Many routes to the same destination: lessons from skeletal muscle development.

The development and differentiation of vertebrate skeletal muscle provide an important paradigm to understand the inductive signals and molecular events controlling differentiation of specific cell types. Recent findings show that a core transcriptional network, initiated by the myogenic regulatory factors (MRFs; MYF5, MYOD, myogenin and MRF4), is activated by separate populations of cells in embryos in response to various signalling pathways. This review will highlight how cells from multiple distinct starting points can converge on a common set of regulators to generate skeletal muscle.

[1]  J. Drouin,et al.  Pitx2 defines alternate pathways acting through MyoD during limb and somitic myogenesis , 2010, Development.

[2]  Y. Asakura,et al.  MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3 , 2010, The Journal of cell biology.

[3]  F. Lescroart,et al.  Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo , 2010, Development.

[4]  Jian-Fu Chen,et al.  microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7 , 2010, The Journal of cell biology.

[5]  K. Patel,et al.  The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature , 2010, Development.

[6]  V. Vedantham,et al.  Direct Reprogramming of Fibroblasts into Functional Cardiomyocytes by Defined Factors , 2010, Cell.

[7]  T. Callis,et al.  MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. , 2010, The international journal of biochemistry & cell biology.

[8]  A. Wagers,et al.  Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors , 2010, Journal of Cell Science.

[9]  Lionel Christiaen,et al.  Early Chordate Origins of the Vertebrate Second Heart Field , 2010, Science.

[10]  A. Blais,et al.  Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation , 2010, Nucleic acids research.

[11]  K. Patel,et al.  Neuromuscular junction morphology, fiber‐type proportions, and satellite‐cell proliferation rates are altered in MyoD−/− mice , 2010, Muscle & nerve.

[12]  Christoph Lepper,et al.  Inducible lineage tracing of Pax7‐descendant cells reveals embryonic origin of adult satellite cells , 2010, Genesis.

[13]  H. Blau,et al.  Nuclear reprogramming to a pluripotent state by three approaches , 2010, Nature.

[14]  W. Filipowicz,et al.  Regulation of mRNA translation and stability by microRNAs. , 2010, Annual review of biochemistry.

[15]  W. L. Ruzzo,et al.  Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. , 2010, Developmental cell.

[16]  M. Buckingham,et al.  A Pax3/Dmrt2/Myf5 Regulatory Cascade Functions at the Onset of Myogenesis , 2010, PLoS genetics.

[17]  D. Sassoon,et al.  Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development , 2010, Nature Cell Biology.

[18]  M. Abu-Elmagd,et al.  Wnt/Lef1 signaling acts via Pitx2 to regulate somite myogenesis. , 2010, Developmental biology.

[19]  C. Angelini,et al.  Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients , 2010, Journal of Translational Medicine.

[20]  E. Olson,et al.  A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. , 2009, Developmental cell.

[21]  P. Fasanaro,et al.  Microrna-221 and Microrna-222 Modulate Differentiation and Maturation of Skeletal Muscle Cells , 2009, PloS one.

[22]  G. Meola,et al.  Common micro‐RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia , 2009, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[23]  R. Young,et al.  Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. , 2009, Molecular cell.

[24]  D. Goldhamer,et al.  Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD. , 2009, Developmental biology.

[25]  Christoph Lepper,et al.  Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements , 2009, Nature.

[26]  G. Kardon,et al.  Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. , 2009, Genes & development.

[27]  E. Tzahor,et al.  Heart and craniofacial muscle development: a new developmental theme of distinct myogenic fields. , 2009, Developmental biology.

[28]  Robert B. White,et al.  Integrated Functions of Pax3 and Pax7 in the Regulation of Proliferation, Cell Size and Myogenic Differentiation , 2009, PloS one.

[29]  T. Golub,et al.  MicroRNA-1 Negatively Regulates Expression of the Hypertrophy-Associated Calmodulin and Mef2a Genes , 2009, Molecular and Cellular Biology.

[30]  T. Dalmay,et al.  Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133. , 2008, Developmental biology.

[31]  T. Borchardt,et al.  Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis , 2008, Development.

[32]  Jian Wang,et al.  Transforming growth factor-β-regulated miR-24 promotes skeletal muscle differentiation , 2008, Nucleic acids research.

[33]  M. Capecchi,et al.  Two cell lineages, myf5 and myf5-independent, participate in mouse skeletal myogenesis. , 2008, Developmental cell.

[34]  I. Harel,et al.  The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development , 2008, Development.

[35]  P. Rigby,et al.  Global transcriptional regulation of the locus encoding the skeletal muscle determination genes Mrf4 and Myf5. , 2008, Genes & development.

[36]  A. Nakamura,et al.  MicroRNA-206 is highly expressed in newly formed muscle fibers: implications regarding potential for muscle regeneration and maturation in muscular dystrophy. , 2008, Cell structure and function.

[37]  Barbara Gayraud-Morel,et al.  A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. , 2007, Developmental biology.

[38]  J. Barrow,et al.  A highly conserved Wnt-dependent TCF4 binding site within the proximal enhancer of the anti-myogenic Msx1 gene supports expression within Pax3-expressing limb bud muscle precursor cells. , 2007, Developmental biology.

[39]  M. Buckingham,et al.  The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. , 2007, Annual review of cell and developmental biology.

[40]  Ruijin Huang,et al.  Amniote somite derivatives , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  P. Rigby,et al.  The Myogenic Factor Myf5 Supports Efficient Skeletal Muscle Regeneration by Enabling Transient Myoblast Amplification , 2007, Stem cells.

[42]  M. Buckingham Skeletal muscle progenitor cells and the role of Pax genes. , 2007, Comptes rendus biologies.

[43]  C. Kioussi,et al.  Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch , 2007, Proceedings of the National Academy of Sciences.

[44]  C. Laclef,et al.  Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. , 2007, Developmental biology.

[45]  P. Scambler,et al.  Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[46]  A. Baldini,et al.  Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle , 2006, Development.

[47]  R. Werner,et al.  MIR-206 regulates connexin43 expression during skeletal muscle development , 2006, Nucleic acids research.

[48]  S. Tapscott,et al.  MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206 , 2006, The Journal of cell biology.

[49]  G. Cossu,et al.  The Wnt/β-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis , 2006, Development.

[50]  M. Buckingham,et al.  A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. , 2006, Genes & development.

[51]  A. Malhotra,et al.  Muscle-specific microRNA miR-206 promotes muscle differentiation , 2006, The Journal of cell biology.

[52]  G. Wheeler,et al.  FGF‐4 signaling is involved in mir‐206 expression in developing somites of chicken embryos , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[53]  Harvey F Lodish,et al.  Myogenic factors that regulate expression of muscle-specific microRNAs. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[54]  P. Francis-West,et al.  The differentiation and morphogenesis of craniofacial muscles , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[55]  K. Patel,et al.  Pax3 and Pax7 expression and regulation in the avian embryo , 2006, Anatomy and Embryology.

[56]  Annick Harel-Bellan,et al.  The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation , 2006, Nature Cell Biology.

[57]  Jian-Fu Chen,et al.  The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation , 2006, Nature Genetics.

[58]  K. Patel,et al.  Ectodermal Wnt-6 promotes Myf5-dependent avian limb myogenesis. , 2005, Developmental biology.

[59]  S. Tapscott,et al.  MyoD and the transcriptional control of myogenesis. , 2005, Seminars in cell & developmental biology.

[60]  C. Marcelle,et al.  A common somitic origin for embryonic muscle progenitors and satellite cells , 2005, Nature.

[61]  A. Mansouri,et al.  A Pax3/Pax7-dependent population of skeletal muscle progenitor cells , 2005, Nature.

[62]  S. Tapscott,et al.  MyoD Targets Chromatin Remodeling Complexes to the Myogenin Locus Prior to Forming a Stable DNA-Bound Complex , 2005, Molecular and Cellular Biology.

[63]  G. Hamard,et al.  Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo , 2005, Development.

[64]  S. Dietrich,et al.  The epaxial-hypaxial subdivision of the avian somite. , 2004, Developmental biology.

[65]  Barbara Gayraud-Morel,et al.  Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice , 2004, Nature.

[66]  M. Bonnin,et al.  Hedgehog can drive terminal differentiation of amniote slow skeletal muscle , 2004, BMC Developmental Biology.

[67]  C. Marcelle,et al.  A two-step mechanism for myotome formation in chick. , 2004, Developmental cell.

[68]  M. Delfini,et al.  Ectopic Myf5 or MyoD prevents the neuronal differentiation program in addition to inducing skeletal muscle differentiation, in the chick neural tube , 2004, Development.

[69]  A. Abzhanov,et al.  Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. , 2003, Genes & development.

[70]  P. Rigby,et al.  The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation. , 2003, Genes & development.

[71]  Anthony M. C. Brown,et al.  Wnt signalling regulates myogenic differentiation in the developing avian wing , 2003, Development.

[72]  C. Tabin,et al.  A Somitic Compartment of Tendon Progenitors , 2003, Cell.

[73]  C. Tabin,et al.  Developmental regulation of somite derivatives: muscle, cartilage and tendon. , 2002, Current opinion in genetics & development.

[74]  C. Marcelle,et al.  FGFR4 signaling is a necessary step in limb muscle differentiation. , 2002, Development.

[75]  C. Ordahl,et al.  Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence. , 2002, Development.

[76]  C. Tabin,et al.  Pax3 and Dach2 positive regulation in the developing somite , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[77]  B. Olwin,et al.  Sonic hedgehog inhibits the terminal differentiation of limb myoblasts committed to the slow muscle lineage. , 2002, Developmental biology.

[78]  Roy C Mootoosamy,et al.  Distinct regulatory cascades for head and trunk myogenesis. , 2002, Development.

[79]  C. Emerson,et al.  Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. , 2002, Annual review of cell and developmental biology.

[80]  W. Denetclaw,et al.  The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. , 2001, Development.

[81]  W. Denetclaw,et al.  Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. , 2001, Development.

[82]  P. Rigby,et al.  A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development. , 2001, Development.

[83]  O. Pourquié,et al.  Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. , 2000, Development.

[84]  Ruijin Huang,et al.  Origin of the epaxial and hypaxial myotome in avian embryos , 2000, Anatomy and Embryology.

[85]  G. Mardon,et al.  Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. , 1999, Genes & development.

[86]  G. Cann,et al.  SF/HGF is a mediator between limb patterning and muscle development , 1999 .

[87]  Y. Cinnamon,et al.  Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. , 1999, Development.

[88]  R. Marcucio,et al.  Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis , 1999, Developmental dynamics : an official publication of the American Association of Anatomists.

[89]  B. Brunk,et al.  Sonic hedgehog controls epaxial muscle determination through Myf5 activation. , 1999, Development.

[90]  P. Rigby,et al.  Mox2 is a component of the genetic hierarchy controlling limb muscle development , 1999, Nature.

[91]  S. Tajbakhsh,et al.  The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. , 1999, Development.

[92]  A. Trounson,et al.  Early human development. , 1999, Human reproduction update.

[93]  G. Cossu,et al.  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. , 1998, Development.

[94]  P. Sharpe,et al.  Specification of the hypaxial musculature. , 1998, Development.

[95]  Y. Cinnamon,et al.  The origin and fate of pioneer myotomal cells in the avian embryo , 1998, Mechanisms of Development.

[96]  K. Patel,et al.  The importance of timing differentiation during limb muscle development , 1998, Current Biology.

[97]  G. Cossu,et al.  Differential activation of Myf 5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf 5 , 1998 .

[98]  J. Cooke,et al.  Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. , 1997, Development.

[99]  C. Marcelle,et al.  Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. , 1997, Development.

[100]  S. Koester,et al.  Ectopic Pax-3 Activates MyoD and Myf-5 Expression in Embryonic Mesoderm and Neural Tissue , 1997, Cell.

[101]  C. Birchmeier,et al.  Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. , 1996, Developmental biology.

[102]  A. McMahon,et al.  Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. , 1995, Genes & development.

[103]  Carmen Birchmeier,et al.  Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud , 1995, Nature.

[104]  A. Lassar,et al.  Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite. , 1995, Development.

[105]  C. Tickle,et al.  Tissue and cellular patterning of the musculature in chick wings. , 1994, Development.

[106]  M. Goulding,et al.  Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. , 1994, Development.

[107]  M. Rudnicki,et al.  MyoD or Myf-5 is required for the formation of skeletal muscle , 1993, Cell.

[108]  William H. Klein,et al.  Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene , 1993, Nature.

[109]  M. Rudnicki,et al.  Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development , 1992, Cell.

[110]  Matthew H. Kaufman,et al.  The Atlas of Mouse Development , 1992 .

[111]  C. Lance‐Jones The somitic level of origin of embryonic chick hindlimb muscles. , 1988, Developmental biology.

[112]  B. Beresford Brachial muscles in the chick embryo: the fate of individual somites. , 1983, Journal of embryology and experimental morphology.

[113]  R. Barr,et al.  The Neuromuscular Junction , 2007 .

[114]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.