The extracellular matrix dimension of skeletal muscle development.

Cells anchor to substrates by binding to extracellular matrix (ECM). In addition to this anchoring function however, cell-ECM binding is a mechanism for cells to sense their surroundings and to communicate and coordinate behaviour amongst themselves. Several ECM molecules and their receptors play essential roles in muscle development and maintenance. Defects in these proteins are responsible for some of the most severe muscle dystrophies at every stage of life from neonates to adults. However, recent studies have also revealed a role of cell-ECM interactions at much earlier stages of development as skeletal muscle forms. Here we review which ECM molecules are present during the early phases of myogenesis, how myogenic cells interact with the ECM that surrounds them and the potential consequences of those interactions. We conclude that cell-ECM interactions play significant roles during all stages of skeletal muscle development in the embryo and suggest that this "extracellular matrix dimension" should be added to our conceptual network of factors contributing to skeletal myogenesis.

[1]  Buzz Baum,et al.  Transitions between epithelial and mesenchymal states in development and disease. , 2008, Seminars in cell & developmental biology.

[2]  Peter D Yurchenco,et al.  Basement membrane assembly, stability and activities observed through a developmental lens. , 2004, Matrix Biology.

[3]  D. Abraham,et al.  Col1a2 enhancer regulates collagen activity during development and in adult tissue repair. , 2004, Matrix biology : journal of the International Society for Matrix Biology.

[4]  D. Duprez,et al.  Signals regulating tendon formation during chick embryonic development , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[5]  J. Sanes,et al.  A simplified laminin nomenclature. , 2005, Matrix biology : journal of the International Society for Matrix Biology.

[6]  H. Blau,et al.  Genetic analysis of alpha 4 integrin functions in the development of mouse skeletal muscle , 1996, The Journal of cell biology.

[7]  F. Stockdale Myogenic cell lineages. , 1992, Developmental biology.

[8]  B. Wold,et al.  Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. , 1995, Development.

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

[10]  Y Ikawa,et al.  Mice develop normally without tenascin. , 1992, Genes & development.

[11]  K. Legate,et al.  ILK, PINCH and parvin: the tIPP of integrin signalling , 2006, Nature Reviews Molecular Cell Biology.

[12]  Allan Bradley,et al.  Requirement of the paraxis gene for somite formation and musculoskeletal patterning , 1996, Nature.

[13]  Denis Wirtz,et al.  Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. , 2008, Genes & development.

[14]  M. Goody,et al.  Dynamic interactions between cells and their extracellular matrix mediate embryonic development , 2010, Molecular reproduction and development.

[15]  D. Taverna,et al.  Dystrophic Muscle in Mice Chimeric for Expression of α5 Integrin , 1998, The Journal of cell biology.

[16]  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.

[17]  Donald E Ingber,et al.  Mechanical control of tissue morphogenesis during embryological development. , 2006, The International journal of developmental biology.

[18]  M. Buckingham,et al.  Muscle‐specific gene expression during myogensis in the mouse , 1995, Microscopy research and technique.

[19]  A. Horwitz,et al.  Alpha 7 beta 1 integrin is a component of the myotendinous junction on skeletal muscle. , 1993, Journal of cell science.

[20]  J. Sanes,et al.  Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. , 1984, Developmental biology.

[21]  Ruijin Huang,et al.  Regulation of ectodermal Wnt6 expression by the neural tube is transduced by dermomyotomal Wnt11: a mechanism of dermomyotomal lip sustainment , 2006, Development.

[22]  J. Thiery,et al.  Distribution of laminin and collagens during avian neural crest development. , 1987, Development.

[23]  J. W. Sanger,et al.  Somitogenesis in the mouse embryo. , 1988, Cell differentiation.

[24]  S. Tajbakhsh,et al.  The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. , 2000, Current topics in developmental biology.

[25]  S. Dietrich,et al.  Extrinsic versus intrinsic cues in avian paraxial mesoderm patterning and differentiation , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[26]  R. Fässler,et al.  Absence of integrin alpha 7 causes a novel form of muscular dystrophy. , 1997, Nature genetics.

[27]  M. Desiderio Hepatocyte growth factor in invasive growth of carcinomas , 2007, Cellular and Molecular Life Sciences.

[28]  A. Rochat,et al.  03-P130 Pax3 and Pax7 play key functions in craniofacial development , 2009, Mechanisms of Development.

[29]  B. Christ,et al.  Experimental analysis of the origin of the wing musculature in avian embryos , 1977, Anatomy and Embryology.

[30]  M. Buckingham Myogenic progenitor cells and skeletal myogenesis in vertebrates. , 2006, Current opinion in genetics & development.

[31]  L. Harrison,et al.  Convergence of bone morphogenetic protein and laminin-1 signaling pathways promotes proliferation and colony formation by fetal mouse pancreatic cells. , 2005, Experimental cell research.

[32]  G. Cossu,et al.  Beta catenin-independent activation of MyoD in presomitic mesoderm requires PKC and depends on Pax3 transcriptional activity. , 2007, Developmental biology.

[33]  M. Parsons,et al.  Collective Chemotaxis Requires Contact-Dependent Cell Polarity , 2010, Developmental cell.

[34]  Christophe Marcelle,et al.  β-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis , 2005, Development.

[35]  M. Duxson,et al.  Formation of primary and secondary myotubes in rat lumbrical muscles. , 1987, Development.

[36]  A. Sonnenberg,et al.  Knock-in of integrin β1D affects primary but not secondary myogenesis in mice , 2003 .

[37]  A. Rapraeger Molecular interactions of syndecans during development. , 2001, Seminars in cell & developmental biology.

[38]  K. Daniels,et al.  Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. , 1997, Human molecular genetics.

[39]  Richard O Hynes,et al.  Integrins Bidirectional, Allosteric Signaling Machines , 2002, Cell.

[40]  C. Tabin,et al.  Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

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

[42]  P. Francis-West,et al.  Regulation of myogenic differentiation in the developing limb bud , 2003, Journal of anatomy.

[43]  K. Patel,et al.  A molecular mechanism enabling continuous embryonic muscle growth - a balance between proliferation and differentiation. , 1999, Development.

[44]  J. Lash,et al.  Fibronectin distribution during somitogenesis in the chick embryo. , 1983, Cell differentiation.

[45]  张哉根,et al.  Leu-M , 1991 .

[46]  Raghu Kalluri,et al.  Structure and Function of Basement Membranes , 2007, Experimental biology and medicine.

[47]  W. Denetclaw,et al.  Location and growth of epaxial myotome precursor cells. , 1997, Development.

[48]  M. Marsden,et al.  Regulation of cell polarity, radial intercalation and epiboly in Xenopus: novel roles for integrin and fibronectin. , 2001, Development.

[49]  M. Duxson,et al.  Myonuclear birthdates distinguish the origins of primary and secondary myotubes in embryonic mammalian skeletal muscles. , 1989, Development.

[50]  M. S. Hansen,et al.  Connective tissue fibroblasts and Tcf4 regulate myogenesis , 2011, Development.

[51]  C. Marcelle,et al.  The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. , 2009, Developmental biology.

[52]  K. Campbell,et al.  Distinct roles for dystroglycan, beta1 integrin and perlecan in cell surface laminin organization. , 2001, Journal of cell science.

[53]  L. Silengo,et al.  Differential onset of expression of alpha 7 and beta 1D integrins during mouse heart and skeletal muscle development. , 1998, Cell adhesion and communication.

[54]  M. Bronner‐Fraser,et al.  Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo , 1986, The Journal of cell biology.

[55]  D. Erle,et al.  Integrin β Cytoplasmic Domains Differentially Bind to Cytoskeletal Proteins* , 1998, The Journal of Biological Chemistry.

[56]  L. W. Williams The somites of the chick , 1910 .

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

[58]  K. Patel,et al.  Skeletal muscle translocation in vertebrates , 2006, Anatomy and Embryology.

[59]  C. Marcelle,et al.  Somite patterning: a few more pieces of the puzzle. , 2002, Results and problems in cell differentiation.

[60]  C. Redies,et al.  Differential expression of R- and N-cadherin in neural and mesodermal tissues during early chicken development. , 1991, Development.

[61]  E. Hirsch,et al.  Genetic analyses of integrin function in mice. , 1996, Current opinion in cell biology.

[62]  L. Silengo,et al.  Muscle β1D Integrin Reinforces the Cytoskeleton–Matrix Link: Modulation of Integrin Adhesive Function by Alternative Splicing , 1997, The Journal of cell biology.

[63]  L. Trusolino,et al.  Interactions between growth factor receptors and adhesion molecules: breaking the rules. , 2003, Current opinion in cell biology.

[64]  R. Mayne,et al.  Novel Isoform of β1 Integrin Expressed in Skeletal and Cardiac Muscle , 1995 .

[65]  Richard O. Hynes,et al.  Integrins: Versatility, modulation, and signaling in cell adhesion , 1992, Cell.

[66]  S. Tajbakhsh,et al.  Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice , 1996, Nature.

[67]  T. Braun,et al.  Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. , 1996, Developmental biology.

[68]  S. Thorsteinsdóttir Basement membrane and fibronectin matrix are distinct entities in the developing mouse blastocyst , 1992, The Anatomical record.

[69]  E. Hirsch,et al.  Mouse myoblasts can fuse and form a normal sarcomere in the absence of beta1 integrin expression. , 1998, Journal of cell science.

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

[71]  R. Hynes,et al.  Extensive Vasculogenesis, Angiogenesis, and Organogenesis Precede Lethality in Mice Lacking All αv Integrins , 1998, Cell.

[72]  R. Hynes,et al.  Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. , 1999, The Journal of clinical investigation.

[73]  A. Kelly,et al.  THE HISTOGENESIS OF RAT INTERCOSTAL MUSCLE , 1969, The Journal of cell biology.

[74]  M. Duxson,et al.  Early development of the myotome in the mouse , 1999, Developmental dynamics : an official publication of the American Association of Anatomists.

[75]  K. Vogan,et al.  Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice. , 1996, Development.

[76]  P. Wigmore,et al.  The generation of fiber diversity during myogenesis. , 1998, The International journal of developmental biology.

[77]  H. Rauvala,et al.  Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. , 2004, Genes & development.

[78]  E. Zycband,et al.  Collagen fibrillogenesis in situ: Fibril segments become long fibrils as the developing tendon matures , 1997, Developmental dynamics : an official publication of the American Association of Anatomists.

[79]  T. Braun,et al.  Early specification of limb muscle precursor cells by the homeobox gene Lbx1h , 1999, Nature Genetics.

[80]  V. Krenn,et al.  Differences in the fibronectin-dependence of migrating cell populations , 2004, Anatomy and Embryology.

[81]  S. Johansson,et al.  Assembly of Laminin Polymers Is Dependent on β1-Integrins , 2001 .

[82]  A. Lassar,et al.  Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. , 1998, Genes & development.

[83]  M. Goulding,et al.  Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. , 2000, Development.

[84]  K. Jagla,et al.  The role of Lbx1 in migration of muscle precursor cells. , 2000, Development.

[85]  R. Tucker,et al.  Connective tissues: signalling by tenascins. , 2004, The international journal of biochemistry & cell biology.

[86]  Le A. Trinh,et al.  Fibronectin regulates epithelial organization during myocardial migration in zebrafish. , 2004, Developmental cell.

[87]  L. Di Marcotullio,et al.  The multiple functions of Numb. , 2010, Experimental cell research.

[88]  P. Lazarovici,et al.  Integrin α9β1 is a receptor for nerve growth factor and other neurotrophins , 2008, Journal of Cell Science.

[89]  Shahragim Tajbakhsh,et al.  Pax3/Pax7 mark a novel population of primitive myogenic cells during development. , 2005, Genes & development.

[90]  A. Horwitz,et al.  SUMMARY 7 1 Integrin is a component of the myotendinous junction on skeletal muscle , 2022 .

[91]  B. Christ,et al.  Formation and differentiation of the avian dermomyotome , 2004, Anatomy and Embryology.

[92]  O. Pourquié,et al.  Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation. , 2001, Development.

[93]  B. Schäfer,et al.  The transcriptional activator PAX3-FKHR rescues the defects of Pax3 mutant mice but induces a myogenic gain-of-function phenotype with ligand-independent activation of Met signaling in vivo. , 2003, Genes & development.

[94]  C. Streuli,et al.  Extracellular matrix remodelling and cellular differentiation. , 1999, Current opinion in cell biology.

[95]  C. ffrench-Constant,et al.  Integrins: versatile integrators of extracellular signals. , 2004, Trends in cell biology.

[96]  R. Hynes,et al.  Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. , 1995, Development.

[97]  N. Zagris,et al.  Appearance and distribution of entactin in the early chick embryo. , 1993, Differentiation; research in biological diversity.

[98]  R. Hynes,et al.  Embryonic mesodermal defects in alpha 5 integrin-deficient mice. , 1993, Development.

[99]  J. Nicolas,et al.  Laminins, via heparan sulfate proteoglycans, participate in zebrafish myotome morphogenesis by modulating the pattern of Bmp responsiveness , 2011, Development.

[100]  Y. Usson,et al.  The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. , 1989, Development.

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

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

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

[104]  M. Artinger,et al.  Developmentally regulated expression of a$ integrin in avian embryos , 2005 .

[105]  S. Selleck,et al.  Heparan sulfate proteoglycans at a glance , 2007, Journal of Cell Science.

[106]  R. Bryson-Richardson,et al.  The genetics of vertebrate myogenesis , 2008, Nature Reviews Genetics.

[107]  S. Winder,et al.  Dystroglycan versatility in cell adhesion: a tale of multiple motifs , 2010, Cell Communication and Signaling.

[108]  R. Schweitzer,et al.  Developmental fate of the mammalian myotome , 2010, Developmental dynamics : an official publication of the American Association of Anatomists.

[109]  Kenneth M. Yamada,et al.  The matrix reorganized: extracellular matrix remodeling and integrin signaling. , 2006, Current opinion in cell biology.

[110]  R. Timpl,et al.  Appearance and distribution of collagens and laminin in the early mouse embryo. , 1980, Developmental biology.

[111]  S. Thorsteinsdóttir,et al.  Integrin repertoire on myogenic cells changes during the course of primary myogenesis in the mouse , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[112]  Melinda Larsen,et al.  Fibronectin requirement in branching morphogenesis , 2003, Nature.

[113]  C. Hui,et al.  Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation , 2005, Development.

[114]  C. Birchmeier,et al.  The role of SF/HGF and c-Met in the development of skeletal muscle. , 1999, Development.

[115]  M. Takeichi,et al.  Adherens junction: molecular architecture and regulation. , 2009, Cold Spring Harbor perspectives in biology.

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

[117]  M. Duxson,et al.  Integrins in the mouse myotome: Developmental changes and differences between the epaxial and hypaxial lineage , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[118]  K. Patel,et al.  A dual fate of the hindlimb muscle mass: cloacal/perineal musculature develops from leg muscle cells , 2005, Development.

[119]  I. Palmeirim,et al.  Redefining the role of ectoderm in somitogenesis: a player in the formation of the fibronectin matrix of presomitic mesoderm , 2007, Development.

[120]  R. Fässler,et al.  Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation , 2002, The Journal of cell biology.

[121]  C. Emerson,et al.  Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. , 2001, Science.

[122]  R. Pedersen,et al.  Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. , 1995, Genes & development.

[123]  D. Sheppard,et al.  Expression of the integrin subunit α9 in the murine embryo , 1995 .

[124]  Arnoud Sonnenberg,et al.  Integrins in regulation of tissue development and function , 2003, The Journal of pathology.

[125]  B. Spiegelman,et al.  PRDM16 controls a brown fat/skeletal muscle switch , 2008, Nature.

[126]  J. Schwarzbauer,et al.  Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. , 2005, Matrix biology : journal of the International Society for Matrix Biology.

[127]  Chaya Kalcheim,et al.  Cell rearrangements during development of the somite and its derivatives. , 2005, Current opinion in genetics & development.

[128]  S. Selleck Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. , 2000, Trends in genetics : TIG.

[129]  S. Thorsteinsdóttir,et al.  Integrin expression patterns during early limb muscle development in the mouse , 2002, Mechanisms of Development.

[130]  A. Sonnenberg,et al.  Integrin α6β1-laminin interactions regulate early myotome formation in the mouse embryo , 2006 .

[131]  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.

[132]  R. Drushel,et al.  The dynamics of compartmentalization of embryonic muscle by extracellular matrix molecules. , 1991, Developmental biology.

[133]  R. Iozzo,et al.  Diverse cell signaling events modulated by perlecan. , 2008, Biochemistry.

[134]  M. Buckingham Skeletal muscle formation in vertebrates. , 2001, Current opinion in genetics & development.

[135]  Expression of muscle genes in the mouse embryo. , 1992, Symposia of the Society for Experimental Biology.

[136]  G. Kardon,et al.  Muscle and tendon morphogenesis in the avian hind limb. , 1998, Development.

[137]  Randy L. Johnson,et al.  Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. , 2006, Developmental biology.

[138]  A. Cumano,et al.  Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells , 2006, The Journal of cell biology.

[139]  E. Vuorio,et al.  Expression of type II and IX collagen isoforms during normal and pathological cartilage and eye development , 1998, Histochemistry and Cell Biology.

[140]  M. Paulsson,et al.  Absence of Basement Membranes after Targeting the LAMC1 Gene Results in Embryonic Lethality Due to Failure of Endoderm Differentiation , 1999, The Journal of cell biology.

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

[142]  J. Couchman Syndecans: proteoglycan regulators of cell-surface microdomains? , 2003, Nature Reviews Molecular Cell Biology.

[143]  J. Epstein,et al.  Pax3 functions in cell survival and in pax7 regulation. , 1999, Development.

[144]  A. Sonnenberg,et al.  A novel β1 integrin isoform produced by alternative splicing: unique expression in cardiac and skeletal muscle , 1995 .

[145]  A. Spicer,et al.  Hyaluronan and morphogenesis. , 2004, Birth defects research. Part C, Embryo today : reviews.

[146]  B. Zhou,et al.  Snail: More than EMT. , 2010, Cell adhesion & migration.

[147]  M. Rudnicki,et al.  Muscle function and dysfunction in health and disease. , 2005, Birth defects research. Part C, Embryo today : reviews.

[148]  R. Fässler,et al.  Consequences of lack of beta 1 integrin gene expression in mice. , 1995, Genes & development.

[149]  D. Gradl,et al.  Cross-regulation of Wnt signaling and cell adhesion. , 2004, Differentiation; research in biological diversity.

[150]  Y. Cinnamon,et al.  Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves , 2006, Development.

[151]  C. Ordahl,et al.  Asymmetric cell divisions are concentrated in the dermomyotome dorsomedial lip during epaxial primary myotome morphogenesis , 2005, Anatomy and Embryology.

[152]  Jeffrey W. Smith,et al.  A Biochemical Characterization of the Binding of Osteopontin to Integrins αvβ1 and αvβ5(*) , 1995, The Journal of Biological Chemistry.

[153]  V. Koteliansky,et al.  D Integrin Displaces the [ 31 A Isoform in Striated Muscles : Localization at Junctional Structures and Signaling Potential in Nonmuscle Cells , 2002 .

[154]  A. Lassar,et al.  Asymmetric localization of numb in the chick somite and the influence of myogenic signals , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[155]  Y. Jan,et al.  Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors , 2007, Nature Neuroscience.

[156]  D. Hammer,et al.  Integrin-mediated signalling through the MAP-kinase pathway. , 2008, IET systems biology.

[157]  W. Denetclaw,et al.  A proliferative role for Wnt-3a in chick somites. , 2004, Developmental biology.

[158]  S. Odelberg,et al.  A transitional extracellular matrix instructs cell behavior during muscle regeneration. , 2010, Developmental biology.

[159]  V. Koteliansky,et al.  Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells , 1996, The Journal of cell biology.

[160]  Douglas W DeSimone,et al.  The extracellular matrix in development and morphogenesis: a dynamic view. , 2010, Developmental biology.

[161]  R. Jaenisch,et al.  Deletion of integrin alpha 1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. , 1996, Developmental biology.

[162]  W. Denetclaw,et al.  The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. , 2000, Development.

[163]  S. Li,et al.  Numb regulates cell–cell adhesion and polarity in response to tyrosine kinase signalling , 2009, The EMBO journal.

[164]  Robert V Farese,et al.  Fatal Bilateral Chylothorax in Mice Lacking the Integrin α9β1 , 2000, Molecular and Cellular Biology.

[165]  J. Hinchliffe,et al.  Experimental analysis of the role of ECM in the patterning of the distal tendons of the developing limb bud. , 1990, Cell differentiation and development : the official journal of the International Society of Developmental Biologists.

[166]  J. Epstein,et al.  Pax3 modulates expression of the c-Met receptor during limb muscle development. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[167]  K. Koishi,et al.  The transforming growth factor-betas: multifaceted regulators of the development and maintenance of skeletal muscles, motoneurons and Schwann cells. , 2002, The International journal of developmental biology.

[168]  I. Bachelet,et al.  The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. , 2001, Development.

[169]  C. Erickson,et al.  MMP‐2 plays an essential role in producing epithelial‐mesenchymal transformations in the avian embryo , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[170]  L. Silengo,et al.  αv Integrin subunit is predominantly located in nervous tissue and skeletal muscle during mouse development , 1994 .

[171]  M. Zhang,et al.  During secondary myotube formation, primary myotubes preferentially absorb new nuclei at their ends , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[172]  R. Fässler,et al.  The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! , 2010, The EMBO journal.

[173]  R. Kosher,et al.  Temporal and spatial distribution of fibronectin during development of the embryonic chick limb bud. , 1982, Cell differentiation.

[174]  S. Winder,et al.  Dystroglycan protein distribution coincides with basement membranes and muscle differentiation during mouse embryogenesis , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[175]  F. Wachtler,et al.  Hyaluronic acid influences the migration of myoblasts within the avian embryonic wing bud. , 1991, The American journal of anatomy.

[176]  C. Marcelle,et al.  WNT11 acts as a directional cue to organize the elongation of early muscle fibres , 2009, Nature.

[177]  N. Zagris,et al.  Spatial and Temporal Expression of Perlecan in the Early Chick Embryo , 2007, Cells Tissues Organs.

[178]  S. Schulz,et al.  CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. , 2005, Genes & development.

[179]  Michael D Schaller,et al.  Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions , 2010, Journal of Cell Science.

[180]  Chelsi J. Snow,et al.  Muscle development is disrupted in zebrafish embryos deficient for fibronectin , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[181]  T. Schilling,et al.  Chemokine Signaling Controls Endodermal Migration During Zebrafish Gastrulation , 2008, Science.

[182]  Claire Anderson,et al.  Sonic hedgehog-dependent synthesis of laminin α1 controls basement membrane assembly in the myotome , 2009, Development.

[183]  C. Tiger,et al.  Integrins during muscle development and in muscular dystrophies. , 1998, Frontiers in bioscience : a journal and virtual library.

[184]  A. Cumano,et al.  Numb Promotes an Increase in Skeletal Muscle Progenitor Cells in the Embryonic Somite , 2009, Stem cells.

[185]  S. Werner,et al.  Skin wounds and severed nerves heal normally in mice lacking tenascin-C. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[186]  J. M. Venuti,et al.  Identification of responsive cells in the developing somite supports a role for β‐catenin‐dependent Wnt signaling in maintaining the DML myogenic progenitor pool , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[187]  J. Riou,et al.  Tenascin: a potential modulator of cell‐extracellular matrix interactions during vertebrate embryogenesis , 1992, Biology of the cell.

[188]  Chaya Kalcheim,et al.  Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates , 2005, Development.

[189]  P. Lonai,et al.  Expression and biological role of laminin-1. , 2003, Matrix biology : journal of the International Society for Matrix Biology.

[190]  D. Jonas,et al.  CXCR4 chemokine receptor engagement modifies integrin dependent adhesion of renal carcinoma cells. , 2007, Experimental cell research.

[191]  E. Brandan,et al.  Expression and localization of proteoglycans during limb myogenic activation , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[192]  J. Schwarzbauer,et al.  Assembly of fibronectin extracellular matrix. , 2010, Annual review of cell and developmental biology.

[193]  R. Hynes,et al.  Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. , 1999, Developmental biology.

[194]  Elaine Fuchs,et al.  Scratching the surface of skin development , 2007, Nature.

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

[196]  Arnoud Sonnenberg,et al.  Function and interactions of integrins , 2001, Cell and Tissue Research.

[197]  R. Hynes,et al.  Mesodermal development in mouse embryos mutant for fibronectin , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[198]  Melinda Larsen,et al.  Extracellular matrix dynamics in development and regenerative medicine , 2008, Journal of Cell Science.

[199]  A. Hidalgo,et al.  Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-mediated multiple myeloma cell adhesion to CS-1/fibronectin and VCAM-1. , 2001, Blood.

[200]  P. Yurchenco,et al.  Form and function: The laminin family of heterotrimers , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[201]  N. Kahane,et al.  Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite , 2003, Development.

[202]  E Ruoslahti,et al.  Extracellular matrix/growth factor interactions. , 1992, Cold Spring Harbor symposia on quantitative biology.

[203]  Valerie M. Weaver,et al.  The extracellular matrix at a glance , 2010, Journal of Cell Science.

[204]  R. Assoian,et al.  Regulation of growth factor signaling and cell cycle progression by cell adhesion and adhesion-dependent changes in cellular tension. , 2005, Cytokine & growth factor reviews.

[205]  B. Rubino,et al.  The role of epithelial-mesenchymal transition in cancer pathology. , 2007, Pathology.

[206]  B. Brand-Saberi,et al.  Limb muscle development. , 2002, The International journal of developmental biology.

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

[208]  D. Macías,et al.  Tendon-muscle crosstalk controls muscle bellies morphogenesis, which is mediated by cell death and retinoic acid signaling. , 2007, Developmental biology.

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

[210]  M. Buckingham,et al.  The formation of skeletal muscle: from somite to limb , 2003, Journal of anatomy.

[211]  Erez Raz,et al.  Chemokine signaling in embryonic cell migration: a fisheye view , 2009, Development.

[212]  R. Hynes,et al.  Embryonic mesodermal defects in 5 integrin-deficient mice , 1996 .

[213]  Mina J. Bissell,et al.  Extracellular matrix control of mammary gland morphogenesis and tumorigenesis: insights from imaging , 2008, Histochemistry and Cell Biology.

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

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

[216]  M. Humphries,et al.  Synergistic control of cell adhesion by integrins and syndecans , 2007, Nature Reviews Molecular Cell Biology.

[217]  E. Godfrey,et al.  Basal lamina molecules are concentrated in myogenic regions of the mouse limb bud , 1998, Anatomy and Embryology.

[218]  M. Humphries,et al.  Linking integrin conformation to function , 2009, Journal of Cell Science.

[219]  A. Gamel,et al.  N-cadherin is involved in myoblast migration and muscle differentiation in the avian limb bud. , 1996, Developmental Biology.

[220]  S. Dedhar,et al.  Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase , 1996, Nature.

[221]  R. Hynes,et al.  Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. , 1993, Development.

[222]  F. Pröls,et al.  Spatial and temporal pattern of Wnt-6 expression during chick development , 2003, Anatomy and Embryology.

[223]  A. Sutherland,et al.  Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation , 2004, Development.

[224]  A. Sonnenberg,et al.  Erratum: Integrins in regulation of tissue development and function. J Pathol; 200: 471–480 , 2003 .

[225]  J. Sanes,et al.  Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis , 1992, Cell.

[226]  R. Jaenisch,et al.  Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. , 1996, Development.

[227]  P. Armstrong,et al.  Intercellular invasion and the organizational stability of tissues: a role for fibronectin. , 2000, Biochimica et biophysica acta.

[228]  A. Bailey,et al.  Has collagen a role in muscle pattern formation in the developing chick wing? 1. An immunofluorescence study. , 1980, Journal of embryology and experimental morphology.

[229]  N. Zagris,et al.  Differential expression of laminin genes in early chick embryo. , 2000, The International journal of developmental biology.

[230]  W. Birchmeier,et al.  Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. , 2010, Cold Spring Harbor perspectives in biology.

[231]  R. Sambasivan,et al.  Skeletal muscle stem cell birth and properties. , 2007, Seminars in cell & developmental biology.

[232]  M. Ontell,et al.  The organogenesis of murine striated muscle: a cytoarchitectural study. , 1984, The American journal of anatomy.

[233]  R. Fässler,et al.  Genetic and cell biological analysis of integrin outside-in signaling. , 2009, Genes & development.

[234]  C. Marcelle,et al.  Intrinsic signals regulate the initial steps of myogenesis in vertebrates , 2003, Development.

[235]  R. Jaenisch,et al.  α3β1 Integrin Is Required for Normal Development of the Epidermal Basement Membrane , 1997, The Journal of cell biology.

[236]  K. Kaibuchi,et al.  Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. , 2007, Developmental cell.

[237]  A. Horwitz,et al.  Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cells secreting an anti-integrin antibody. , 1988, Development.

[238]  M. Durbeej,et al.  Distinct α7Aβ1 and α7Bβ1 integrin expression patterns during mouse development: α7A is restricted to skeletal muscle but α7B is expressed in striated muscle, vasculature, and nervous system , 1996 .

[239]  J. Hinchliffe,et al.  Immunohistological and ultrastructural study of the developing tendons of the avian foot , 1995, Anatomy and Embryology.

[240]  R. Hynes,et al.  Mesodermal defects and cranial neural crest apoptosis in alpha5 integrin-null embryos. , 1997, Development.

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

[242]  K. Venstrom,et al.  Beta 8 integrins mediate interactions of chick sensory neurons with laminin-1, collagen IV, and fibronectin. , 1995, Molecular biology of the cell.

[243]  U. Müller,et al.  Beta1 integrins regulate myoblast fusion and sarcomere assembly. , 2003, Developmental cell.

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

[245]  C. Erickson,et al.  Neural crest cells prefer the myotome's basal lamina over the sclerotome as a substratum. , 1994, Developmental biology.

[246]  M. Goumans,et al.  Knockout and knockin of the beta1 exon D define distinct roles for integrin splice variants in heart function and embryonic development. , 1998, Genes & development.

[247]  H. Kondoh,et al.  Integrinalpha5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos. , 2005, Developmental cell.

[248]  Douglas W DeSimone,et al.  Cell adhesion receptors in mechanotransduction. , 2008, Current opinion in cell biology.

[249]  G M Edelman,et al.  Adhesion molecules during somitogenesis in the avian embryo , 1987, The Journal of cell biology.

[250]  S. Patterson,et al.  BMP regulation of myogenesis in zebrafish , 2010, Developmental dynamics : an official publication of the American Association of Anatomists.

[251]  M. Molinaro,et al.  Cellular heterogeneity during vertebrate skeletal muscle development. , 2007, Developmental biology.

[252]  M. Kieny,et al.  Limb-somite relationship: origin of the limb musculature. , 1977, Journal of embryology and experimental morphology.

[253]  J. Wilson-Rawls,et al.  Differential regulation of epaxial and hypaxial muscle development by paraxis. , 1999, Development.

[254]  A. Sonnenberg,et al.  Spatial and temporal expression of the β1D integrin during mouse development , 1997 .

[255]  C. McGlade,et al.  Mammalian Numb Proteins Promote Notch1 Receptor Ubiquitination and Degradation of the Notch1 Intracellular Domain* , 2003, Journal of Biological Chemistry.

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