Abstract
Adult skeletal muscle can regenerate in response to muscle damage. This ability is conferred by the presence of myogenic stem cells called satellite cells. In response to stimuli such as injury or exercise, these cells become activated and express myogenic regulatory factors (MRFs), i.e., transcription factors of the myogenic lineage including Myf5, MyoD, myogenin, and Mrf4 to proliferate and differentiate into myofibers. The MRF family of proteins controls the transcription of important muscle-specific proteins such as myosin heavy chain and muscle creatine kinase. Different growth factors are secreted during muscle repair among which insulin-like growth factors (IGFs) are the only ones that promote both muscle cell proliferation and differentiation and that play a key role in muscle regeneration and hypertrophy. Different isoforms of IGFs are expressed during muscle repair: IGF-IEa, IGF-IEb, or IGF-IEc (also known as mechano growth factor, MGF) and IGF-II. MGF is expressed first and is observed in satellite cells and in proliferating myoblasts whereas IGF-Ia and IGF-II expression occurs at the state of muscle fiber formation. Interestingly, several studies report the induction of MRFs in response to IGFs stimulation. Inversely, IGFs expression may also be regulated by MRFs. Various mechanisms are proposed to support these interactions. In this review, we describe the general process of muscle hypertrophy and regeneration and decipher the interactions between the two groups of factors involved in the process.
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Schmalbruch H, Lewis DM (2000) Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 23:617–626
Irintchev A, Wernig A (1987) Muscle damage and repair in voluntarily running mice: strain and muscle differences. Cell Tissue Res 249:509–521
Papadimitriou JM, Robertson TA, Mitchell CA, Grounds MD (1990) The process of new plasmalemma formation in focally injured skeletal muscle fibers. J Struct Biol 103:124–134
Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Carlson BM, Faulkner JA (1983) The regeneration of skeletal muscle fibers following injury: a review. Med Sci Sports Exerc 15:187–198
Ciciliot S, Schiaffino S (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16:906–914
Czerwinska AM, Streminska W, Ciemerych MA, Grabowska I (2012) Mouse gastrocnemius muscle regeneration after mechanical or cardiotoxin injury. Folia Histochem Cytobiol 50:144–153
Sakamoto K, Nosaka K, Shimegi S, Ohmori H, Katsuta S (1996) Creatine kinase release from regenerated muscles after eccentric contractions in rats. Eur J Appl Physiol Occup Physiol 73:516–520
Jackson RC (1970) Exercise-induced renal failure and muscle damage. Proc R Soc Med 63:566–570
Darr KC, Schultz E (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63:1816–1821
Tsatalas T, Giakas G, Spyropoulos G, Sideris V, Lazaridis S, Kotzamanidis C, Koutedakis Y (2013) The effects of eccentric exercise-induced muscle damage on running kinematics at different speeds. J Sports Sci 31:288–298
Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158:1089–1096
Gailly P (2012) TRP channels in normal and dystrophic skeletal muscle. Curr Opin Pharmacol 12(3):326–334
De Backer F, Vandebrouck C, Gailly P, Gillis JM (2002) Long-term study of Ca2+ homeostasis and of survival in collagenase-isolated muscle fibres from normal and mdx mice. J Physiol Lond 542:855–865
Gailly P, De Backer F, Van Schoor M, Gillis JM (2007) In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J Physiol 582:1261–1275
Monaco AP, Neve RL, Collettifeener C, Bertelson CJ, Kurnit DM, Kunkel LM (1986) Isolation of candidate cDNAs for portions of the Duchenne muscular-dystrophy gene. Nature 323:646–650
Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928
Moens P, Baatsen PHWW, Marechal G (1993) Increased susceptibility of EDL muscles from mdx mice to damage-induced by contractions with stretch. J Muscle Res Cell Motil 14:446–451
Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90:3710–3714
Zanou N, Iwata Y, Schakman O, Lebacq J, Wakabayashi S, Gailly P (2009) Essential role of TRPV2 ion channel in the sensitivity of dystrophic muscle to eccentric contractions. FEBS Lett 583:3600–3604
Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P (2006) Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575:913–924
Chiu D, Wang HH, Blumenthal MR (1976) Creatine phosphokinase release as a measure of tourniquet effect on skeletal muscle. Arch Surg 111:71–74
Park CY, Pierce SA, von Drehle M, Ivey KN, Morgan JA, Blau HM, Srivastava D (2010) skNAC, a smyd1-interacting transcription factor, is involved in cardiac development and skeletal muscle growth and regeneration. Proc Natl Acad Sci USA 107:20750–20755
Zanou N, Schakman O, Louis P, Ruegg UT, Dietrich A, Birnbaumer L, Gailly P (2012) Trpc1 channel modulates PI3K/Akt pathway during myoblast differentiation and muscle regeneration. J Biol Chem 287(18):14524–14534
Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345–R353
Chazaud B et al (2003) Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 163:1133–1143
Mourkioti F, Rosenthal N (2005) IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol 26:535–542
Grounds MD (2002) Reasons for the degeneration of ageing skeletal muscle: a central role for IGF-1 signalling. Biogerontology 3:19–24
Cantini M, Carraro U (1995) Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J Neuropathol Exp Neurol 54:121–128
Cantini M et al (2002) Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurol Sci 23:189–194
Sonnet C et al (2006) Human macrophages rescue myoblasts and myotubes from apoptosis through a set of adhesion molecular systems. J Cell Sci 119:2497–2507
Segawa M et al (2008) Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp Cell Res 314:3232–3244
Beauchamp JR et al (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234
Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786
Schultz E, Jaryszak DL, Valliere CR (1985) Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8:217–222
Seale P, Polesskaya A, Rudnicki MA (2003) Adult stem cell specification by Wnt signaling in muscle regeneration. Cell Cycle 2:418–419
Parker MH, Seale P, Rudnicki MA (2003) Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet 4:497–507
Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010
Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677–687
Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441:1075–1079
Artavanis-Tsakonas S, Matsuno K, Fortini ME (1995) Notch signaling. Science 268:225–232
Conboy IM, Rando TA (2002) The regulation of notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3:397–409
Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA (2008) A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2:50–59
Kelly AM (1978) Satellite cells and myofiber growth in the rat soleus and extensor digitorum longus muscles. Dev Biol 65:1–10
Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, Esser KA (2002) Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol 545:27–41
Barash IA, Mathew L, Ryan AF, Chen J, Lieber RL (2004) Rapid muscle-specific gene expression changes after a single bout of eccentric contractions in the mouse. Am J Physiol Cell Physiol 286:C355–C364
Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530
Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401:390–394
Torrente Y et al (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114:182–195
Kuang S, Rudnicki MA (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14:82–91
Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646
Louis M, Zanou N, Van Schoor M, Gailly P (2008) TRPC1 regulates skeletal myoblast migration and differentiation. J Cell Sci 121:3951–3959
Zanou N et al (2010) Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 298:C149–C162
Jerkovic R, Argentini C, Serrano-Sanchez A, Cordonnier C, Schiaffino S (1997) Early myosin switching induced by nerve activity in regenerating slow skeletal muscle. Cell Struct Funct 22:147–153
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
Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lomo T, Schiaffino S (2001) Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci USA 98:13108–13113
Li L, Stefan MI, Le Novere N (2012) Calcium input frequency, duration and amplitude differentially modulate the relative activation of calcineurin and CaMKII. PLoS One 7:e43810
Liu HM (1992) The role of extracellular matrix in peripheral nerve regeneration: a wound chamber study. Acta Neuropathol 83:469–474
Saksela O, Laiho M (1990) Growth factors and the extracellular matrix. Duodecim 106:297–306
Lijnen HR, Van Hoef B, Lupu F, Moons L, Carmeliet P, Collen D (1998) Function of the plasminogen/plasmin and matrix metalloproteinase systems after vascular injury in mice with targeted inactivation of fibrinolytic system genes. Arterioscler Thromb Vasc Biol 18:1035–1045
Weintraub H et al (1991) The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251:761–766
Sassoon D, Lyons G, Wright WE, Lin V, Lassar A, Weintraub H, Buckingham M (1989) Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341:303–307
Davis RL, Cheng PF, Lassar AB, Weintraub H (1990) The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733–746
Le Grand F, Rudnicki MA (2007) Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19:628–633
Choi J, Costa ML, Mermelstein CS, Chagas C, Holtzer S, Holtzer H (1990) MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci USA 87:7988–7992
Davis RL, Weintraub H, Lassar AB (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987–1000
Megeney LA, Rudnicki MA (1995) Determination versus differentiation and the MyoD family of transcription factors. Biochem Cell Biol 73:723–732
Rudnicki MA, Jaenisch R (1995) The MyoD family of transcription factors and skeletal myogenesis. BioEssays 17:203–209
Buckingham M, Houzelstein D, Lyons G, Ontell M, Ott MO, Sassoon D (1992) Expression of muscle genes in the mouse embryo. Symp Soc Exp Biol 46:203–217
Crescenzi M, Fleming TP, Lassar AB, Weintraub H, Aaronson SA (1990) MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc Natl Acad Sci USA 87:8442–8446
Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB (1995) Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018–1021
Wilson EM, Rotwein P (2006) Control of MyoD function during initiation of muscle differentiation by an autocrine signaling pathway activated by insulin-like growth factor-II. J Biol Chem 281:29962–29971
Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA (1999) Reduced differentiation potential of primary MyoD−/− myogenic cells derived from adult skeletal muscle. J Cell Biol 144:631–643
Beylkin DH, Allen DL, Leinwand LA (2006) MyoD, Myf5, and the calcineurin pathway activate the developmental myosin heavy chain genes. Dev Biol 294:541–553
Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ (2002) Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 9:587–600
Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, Klein WH (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364:501–506
Kassar-Duchossoy L, Gayraud-Morel B, Gomes D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S (2004) Mrf4 determines skeletal muscle identity in Myf5: MyoD double-mutant mice. Nature 431:466–471
Weintraub H (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75:1241–1244
Buckingham M (2001) Skeletal muscle formation in vertebrates. Curr Opin Genet Dev 11:440–448
Molkentin JD, Black BL, Martin JF, Olson EN (1995) Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125–1136
Molkentin JD, Olson EN (1996) Combinatorial control of muscle development by basic helix–loop–helix and MADS-box transcription factors. Proc Natl Acad Sci USA 93:9366–9373
Buckingham M (2007) Skeletal muscle progenitor cells and the role of Pax genes. C R Biol 330:530–533
Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953
Buckingham M, Bajard L, Daubas P, Esner M, Lagha M, Relaix F, Rocancourt D (2006) Myogenic progenitor cells in the mouse embryo are marked by the expression of Pax3/7 genes that regulate their survival and myogenic potential. Anat Embryol (Berl) 211(Suppl 1):51–56
Buckingham ME (1994) Muscle: the regulation of myogenesis. Curr Opin Genet Dev 4:745–751
Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA (2006) Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol 172:103–113
Karalaki M, Fili S, Philippou A, Koutsilieris M (2009) Muscle regeneration: cellular and molecular events. In Vivo 23:779–796
Jiao S, Ren H, Li Y, Zhou J, Duan C, Lu L (2013) Differential regulation of IGF-I and IGF-II gene expression in skeletal muscle cells. Mol Cell Biochem 373:107–113
Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17:481–517
Engert JC, Berglund EB, Rosenthal N (1996) Proliferation precedes differentiation in IGF-I-stimulated myogenesis. J Cell Biol 135:431–440
Allen RE, Boxhorn LK (1989) Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138:311–315
Doumit ME, Cook DR, Merkel RA (1993) Fibroblast growth factor, epidermal growth factor, insulin-like growth factors, and platelet-derived growth factor-BB stimulate proliferation of clonally derived porcine myogenic satellite cells. J Cell Physiol 157:326–332
Vandenburgh HH, Karlisch P, Shansky J, Feldstein R (1991) Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. Am J Physiol 260:C475–C484
Owino V, Yang SY, Goldspink G (2001) Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett 505:259–263
Hill M, Goldspink G (2003) Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J Physiol 549:409–418
Yang SY, Goldspink G (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522:156–160
Dobrowolny G et al (2005) Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 168:193–199
Musaro A et al (2004) Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc Natl Acad Sci USA 101:1206–1210
Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, Rotwein PS (1991) “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J Biol Chem 266:15917–15923
Ge Y, Sun Y, Chen J (2011) IGF-II is regulated by microRNA-125b in skeletal myogenesis. J Cell Biol 192:69–81
Wilson EM, Hsieh MM, Rotwein P (2003) Autocrine growth factor signaling by insulin-like growth factor-II mediates MyoD-stimulated myocyte maturation. J Biol Chem 278:41109–41113
Ge Y et al (2009) mTOR regulates skeletal muscle regeneration in vivo through kinase-dependent and kinase-independent mechanisms. Am J Physiol Cell Physiol 297:C1434–C1444
Levinovitz A, Jennische E, Oldfors A, Edwall D, Norstedt G (1992) Activation of insulin-like growth factor II expression during skeletal muscle regeneration in the rat: correlation with myotube formation. Mol Endocrinol 6:1227–1234
Edwall D, Schalling M, Jennische E, Norstedt G (1989) Induction of insulin-like growth factor I messenger ribonucleic acid during regeneration of rat skeletal muscle. Endocrinology 124:820–825
Huard J, Li Y, Fu FH (2002) Muscle injuries and repair: current trends in research. J Bone Jt Surg Am 84-A:822–832
Barton ER, Morris L, Musaro A, Rosenthal N, Sweeney HL (2002) Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice. J Cell Biol 157:137–148
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
Semsarian C, Sutrave P, Richmond DR, Graham RM (1999) Insulin-like growth factor (IGF-I) induces myotube hypertrophy associated with an increase in anaerobic glycolysis in a clonal skeletal-muscle cell model. Biochem J 339(Pt 2):443–451
Musaro A et al (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27:195–200
Clemmons DR (2009) Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab 20:349–356
Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR (1997) The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272:6653–6662
Fuentes EN, Bjornsson BT, Valdes JA, Einarsdottir IE, Lorca B, Alvarez M, Molina A (2011) IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. Am J Physiol Regul Integr Comp Physiol 300:R1532–R1542
Wilson EM, Rotwein P (2007) Selective control of skeletal muscle differentiation by Akt1. J Biol Chem 282:5106–5110
Rotwein P, Wilson EM (2009) Distinct actions of Akt1 and Akt2 in skeletal muscle differentiation. J Cell Physiol 219:503–511
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
Bodine SC 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
Jiang BH, Aoki M, Zheng JZ, Li J, Vogt PK (1999) Myogenic signaling of phosphatidylinositol 3-kinase requires the serine–threonine kinase Akt/protein kinase B. Proc Natl Acad Sci USA 96:2077–2081
Sasai N, Agata N, Inoue-Miyazu M, Kawakami K, Kobayashi K, Sokabe M, Hayakawa K (2010) Involvement of PI3K/Akt/TOR pathway in stretch-induced hypertrophy of myotubes. Muscle Nerve 41:100–106
Wilson EM, Tureckova J, Rotwein P (2004) Permissive roles of phosphatidyl inositol 3-kinase and Akt in skeletal myocyte maturation. Mol Biol Cell 15:497–505
Leevers SJ, Vanhaesebroeck B, Waterfield MD (1999) Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr Opin Cell Biol 11:219–225
Cleasby ME, Reinten TA, Cooney GJ, James DE, Kraegen EW (2007) Functional studies of Akt isoform specificity in skeletal muscle in vivo; maintained insulin sensitivity despite reduced insulin receptor substrate-1 expression. Mol Endocrinol 21:215–228
Glass DJ (2010) PI3 kinase regulation of skeletal muscle hypertrophy and atrophy phosphoinositide 3-kinase in health and disease. Curr Top Microbiol Immunol 346:267–278
Park IH, Erbay E, Nuzzi P, Chen J (2005) Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp Cell Res 309:211–219
Willett M, Cowan JL, Vlasak M, Coldwell MJ, Morley SJ (2009) Inhibition of mammalian target of rapamycin (mTOR) signalling in C2C12 myoblasts prevents myogenic differentiation without affecting the hyperphosphorylation of 4E-BP1. Cell Signal 21:1504–1512
Hribal ML, Nakae J, Kitamura T, Shutter JR, Accili D (2003) Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J Cell Biol 162:535–541
Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37:1974–1984
Blaauw B et al (2009) Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 23:3896–3905
Kalista S, Schakman O, Gilson H, Lause P, Demeulder B, Bertrand L, Pende M, Thissen JP (2012) The type 1 insulin-like growth factor receptor (IGF-IR) pathway is mandatory for the follistatin-induced skeletal muscle hypertrophy. Endocrinology 153:241–253
Adams GR, McCue SA (1998) Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol 84:1716–1722
Awede B, Thissen J, Gailly P, Lebacq J (1999) Regulation of IGF-I, IGFBP-4 and IGFBP-5 gene expression by loading in mouse skeletal muscle. FEBS Lett 461:263–267
Rosenblatt JD, Yong D, Parry DJ (1994) Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 17:608–613
Li P, Akimoto T, Zhang M, Williams RS, Yan Z (2006) Resident stem cells are not required for exercise-induced fiber-type switching and angiogenesis but are necessary for activity-dependent muscle growth. Am J Physiol Cell Physiol 290:C1461–C1468
Gilson H, Schakman O, Kalista S, Lause P, Tsuchida K, Thissen JP (2009) Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am J Physiol Endocrinol Metab 297:E157–E164
Miyazaki M, McCarthy JJ, Fedele MJ, Esser KA (2011) Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J Physiol 589:1831–1846
Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708
Leshem Y, Spicer DB, Gal-Levi R, Halevy O (2000) Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J Cell Physiol 184:101–109
Floss T, Arnold HH, Braun T (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11:2040–2051
Fujita J, Tsujinaka T, Yano M, Ogawa J, Morita T, Taniguchi H, Shiozaki H, Monden M (1998) Participation of interleukin-6 to skeletal muscle proteolysis: the effect of IL-6 administration on mRNA expression by the skeletal muscle cell proteolytic system. Nihon Geka Gakkai Zasshi 99:332
Langen RC, Van Der Velden JL, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM (2004) Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization. FASEB J 18:227–237
Warren GL, Hulderman T, Jensen N, McKinstry M, Mishra M, Luster MI, Simeonova PP (2002) Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J 16:1630–1632
Alvarez B, Quinn LS, Busquets S, Quiles MT, Lopez-Soriano FJ, Argiles JM (2002) Tumor necrosis factor-alpha exerts interleukin-6-dependent and -independent effects on cultured skeletal muscle cells. Biochim Biophys Acta 1542:66–72
Baeza-Raja B, Munoz-Canoves P (2004) p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell 15:2013–2026
Florini JR, Ewton DZ, Magri KA (1991) Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 53:201–216
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 277:49831–49840
McFarlane C et al (2011) Human myostatin negatively regulates human myoblast growth and differentiation. Am J Physiol Cell Physiol 301:C195–C203
Grobet L et al (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17:71–74
White JD, Davies M, Grounds MD (2001) Leukaemia inhibitory factor increases myoblast replication and survival and affects extracellular matrix production: combined in vivo and in vitro studies in post-natal skeletal muscle. Cell Tissue Res 306:129–141
Phillips DJ, de Kretser DM, Pfeffer A, Chie WN, Moore LG (1998) Follistatin has a biphasic response but follicle-stimulating hormone is unchanged during an inflammatory episode in growing lambs. J Endocrinol 156:77–82
Hu SY, Tai CC, Li YH, Wu JL (2012) Progranulin compensates for blocked IGF-1 signaling to promote myotube hypertrophy in C2C12 myoblasts via the PI3K/Akt/mTOR pathway. FEBS Lett 586:3485–3492
Li YH et al (2013) Progranulin regulates zebrafish muscle growth and regeneration through maintaining the pool of myogenic progenitor cells. Sci Rep 3:1176
Sun L, Liu L, Yang XJ, Wu Z (2004) Akt binds prohibitin 2 and relieves its repression of MyoD and muscle differentiation. J Cell Sci 117:3021–3029
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
Schultz E, Jaryszak DL (1985) Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech Ageing Dev 30:63–72
Miyabara EH et al (2010) Mammalian target of rapamycin complex 1 is involved in differentiation of regenerating myofibers in vivo. Muscle Nerve 42:778–787
Florini JR, Ewton DZ, Roof SL (1991) Insulin-like growth factor-I stimulates terminal myogenic differentiation by induction of myogenin gene expression. Mol Endocrinol 5:718–724
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 cells. J Biol Chem 275:36750–36757
Hsu HH, Zdanowicz MM, Agarwal VR, Speiser PW (1997) Expression of myogenic regulatory factors in normal and dystrophic mice: effects of IGF-1 treatment. Biochem Mol Med 60:142–148
Imanaka M et al (2008) Growth hormone stimulates mechano growth factor expression and activates myoblast transformation in C2C12 cells. Kobe J Med Sci 54:E46–E54
Fernandez AM, Dupont J, Farrar RP, Lee S, Stannard B, Le Roith D (2002) Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J Clin Invest 109:347–355
Miyake M et al (2007) Myostatin and MyoD family expression in skeletal muscle of IGF-1 knockout mice. Cell Biol Int 31:1274–1279
Zhang L, Wang XH, Wang H, Du J, Mitch WE (2010) Satellite cell dysfunction and impaired IGF-1 signaling cause CKD-induced muscle atrophy. J Am Soc Nephrol 21:419–427
Nijtmans LG et al (2000) Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19:2444–2451
Sun Y, Ge Y, Drnevich J, Zhao Y, Band M, Chen J (2010) Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J Cell Biol 189:1157–1169
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233
Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228–233
Aguiar AF, Vechetti-Junior IJ, Alves de Souza RW, Castan EP, Milanezi-Aguiar RC, Padovani CR, Carvalho RF, Silva MD (2012) Myogenin, MyoD and IGF-I regulate muscle mass but not fiber-type conversion during resistance training in rats. Int J Sports Med (Epub ahead of print)
Crist CG, Montarras D, Buckingham M (2012) Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11:118–126
Gayraud-Morel B et al (2012) Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J Cell Sci 125:1738–1749
Mangiacapra FJ, Roof SL, Ewton DZ, Florini JR (1992) Paradoxical decrease in myf-5 messenger RNA levels during induction of myogenic differentiation by insulin-like growth factors. Mol Endocrinol 6:2038–2044
Perez-Ruiz A, Gnocchi VF, Zammit PS (2007) Control of Myf5 activation in adult skeletal myonuclei requires ERK signalling. Cell Signal 19:1671–1680
Ijuin T, Takenawa T (2012) Role of phosphatidylinositol 3,4,5-trisphosphate (PIP3) 5-phosphatase skeletal muscle- and kidney-enriched inositol polyphosphate phosphatase (SKIP) in myoblast differentiation. J Biol Chem 287:31330–31341
Ijuin T, Takenawa T (2003) SKIP negatively regulates insulin-induced GLUT4 translocation and membrane ruffle formation. Mol Cell Biol 23:1209–1220
Ijuin T, Yu YE, Mizutani K, Pao A, Tateya S, Tamori Y, Bradley A, Takenawa T (2008) Increased insulin action in SKIP heterozygous knockout mice. Mol Cell Biol 28:5184–5195
Huang MB, Xu H, Xie SJ, Zhou H, Qu LH (2011) Insulin-like growth factor-1 receptor is regulated by microRNA-133 during skeletal myogenesis. PLoS One 6:e29173
McLellan AS, Kealey T, Langlands K (2006) An E box in the exon 1 promoter regulates insulin-like growth factor-I expression in differentiating muscle cells. Am J Physiol Cell Physiol 291:C300–C307
Acknowledgments
Our research is supported by the “Association française contre les myopathies” (AFM), the “Association belge contre les maladies neuro-musculaires” (ABMM), the “Fonds national de la recherche scientifique” (FNRS, Belgium), by grant ARC 10/15-029 from the General Direction of Scientific Research of the French Community of Belgium and by the Interuniversity Attraction Poles program initiated by the Belgian Science Policy Office.
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Zanou, N., Gailly, P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cell. Mol. Life Sci. 70, 4117–4130 (2013). https://doi.org/10.1007/s00018-013-1330-4
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DOI: https://doi.org/10.1007/s00018-013-1330-4