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Key regulators of skeletal myogenesis

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Abstract

Skeletal myogenesis has been extensively studied at both morphological and molecular levels. This review considers the main stages of embryonic skeletal myogenesis and myogenic factors that trigger their initiation, focusing on specific protein interactions involved in somitic myogenesis, head myogenesis, and limb myogenesis. The second part of the review describes the role of noncoding RNAs (microRNAs and long noncoding RNAs) in myogenesis. This information is of particular interest, because regulation of cell processes by noncoding RNAs is an actively developing field of molecular biology. Knowledge of mechanisms of skeletal myogenesis is of applied significance. Various transcription factors, noncoding RNAs, and other myogenic regulators can be employed in the induction of myogenic reprogramming in stem cells and differentiated somatic cells. Current trends and strategies in the field of skeletal myogenic reprogramming are discussed in the last part of the review.

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Abbreviations

EMT:

epithelial–mesenchymal transition

MEF:

myocyte enhancer factor

MRF:

myogenic regulatory factor

ATK:

alanine–threonine–lysine

HLH:

helix–loop–helix

HDAC:

histone deacetylase

IGF:

insulin-like growth factor

References

  1. Davis R.L., Weintraub H., Lassar A.B. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 51, 987–1000.

    Article  CAS  PubMed  Google Scholar 

  2. Weintraub H., Tapscott S.J., Davis R.L., Thayer M.J., Adam M.A., Lassar A.B, Miller A.D. 1987. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. U. S. A. 86, 5434–5438.

    Article  Google Scholar 

  3. Blackwell T.K., Weintraub H. 1990. Differences and similarities in DNA binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science. 250, 1104–1110.

    Article  CAS  PubMed  Google Scholar 

  4. Lassar A.B., Buskin J.N., Lockshon D., Davis R.L., Apone S., Hauschka S.D., Weintraub H. 1989. MyoD is a sequence-specific DNA-binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 58, 823–831.

    Article  CAS  PubMed  Google Scholar 

  5. Braun T., Buschhausen-Denker G., Bober E., Tannich E., Arnold H.H. 1989. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J. 8, 701–709.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Edmondson D.G., Olson E.N. 1989. A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev. 3, 628–640.

    Article  CAS  PubMed  Google Scholar 

  7. Miner J.H., Wold B. 1990. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc. Natl. Acad. Sci. U. S. A. 87, 1089–1093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Berkes C.A., Tapscott S.J. 2005. MyoD and the transcriptional control of myogenesis. Cell Dev. Biol. 16, 585–595.

    Article  CAS  Google Scholar 

  9. Kablar B., Asakura A., Krastel K., Ying C., May L.L., Goldhamer D.J., Rudnicki M.A. 1998. MyoD and Myf5 define the specification of musculature of distinct embryonic origin. Biochem. Cell Biol. 76, 1079–1091.

    Article  CAS  PubMed  Google Scholar 

  10. Hasty P., Bradley A., Morris J.H., Edmondson D.G., Venuti J.M., Olson E.N., Klein W.H. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 364, 501–506.

    Article  CAS  PubMed  Google Scholar 

  11. Wang Y., Jaenisch R. 1997. Myogenin can substitute for Myf5 in promoting myogenesis but less efficiently. Development. 124, 2507–2513.

    CAS  PubMed  Google Scholar 

  12. Bober E., Lyons G.E., Braun T., Cossu G., Buckingham M., Arnold H.H. 1991. The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J. Cell Biol. 113, 1255–1265.

    Article  CAS  PubMed  Google Scholar 

  13. Zhu Z., Miller J.B. 1997. MRF4 can substitute for myogenin during early stages of myogenesis. Dev. Dyn. 209, 233–241.

    Article  CAS  PubMed  Google Scholar 

  14. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. 2004. Mrf4 determines skeletal muscle identitiy in Myf5:MyoD double-mutant mice. Nature. 431, 466–471.

    Article  CAS  PubMed  Google Scholar 

  15. Davis R.L., Cheng P.F., Lassar A.B., Weintraub H. 1990. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 60, 733–746.

    Article  CAS  PubMed  Google Scholar 

  16. Black B.L., Molkentin J.D., Olson E.N. 1998. Multiple roles for the MyoD basic region in transmission of transcriptional activation signals and interaction with MEF2. Mol. Cell. Biol. 18, 69–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Huang J., Weintraub H., Kedes L. 1998. Intramolecular regulation of MyoD activation domain conformation and function. Mol. Cell. Biol. 18, 5478–5484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Weintraub H., Dwarki V.J., Verma I., Davis R.L., Hollenberg S., Snider L., Lassar A., Tapscott, S.J. 1991. Muscle-specific transcriptional activation by MyoD. Genes Dev. 5, 1377–1386.

    Article  CAS  PubMed  Google Scholar 

  19. Gerber A.N., Klesert T.R., Bergstrom D.A., Tapscott S.J. 1997. Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev. 11, 436–450.

    Article  CAS  PubMed  Google Scholar 

  20. Bergstrom D.A., Tapscott S.J. 2001. Molecular distinction between specification and differentiation in the myogenic basic helix-loophelix transcription factor family. Mol. Cell. Biol. 21, 2404–2412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wu Z., Woodring P.J., Bhakta K.S., Tamura K., Wen F., Feramisco J.R., Karin M., Wang J.Y., Puri P.L. 2000. p38 and extracellular signal-regulated kinase regulate the myogenic program at multiple steps. Mol. Cell. Biol. 20, 3951–3964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gossett L.A., Kelvin D.J., Sternberg E.A., Olson E.N. 1989. A new myocytespecific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol. Cell. Biol. 9, 5022–5033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Molkentin J.D., Black B.L., Martin J.F., Olson E.N. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 83, 1125–1136.

    Article  CAS  PubMed  Google Scholar 

  24. Naya F.J., Olson E. 1999. MEF2: A transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr. Opin. Cell Biol. 11, 683–688

    Article  CAS  PubMed  Google Scholar 

  25. Black B.L., Molkentin J.D., Olson E.N. 1998. Multiple roles for the MyoD basic region in transmission of transcriptional activation signals and interaction with MEF2. Mol. Cell. Biol. 18, 69–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. De Angelis L., Borghi S., Melchionna R., Berghella L., Baccarani, Contri M., Parise F., Ferrari S., Cossu G. 1998. Inhibition of myogenesis by transforming growth factor b is density-dependent and related to the translocation of transcription factor MEF2 to the cytoplasm. Proc. Natl. Acad. Sci. U. S. A. 95, 12358–12363.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Wilson-Rawls J., Molkentin J., Black B., Olson E. 1999. Activated Notch inhibits myogenic activity of the MADS-box transcription factor myocyte enhancer factor 2C. Mol. Cell. Biol. 19, 2853–2862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yang C.-C., Ornatsky O., McDermott J.C., Cruz T.F., Prody C.A. 1998. Interaction of myocyte enhancer factor 2 (MEF2) with a mitogenactivated protein kinase, ERK5/BMK1. Nucleic Acids Res. 26, 4771–4777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yang S., Galanis A., Sharrocks A.D. 1999. Targeting of p38 mitogen activated protein kinases to MEF2 transcription factors. Mol. Cell. Biol. 19, 4028–4038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Relaix F., Montarras D., Zaffran S., Gayraud-Morel B., Rocancourt D., Tajbakhsh S., Mansouri A., Cumano A., Buckingham M. 2006. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 91–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Otto A., Schmidt C., Patel K. 2006. Pax3 and Pax7 expression and regulation in the avian embryo. Anat. Embryol. (Berl.) 211, 293–310.

    Article  CAS  Google Scholar 

  32. Bajard L., Relaix F., Lagha M., Rocancourt D., Daubas P., Buckingham M.E. 2006. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20, 2450–2464.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Epstein J.A., Shapiro D.N., Cheng J., Lam P.Y., Maas R.L. 1996. Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl. Acad. Sci. U. S. A. 93, 4213–4218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lagha M., Sato L., Bajard L., Daubas P., Esner M., Montarras D., Relaix F., Buckingham M. 2008. Regulation of skeletal muscle stem cell behavior by Pax3 and Pax7. Cold Spring Harbor Symp. Quant. Biol. 73, 307–315.

    Article  CAS  PubMed  Google Scholar 

  35. Relaix F., Rocancourt D., Mansouri A., Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature. 435, 948–953.

    Article  CAS  PubMed  Google Scholar 

  36. Kuang S., Charge S.B., Seale P., Huh M., Rudnicki M.A. 2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172, 103–113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. McKinnell I.W., Ishibashi J., Le Grand F., Punch V.G., Addicks G.C., Greenblatt J.F., Dilworth F.J., Rudnicki M.A. 2008. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat. Cell Biol. 10, 77–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zammit P.S., Golding J.P., Nagata Y., Hudon V., Partridge T.A., Beauchamp J.R. 2004. Muscle satellite cells adopt divergent fates: A mechanism for selfrenewal? J. Cell Biol. 166, 347–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. 1990. The protein Id: A negative regulator of helix-loop-helix DNA-binding proteins. Cell. 61, 49–59.

    Article  CAS  PubMed  Google Scholar 

  40. Lemercier C., To R.Q., Carrasco R.A., Konieczny S.F. 1998. The basic helix-loop-helix transcription factor Mist1 functions as a transcriptional repressor of MyoD. EMBO J. 17, 1412–1422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lu J., Webb R., Richardson J.A., Olson E.N. 1999. MyoR: A musclerestricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc. Natl. Acad. Sci. U. S. A. 96, 552–557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Spicer D.B., Rhee J., Cheung W.L., Lassar A.B. 1996. Inhibition of myogenic bHLH and Mef2 transcription factors by the bHLH protein Twist. Science. 272, 1476–1480.

    Article  CAS  PubMed  Google Scholar 

  43. Chen A.C., Kraut N., Groudine M., Weintraub H. 1996. I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell. 86, 731–741.

    Article  CAS  PubMed  Google Scholar 

  44. Buckingham M., Rigby P.W.J. 2014. Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev. Cell. 28, 225–238.

    Article  CAS  PubMed  Google Scholar 

  45. Niro C., Demignon J., Vincent S., Liu Y., Giordani J., Sgarioto N., Favier M., Guillet-Deniau I., Blais A., Maire P. 2010. Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome. Dev. Biol. 338, 168–182.

    Article  CAS  PubMed  Google Scholar 

  46. Giordani J., Bajard L., Demignon J., Daubas P., Buckingham M., Maire P. 2007. Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc. Natl. Acad. Sci. U. S. A. 104, 11310–11315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Relaix F., Demignon J., Laclef C., Pujol J., Santolini M., Niro C., Lagha M., Rocancourt D., Buckingham M., Maire, P. 2013. Six homeoproteins directly activate Myod expression in the gene regulatory networks that control early myogenesis. PLoS Genet. 9, e1003425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Grifone R., Demignon J., Giordani J., Niro C., Souil E., Bertin F., Laclef C., Xu P.-X., Maire P. 2007. Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev. Biol. 302, 602–616.

    Article  CAS  PubMed  Google Scholar 

  49. Le Grand F., Grifone R., Mourikis P., Houbron C., Gigaud C., Pujol J., Maillet M., Pagès G., Rudnicki M., Tajbakhsh S., Maire P. 2012. Six1 regulates stem cell repair potential and self-renewal during skeletal muscle regeneration. J. Cell Biol. 198, 815–832.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Heanue T.A., Reshef R., Davis R.J., Mardon G., Oliver G., Tomarev S., Lassar A.B., Tabin C.J. 1999. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 13, 3231–3243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. L’Honoré A., Coulon V., Marcil A., Lebel M., Lafrance-Vanasse J., Gage P., Camper S., Drouin J. 2007. Sequential expression and redundancy of Pitx2 and Pitx3 genes during muscle development. Dev. Biol. 307, 421–433.

    Article  PubMed  CAS  Google Scholar 

  52. L’Honoré A., Ouimette J.-F., Lavertu-Jolin M., Drouin J. 2010. Pitx2 defines alternate pathways acting through MyoD during limb and somatic myogenesis. Development. 137, 3847–3856.

    Article  PubMed  CAS  Google Scholar 

  53. Zacharias A.L., Lewandoski M., Rudnicki M.A., Gage P.J. 2011. Pitx2 is an upstream activator of extraocular myogenesis and survival. Dev. Biol. 349, 395–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Zhou Y., Gong B., Kaminski H.J. 2012. Genomic profiling reveals Pitx2 controls expression of mature extraocular muscle contraction-related genes. Invest. Ophthalmol. Vis. Sci. 53, 1821–1829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lagha M., Sato T., Regnault B., Cumano A., Zuniga A., Licht J., Relaix F., Buckingham M. 2010. Transcriptome analyses based on genetic screens for Pax3 myogenic targets in the mouse embryo. BMC Genomics. 11, 696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Dong F., Sun X., Liu W., Ai D., Klysik E., Lu M.-F., Hadley J., Antoni L., Chen L., Baldini A., Francis-West P., Martin J.F. 2006. Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development. 133, 4891–4899.

    Article  CAS  PubMed  Google Scholar 

  57. Kelly R.G., Jerome-Majewska L.A., Papaioannou V.E. 2004. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum. Mol. Genet. 13, 2829–2840.

    Article  CAS  PubMed  Google Scholar 

  58. Lu J.R., Bassel-Duby R., Hawkins A., Chang P., Valdez R., Wu H., Gan L., Shelton J.M., Richardson J.A., Olson E.N. 2002. Control of facial muscle development by MyoR and capsulin. Science. 298, 2378–2381.

    Article  CAS  PubMed  Google Scholar 

  59. Moncaut N., Cross J.W., Siligan C., Keith A., Taylor K., Rigby P.W.J., Carvajal J.J. 2012. Musculin and TCF21 coordinate the maintenance of myogenic regulatory factor expression levels during mouse craniofacial development. Development. 139, 958–967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Shih H.P., Gross M.K., Kioussi C. 2007. Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc. Natl. Acad. Sci. U. S. A. 104, 5907–5912.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Harel I., Maezawa Y., Avraham R., Rinon A., Ma H.-Y., Cross J.W., Leviatan N., Hegesh J., Roy A., Jacob-Hirsch J., Rechavi G., Carvajal J., Tole S., Kioussi C., Quaggin S., Tzahor E. 2012. Pharyngeal mesoderm regulatory network controls cardiac and head muscle morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 109, 18839–18844.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jagla K., Dollé P., Mattei M.G., Jagla T., Schuhbaur B., Dretzen G., Bellard F., Bellard M. 1995. Mouse Lbx1 and human Lbx1 define a novel mammalian homeobox gene family related to the Drosophila lady bird genes. Mech. Dev. 53, 345–356.

    Article  CAS  PubMed  Google Scholar 

  63. Gross M.K., Moran-Rivard L., Velasquez T., Nakatsu M.N., Jagla K., Goulding M. 2000. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development. 127, 413–424.

    CAS  PubMed  Google Scholar 

  64. Mennerich D., Schäfer K., Braun T. 1998. Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech. Dev. 73, 147–158.

    Article  CAS  PubMed  Google Scholar 

  65. Alvares L.E., Schubert F.R., Thorpe C., Mootoosamy R.C., Cheng L., Parkyn G., Lumsden A., Dietrich S. 2003. Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev. Cell. 5, 379–390.

    Article  CAS  PubMed  Google Scholar 

  66. Mankoo B.S., Collins N.S., Ashby P., Grigorieva E., Pevny L.H., Candia A., Wright C.V., Rigby P.W.J., Pachnis V. 1999. Meox2 is a component of the genetic hierarchy controlling limb muscle development. Nature. 400, 69–73.

    Article  CAS  PubMed  Google Scholar 

  67. Houzelstein D., Auda-Boucher G., Cheraud Y., Rouaud T., Blanc I., Tajbakhsh S., Buckingham M.E., Fontaine-Perus J., Robert B. 1999. The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development. 126, 2689–2701.

    CAS  PubMed  Google Scholar 

  68. Wang J., Kumar R.M., Biggs V.J., Lee H., Chen Y., Kagey M.H., Young R.A., Abate-Shen C. 2011. The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development. Dev. Cell. 21, 575–588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Hill T.P., Taketo M.M., Birchmeier W., Hartmann C. 2006. Multiple roles of mesenchymal β-catenin during murine limb patterning. Development. 133, 1219–1229.

    Article  CAS  PubMed  Google Scholar 

  70. Havis E., Coumailleau P., Bonnet A., Bismuth K., Bonnin M.-A., Johnson R., Fan C.-M., Relaix F., Shi D.-L., Duprez D. 2012. Sim2 prevents entry into the myogenic program by repressing MyoD transcription during limb embryonic myogenesis. Development. 139, 1910–1920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. De la Serna I.L., Ohkawa Y., Berkes C.A., Bergstrom D.A., Dacwag C.S., Tapscott S.J., Imbalzano A.N. 2005. MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol. 25, 3997–4009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Maves L., Waskiewicz A.J., Paul B., Cao Y., Tyler A., Moens C.B., Tapscott S.J. 2007. Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation. Development. 134, 3371–3382.

    Article  CAS  PubMed  Google Scholar 

  73. Munger J., Harpel J., Gleizes P.E., Mazzieri R., Nunes I., Rifkin D.B. 1997. Latent transforming growth factor-β: Structural features and mechanisms of activation. Kidney Int. 51, 1376–1382.

    Article  CAS  PubMed  Google Scholar 

  74. Cook D.R., Doumit M.E., Merkel R.A. 1993. Transforming growth factor β, basic fibroblast growth factor, and platelet-derived growth factor-BB interact to affect proliferation of clonaly derived porcine satellite cells. J. Cell. Physiol. 157, 307–331

    Article  CAS  PubMed  Google Scholar 

  75. Cusella-de Angelis M.G., Molinari S., Ledonne A., Coletta M., Vivarelli E., Bouche M., Molinaro M., Ferrari S., Cossu G. 1994. Differential response of embryonic and fetal myoblasts to TGF β—a possible regulatory mechanism of skeletal muscle histogenesis. Development. 120, 925–933.

    CAS  PubMed  Google Scholar 

  76. Mclennan I.S., Poussart Y., Koishi K. 2000. Development of skeletal muscles in transforming growth factor-β 1 (TGF-β1) null-mutant mice. Dev. Dyn. 217, 250–256.

    Article  CAS  PubMed  Google Scholar 

  77. Amthor H., Christ B., Weil M., Patel K. 1998. The importance of timing differentiation during limb muscle development. Curr. Biol. 8, 642–652.

    Article  CAS  PubMed  Google Scholar 

  78. Reshef R., Maroto M., Lassar A.B. 1998. Regulation of dorsal somitic cell fates: BMPs and noggin control the timing and pattern of myogenic regulator expression. Genes Dev. 12, 290–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. McPherron A.C., Lee S.J. 1997. Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. U. S. A. 94, 12457–12461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Artaza J.N., Bhasin S., Mallidis C., Taylor W., Ma K., Gonzalez-Cadavid N.F. 2002. Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells. J. Cell. Physiol 190, 170–179.

    Article  CAS  PubMed  Google Scholar 

  81. 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-kappaBindependent independent, FoxO1-dependent mechanism. J. Cell. Physiol. 209, 501–514.

    Article  CAS  PubMed  Google Scholar 

  82. Dasarathy S., Dodig M., Muc S.M., Kalhan S.C., McCullough A.J. 2004. Skeletal muscle atrophy is associated with an increased expression of myostatin and impaired satellite cell function in the portacaval anastamosis rat. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G1124–G1130.

    Article  CAS  PubMed  Google Scholar 

  83. Seino S., Seino M., Nishi S., Bell G.I. 1989. Structure of the human insulin receptor gene and characterization of its promoter. Proc. Natl Acad. Sci. U. S. A. 86, 114–118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Florini J.R., Ewton D.Z. 1992. Induction of gene expression in muscle by the IGFs. Growth Regul. 2, 23–29.

    CAS  PubMed  Google Scholar 

  85. Stewart C.E., James P.L., Fant M.E., Rotwein P. 1996. Overexpression of insulinlike growth factor-II induces accelerated myoblast differentiation. J. Cell. Physiol. 169, 23–32.

    Article  CAS  PubMed  Google Scholar 

  86. Florini J.R., Magri K.A., Ewton D.Z., James P., Grindstaff K., Rotwein P.S. 1991. Spontaneous differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J. Biol. Chem. 266, 15917–15923.

    CAS  PubMed  Google Scholar 

  87. Jones J.I., Clemmons D.R. 1995. Insulin-like growth factors and their binding proteins: Biological actions. Endocr. Rev. 16, 3–34.

    CAS  PubMed  Google Scholar 

  88. Bayol S., Loughna P.T., Brownson C. 2000. Phenotypic expression of IGF-binding protein transcripts in muscle, in vitro and in vivo. Biochem. Biophys. Res. Commun. 273, 282–286.

    Article  CAS  PubMed  Google Scholar 

  89. Ren H.X., Yin P., Duan C.M. 2008. IGFBP-5 regulates muscle cell differentiation by binding to IGF-II and switching on the IGF-II auto-regulation loop. J. Cell Biol. 182, 979–991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ren H.X., Accili D., Duan C.M., 2010. Hypoxia converts the myogenic action of insulin-like growth factors into mitogenic action by differentially regulating multiple signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 107, 5857–5862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Christ B., Ordahl C.P. 1995. Early stages of chick somite development. Anat. Embryol. 191, 381–396.

    Article  CAS  PubMed  Google Scholar 

  92. Yusuf F., Brand-Saberi B. 2006. The eventful somite: Patterning, fate determination and cell division in the somite. Anat. Embryol. 211, 21–30.

    PubMed  Google Scholar 

  93. Williams B.A., Ordahl C.P. 1994. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development. 120, 785–796.

    CAS  PubMed  Google Scholar 

  94. Galli L.M., Knight S.R., Barnes T.L., Doak A.K., Kadzik R.S., Burrus L.W. 2008. Identification and characterization of subpopulations of Pax3 and Pax7 expressing cells in developing chick somites and limb buds. Dev. Dyn. 237, 1862–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Nimmagadda S., Geetha Loganathan P., Huang R., Scaal M., Schmidt C., Christ B. 2005. BMP4 and noggin control embryonic blood vessel formation by antagonistic regulation of VEGFR-2 (Quek1) expression. Dev. Biol 280, 100–110.

    Article  CAS  PubMed  Google Scholar 

  96. Ben-Yair R., Kalcheim C. 2008. Notch and bone morphogenetic protein differentially act on dermomyotome cells to generate endothelium, smooth, and striated muscle. J. Cell Biol. 180, 607–618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Cairns D., Sato M., Lee P., Lassar A., Zeng L. 2008. A gradient of Shh establishes mutually repressing somitic cell fates induced by Nkx3.2 and Pax3. Dev. Biol. 323, 152–165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Aziz A., Miyake T., Engleka K.A., Epstein J., Mcdermott J.C. 2009. Menin expression modulates mesenchymal cell commitment to the myogenic and osteogenic lineages. Dev. Biol. 332, 116–130.

    Article  CAS  PubMed  Google Scholar 

  99. Kahane N., Ben-Yair R., Kalcheim C. 2007. Medial pioneer fibers pattern the morphogenesis of early myoblasts derived from the lateral somite. Dev. Biol. 305, 439–50.

    Article  CAS  PubMed  Google Scholar 

  100. Kahane N., Cinnamon Y., Bachelet I., Kalcheim C. 2001. The third wave of myotome colonization by mitotically competent progenitors: Regulating the balance between differentiation and proliferation during muscle development. Development. 128, 2187–2198.

    CAS  PubMed  Google Scholar 

  101. Linker C., Lesbros C., Gros J., Burrus L.W., Rawls A., Marcelle C. 2005. β-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development. 132, 3895–3905.

    Article  CAS  PubMed  Google Scholar 

  102. Borello U., Berarducci B., Murphy P., Bajard L., Buffa V., Piccolo S., Buckingham M., Cossu G. 2006. The Wnt/β-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development. 133, 3723–3732.

    Article  CAS  PubMed  Google Scholar 

  103. Münsterberg A.E., Lassar A.B. 1995. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911–2922.

    Article  PubMed  Google Scholar 

  104. Brunelli S., Relaix F., Baesso S., Buckingham M., Cossu G. 2007. β-Catenin-independent activation of MyoD in presomitic mesoderm requires PKC and depends on Pax3 transcriptional activity. Dev. Biol. 304, 604–614.

    Article  CAS  PubMed  Google Scholar 

  105. Tajbakhsh S., Borello U., Vivarelli E., Kelly R., Papkoff J., Duprez D., Buckingham M., Cossu G. 1998. Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development. 125, 4155–4162.

    CAS  PubMed  Google Scholar 

  106. Gros J., Serralbo O., Marcelle C. 2009. Wnt11 acts as a directional cue to organize the elongation of early muscle fibres. Nature. 457, 589–593.

    Article  CAS  PubMed  Google Scholar 

  107. Daubas P., Buckingham M.E. 2013. Direct molecular regulation of the myogenic determination gene Myf5 by Pax3, with modulation by Six1/4 factors, is exemplified by the–111 kb-Myf5 enhancer. Dev. Biol. 376, 236–244.

    Article  CAS  PubMed  Google Scholar 

  108. Grifone R., Demignon J., Houbron C., Souil E., Niro C., Seller M.J., Hamard G., Maire P. 2005. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development. 132, 2235–2249.

    Article  CAS  PubMed  Google Scholar 

  109. Gros J., Scaal M., Marcelle C. 2004. A two-step mechanism for myotome formation in chick. Dev. Cell. 6, 875–882.

    Article  CAS  PubMed  Google Scholar 

  110. McMahon J.A., Takada S., Zimmerman L.B., Fan C.M., Harland R.M., McMahon A.P. 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438–1452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Delfini M.C., De La Celle M., Gros J., Serralbo O., Marics I., Seux M., Scaal M., Marcelle C. 2009. The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. Dev. Biol. 333, 229–237.

    Article  CAS  PubMed  Google Scholar 

  112. Schuster-Gossler K., Cordes R., Gossler A. 2007. Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc. Natl. Acad. Sci. U. S. A. 104, 537–542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Lagha M., Kormish J.D., Rocancourt D., Manceau M., Epstein J.A., Zaret K.S., Relaix F., Buckingham M.E. 2008. Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program. Genes Dev. 22, 1828–1837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Manceau M., Gros J., Savage K., Thomé V., McPherron A., Paterson B., Marcelle C. 2008. Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes Dev. 22, 668–681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Montarras D., Buckingham M. 2008. Isolation, characterization and origin of muscle satellite cells. In: Recent Advances in Skeletal Myogenesis, vol. 104. Ed. Tsuchida K. Trivandrum, Kerala, India: Research Signpost, pp. 537–542.

    Google Scholar 

  116. Zammit P.S., Partridge T.A., Yablonka-Reuveni Z. 2006. The skeletal muscle satellite cell: The stem cell that came in from the cold. J. Histochem. Cytochem. 54, 1177–1191.

    Article  CAS  PubMed  Google Scholar 

  117. Schultz E. 1996. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175, 84–94.

    Article  CAS  PubMed  Google Scholar 

  118. Zammit PS. 2008. All muscle satellite cells are equal, but are some more equal than others? J. Cell Sci. 121, 2975–2982.

    Article  CAS  PubMed  Google Scholar 

  119. Kuang S., Kuroda K., Le Grand F., Rudnicki M.A. 2007. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 129, 999–1010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Kumar D., Shadrach J.L., Wagers A.J., Lassar A.B. 2009. Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol. Biol. Cell. 20, 3170–3177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Polesskaya A., Seale P., Rudnicki M.A. 2003. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell. 113, 841–852.

    Article  CAS  PubMed  Google Scholar 

  122. Conboy I.M., Rando T.A. 2002. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell. 3, 397–409.

    Article  CAS  PubMed  Google Scholar 

  123. Brack A.S., Conboy I.M., Conboy M.J., Shen J., Rando T.A. 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.

    Article  CAS  PubMed  Google Scholar 

  124. Rochat A., Fernandez A., Vandromme M., Molès J.P., Bouschet T., Carnac G., Lamb N.J. 2004. Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol. Biol. Cell. 15, 4544–4555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Le Grand F., Jones A.E., Seale V., Scimè A., Rudnicki M.A. 2009. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell. 4, 535–547.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Grim M. 1970. Differentiation of myoblasts and the relationship between somites and the wing bud of the chick embryo. Z. Anat. Entwicklungsgesch. 132, 260–271.

    Article  CAS  PubMed  Google Scholar 

  127. Uchiyama K., Ishikawa A., Hanaoka K. 2000. Expression of lbx1 involved in the hypaxial musculature formation of the mouse embryo. J. Exp. Zool. 286, 270–279.

    Article  CAS  PubMed  Google Scholar 

  128. Daston G., Lamar E., Olivier M., Goulding M. 1996. Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development. 122, 1017–1027.

    CAS  PubMed  Google Scholar 

  129. Brand-Saberi B., Muller T.S., Wilting J., Christ B., Birchmeier C. 1996. Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. Dev. Biol. 179, 303–308.

    Article  CAS  PubMed  Google Scholar 

  130. Schäfer K., Braun T. 1999. Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat. Genet. 23, 213–216.

    Article  PubMed  Google Scholar 

  131. Laclef C., Hamard G., Demignon J., Souil E., Houbron C., Maire P. 2003. Altered myogenesis in Six1-deficient mice. Development. 130, 2239–2252.

    Article  CAS  PubMed  Google Scholar 

  132. Swartz M.E., Eberhart J., Pasquale E.B., Krull C.E. 2001. EphA4/ephrin–A5 interactions in muscle precursor cell migration in the avian forelimb. Development. 128, 4669–4680.

    CAS  PubMed  Google Scholar 

  133. Brand-saberi M., Gamel A.J., Krenn V., Müller T.S., Wilting J., Christ B. 1996. N-Cadherin is involved in myoblast migration and muscle differentiation in the avian limb bud. Dev. Biol. 178, 160–173.

    Article  CAS  PubMed  Google Scholar 

  134. Scaal M., Bonafede A., Dathe V., Sachs M., Cann G., Christ B., Brand-Saberi B. 1999. SF/HGF is a mediator between limb patterning and muscle development. Development. 126, 4885–4893.

    CAS  PubMed  Google Scholar 

  135. Jacob M., Christ B., Jacob H.J. 1978. On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat. Embryol. 153, 179–193.

    Article  CAS  PubMed  Google Scholar 

  136. Pourquie O., Fan C.M., Coltey M., Hirsinger E., Watanabe Y., Breant C., Francis-West P., Brickell P., Tessier-Lavigne M., Le Douarin N.M. 1996. Lateral and axial signals involved in avian somite patterning: A role for BMP4. Cell. 84, 461–471.

    Article  CAS  PubMed  Google Scholar 

  137. Bendall A.J., Ding J., Hu G., Shen M.M., Abate-Shen C. 1999. Msx1 antagonizes the myogenic activity of Pax3 in migrating limb muscle precursors. Development. 126, 4965–4976.

    CAS  PubMed  Google Scholar 

  138. Christ B, Jacob HJ, Jacob M. 1977. Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. 150, 171–186.

    Article  CAS  PubMed  Google Scholar 

  139. Christ, B, Jacob, HJ. 1980. Origin, distribution and determination of chick limb mesenchymal cells. In: Teratology of the Limbs, Symp. on Prenatal Dev. Biol, 4th Symp. Eds. Merker H.-J., Nau H., Neubert D. Berlin: W. de Gruyter, pp. 67–77.

    Google Scholar 

  140. Patel K., Christ B., Stockdale F.E. 2002. Control of muscle size during embryonic, fetal, and adult life. In: Vertebrate Myogenesis: Results and Problems in Cell Differentiation, vol. 38. Ed. Brand-Saberi B. Berlin: Springer-Verlag, pp. 163–186.

    Chapter  Google Scholar 

  141. Amthor H., Christ B., Patel K. 1999. A molecular mechanism enabling continuous embryonic muscle growth: A balance between proliferation and differentiation. Development. 126, 1041–1053.

    CAS  PubMed  Google Scholar 

  142. Anakwe K., Robson L., Hadley J., Buxton P., Church V., Allen S., Hartmann C., Harfe B., Nohno T., Brown A.M., Evans D.J., Francis-West P. 2003. Wnt signalling regulates myogenic differentiation in the developing avian wing. Development. 130, 3503–3514.

    Article  CAS  PubMed  Google Scholar 

  143. Noden D.M., Francis-West P. 2006. The differentiation and morphogenesis of craniofacial muscles. Dev. Dyn. 235, 1194–1218.

    Article  CAS  PubMed  Google Scholar 

  144. Theis S., Patel K., Valasek P., Otto A., Pu Q., Harel I., Tzahor E., Tajbakhsh S., Christ B., Huang R. 2010. The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development. 137, 2961–2971.

    Article  CAS  PubMed  Google Scholar 

  145. Grifone R., Kelly R.G. 2007. Heartening news for head muscle development. Trends Genet. 23, 365–369.

    Article  CAS  PubMed  Google Scholar 

  146. Schoenwolf G.C., Bleyl B., Brauer P.R., Francis-West B.P. 2009. Larsen’s Human Embryology, 4th ed. Churchill Livingston: Elsevier.

    Google Scholar 

  147. Tajbakhsh S., Rocancourt D., Cossu G., Buckingham M. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 89, 127–138.

    Article  CAS  PubMed  Google Scholar 

  148. Lin C.Y., Chen W.T., Lee H.C., Yang P.H., Yang H.J., Tsai H.J. 2009. The transcription factor Six1a plays an essential role in the craniofacial myogenesis of zebrafish. Dev. Biol. 331, 152–166.

    Article  CAS  PubMed  Google Scholar 

  149. Tzahor E., Kempf H., Mootoosamy H.C., Poon A.C., Abzhanov A., Tabin C.J., Dietrich S., Lassar A.B. 2003. Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev. 17, 3087–3099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Tirosh-Finkel L., Elhanany H., Rinon A., Tzahor E. 2006. Mesoderm progenitor cells ofcommonorigin contribute to the head musculature and the cardiac outflow tract. Development. 133, 1943–1953.

    Article  CAS  PubMed  Google Scholar 

  151. Knight R.D., Mebus K., Roehl H.H. 2008. Mandibular arch muscle identity is regulated by a conserved molecular process during vertebrate development. J. Exp. Zool. 310, 355–369.

    Article  Google Scholar 

  152. Evans M., Morine K., Kulkarni C., Barton E.R. 2008. Expression profiling reveals heightened apoptosis and supports fiber size economy in the murine muscles of mastication. Physiol. Genomics. 35, 86–95.

    Article  CAS  PubMed  Google Scholar 

  153. Pavlath G.K., Thaloor D., Rando T.A., Cheong M., English A.W., Zheng B. 1998. Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Dev. Dyn. 212, 495–508.

    Article  CAS  PubMed  Google Scholar 

  154. Harel I., Nathan E., Tirosh-Finkel I., Zigdon H., Guimaraes-Camboa N., Evans S.M., Tzahor E. 2009. Distinct origins and genetic programs of head muscle satellite cells. Dev. Cell. 16, 822–832.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Schiaffino S., Reggiani C. 2011. Fiber types in mammalian skeletal muscles. Physiol. Rev. 91, 1447–1531.

    Article  CAS  PubMed  Google Scholar 

  156. Devoto S.H., Melancon E., Eisen J.S., Westerfield M. 1996. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development, 122, 3371–3380.

    CAS  PubMed  Google Scholar 

  157. Glasgow E., Tomarev S.I. 1998. Restricted expression of the homeobox gene Prox1 in developing zebrafish. Mech. Dev. 76, 175–178.

    Article  CAS  PubMed  Google Scholar 

  158. Stellabotte F., Dobbs-McAuliffe B., Fernandez D.A., Feng X., Devoto S.H. 2007. Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development. 134, 1253–1257.

    Article  CAS  PubMed  Google Scholar 

  159. Baxendale S., Davison C., Muxworthy C., Wolff C., Ingham P.W., Roy S. 2004. The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signaling. Nat. Genet. 36, 88–93.

    Article  CAS  PubMed  Google Scholar 

  160. Blagden C.S., Currie P.D., Ingham P.W., Hughes S.M. 1997. Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163–2175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Du S.J., Devoto S.H., Westerfield M., Moon R.T. 1997. Positive and negative regulation of muscle cell identity by members of the Hedgehog and TGF-β gene families. J. Cell Biol. 139, 145–156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Currie P.D., Ingham P.W. 1996. Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature. 382, 452–455.

    Article  CAS  PubMed  Google Scholar 

  163. Von Hofsten J., Elworthy S., Gilchrist M.J., Smith J.C., Wardle F.C., Ingham P.W. 2008. Prdm1-and Sox6-mediated transcriptional repression specifies muscle fibre type in the zebrafish embryo. EMBO Rep. 9, 683–689.

    Article  CAS  Google Scholar 

  164. Wang X., Ono Y., Tan S.C., Chai R.J., Parkin C., Ingham P.W. 2011. Prdm1a and miR-499 act sequentially to restrict Sox6 activity to the fast-twitch muscle lineage in the zebrafish embryo. Development. 138, 4399–4404.

    Article  CAS  PubMed  Google Scholar 

  165. Bessarab D.A., Chong S.W., Srinivas B.P., Korzh V. 2008. Six1a is required for the onset of fast muscle differentiation in zebrafish. Dev. Biol. 323, 216–228.

    Article  CAS  PubMed  Google Scholar 

  166. Jackson H.E., Ingham P.W. 2013. Control of muscle fibre-type diversity during embryonic development: The zebrafish paradigm. Mech. Dev. 130, 447–457.

    Article  CAS  PubMed  Google Scholar 

  167. Beermann M.L., Ardelt M., Girgenrath M., Millek J.B. 2010. Prdm1 (Blimp-1) and the expression of fast and slow myosin heavy chain isoforms during avian myogenesis in vitro. PLoS ONE. 5, e9951.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Hagiwara N., Yeh M., Liu A. 2007. Sox6 is required for normal fiber type differentiation of fetal skeletal muscle in mice. Dev. Dyn. 236, 2062–2076.

    Article  CAS  PubMed  Google Scholar 

  169. McCarthy J.J., Esser K.A., Peterson C.A., Dupont-Versteegden E.E. 2009. Evidence of MyomiR network regulation of β myosin heavy chain gene expression during skeletal muscle atrophy. Physiol. Genomics. 39, 219–226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Valencia-Sanchez M.A., Liu J., Hannon G.J., Parker R. 2006. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20, 515–254.

    Article  CAS  PubMed  Google Scholar 

  171. O’Rourke J.R., Georges S.A., Seay H.R., Tapscott S.J., McManus M.T., Goldhamer D.J., Swanson M.S., Harfe B.D. 2007. Essential role for Dicer during skeletal muscle development. Dev. Biol. 311, 359–368.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  172. Wienholds E., Kloosterman W.P., Miska E., Alvarez-Saavedra E., Berezikov E., de Bruijn E., Horvitz H.R., Kauppinen S., Plasterk R.H. 2005. MicroRNA expression in zebrafish embryonic development. Science. 309 (5732), 310–311.

    Article  CAS  PubMed  Google Scholar 

  173. Chen J.F., Mandel E.M., Thomson J.M., Wu Q., Callis T.E., Hammond S.M., Conlon F.L., Wang D.Z. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38, 228–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Kim H.K., Lee Y.S., Sivaprasad U., Malhotra A., Dutta A. 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. J. Cell Biol. 174, 677–687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Liu N., Williams A.H., Kim Y., McAnally J., Bezprozvannaya S., Sutherland L.B., Richardson J.A., Bassel-Duby R., Olson E.N. 2007. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc. Natl. Acad. Sci. U. S. A. 104, 20844–20849.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Sweetman D., Goljanek K., Rathjen T., Oustanina S., Braun T., Dalmay T., Münsterberg A. 2008. Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133. Dev. Biol. 321, 491–499.

    Article  CAS  PubMed  Google Scholar 

  177. Rao P.K., Kumar R.M., Farkhondeh M., Baskerville S., Lodish H.F. 2006. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl. Acad. Sci. U. S. A. 103, 8721–8726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Rosenberg M.I., Georges S.A., Asawachaicharn A., Analau E., Tapscott S.J. 2006. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J. Cell Biol. 175, 77–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Lu L., Zhou L., Chen E.Z., Sun K., Jiang P., Wang L., Su X., Sun H., Wang H. 2012. A novel YY1-miR-1 regulatory circuit in skeletal myogenesis revealed by genome-wide prediction of YY1-miRNA network. PLoS ONE. 7, e27596.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., Chiaretti S., Foá R., Schliwka J., Fuchs U., Novosel A., Müller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter H.I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 129, 1401–1414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Crist C.G., 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.

    Article  CAS  PubMed  Google Scholar 

  182. Kuang W., Tan J., Duan Y., Duan J., Wang W., Jin F., Jin Z., Yuan X., Liu Y. 2009. Cyclic stretch induced miR-146a upregulation delays C2C12 myogenic differentiation through inhibition of Numb. Biochem. Biophys. Res. Commun. 378, 259–263.

    Article  CAS  PubMed  Google Scholar 

  183. Cesana M., Cacchiarelli D., Legnini I., Santini T., Sthandier O., Chinappi M., Tramontano A., Bozzoni I. 2011. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 147, 358–369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Boutz P.L., Chawla G., Stoilov P., Black D.I. 2007. MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes Dev. 21, 71–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Huang M.B., Xu H., Xie S.J., Zhou H., Qu L.H. 2011. Insulin-like growth factor-1 receptor is regulated by microRNA-133 during skeletal myogenesis. PLoS ONE. 6, e29173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Ge Y., Sun Y., Chen J. 2011. IGF-II is regulated by microRNA-125b in skeletal myogenesis. J. Cell Biol. 192, 69–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Cardinali B., Castellani L., Fasanaro P., Basso A., Alema S., Martelli F., Falcone G. 2009. Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS ONE. 4, e7607.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Yaffe D., Saxel O. 1977. A myogenic cell line with altered serum requirements for differentiation. Differentiation. 7, 159–166.

    Article  CAS  PubMed  Google Scholar 

  189. Crippa S., Cassano M., Messina G., Galli D., Galvez B.G., Curk T., Altomare C., Ronzoni F., Toelen J., Gijsbers R., Debyser Z., Janssens S., Zupan B., Zaza A., Cossu G., Sampaolesi M. 2011. MiR669a and miR669q prevent skeletal muscle differentiation in postnatal cardiac progenitors. J. Cell Biol. 193, 1197–1212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Chen J.F., Tao Y., Li J., Deng Z., Yan Z., Xiao X., Wang D.Z. 2010. MicroRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J. Cell Biol. 190, 867–879.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Crist G., Montarras D., Pallafacchina G., Rocancourt D., Cumano A., Conway S.J., Buckingham M. 2009. Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc. Natl. Acad. Sci. U. S. A. 106, 13383–13387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Dey B.K., Gagan J., Dutta A. 2011. MiR-206 and -486 induce myoblast differentiation by downregulating Pax7. Mol. Cell. Biol. 31, 203–214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Wang H., Garzon R., Sun H., Ladner K.J., Singh R., Dahlman J., Cheng A., Hall B.M., Qualman S.J., Chandler D.S., Croce C.M., Guttridge D.C. 2008. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell. 14, 369–381.

    Article  CAS  PubMed  Google Scholar 

  194. Sarkar S., Dey B.K., Dutta A. 2010. MiR-322/424 and -503 are induced during muscle differentiation and promote cell cycle quiescence and differentiation by down-regulation of Cdc25A. Mol. Biol. Cell. 21, 2138–2149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Anderson C., Catoe H., Werner R. 2006. MiR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res. 34, 5863–5871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Sun Q., Zhang Y., Yang G., Chen X., Zhang Y., Cao G., Wang J., Sun Y., Zhang P., Fan M., Shao N., Yang X. 2008. Transforming growth factor-β-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res. 36, 2690–2699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Naguibneva I., Ameyar-Zazoua M., Polesskaya A., Ait- Si-Ali S., Groisman R., Souidi M., Cuvellier S., Harel-Bellan A. 2006. The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat. Cell Biol. 8, 278–284.

    Article  CAS  PubMed  Google Scholar 

  198. Van Rooij E., Quiat D., Johnson B.A., Sutherland L.B., Qi X., Richardson J.A., Kelm R.J., Olson E.N. 2009. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell. 17, 662–673.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  199. Wong C.F., Tellam R.L. 2008. MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J. Biol. Chem. 283, 9836–9843.

    Article  CAS  PubMed  Google Scholar 

  200. Chen Z., Liang S., Zhao Y., Han Z. 2012. MiR-92b regulates Mef2 levels through a negative-feedback circuit during Drosophila muscle development. Development. 139, 3543–3552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Seok H.Y., Tatsuguchi M., Callis T.E., He A., Pu W.T., Wang D.Z. 2011. MiR-155 inhibits expression of the MEF2A protein to repress skeletal muscle differentiation. J. Biol. Chem. 286, 35339–35346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Juan A.H., Kumar R.M., Marx J.G., Young R.A., Sartorelli V. 2009. Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. Mol. Cell. 36, 61–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Gagan J., Dey B.K., Layer R., Yan Z., Dutta A. 2011. MicroRNA-378 targets the myogenic repressor MyoR during myoblast differentiation. J. Biol. Chem. 286, 19431–19438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Derrien T., Guigó R., Johnson R. 2011. The long noncoding RNAs: A new (p)layer in the “Dark Matter”. Front Genet. 2, 107.

    PubMed  PubMed Central  Google Scholar 

  205. Flynn R.A., Chang H.Y. 2014. Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell. 14, 752–761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Figueroa A., Cuadrado A., Fan J., Atasoy U., Muscat G.E., Muñoz-Canoves P., Gorospe M., Muñoz A. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol. Cell. Biol. 23, 4991–5004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Legnini I., Morlando M., Mangiavacchi A., Fatica A., Bozzoni I. 2014. A feedforward regulatory loop between HuR and the long noncoding RNA linc-MD1 controls early phases of myogenesis. Mol. Cell. 53, 506–514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Lu L., Sun K., Chen X., Zhao Y., Wang L., Zhou L., Sun H., Wang H. 2013. Genome-wide survey by ChIP-seq reveals YY1 regulation of lincRNAs in skeletal myogenesis. EMBO J. 32, 2575–2588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Hubé F., Velasco G., Rollin J., Furling D., Francastel C. 2011. Steroid receptor RNA activator protein binds to and counteracts SRA RNA-mediated activation of MyoD and muscle differentiation. Nucleic Acids Res. 39, 513–525.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  210. Bovolenta M., Erriquez D., Valli E., Brioschi S., Scotton C., Neri M., Falzarano M.S., Gherardi S., Fabris M., Rimessi P. 2012. The DMD locus harbours multiple long non-coding RNAs which orchestrate and control transcription of muscle dystrophin mRNA isoforms. PLoS ONE. 7, e45328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Cabianca D.S., Casa V., Bodega B., Xynos A., Ginelli E., Tanaka Y., Gabellini D. 2012. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell. 149, 819–831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., Alfonso Z.C., Fraser J.K., Benhaim P., Hedrick M.H. 2002. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell. 13, 4279–4295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Goudenege S., Pisani D.F., Wdziekonski B., Di Santo J.P., Bagnis C., Dani C., Dechesne C.A. 2009. Enhancement of myogenic and muscle repair capacities of human adipose-derived stem cells with forced expression of MyoD. Mol. Ther. 17, 1064–1072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Gonçalves M.A., Janssen J.M., Nguyen Q.G., Athanasopoulos T., Hauschka S.D., Dickson G., de Vries A.A. 2011. Transcription factor rational design improves directed differentiation of human mesenchymal stem cells into skeletal myocytes. Mol. Ther. 19, 1331–1341.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  215. Albini S., Coutinho P., Malecova B., Giordani L., Savchenko A., Forcales S.V., Puri P.L. 2013. Epigenetic reprogramming of human embryonic stem cells into skeletal muscle cells and generation of contractile myospheres. Cell Rep. 3, 661–670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Dimicoli-Salazar S., Bulle F., Yacia A., Massé J.M., Fichelson S., Vigon I. 2011. Efficient in vitro myogenic reprogramming of human primary mesenchymal stem cells and endothelial cells by Myf5. Biol. Cell. 103, 531–542.

    Article  PubMed  Google Scholar 

  217. Bichsel C., Neeld D.K., Hamazaki T., Wu D., Chang L.J., Yang L., Terada N., Jin S. 2011. Bacterial delivery of nuclear proteins into pluripotent and differentiated cells. PLoS ONE. 6, e16465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Bichsel C., Neeld D., Hamazaki T., Chang L.J., Yang L.J., Terada N., Jin S. 2013. Direct reprogramming of fibroblasts to myocytes via bacterial injection of MyoD protein. Cell Reprogram. 15, 117–125.

    CAS  PubMed  PubMed Central  Google Scholar 

  219. Warren L., Manos P.D., Ahfeldt T., Loh Y.H., Li H., Lau F., Ebina W., Mandal P.K., Smith Z.D., Meissner A., Daley G.Q., Brack A.S., Collins J.J., Cowan C., Schlaeger T.M., Rossi D.J. 2010. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell. 7, 618–630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Jayawardena T.M., Egemnazarov B., Finch E.A., Zhang L., Payne J.A., Pandya K., Zhang Z., Rosenberg P., Mirotsou M., Dzau V.J. 2012. MicroRNAmediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ. Res. 110, 1465–1473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Muraoka N., Yamakawa H., Miyamoto K., Sadahiro T., Umei T., Isomi M., Nakashima H., Akiyama M., Wada R., Inagawa K., Nishiyama T., Kaneda R., Fukuda T., Takeda S., Tohyama S., Hashimoto H., Kawamura Y., Goshima N., Aeba R., Yamagishi H., Fukuda K., Ieda M. 2014. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. 33, 1565–1581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Collins-Hooper H., Luke G., Cranfield M., Otto W.R., Ray S., Patel K. 2011. Efficient myogenic reprogramming of adult white fat stem cells and bone marrow stem cells by freshly isolated skeletal muscle fibers. Transl. Res. 158, 334–343.

    Article  PubMed  Google Scholar 

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Correspondence to E. E. Kopantseva.

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Original Russian Text © E.E. Kopantseva, A.V. Belyavsky, 2016, published in Molekulyarnaya Biologiya, 2016, Vol. 50, No. 2, pp. 195–222.

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Kopantseva, E.E., Belyavsky, A.V. Key regulators of skeletal myogenesis. Mol Biol 50, 169–192 (2016). https://doi.org/10.1134/S0026893316010076

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