Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways

Cellular and Molecular Life Sciences

Volumn 71, Issue 22, 2014, Pages 4361-4371

  Rodriguez, J ^a   Vernus, B ^a   Chelh, I ^b   Cassar Malek, I ^b   Gabillard, J C ^d   Hadj Sassi, A ^c   Seiliez, I ^e   Picard, B ^b   Bonnieu, A ^a  

^a University of Montpellier   (France)

^b UMR1213 HERBIVORES   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d Campus de Beaulieu   (France)

^e UR1067 Nutrition Metabolism Aquaculture   (France)

Author keywords

Growth differentiation factor 8; mTOR; Muscle differentiation; Muscle homeostasis; Protein degradation; Translational machinery

Indexed keywords

MYOSTATIN; TARGET OF RAPAMYCIN KINASE;

CELL ACTIVATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; METABOLIC REGULATION; MOLECULAR PATHOLOGY; MUSCLE ATROPHY; MUSCLE HYPERTROPHY; MUSCLE METABOLISM; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REVIEW; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSLATION REGULATION; HYPERTROPHY; METABOLISM; PATHOLOGY;

RODENTIA;

CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; HYPERTROPHY; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSTATIN; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84925285790     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1689-x     Document Type: Review

References (100)

1. Ruegg MA, Glass DJ (2011) Molecular mechanisms and treatment options for muscle wasting diseases. Annu Rev Pharmacol Toxicol 51:373-395. doi: 10.1146/annurev-pharmtox-010510-100537
2. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37(10):1974-1984. doi: 10.1016/j.biocel.2005.04.018
3. Sandri M (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23:160-170. doi: 10.1152/physiol.00041.2007
4. Elliott B, Renshaw D, Getting S, Mackenzie R (2012) The central role of myostatin in skeletal muscle and whole body homeostasis. Acta Physiol (Oxf) 205(3):324-340. doi: 10.1111/j.1748-1716.2012.02423.x
5. McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387(6628):83-90
6. Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA (2007) A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 3(5):e79. doi: 10.1371/journal.pgen.0030079
7. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17(1):71-74. doi: 10.1038/ng0997-71
8. Kambadur R, Sharma M, Smith TP, Bass JJ (1997) Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7(9):910-916
9. Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe B, Bouix J, Caiment F, Elsen JM, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M (2006) A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38(7):813-818. doi: 10.1038/ng1810
10. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ (2004) Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350(26):2682-2688. doi: 10.1056/NEJMoa040933
11. Szabo G, Dallmann G, Muller G, Patthy L, Soller M, Varga L (1998) A deletion in the myostatin gene causes the compact (Cmpt) hypermuscular mutation in mice. Mamm Genome 9(8):671-672
12. Grobet L, Pirottin D, Farnir F, Poncelet D, Royo LJ, Brouwers B, Christians E, Desmecht D, Coignoul F, Kahn R, Georges M (2003) Modulating skeletal muscle mass by postnatal, muscle-specific inactivation of the myostatin gene. Genesis 35(4):227-238. doi: 10.1002/gene.10188
13. Whittemore LA, Song K, Li X, Aghajanian J, Davies M, Girgenrath S, Hill JJ, Jalenak M, Kelley P, Knight A, Maylor R, O'Hara D, Pearson A, Quazi A, Ryerson S, Tan XY, Tomkinson KN, Veldman GM, Widom A, Wright JF, Wudyka S, Zhao L, Wolfman NM (2003) Inhibition of myostatin in adult mice increases skeletal muscle mass and strength. Biochem Biophys Res Commun 300(4):965-971 (pii):S0006291X02029534
14. Rebbapragada A, Benchabane H, Wrana JL, Celeste AJ, Attisano L (2003) Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol Cell Biol 23(20):7230-7242
15. Lee SJ, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98(16):9306-9311
16. Derynck R, Zhang Y, Feng XH (1998) Smads: transcriptional activators of TGF-beta responses. Cell 95(6):737-740
17. Forbes D, Jackman M, Bishop A, Thomas M, Kambadur R, Sharma M (2006) Myostatin auto-regulates its expression by feedback loop through Smad7 dependent mechanism. J Cell Physiol 206(1):264-272
18. Zhu X, Topouzis S, Liang LF, Stotish RL (2004) Myostatin signaling through Smad2, Smad3 and Smad4 is regulated by the inhibitory Smad7 by a negative feedback mechanism. Cytokine 26(6):262-272. doi: 10.1016/j.cyto.2004.03.007
19. Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, Abraham R, Sandri M (2009) Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol 296(6):C1248-C1257. doi: 10.1152/ajpcell.00104.2009
20. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ (2009) Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296(6):C1258-C1270. doi: 10.1152/ajpcell.00105.2009
21. Sartori R, Schirwis E, Blaauw B, Bortolanza S, Zhao J, Enzo E, Stantzou A, Mouisel E, Toniolo L, Ferry A, Stricker S, Goldberg AL, Dupont S, Piccolo S, Amthor H, Sandri M (2013) BMP signaling controls muscle mass. Nat Genet 45(11):1309-1318. doi: 10.1038/ng.2772
22. Liu W, Thomas SG, Asa SL, Gonzalez-Cadavid N, Bhasin S, Ezzat S (2003) Myostatin is a skeletal muscle target of growth hormone anabolic action. J Clin Endocrinol Metab 88(11):5490-5496
23. Brill KT, Weltman AL, Gentili A, Patrie JT, Fryburg DA, Hanks JB, Urban RJ, Veldhuis JD (2002) Single and combined effects of growth hormone and testosterone administration on measures of body composition, physical performance, mood, sexual function, bone turnover, and muscle gene expression in healthy older men. J Clin Endocrinol Metab 87(12):5649-5657
24. Mendler L, Baka Z, Kovacs-Simon A, Dux L (2007) Androgens negatively regulate myostatin expression in an androgen-dependent skeletal muscle. Biochem Biophys Res Commun 361(1):237-242
25. Braga M, Bhasin S, Jasuja R, Pervin S, Singh R (2012) Testosterone inhibits transforming growth factor-beta signaling during myogenic differentiation and proliferation of mouse satellite cells: potential role of follistatin in mediating testosterone action. Mol Cell Endocrinol 350(1):39-52. doi: 10.1016/j.mce.2011.11.019
26. Dubois V, Laurent MR, Sinnesael M, Cielen N, Helsen C, Clinckemalie L, Spans L, Gayan-Ramirez G, Deldicque L, Hespel P, Carmeliet G, Vanderschueren D, Claessens F (2014) A satellite cell-specific knockout of the androgen receptor reveals myostatin as a direct androgen target in skeletal muscle. FASEB J. doi: 10.1096/fj.14-249748
27. Kim JS, Cross JM, Bamman MM (2005) Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women. Am J Physiol Endocrinol Metab 288(6):E1110-E1119. doi: 10.1152/ajpendo.00464.2004
28. Michel RN, Dunn SE, Chin ER (2004) Calcineurin and skeletal muscle growth. Proc Nutr Soc 63(2):341-349
29. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM (2012) A PGC-1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151(6):1319-1331. doi: 10.1016/j.cell.2012.10.050
30. Roth SM, Martel GF, Ferrell RE, Metter EJ, Hurley BF, Rogers MA (2003) Myostatin gene expression is reduced in humans with heavy-resistance strength training: a brief communication. Exp Biol Med (Maywood) 228(6):706-709
31. Willoughby DS (2004) Effects of an alleged myostatin-binding supplement and heavy resistance training on serum myostatin, muscle strength and mass, and body composition. Int J Sport Nutr Exerc Metab 14(4):461-472
32. Willoughby DS (2004) Effects of heavy resistance training on myostatin mRNA and protein expression. Med Sci Sports Exerc 36(4):574-582 (pii):00005768-200404000-00004
33. Hayot M, Rodriguez J, Vernus B, Carnac G, Jean E, Allen D, Goret L, Obert P, Candau R, Bonnieu A (2011) Myostatin up-regulation is associated with the skeletal muscle response to hypoxic stimuli. Mol Cell Endocrinol 332(1-2):38-47. doi: 10.1016/j.mce.2010.09.008
34. Yarasheski KE, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid NF (2002) Serum myostatin-immunoreactive protein is increased in 60-92 year old women and men with muscle wasting. J Nutr Health Aging 6(5):343-348
35. Ratkevicius A, Joyson A, Selmer I, Dhanani T, Grierson C, Tommasi AM, DeVries A, Rauchhaus P, Crowther D, Alesci S, Yaworsky P, Gilbert F, Redpath TW, Brady J, Fearon KC, Reid DM, Greig CA, Wackerhage H (2011) Serum concentrations of myostatin and myostatin-interacting proteins do not differ between young and sarcopenic elderly men. J Gerontol A Biol Sci Med Sci 66(6):620-626. doi: 10.1093/gerona/glr025
36. Siriett V, Platt L, Salerno MS, Ling N, Kambadur R, Sharma M (2006) Prolonged absence of myostatin reduces sarcopenia. J Cell Physiol 209(3):866-873
37. 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(11):4433-4442. doi: 10.1096/fj.10-159608
38. Kawada S, Tachi C, Ishii N (2001) Content and localization of myostatin in mouse skeletal muscles during aging, mechanical unloading and reloading. J Muscle Res Cell Motil 22(8):627-633
39. Baumann AP, Ibebunjo C, Grasser WA, Paralkar VM (2003) Myostatin expression in age and denervation-induced skeletal muscle atrophy. J Musculoskelet Neuronal Interact 3(1):8-16
40. Carlson CJ, Booth FW, Gordon SE (1999) Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am J Physiol 277(2 Pt 2):R601-R606
41. Oldham JM, Osepchook CC, Jeanplong F, Falconer SJ, Matthews KG, Conaglen JV, Gerrard DF, Smith HK, Wilkins RJ, Bass JJ, McMahon CD (2009) The decrease in mature myostatin protein in male skeletal muscle is developmentally regulated by growth hormone. J Physiol 587(Pt 3):669-677. doi: 10.1113/jphysiol.2008.161521
42. Ohsawa Y, Hagiwara H, Nakatani M, Yasue A, Moriyama K, Murakami T, Tsuchida K, Noji S, Sunada Y (2006) Muscular atrophy of caveolin-3-deficient mice is rescued by myostatin inhibition. J Clin Invest 116(11):2924-2934
43. Gilson H, Schakman O, Combaret L, Lause P, Grobet L, Attaix D, Ketelslegers JM, Thissen JP (2007) Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148(1):452-460
44. Salehian B, Mahabadi V, Bilas J, Taylor WE, Ma K (2006) The effect of glutamine on prevention of glucocorticoid-induced skeletal muscle atrophy is associated with myostatin suppression. Metabolism 55(9):1239-1247. doi: 10.1016/j.metabol.2006.05.009
45. Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, McPherron AC, Wolfman NM, Lee SJ (2002) Induction of cachexia in mice by systemically administered myostatin. Science 296(5572):1486-1488. doi: 10.1126/science.1069525
46. Durieux AC, Amirouche A, Banzet S, Koulmann N, Bonnefoy R, Pasdeloup M, Mouret C, Bigard X, Peinnequin A, Freyssenet D (2007) Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression. Endocrinology 148(7):3140-3147
47. Amirouche A, Durieux AC, Banzet S, Koulmann N, Bonnefoy R, Mouret C, Bigard X, Peinnequin A, Freyssenet D (2009) Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150(1):286-294. doi: 10.1210/en.2008-0959
48. McMahon CD, Popovic L, Oldham JM, Jeanplong F, Smith HK, Kambadur R, Sharma M, Maxwell L, Bass JJ (2003) Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension. Am J Physiol Endocrinol Metab 285(1):E82-E87
49. Bischoff R, Heintz C (1994) Enhancement of skeletal muscle regeneration. Dev Dyn 201(1):41-54. doi: 10.1002/aja.1002010105
50. Schmalbruch H, al-Amood WS, Lewis DM (1991) Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J Physiol 441:233-241
51. Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112(Pt 17):2895-2901
52. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162(6):1135-1147. doi: 10.1083/jcb.200207056
53. Magee TR, Artaza JN, Ferrini MG, Vernet D, Zuniga FI, Cantini L, Reisz-Porszasz S, Rajfer J, Gonzalez-Cadavid NF (2006) Myostatin short interfering hairpin RNA gene transfer increases skeletal muscle mass. J Gene Med 8(9):1171-1181. doi: 10.1002/jgm.946
54. Amthor H, Otto A, Vulin A, Rochat A, Dumonceaux J, Garcia L, Mouisel E, Hourde C, Macharia R, Friedrichs M, Relaix F, Zammit PS, Matsakas A, Patel K, Partridge T (2009) Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity. Proc Natl Acad Sci USA 106(18):7479-7484. doi: 10.1073/pnas.0811129106
55. Welle S, Mehta S, Burgess K (2011) Effect of postdevelopmental myostatin depletion on myofibrillar protein metabolism. Am J Physiol Endocrinol Metab 300(6):E993-E1001. doi: 10.1152/ajpendo.00509.2010
56. Lee SJ, Huynh TV, Lee YS, Sebald SM, Wilcox-Adelman SA, Iwamori N, Lepper C, Matzuk MM, Fan CM (2012) Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway. Proc Natl Acad Sci USA 109(35):E2353-E2360. doi: 10.1073/pnas.1206410109
57. Rodriguez J, Vernus B, Toubiana M, Jublanc E, Tintignac L, Leibovitch S, Bonnieu A (2011) Myostatin inactivation increases myotube size through regulation of translational initiation machinery. J Cell Biochem 112(12):3531-3542. doi: 10.1002/jcb.23280
58. Wang Q, McPherron AC (2012) Myostatin inhibition induces muscle fibre hypertrophy prior to satellite cell activation. J Physiol 590(Pt 9):2151-2165. doi: 10.1113/jphysiol.2011.226001
59. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275(51):40235-40243
60. Rios R, Carneiro I, Arce VM, Devesa J (2002) Myostatin is an inhibitor of myogenic differentiation. Am J Physiol Cell Physiol 282(5):C993-C999
61. Taylor WE, Bhasin S, Artaza J, Byhower F, Azam M, Willard DH Jr, Kull FC Jr, Gonzalez-Cadavid N (2001) Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. Am J Physiol Endocrinol Metab 280(2):E221-E228
62. Joulia D, Bernardi H, Garandel V, Rabenoelina F, Vernus B, Cabello G (2003) Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp Cell Res 286(2):263-275 (pii):S0014482703000740
63. Yang W, Zhang Y, Li Y, Wu Z, Zhu D (2007) Myostatin induces cyclin D1 degradation to cause cell cycle arrest through a phosphatidylinositol 3-kinase/AKT/GSK-3 beta pathway and is antagonized by insulin-like growth factor 1. J Biol Chem 282(6):3799-3808
64. Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277(51):49831-49840
65. McFarlane C, Hui GZ, Amanda WZ, Lau HY, Lokireddy S, Xiaojia G, Mouly V, Butler-Browne G, Gluckman PD, Sharma M, Kambadur R (2011) Human myostatin negatively regulates human myoblast growth and differentiation. Am J Physiol Cell Physiol 301(1):C195-C203. doi: 10.1152/ajpcell.00012.2011
66. Amthor H, Huang R, McKinnell I, Christ B, Kambadur R, Sharma M, Patel K (2002) The regulation and action of myostatin as a negative regulator of muscle development during avian embryogenesis. Dev Biol 251(2):241-257
67. Salerno MS, Thomas M, Forbes D, Watson T, Kambadur R, Sharma M (2004) Molecular analysis of fiber type-specific expression of murine myostatin promoter. Am J Physiol Cell Physiol 287(4):C1031-C1040
68. Yang W, Chen Y, Zhang Y, Wang X, Yang N, Zhu D (2006) Extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase pathway is involved in myostatin-regulated differentiation repression. Cancer Res 66(3):1320-1326
69. Chelh I, Meunier B, Picard B, Reecy MJ, Chevalier C, Hocquette JF, Cassar-Malek I (2009) Molecular profiles of Quadriceps muscle in myostatin-null mice reveal PI3K and apoptotic pathways as myostatin targets. BMC Genom 10:196
70. Chelh I, Picard B, Hocquette JF, Cassar-Malek I (2011) Myostatin inactivation induces a similar muscle molecular signature in double-muscled cattle as in mice. Animal 5(2):278-286. doi: 10.1017/S1751731110001862
71. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) 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(11):1009-1013. doi: 10.1038/ncb1101-1009
72. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3(11):1014-1019
73. 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(14):9213-9218. doi: 10.1073/pnas.142166599
74. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471-484. doi: 10.1016/j.cell.2006.01.016
75. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18(16):1926-1945. doi: 10.1101/gad.1212704
76. Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10(5):307-318. doi: 10.1038/nrm2672
77. Tee AR, Blenis J (2005) mTOR, translational control and human disease. Semin Cell Dev Biol 16(1):29-37. doi: 10.1016/j.semcdb.2004.11.005
78. Meyuhas O (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267(21):6321-6330 (pii):ejb1719
79. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB, Hannan RD (2003) mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23(23):8862-8877
80. Morissette MR, Cook SA, Buranasombati C, Rosenberg MA, Rosenzweig A (2009) Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am J Physiol Cell Physiol 297(5):C1124-C1132. doi: 10.1152/ajpcell.00043.2009
81. Lipina C, Kendall H, McPherron AC, Taylor PM, Hundal HS (2010) Mechanisms involved in the enhancement of mammalian target of rapamycin signalling and hypertrophy in skeletal muscle of myostatin-deficient mice. FEBS Lett 584(11):2403-2408. doi: 10.1016/j.febslet.2010.04.039
82. Suryawan A, Frank JW, Nguyen HV, Davis TA (2006) Expression of the TGF-beta family of ligands is developmentally regulated in skeletal muscle of neonatal rats. Pediatr Res 59(2):175-179. doi: 10.1203/01.pdr.0000196718.47935.6e
83. Welle S, Bhatt K, Pinkert CA (2006) Myofibrillar protein synthesis in myostatin-deficient mice. Am J Physiol Endocrinol Metab 290(3):E409-E415. doi: 10.1152/ajpendo.00433.2005
84. Welle S, Burgess K, Mehta S (2009) Stimulation of skeletal muscle myofibrillar protein synthesis, p70 S6 kinase phosphorylation, and ribosomal protein S6 phosphorylation by inhibition of myostatin in mature mice. Am J Physiol Endocrinol Metab 296(3):E567-E572. doi: 10.1152/ajpendo.90862.2008
85. Steelman CA, Recknor JC, Nettleton D, Reecy JM (2006) Transcriptional profiling of myostatin-knockout mice implicates Wnt signaling in postnatal skeletal muscle growth and hypertrophy. FASEB J 20(3):580-582. doi: 10.1096/fj.05-5125fje
86. Csibi A, Cornille K, Leibovitch MP, Poupon A, Tintignac LA, Sanchez AM, Leibovitch SA (2010) The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS One 5(2):e8994. doi: 10.1371/journal.pone.0008994
87. Lagirand-Cantaloube J, Offner N, Csibi A, Leibovitch MP, Batonnet-Pichon S, Tintignac LA, Segura CT, Leibovitch SA (2008) The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J 27(8):1266-1276. doi: 10.1038/emboj.2008.52
88. Mayhew DL, Hornberger TA, Lincoln HC, Bamman MM (2011) Eukaryotic initiation factor 2B epsilon induces cap-dependent translation and skeletal muscle hypertrophy. J Physiol 589(Pt 12):3023-3037. doi: 10.1113/jphysiol.2010.202432
89. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117(3):399-412 (pii):S0092867404004003
90. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14(3):395-403 (pii):S1097276504002114
91. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209(2):501-514
92. Allen DL, Unterman TG (2007) Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 292(1):C188-C199
93. Lokireddy S, Mouly V, Butler-Browne G, Gluckman PD, Sharma M, Kambadur R, McFarlane C (2011) Myostatin promotes the wasting of human myoblast cultures through promoting ubiquitin-proteasome pathway-mediated loss of sarcomeric proteins. Am J Physiol Cell Physiol 301(6):C1316-C1324. doi: 10.1152/ajpcell.00114.2011
94. Lokireddy S, Wijesoma IW, Sze SK, McFarlane C, Kambadur R, Sharma M (2012) Identification of atrogin-1-targeted proteins during the myostatin-induced skeletal muscle wasting. Am J Physiol Cell Physiol 303(5):C512-C529. doi: 10.1152/ajpcell.00402.2011
95. Mendias CL, Kayupov E, Bradley JR, Brooks SV, Claflin DR (2011) Decreased specific force and power production of muscle fibers from myostatin-deficient mice are associated with a suppression of protein degradation. J Appl Physiol 111(1):185-191. doi: 10.1152/japplphysiol.00126.2011
96. Sriram S, Subramanian S, Juvvuna PK, Ge X, Lokireddy S, McFarlane CD, Wahli W, Kambadur R, Sharma M (2014) Myostatin augments muscle-specific ring finger protein-1 expression through an NF-kB independent mechanism in SMAD3 null muscle. Mol Endocrinol 28(3):317-330. doi: 10.1210/me.2013-1179
97. Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, Rosenfeld R, Chen Q, Boone T, Simonet WS, Lacey DL, Goldberg AL, Han HQ (2010) Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142(4):531-543. doi: 10.1016/j.cell.2010.07.011
98. Lee JY, Hopkinson NS, Kemp PR (2011) Myostatin induces autophagy in skeletal muscle in vitro. Biochem Biophys Res Commun 415(4):632-636. doi: 10.1016/j.bbrc.2011.10.124
99. Seiliez I, Taty Taty GC, Bugeon J, Dias K, Sabin N, Gabillard JC (2013) Myostatin induces atrophy of trout myotubes through inhibiting the TORC1 signaling and promoting ubiquitin-proteasome and autophagy-lysosome degradative pathways. Gen Comp Endocrinol 186:9-15. doi: 10.1016/j.ygcen.2013.02.008
100. Garikipati DK, Rodgers BD (2012) Myostatin stimulates myosatellite cell differentiation in a novel model system: evidence for gene subfunctionalization. Am J Physiol Regul Integr Comp Physiol 302(9):R1059-R1066. doi: 10.1152/ajpregu.00523.2011