Mechanisms regulating skeletal muscle growth and atrophy

FEBS Journal

Volumn 280, Issue 17, 2013, Pages 4294-4314

  Schiaffino, Stefano ^a,b   Dyar, Kenneth A ^a   Ciciliot, Stefano ^a   Blaauw, Bert ^a,c   Sandri, Marco ^a,c  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

FoxO; IGF1; mTOR; muscle atrophy; muscle hypertrophy; myostatin; protein degradation; protein synthesis; satellite cells

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MYOSTATIN; PROTEIN KINASE B; SMAD2 PROTEIN; SMAD3 PROTEIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UBIQUITIN;

AGING; AUTOPHAGOSOME; CACHEXIA; CELL ACTIVATION; CELL FUSION; DENERVATION; HEART FAILURE; HUMAN; LYSOSOME; MUSCLE ATROPHY; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STARVATION;

FOXO; IGF1; MTOR; MUSCLE ATROPHY; MUSCLE HYPERTROPHY; MYOSTATIN; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SATELLITE CELLS;

ANIMALS; HUMANS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; SIGNAL TRANSDUCTION;

EID: 84882733761     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12253     Document Type: Review

References (179)

1. Aravamudan B, Mantilla CB, Zhan WZ, &, Sieck GC, (2006) Denervation effects on myonuclear domain size of rat diaphragm fibers. J Appl Physiol 100, 1617-1622.
2. Li JB, &, Goldberg AL, (1976) Effects of food deprivation on protein synthesis and degradation in rat skeletal muscles. Am J Physiol 231, 441-448.
3. Goldberg AL, &, Goodman HM, (1969) Relationship between cortisone and muscle work in determining muscle size. J Physiol 200, 667-675.
4. Verheul AJ, Mantilla CB, Zhan WZ, Bernal M, Dekhuijzen PN, &, Sieck GC, (2004) Influence of corticosteroids on myonuclear domain size in the rat diaphragm muscle. J Appl Physiol 97, 1715-1722.
5. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, &, Spiegelman BM, (2006) PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103, 16260-16265.
6. Goldberg AL, (1969) Protein turnover in skeletal muscle. I. Protein catabolism during work-induced hypertrophy and growth induced with growth hormone. J Biol Chem 244, 3217-3222.
7. Argadine HM, Hellyer NJ, Mantilla CB, Zhan WZ, &, Sieck GC, (2009) The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol 107, 438-444.
8. Quy PN, Kuma A, Pierre P, &, Mizushima N, (2012) Proteasome-dependent activation of mammalian target of rapamycin complex 1 (mTORC1) is essential for autophagy suppression and muscle remodeling following denervation. J Biol Chem 288, 1125-1143.
9. Van der Meer SF, Jaspers RT, &, Degens H, (2011) Is the myonuclear domain size fixed? J Musculoskelet Neuronal Interact 11, 286-297.
10. Bruusgaard JC, Egner IM, Larsen TK, Dupre-Aucouturier S, Desplanches D, &, Gundersen K, (2012) No change in myonuclear number during muscle unloading and reloading. J Appl Physiol 113, 290-296.
11. Bruusgaard JC, &, Gundersen K, (2008) In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J Clin Invest 118, 1450-1457.
12. Ciciliot S, &, Schiaffino S, (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16, 906-914.
13. Schiaffino S, &, Mammucari C, (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1, 4.
14. Mavalli MD, DiGirolamo DJ, Fan Y, Riddle RC, Campbell KS, van Groen T, Frank SJ, Sperling MA, Esser KA, Bamman MM, et al,. (2010) Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest 120, 4007-4020.
15. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL, &, Rosenthal N, (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27, 195-200.
16. Murgia M, Serrano AL, Calabria E, Pallafacchina G, Lomo T, &, Schiaffino S, (2000) Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat Cell Biol 2, 142-147.
17. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, et al,. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
18. 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.
19. Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C, Masiero E, Abraham R, Sandri M, Schiaffino S, &, Reggiani C, (2009) Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 23, 3896-3905.
20. Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J, Hamilton JA, Ouchi N, Lebrasseur NK, &, Walsh K, (2008) Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab 7, 159-172.
21. Lai KM, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AN, Yancopoulos GD, &, Glass DJ, (2004) Conditional activation of Akt in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24, 9295-9304.
22. Laplante M, &, Sabatini DM, (2012) mTOR signaling in growth control and disease. Cell 149, 274-293.
23. Risson V, Mazelin L, Roceri M, Sanchez H, Moncollin V, Corneloup C, Richard-Bulteau H, Vignaud A, Baas D, Defour A, et al,. (2009) Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187, 859-874.
24. Bentzinger CF, Romanino K, Cloetta D, Lin S, Mascarenhas JB, Oliveri F, Xia J, Casanova E, Costa CF, Brink M, et al,. (2008) Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8, 411-424.
25. Bodine SC, (2006) mTOR signaling and the molecular adaptation to resistance exercise. Med Sci Sports Exerc 38, 1950-1957.
26. Le Bacquer O, Petroulakis E, Paglialunga S, Poulin F, Richard D, Cianflone K, &, Sonenberg N, (2007) Elevated sensitivity to diet-induced obesity and insulin resistance in mice lacking 4E-BP1 and 4E-BP2. J Clin Invest 117, 387-396.
27. Mounier R, Lantier L, Leclerc J, Sotiropoulos A, Foretz M, &, Viollet B, (2011) Antagonistic control of muscle cell size by AMPK and mTORC1. Cell Cycle 10, 2640-2646.
28. Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, &, Hornberger TA, (2011) The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589, 5485-5501.
29. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, &, Glass DJ, (2005) Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280, 2737-2744.
30. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, &, Puigserver P, (2007) mTOR controls mitochondrial oxidative function through a YY1-PGC-1α transcriptional complex. Nature 450, 736-740.
31. Blattler SM, Cunningham JT, Verdeguer F, Chim H, Haas W, Liu H, Romanino K, Ruegg MA, Gygi SP, Shi Y, et al,. (2012) Yin Yang 1 deficiency in skeletal muscle protects against rapamycin-induced diabetic-like symptoms through activation of insulin/IGF signaling. Cell Metab 15, 505-517.
32. Lee SJ, (2004) Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20, 61-86.
33. 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, E221-E228.
34. 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, C1248-C1257.
35. 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, C1258-C1270.
36. Kalista S, Schakman O, Gilson H, Lause P, Demeulder B, Bertrand L, Pende M, &, Thissen JP, (2011) The type 1 insulin-like growth factor receptor (IGF-IR) pathway is mandatory for the follistatin-induced skeletal muscle hypertrophy. Endocrinology 153, 241-253.
37. Winbanks CE, Weeks KL, Thomson RE, Sepulveda PV, Beyer C, Qian H, Chen JL, Allen JM, Lancaster GI, Febbraio MA, et al,. (2012) Follistatin-mediated skeletal muscle hypertrophy is regulated by Smad3 and mTOR independently of myostatin. J Cell Biol 197, 997-1008.
38. Remy I, Montmarquette A, &, Michnick SW, (2004) PKB/Akt modulates TGF-β signalling through a direct interaction with Smad3. Nat Cell Biol 6, 358-365.
39. Conery AR, Cao Y, Thompson EA, Townsend CM Jr, Ko TC, &, Luo K, (2004) Akt interacts directly with Smad3 to regulate the sensitivity to TGF-β induced apoptosis. Nat Cell Biol 6, 366-372.
40. Li S, Czubryt MP, McAnally J, Bassel-Duby R, Richardson JA, Wiebel FF, Nordheim A, &, Olson EN, (2005) Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc Natl Acad Sci USA 102, 1082-1087.
41. Charvet C, Houbron C, Parlakian A, Giordani J, Lahoute C, Bertrand A, Sotiropoulos A, Renou L, Schmitt A, Melki J, et al,. (2006) New role for serum response factor in postnatal skeletal muscle growth and regeneration via the interleukin 4 and insulin-like growth factor 1 pathways. Mol Cell Biol 26, 6664-6674.
42. Guerci A, Lahoute C, Hebrard S, Collard L, Graindorge D, Favier M, Cagnard N, Batonnet-Pichon S, Precigout G, Garcia L, et al,. (2012) Srf-dependent paracrine signals produced by myofibers control satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 15, 25-37.
43. Small EM, O'Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD, Richardson JA, &, Olson EN, (2010) Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci USA 107, 4218-4223.
44. White JP, Gao S, Puppa MJ, Sato S, Welle SL, &, Carson JA, (2012) Testosterone regulation of Akt/mTORC1/FoxO3a signaling in skeletal muscle. Mol Cell Endocrinol 365, 174-186.
45. Koopman R, Gehrig SM, Leger B, Trieu J, Walrand S, Murphy KT, &, Lynch GS, (2010) Cellular mechanisms underlying temporal changes in skeletal muscle protein synthesis and breakdown during chronic β-adrenoceptor stimulation in mice. J Physiol 588, 4811-4823.
46. Kline WO, Panaro FJ, Yang H, &, Bodine SC, (2007) Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol. J Appl Physiol 102, 740-747.
47. Le Grand F, Jones AE, Seale V, Scime A, &, Rudnicki MA, (2009) Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535-547.
48. von Maltzahn J, Renaud JM, Parise G, &, Rudnicki MA, (2011) Wnt7a treatment ameliorates muscular dystrophy. Proc Natl Acad Sci USA 109, 20614-20619.
49. Ito N, Ruegg UT, Kudo A, Miyagoe-Suzuki Y, &, Takeda S, (2012) Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy. Nat Med 19, 101-106.
50. Hornberger TA, Chu WK, Mak YW, Hsiung JW, Huang SA, &, Chien S, (2006) The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc Natl Acad Sci USA 103, 4741-4746.
51. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, et al,. (2012) A PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151, 1319-1331.
52. Puigserver P, Wu Z, Park CW, Graves R, Wright M, &, Spiegelman BM, (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839.
53. Pallafacchina G, Blaauw B, &, Schiaffino S, (2013) Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr Metab Cardiovasc Dis, in press.
54. Abmayr SM, &, Pavlath GK, (2012) Myoblast fusion: lessons from flies and mice. Development 139, 641-656.
55. Horsley V, Jansen KM, Mills ST, &, Pavlath GK, (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113, 483-494.
56. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, &, Munoz-Canoves P, (2008) Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7, 33-44.
57. Moss FP, &, Leblond CP, (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170, 421-435.
58. White RB, Bierinx AS, Gnocchi VF, &, Zammit PS, (2010) Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol 10, 21.
59. Saclier M, Cuvellier S, Magnan M, Mounier R, &, Chazaud B, (2013) Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J, doi: 10.1111/febs.12166.
60. Maltin CA, &, Delday MI, (1992) Satellite cells in innervated and denervated muscles treated with clenbuterol. Muscle Nerve 15, 919-925.
61. Kadi F, (2008) Cellular and molecular mechanisms responsible for the action of testosterone on human skeletal muscle. A basis for illegal performance enhancement. Br J Pharmacol 154, 522-528.
62. Jackson JR, Mula J, Kirby TJ, Fry CS, Lee JD, Ubele MF, Campbell KS, McCarthy JJ, Peterson CA, &, Dupont-Versteegden EE, (2012) Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy. Am J Physiol Cell Physiol 303, C854-C861.
63. Raffaello A, Milan G, Masiero E, Carnio S, Lee D, Lanfranchi G, Goldberg AL, &, Sandri M, (2010) JunB transcription factor maintains skeletal muscle mass and promotes hypertrophy. J Cell Biol 191, 101-113.
64. Amthor H, Otto A, Vulin A, Rochat A, Dumonceaux J, Garcia L, Mouisel E, Hourde C, Macharia R, Friedrichs M, et al,. (2009) Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity. Proc Natl Acad Sci USA 106, 7479-7484.
65. Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, Rosenfeld R, Chen Q, Boone T, Simonet WS, et al,. (2010) Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142, 531-543.
66. 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, E2353-E2360.
67. Schiaffino S, Bormioli SP, &, Aloisi M, (1972) Cell proliferation in rat skeletal muscle during early stages of compensatory hypertrophy. Virchows Arch B Cell Pathol 11, 268-273.
68. Snow MH, (1990) Satellite cell response in rat soleus muscle undergoing hypertrophy due to surgical ablation of synergists. Anat Rec 227, 437-446.
69. Bruusgaard JC, Johansen IB, Egner IM, Rana ZA, &, Gundersen K, (2010) Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining. Proc Natl Acad Sci USA 107, 15111-15116.
70. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, Olesen JL, Suetta C, Teisner B, &, Kjaer M, (2004) Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol 558, 333-340.
71. Barton-Davis ER, Shoturma DI, &, Sweeney HL, (1999) Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 167, 301-305.
72. Adams GR, Caiozzo VJ, Haddad F, &, Baldwin KM, (2002) Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol 283, C1182-C1195.
73. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C, et al,. (2011) Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657-3666.
74. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, et al,. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708.
75. 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.
76. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, &, Goldberg AL, (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18, 39-51.
77. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, &, Goldberg AL, (2007) Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21, 140-155.
78. Sandri M, (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23, 160-170.
79. 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, 399-412.
80. 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, 395-403.
81. Lee SW, Dai G, Hu Z, Wang X, Du J, &, Mitch WE, (2004) Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin-proteasome systems by phosphatidylinositol 3 kinase. J Am Soc Nephrol 15, 1537-1545.
82. Cong H, Sun L, Liu C, &, Tien P, (2011) Inhibition of atrogin-1/MAFbx expression by adenovirus-delivered small hairpin RNAs attenuates muscle atrophy in fasting mice. Hum Gene Ther 22, 313-324.
83. Baehr LM, Furlow JD, &, Bodine SC, (2011) Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J Physiol 589, 4759-4776.
84. 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, e8994.
85. Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP, &, Leibovitch SA, (2005) Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem 280, 2847-2856.
86. Li HH, Kedar V, Zhang C, McDonough H, Arya R, Wang DZ, &, Patterson C, (2004) Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest 114, 1058-1071.
87. 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, C512-C529.
88. 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.
89. Fielitz J, Kim MS, Shelton JM, Latif S, Spencer JA, Glass DJ, Richardson JA, Bassel-Duby R, &, Olson EN, (2007) Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3. J Clin Invest 117, 2486-2495.
90. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, et al,. (2007) The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6, 376-385.
91. Polge C, Heng AE, Jarzaguet M, Ventadour S, Claustre A, Combaret L, Bechet D, Matondo M, Uttenweiler-Joseph S, Monsarrat B, et al,. (2011) Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J 25, 3790-3802.
92. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, &, Goldberg AL, (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185, 1083-1095.
93. Cohen S, Zhai B, Gygi SP, &, Goldberg AL, (2012) Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J Cell Biol 198, 575-589.
94. Kudryashova E, Kramerova I, &, Spencer MJ, (2012) Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H. J Clin Invest 122, 1764-1776.
95. Paul PK, Gupta SK, Bhatnagar S, Panguluri SK, Darnay BG, Choi Y, &, Kumar A, (2010) Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J Cell Biol 191, 1395-1411.
96. Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, et al,. (2009) A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 33, 505-516.
97. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, et al,. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163.
98. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, &, Johansen T, (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282, 24131-24145.
99. Paul PK, Bhatnagar S, Mishra V, Srivastava S, Darnay BG, Choi Y, &, Kumar A, (2012) The E3 ubiquitin ligase TRAF6 intercedes in starvation-induced skeletal muscle atrophy through multiple mechanisms. Mol Cell Biol 32, 1248-1259.
100. Kumar A, Bhatnagar S, &, Paul PK, (2012) TWEAK and TRAF6 regulate skeletal muscle atrophy. Curr Opin Clin Nutr Metab Care 15, 233-239.
101. Nagpal P, Plant PJ, Correa J, Bain A, Takeda M, Kawabe H, Rotin D, Bain JR, &, Batt JA, (2012) The ubiquitin ligase nedd4-1 participates in denervation-induced skeletal muscle atrophy in mice. PLoS One 7, e46427.
102. Lokireddy S, Wijesoma IW, Teng S, Bonala S, Gluckman PD, McFarlane C, Sharma M, &, Kambadur R, (2012) The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab 16, 613-624.
103. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, et al,. (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29, 1774-1785.
104. Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Furst DO, Saftig P, Saint R, Fleischmann BK, et al,. (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 20, 143-148.
105. Bello NF, Lamsoul I, Heuze ML, Metais A, Moreaux G, Calderwood DA, Duprez D, Moog-Lutz C, &, Lutz PG, (2009) The E3 ubiquitin ligase specificity subunit ASB2β is a novel regulator of muscle differentiation that targets filamin B to proteasomal degradation. Cell Death Differ 16, 921-932.
106. Shi J, Luo L, Eash J, Ibebunjo C, &, Glass DJ, (2011) The SCF-Fbxo40 complex induces IRS1 ubiquitination in skeletal muscle, limiting IGF1 signaling. Dev Cell 21, 835-847.
107. Hishiya A, Iemura S, Natsume T, Takayama S, Ikeda K, &, Watanabe K, (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J 25, 554-564.
108. Piccirillo R, &, Goldberg AL, (2012) The p97/VCP ATPase is critical in muscle atrophy and the accelerated degradation of muscle proteins. EMBO J 31, 3334-3350.
109. Combaret L, Adegoke OA, Bedard N, Baracos V, Attaix D, &, Wing SS, (2005) USP19 is a ubiquitin-specific protease regulated in rat skeletal muscle during catabolic states. Am J Physiol Endocrinol Metab 288, E693-E700.
110. Sundaram P, Pang Z, Miao M, Yu L, &, Wing SS, (2009) USP19-deubiquitinating enzyme regulates levels of major myofibrillar proteins in L6 muscle cells. Am J Physiol Endocrinol Metab 297, E1283-E1290.
111. Sandri M, (2010) Autophagy in skeletal muscle. FEBS Lett 584, 1411-1416.
112. Bonaldo P, &, Sandri M, (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6, 25-39.
113. Mizushima N, &, Komatsu M, (2011) Autophagy: renovation of cells and tissues. Cell 147, 728-741.
114. Bothe GW, Haspel JA, Smith CL, Wiener HH, &, Burden SJ, (2000) Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26, 165-166.
115. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, et al,. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889.
116. Narendra DP, &, Youle RJ, (2011) Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal 14, 1929-1938.
117. Youle RJ, &, Narendra DP, (2011) Mechanisms of mitophagy. Nat Rev Mol Cell Biol 12, 9-14.
118. Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, &, Gustafsson AB, (2012) Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 287, 19094-19104.
119. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Lohr F, Popovic D, Occhipinti A, et al,. (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11, 45-51.
120. Romanello V, &, Sandri M, (2010) Mitochondrial biogenesis and fragmentation as regulators of muscle protein degradation. Curr Hypertens Rep 12, 433-439.
121. O'Leary MF, Vainshtein A, Iqbal S, Ostojic O, &, Hood DA, (2012) Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle. Am J Physiol Cell Physiol 304, C422-C430.
122. Mofarrahi M, Sigala I, Guo Y, Godin R, Davis EC, Petrof B, Sandri M, Burelle Y, &, Hussain SN, (2012) Autophagy and skeletal muscles in sepsis. PLoS One 7, e47265.
123. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, Blaauw B, Urciuolo A, Tiepolo T, Merlini L, et al,. (2010) Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 16, 1313-1320.
124. Chang NC, Nguyen M, Bourdon J, Risse PA, Martin J, Danialou G, Rizzuto R, Petrof BJ, &, Shore GC, (2012) Bcl-2-associated autophagy regulator Naf-1 required for maintenance of skeletal muscle. Hum Mol Genet 21, 2277-2287.
125. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, &, Sandri M, (2009) Autophagy is required to maintain muscle mass. Cell Metab 10, 507-515.
126. Raben N, Hill V, Shea L, Takikita S, Baum R, Mizushima N, Ralston E, &, Plotz P, (2008) Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum Mol Genet 17, 3897-3908.
127. Moresi V, Carrer M, Grueter CE, Rifki OF, Shelton JM, Richardson JA, Bassel-Duby R, &, Olson EN, (2012) Histone deacetylases 1 and 2 regulate autophagy flux and skeletal muscle homeostasis in mice. Proc Natl Acad Sci USA 109, 1649-1654.
128. Moresi V, Williams AH, Meadows E, Flynn JM, Potthoff MJ, McAnally J, Shelton JM, Backs J, Klein WH, Richardson JA, et al,. (2010) Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143, 35-45.
129. Sacheck JM, Ohtsuka A, McLary SC, &, Goldberg AL, (2004) IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am J Physiol Endocrinol Metab 287, E591-E601.
130. Monier S, Le Cam A, &, Le Marchand-Brustel Y, (1983) Insulin and insulin-like growth factor I. Effects on protein synthesis in isolated muscles from lean and goldthioglucose-obese mice. Diabetes 32, 392-397.
131. 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, 1009-1013.
132. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, et al,. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6, 458-471.
133. Calnan DR, &, Brunet A, (2008) The FoxO code. Oncogene 27, 2276-2288.
134. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, et al,. (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279, 41114-41123.
135. Southgate RJ, Neill B, Prelovsek O, El-Osta A, Kamei Y, Miura S, Ezaki O, McLoughlin TJ, Zhang W, Unterman TG, et al,. (2007) FOXO1 regulates the expression of 4E-BP1 and inhibits mTOR signaling in mammalian skeletal muscle. J Biol Chem 282, 21176-21186.
136. Liu CM, Yang Z, Liu CW, Wang R, Tien P, Dale R, &, Sun LQ, (2007) Effect of RNA oligonucleotide targeting Foxo-1 on muscle growth in normal and cancer cachexia mice. Cancer Gene Ther 14, 945-952.
137. Demontis F, &, Perrimon N, (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143, 813-825.
138. Lee JH, Budanov AV, Park EJ, Birse R, Kim TE, Perkins GA, Ocorr K, Ellisman MH, Bodmer R, Bier E, et al,. (2010) Sestrin as a feedback inhibitor of TOR that prevents age-related pathologies. Science 327, 1223-1228.
139. Reed SA, Sandesara PB, Senf SM, &, Judge AR, (2012) Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J 26, 987-1000.
140. Huang H, &, Tindall DJ, (2007) Dynamic FoxO transcription factors. J Cell Sci 120, 2479-2487.
141. Senf SM, Sandesara PB, Reed SA, &, Judge AR, (2011) p300 acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300, C1490-C1501.
142. Bertaggia E, Coletto L, &, Sandri M, (2012) Posttranslational modifications control FoxO3 activity during denervation. Am J Physiol Cell Physiol 302, C587-C596.
143. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, &, Brunet A, (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17, 1646-1656.
144. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, &, Brunet A, (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282, 30107-30119.
145. Nakashima K, &, Yakabe Y, (2007) AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71, 1650-1656.
146. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H, &, Candau R, (2012) AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 113, 695-710.
147. Suzuki N, Motohashi N, Uezumi A, Fukada S, Yoshimura T, Itoyama Y, Aoki M, Miyagoe-Suzuki Y, &, Takeda S, (2007) NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J Clin Invest 117, 2468-2476.
148. Pietri-Rouxel F, Gentil C, Vassilopoulos S, Baas D, Mouisel E, Ferry A, Vignaud A, Hourde C, Marty I, Schaeffer L, et al,. (2010) DHPR α1S subunit controls skeletal muscle mass and morphogenesis. EMBO J 29, 643-654.
149. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, et al,. (2008) Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358, 1327-1335.
150. Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, et al,. (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423, 550-555.
151. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, et al,. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124.
152. Geng T, Li P, Yin X, &, Yan Z, (2011) PGC-1α promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice. Am J Pathol 178, 1738-1748.
153. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, &, Moraes CT, (2009) Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA 106, 20405-20410.
154. Brault JJ, Jespersen JG, &, Goldberg AL, (2010) Peroxisome proliferator-activated receptor γ coactivator 1α or 1β overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 285, 19460-19471.
155. Peterson JM, Bakkar N, &, Guttridge DC, (2011) NF-κB signaling in skeletal muscle health and disease. Curr Top Dev Biol 96, 85-119.
156. Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, Hasselgren PO, Frontera WR, Lee J, Glass DJ, et al,. (2004) IKKβ/NF-κB activation causes severe muscle wasting in mice. Cell 119, 285-298.
157. Judge AR, Koncarevic A, Hunter RB, Liou HC, Jackman RW, &, Kandarian SC, (2007) Role for IκBα, but not c-Rel, in skeletal muscle atrophy. Am J Physiol Cell Physiol 292, C372-C382.
158. Hunter RB, &, Kandarian SC, (2004) Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J Clin Invest 114, 1504-1511.
159. de Alvaro C, Teruel T, Hernandez R, &, Lorenzo M, (2004) Tumor necrosis factor α produces insulin resistance in skeletal muscle by activation of inhibitor κB kinase in a p38 MAPK-dependent manner. J Biol Chem 279, 17070-17078.
160. Dogra C, Changotra H, Wedhas N, Qin X, Wergedal JE, &, Kumar A, (2007) TNF-related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle-wasting cytokine. FASEB J 21, 1857-1869.
161. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, &, Hotamisligil GS, (2002) A central role for JNK in obesity and insulin resistance. Nature 420, 333-336.
162. Mourkioti F, Kratsios P, Luedde T, Song YH, Delafontaine P, Adami R, Parente V, Bottinelli R, Pasparakis M, &, Rosenthal N, (2006) Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration. J Clin Invest 116, 2945-2954.
163. Minetti GC, Feige JN, Rosenstiel A, Bombard F, Meier V, Werner A, Bassilana F, Sailer AW, Kahle P, Lambert C, et al,. (2011) Gαi2 signaling promotes skeletal muscle hypertrophy, myoblast differentiation, and muscle regeneration. Sci Signal 4, ra80.
164. Mittal A, Bhatnagar S, Kumar A, Lach-Trifilieff E, Wauters S, Li H, Makonchuk DY, &, Glass DJ, (2010) The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol 188, 833-849.
165. Bonetto A, Aydogdu T, Jin X, Zhang Z, Zhan R, Puzis L, Koniaris LG, &, Zimmers TA, (2012) JAK/STAT3 pathway inhibition blocks skeletal muscle wasting downstream of IL-6 and in experimental cancer cachexia. Am J Physiol Endocrinol Metab 303, E410-E421.
166. Yamada E, Bastie CC, Koga H, Wang Y, Cuervo AM, &, Pessin JE, (2012) Mouse skeletal muscle fiber-type-specific macroautophagy and muscle wasting are regulated by a Fyn/STAT3/Vps34 signaling pathway. Cell Rep 1, 557-569.
167. 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, 1486-1488.
168. 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, 3140-3147.
169. Reisz-Porszasz S, Bhasin S, Artaza JN, Shen R, Sinha-Hikim I, Hogue A, Fielder TJ, &, Gonzalez-Cadavid NF, (2003) Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin. Am J Physiol Endocrinol Metab 285, E876-E888.
170. 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-κB-independent, FoxO1-dependent mechanism. J Cell Physiol 209, 501-514.
171. Allen DL, &, Unterman TG, (2007) Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 292, C188-C199.
172. Schakman O, Gilson H, &, Thissen JP, (2008) Mechanisms of glucocorticoid-induced myopathy. J Endocrinol 197, 1-10.
173. Menconi M, Fareed M, O'Neal P, Poylin V, Wei W, &, Hasselgren PO, (2007) Role of glucocorticoids in the molecular regulation of muscle wasting. Crit Care Med 35, S602-S608.
174. Shimizu N, Yoshikawa N, Ito N, Maruyama T, Suzuki Y, Takeda S, Nakae J, Tagata Y, Nishitani S, Takehana K, et al,. (2011) Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab 13, 170-182.
175. 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.
176. +-ATPase. Science 334, 678-683.
177. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, et al,. (2011) TFEB links autophagy to lysosomal biogenesis. Science 332, 1429-1433.
178. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, et al,. (2012) A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 31, 1095-1108.
179. Schiaffino S, Gorza L, Sartore S, Saggin L, &, Carli M, (1986) Embryonic myosin heavy chain as a differentiation marker of developing human skeletal muscle and rhabdomyosarcoma. A monoclonal antibody study. Exp Cell Res 163, 211-220.