hormone improves muscle amino acid uptake and whole-body protein metabolism in chronic hemodialysis patients. Am J Clin Nutr 82:1235–1243PubMedGoogle Scholar
  99. Qi M, Elion EA (2005) MAP kinase pathways. J Cell Sci 118:3569–3572. doi: 10.1242/jcs.02470 PubMedCrossRefGoogle Scholar
  100. Reisz-Porszasz S et al (2003) Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin. Am J Physiol Endocrinol Metab 285:E876–E888. doi: 10.1152/ajpendo.00107.200300107.2003 PubMedCrossRefGoogle Scholar
  101. Risson V et al (2009) Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187:859–874. doi: 10.1083/jcb.200903131 PubMedCentralPubMedCrossRefGoogle Scholar
  102. Romanick M, Thompson LV, Brown-Borg HM (2013) Murine models of atrophy, cachexia, and sarcopenia in skeletal muscle. Biochim Biophys Acta 1832:1410–1420PubMedCentralPubMedCrossRefGoogle Scholar
  103. Sadowski M, Sarcevic B (2010) Mechanisms of mono- and poly-ubiquitination: ubiquitination specificity depends on compatibility between the E2 catalytic core and amino acid residues proximal to the lysine. Cell Div 5:19. doi: 10.1186/1747-1028-5-19 PubMedCentralPubMedCrossRefGoogle Scholar
  104. Sakkas GK, Karatzaferi C (2012) Hemodialysis fatigue: just “simple” fatigue or a syndrome on its own right? Front Physiol 3:1–4CrossRefGoogle Scholar
  105. Sakkas GK, Ball D, Mercer TH, Sargeant AJ, Tolfrey K, Naish PF (2003a) Atrophy of non-locomotor muscle in patients with end-stage renal failure. Nephrol Dial Transpl 18:2074–2081CrossRefGoogle Scholar
  106. Sakkas GK, Sargeant AJ, Mercer TH, Ball D, Koufaki P, Karatzaferi C, Naish PF (2003b) Changes in muscle morphology in dialysis patients after 6 months of aerobic exercise training. Nephrol Dial Transpl 18:1854–1861CrossRefGoogle Scholar
  107. Sakkas GK et al (2008) Haemodialysis patients with sleep apnoea syndrome experience increased central adiposity and altered muscular composition and functionality. Nephrol Dial Transpl 23:336–344CrossRefGoogle Scholar
  108. Sakuma K, Watanabe K, Hotta N, Koike T, Ishida K, Katayama K, Akima H (2009) The adaptive responses in several mediators linked with hypertrophy and atrophy of skeletal muscle after lower limb unloading in humans. Acta Physiol (Oxf) 197:151–159. doi: 10.1111/j.1748-1716.2009.01995.x CrossRefGoogle Scholar
  109. Salanova M, Schiffl G, Puttmann B, Schoser BG, Blottner D (2008) Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long-term bed rest with and without countermeasures. J Anat 212:306–318. doi: 10.1111/j.1469-7580.2008.00854.x PubMedCentralPubMedCrossRefGoogle Scholar
  110. Sandri M (2013) Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome. Int J Biochem Cell Biol 45:2121–2129. doi: 10.1016/j.biocel.2013.04.023 PubMedCentralPubMedCrossRefGoogle Scholar
  111. Sandri M et al (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399–412PubMedCentralPubMedCrossRefGoogle Scholar
  112. Schakman O, Gilson H, Thissen JP (2008) Mechanisms of glucocorticoid-induced myopathy. J Endocrinol 197:1–10. doi: 10.1677/JOE-07-0606 PubMedCrossRefGoogle Scholar
  113. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1:4. doi: 10.1186/2044-5040-1-4 PubMedCentralPubMedCrossRefGoogle Scholar
  114. Senf SM, Dodd SL, McClung JM, Judge AR (2008) Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 22:3836–3845. doi: 10.1096/fj.08-110163 PubMedCrossRefGoogle Scholar
  115. Senf SM, Dodd SL, Judge AR (2010) FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol Cell Physiol 298:C38–C45. doi: 10.1152/ajpcell.00315.2009 PubMedCentralPubMedCrossRefGoogle Scholar
  116. Servais S, Letexier D, Favier R, Duchamp C, Desplanches D (2007) Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic Biol Med 42:627–635. doi: 10.1016/j.freeradbiomed.2006.12.001 PubMedCentralPubMedCrossRefGoogle Scholar
  117. Shao C, Liu M, Wu X, Ding F (2007) Time-dependent expression of myostatin RNA transcript and protein in gastrocnemius muscle of mice after sciatic nerve resection. Microsurgery 27:487–493. doi: 10.1002/micr.20392 PubMedCrossRefGoogle Scholar
  118. Smith RC, Lin BK (2013) Myostatin inhibitors as therapies for muscle wasting associated with cancer and other disorders. Curr Opin Support Palliat Care 7:352–360PubMedCentralPubMedCrossRefGoogle Scholar
  119. Stefanetti RJ, Zacharewicz E, Della Gatta P, Garnham A, Russell AP, Lamon S (2014) Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Front Physiol 5:1–10CrossRefGoogle Scholar
  120. Stitt TN et al (2004) The IGF-1/PI3 K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395–403PubMedCrossRefGoogle Scholar
  121. Talmadge RJ, Roy RR, Edgerton VR (1996) Distribution of myosin heavy chain isoforms in non-weight-bearing rat soleus muscle fibers. J Appl Physiol 81:2540–2546PubMedGoogle Scholar
  122. Thomason DB, Booth FW (1990) Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68:1–12PubMedCrossRefGoogle Scholar
  123. Thompson MG, Thom A, Partridge K, Garden K, Campbell GP, Calder G, Palmer RM (1999) Stimulation of myofibrillar protein degradation and expression of mRNA encoding the ubiquitin-proteasome system in C(2)C(12) myotubes by dexamethasone: effect of the proteasome inhibitor MG-132. J Cell Physiol 181:455–461. doi: 10.1002/(SICI)1097-4652(199912)181:3<455:AID-JCP9>3.0.CO;2-K PubMedCrossRefGoogle Scholar
  124. Tran H, Brunet A, Griffith EC, Greenberg ME (2003) The many forks in FOXO’s road. Sci Signal 172:RE5. doi: 10.1126/stke.2003.172.re5 CrossRefGoogle Scholar
  125. Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P (2004) Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 557:501–513. doi: 10.1113/jphysiol.2004.062166 PubMedCentralPubMedCrossRefGoogle Scholar
  126. Urso ML, Scrimgeour AG, Chen YW, Thompson PD, Clarkson PM (2006) Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J Appl Physiol 101:1136–1148. doi: 10.1152/japplphysiol.00180.2006 PubMedCrossRefGoogle Scholar
  127. van de Vyver M, Myburgh KH (2012) Cytokine and satellite cell responses to muscle damage: interpretation and possible confounding factors in human studies. J Muscle Res Cell Motil 33:177–185. doi: 10.1007/s10974-012-9303-z PubMedCentralPubMedCrossRefGoogle Scholar
  128. Waddell DS, Baehr LM, van den Brandt J, Johnsen SA, Reichardt HM, Furlow JD, Bodine SC (2008) The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 295:E785–E797. doi: 10.1152/ajpendo.00646.2007 PubMedCentralPubMedCrossRefGoogle Scholar
  129. Wall BT, Dirks ML, van Loon LJ (2013) Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev 12:898–906PubMedCrossRefGoogle Scholar
  130. Wang X, Hu Z, Hu J, Du J, Mitch WE (2006) Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signalling. Endocrinology 147:4160–4168. doi: 10.1210/en.2006-0251 PubMedCrossRefGoogle Scholar
  131. Wang M, Yu H, Kim YS, Bidwell CA, Kuang S (2012) Myostatin facilitates slow and inhibits fast myosin heavy chain expression during myogenic differentiation. Biochem Biophys Res Commun 426:83–88. doi: 10.1016/j.bbrc.2012.08.040 PubMedCentralPubMedCrossRefGoogle Scholar
  132. Wannamethee SG, Atkins JL (2015) Muscle loss and obesity: the health implications of sarcopenia and sarcopenic obesity. Proc Nutr Soc 27:1–8Google Scholar
  133. Whidden MA, Smuder AJ, Wu M, Hudson MB, Nelson WB, Powers SK (2010) Oxidative stress is required for mechanical ventilation-induced protease activation in the diaphragm. J Appl Physiol 108:1376–1382. doi: 10.1152/japplphysiol.00098.2010 PubMedCentralPubMedCrossRefGoogle Scholar
  134. Woelk T, Sigismund S, Penengo L, Polo S (2007) The ubiquitination code: a signalling problem. Cell Div 2:11. doi: 10.1186/1747-1028-2-11 PubMedCentralPubMedCrossRefGoogle Scholar
  135. Wyke SM, Tisdale MJ (2005) NF-kappaB mediates proteolysis-inducing factor induced protein degradation and expression of the ubiquitin-proteasome system in skeletal muscle. Br J Cancer 92:711–721. doi: 10.1038/sj.bjc.6602402 PubMedCentralPubMedCrossRefGoogle Scholar
  136. Xu Q, Wu Z (2000) The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cell. J Biol Chem 275(47):36750–36757. doi: 10.1074/jbc.M005030200 PubMedCrossRefGoogle Scholar
  137. Yiu EM, Kornberg AJ (2015) Duchenne muscular dystrophy. J Paediatr Child Health 51(8):759–764. doi: 10.1111/jpc.12868 PubMedCrossRefGoogle Scholar
  138. Zhang P, Chen X, Fan M (2007) Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses 69:310–321. doi: 10.1016/j.mehy.2006.11.043 PubMedCrossRefGoogle Scholar
  139. Zhao J et al (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483. doi: 10.1016/j.cmet.2007.11.004 PubMedCrossRefGoogle Scholar
  140. Zhao J, Brault JJ, Schild A, Goldberg AL (2008) Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4:378–380PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • C. J. Malavaki
    • 1
    • 2
  • G. K. Sakkas
    • 1
    • 2
    • 4
  • G. I. Mitrou
    • 1
  • A. Kalyva
    • 1
    • 4
  • I. Stefanidis
    • 2
  • K. H. Myburgh
    • 3
  • C. Karatzaferi
    • 1
    • 4
  1. 1.Muscle Physiology & Mechanics Lab DPESSUniversity of ThessalyTrikalaGreece
  2. 2.Division of Nephrology, Department of Medicine, School of Health SciencesUniversity of Thessaly, BIOPOLISLarissaGreece
  3. 3.Department of Physiological SciencesStellenbosch UniversityStellenboschSouth Africa
  4. 4.Department of KinesiologyInstitute for Research and Technology Thessaly, CERTHTrikalaGreece

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