Global patterning of the vertebrate mesoderm

We describe recent advances in the understanding of patterning in the vertebrate post‐cranial mesoderm. Specifically, we discuss the integration of local information into global level information that results in the overall coordination along the anterioposterior axis. Experiments related to the integration of the axial and appendicular musculoskeletal systems are considered, and examples of genetic interactions between these systems are outlined. We emphasize the utility of the terms primaxial and abaxial as an aid to understanding development of the vertebrate musculoskeletal system, and hypothesize that the lateral somitic frontier is a catalyst for evolutionary change. Developmental Dynamics 236:2371–2381, 2007. © 2007 Wiley‐Liss, Inc.

[1]  O. Pourquié,et al.  Hox genes in time and space during vertebrate body formation , 2007, Development, growth & differentiation.

[2]  A. Streit,et al.  Mesoderm patterning and somite formation during node regression: differential effects of chordin and noggin , 1999, Mechanisms of Development.

[3]  M. Crawford.  Hox genes as synchronized temporal regulators: implications for morphological innovation. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[4]  V. Papaioannou,et al.  Evidence of a role for T-☐ genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity , 1996, Mechanisms of Development.

[5]  S. Dietrich.  Regulation of hypaxial muscle development , 1999, Cell and Tissue Research.

[6]  D. Saito,et al.  Level-specific role of paraxial mesoderm in regulation of Tbx5/Tbx4 expression and limb initiation. , 2006, Developmental biology.

[7]  P. Sengel,et al.  Early regionalization of somitic mesoderm as studied by the development of axial skeleton of the chick embryo. , 1972, Developmental biology.

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

[9]  D. Bartel,et al.  MicroRNA-Directed Cleavage of HOXB8 mRNA , 2004, Science.

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

[11]  R. Harland,et al.  Hedgehog signaling regulates the amount of hypaxial muscle development during Xenopus myogenesis. , 2007, Developmental biology.

[12]  B. Barrell,et al.  Maintenance of functional equivalence during paralogous Hox gene evolution , 2022 .

[13]  V. García-Martínez,et al.  Mesoderm movement and fate during avian gastrulation and neurulation , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[14]  K. Steel,et al.  Analysis of the Pax-3 gene in the mouse mutant splotch. , 1993, Genomics.

[15]  P. Rigby,et al.  The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. , 2000, Development.

[16]  T. Ogura,et al.  Correlation of wing-leg identity in ectopic FGF-induced chimeric limbs with the differential expression of chick Tbx5 and Tbx4. , 1998, Development.

[17]  K. Jagla,et al.  Mouse Lbx1 and human LBX1 define a novel mammalian homeo☐ gene family related to the Drosophila lady bird genes , 1995, Mechanisms of Development.

[18]  D. Melton,et al.  Vertebrate endoderm development. , 1999, Annual review of cell and developmental biology.

[19]  G. Morata,et al.  Colinearity and functional hierarchy among genes of the homeotic complexes. , 1994, Trends in genetics : TIG.

[20]  E. Boncinelli,et al.  Novel interactions between vertebrate Hox genes. , 1999, The International journal of developmental biology.

[21]  M. Logan,et al.  Tbx5 is dispensable for forelimb outgrowth , 2007, Development.

[22]  R. Krumlauf,et al.  Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. , 2002, Development.

[23]  A. Kuroiwa,et al.  Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. , 2001, Development.

[24]  Jeh-Ping Liu.  The function of growth/differentiation factor 11 (Gdf11) in rostrocaudal patterning of the developing spinal cord , 2006, Development.

[25]  D. Roberts,et al.  Molecular mechanisms of development of the gastrointestinal tract , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[26]  C. Stern,et al.  Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. , 1991, Development.

[27]  O. Pourquié,et al.  Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. , 2000, Development.

[28]  E. C. Zeeman,et al.  A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. , 1976, Journal of theoretical biology.

[29]  O. Pourquié,et al.  Avian hairy Gene Expression Identifies a Molecular Clock Linked to Vertebrate Segmentation and Somitogenesis , 1997, Cell.

[30]  A. Durston,et al.  The small GTPase Rap1 is an immediate downstream target for Hoxb4 transcriptional regulation , 2002, Mechanisms of Development.

[31]  S. Dietrich,et al.  Establishment of the epaxial–hypaxial boundary in the avian myotome , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[32]  T. Jessell,et al.  Assigning the Positional Identity of Spinal Motor Neurons Rostrocaudal Patterning of Hox-c Expression by FGFs, Gdf11, and Retinoids , 2001, Neuron.

[33]  Siming W. Chen,et al.  A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. , 1998, Development.

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

[35]  B. Brand-Saberi,et al.  Angiogenic potential of the avian somite , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[36]  K. Storey,et al.  Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  V. Papaioannou,et al.  Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth , 2007, Development.

[38]  Monte Westerfield,et al.  Multiple upstream modules regulate zebrafish myf5 expression , 2007, BMC Developmental Biology.

[39]  Lydia Teboul,et al.  The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. , 2002, Development.

[40]  C. Minguillon,et al.  Tbx5 and Tbx4 are not sufficient to determine limb-specific morphologies but have common roles in initiating limb outgrowth. , 2005, Developmental cell.

[41]  C. Ordahl,et al.  Two myogenic lineages within the developing somite. , 1992, Development.

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

[43]  Olivier Pourquié,et al.  FGF Signaling Controls Somite Boundary Position and Regulates Segmentation Clock Control of Spatiotemporal Hox Gene Activation , 2001, Cell.

[44]  Michael Zuker,et al.  MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression , 2004, Nature Genetics.

[45]  R. Harland,et al.  A novel role for lbx1 in Xenopus hypaxial myogenesis , 2005, Development.

[46]  S. Forlani,et al.  Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo , 2003, Development.

[47]  S. Meier.  Development of the chick embryo mesoblast: pronephros, lateral plate, and early vasculature. , 1980, Journal of embryology and experimental morphology.

[48]  C. Birchmeier,et al.  Expression of the met-receptor and its ligand, HGF-SF during mouse embryogenesis. , 1993, EXS.

[49]  K. Patel,et al.  Tbx genes and limb identity in chick embryo development. , 1998, Development.

[50]  R. Balling,et al.  Expression of avian Pax1 and Pax9 is intrinsically regulated in the pharyngeal endoderm, but depends on environmental influences in the paraxial mesoderm. , 1996, Developmental biology.

[51]  O. Pourquié,et al.  Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression , 2006, Nature.

[52]  T J Poole,et al.  Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. , 1989, The Journal of experimental zoology.

[53]  J. Epstein,et al.  Identification of a hypaxial somite enhancer element regulating Pax3 expression in migrating myoblasts and characterization of hypaxial muscle Cre transgenic mice , 2005, Genesis.

[54]  F. Stockdale,et al.  Molecular and cellular biology of avian somite development , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[55]  R. Spörle.  Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication , 2001, Development Genes and Evolution.

[56]  O. Pourquié,et al.  Lateral and Axial Signals Involved in Avian Somite Patterning: A Role for BMP4 , 1996, Cell.

[57]  D. Luton,et al.  Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. , 1996, Development.

[58]  D. Noden.  Origins and patterning of craniofacial mesenchymal tissues. , 1986, Journal of craniofacial genetics and developmental biology. Supplement.

[59]  D. Duboule,et al.  The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. , 1989, The EMBO journal.

[60]  D. Duboule,et al.  Large scale transgenic and cluster deletion analysis of the HoxD complex separate an ancestral regulatory module from evolutionary innovations. , 2001, Genes & development.

[61]  V. Laudet,et al.  Conserved RARE localization in amphioxus Hox clusters and implications for Hox code evolution in the vertebrate neural crest , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[62]  C. Tabin,et al.  Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer , 2002, Genesis.

[63]  Marc Vidal,et al.  Predictive models of molecular machines involved in Caenorhabditis elegans early embryogenesis , 2005, Nature.

[64]  C. Tabin,et al.  Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity. , 1998, Development.

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

[66]  T. Braun,et al.  Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb , 1998, Mechanisms of Development.

[67]  G. ELLIOT SMITH,et al.  Studies on the Structure and Development of Vertebrates , 1930, Nature.

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

[69]  E. Davidson,et al.  Gene Regulatory Networks and the Evolution of Animal Body Plans , 2006, Science.

[70]  R. Morgan,et al.  TALE class homeodomain gene Irx5 is an immediate downstream target for Hoxb4 transcriptional regulation , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[71]  L. Gudas,et al.  Analysis of two distinct retinoic acid response elements in the homeobox gene Hoxb1 in transgenic mice , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[72]  T. Ogura,et al.  Coelom formation: binary decision of the lateral plate mesoderm is controlled by the ectoderm. , 1999, Development.

[73]  R. Krumlauf,et al.  The murine and Drosophila homeobox gene complexes have common features of organization and expression , 1989, Cell.

[74]  D M Noden,et al.  The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. , 1983, Developmental biology.

[75]  N. Ueno,et al.  Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4. , 1997, Development.

[76]  Craig Nelson,et al.  Hox genes and the evolution of vertebrate axial morphology. , 1995, Development.

[77]  Michael T. McManus,et al.  The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development , 2005, Nature.

[78]  R. Krumlauf,et al.  Retinoids and Hox genes , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[79]  R. Balling,et al.  The ventralizing effect of the notochord on somite differentiation in chick embryos , 1993, Anatomy and Embryology.

[80]  R. Bryson-Richardson,et al.  Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish , 2004, Development.

[81]  M. Capecchi,et al.  Materials and Methods Som Text Figs. S1 to S4 Tables S1 and S2 References and Notes Hox10 and Hox11 Genes Are Required to Globally Pattern the Mammalian Skeleton , 2022 .

[82]  Ruijin Huang,et al.  Cells of all somitic compartments are determined with respect to segmental identity , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[83]  L. Pardanaud,et al.  Expression of C-ETS1 in early chick embryo mesoderm: relationship to the hemangioblastic lineage. , 1993, Cell adhesion and communication.

[84]  Se-Jin Lee,et al.  Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11 , 1999, Nature Genetics.

[85]  D. Noden.  Embryonic origins and assembly of blood vessels. , 1989, The American review of respiratory disease.

[86]  Peter Gruss,et al.  Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid , 1991, Cell.

[87]  F. Myokai,et al.  Expression of the hepatocyte growth factor gene during chick limb development , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[88]  H. Nakamura,et al.  Somites and the pattern formation of trunk muscles: a study in quail-chick chimera. , 1991, Archives of histology and cytology.

[89]  B. Williams,et al.  Determination and morphogenesis in myogenic progenitor cells: an experimental embryological approach. , 2000, Current topics in developmental biology.

[90]  K. Shiota,et al.  Heat shock-induced homeotic transformations of the axial skeleton and associated shifts of Hox gene expression domains in mouse embryos. , 1997, Reproductive toxicology.

[91]  C. Théry,et al.  Expression of HGF/SF, HGF1/MSP, and c-met suggests new functions during early chick development. , 1995, Developmental genetics.

[92]  R. Morgan,et al.  FLASH, a component of the FAS-CAPSASE8 apoptotic pathway, is directly regulated by Hoxb4 in the notochord. , 2004, Developmental biology.

[93]  O. Pourquié,et al.  Control of somite patterning by signals from the lateral plate. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[94]  P. Currie,et al.  Morphogenesis and evolution of vertebrate appendicular muscle , 2001, Journal of anatomy.

[95]  O. Pourquié,et al.  From head to tail: links between the segmentation clock and antero-posterior patterning of the embryo. , 2002, Current opinion in genetics & development.

[96]  V. Rosen,et al.  Gdf11 is a negative regulator of chondrogenesis and myogenesis in the developing chick limb. , 2001, Developmental biology.

[97]  A. Nóvoa,et al.  Hox genes specify vertebral types in the presomitic mesoderm. , 2005, Genes & development.

[98]  R. Harland,et al.  Hypaxial muscle migration during primary myogenesis in Xenopus laevis. , 2001, Developmental biology.

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

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

[101]  A. Der-Avakian,et al.  Targeted disruption of Hoxd9 and Hoxd10 alters locomotor behavior, vertebral identity, and peripheral nervous system development. , 1999, Developmental biology.

[102]  L. Pardanaud,et al.  Manipulation of the angiopoietic/hemangiopoietic commitment in the avian embryo. , 1999, Development.

[103]  A. Lumsden,et al.  Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. , 2003, Developmental cell.

[104]  A. Burke,et al.  Hox genes and morphological identity: axial versus lateral patterning in the vertebrate mesoderm. , 2000, Development.

[105]  P. Rigby,et al.  Transcriptional regulation during somitogenesis. , 2000, Current topics in developmental biology.

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

[107]  O. Medina-Martinez,et al.  A large targeted deletion of Hoxb1-Hoxb9 produces a series of single-segment anterior homeotic transformations. , 2000, Developmental biology.

[108]  R. Maas,et al.  Characterization of Hoxa-10/Hoxa-11 transheterozygotes reveals functional redundancy and regulatory interactions. , 2000, Developmental biology.

[109]  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.

[110]  C. Ordahl,et al.  Dorsoventral axis determination in the somite: a re-examination. , 2000, Development.

[111]  B. Williams,et al.  Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. , 1994, Development.

[112]  O. Pourquié,et al.  Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Joseph C. Pearson,et al.  Modulating Hox gene functions during animal body patterning , 2005, Nature Reviews Genetics.

[114]  C. Tabin,et al.  Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. , 2002, Developmental cell.

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

[116]  R. Krumlauf.  Hox genes in vertebrate development , 1994, Cell.

[117]  H. Suemori,et al.  Hox C cluster genes are dispensable for overall body plan of mouse embryonic development. , 2000, Developmental biology.

[118]  Bernhard G Herrmann,et al.  Segmentation in vertebrates: clock and gradient finally joined. , 2004, Genes & development.

[119]  V. Bautch,et al.  Assembly of trunk and limb blood vessels involves extensive migration and vasculogenesis of somite-derived angioblasts. , 2001, Developmental biology.

[120]  M. Primig,et al.  Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. , 2000, Development.

[121]  Darrell J. R. Evans,et al.  Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[122]  R. Mishra,et al.  "Mir"acles in hox gene regulation. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[123]  R. Ho,et al.  The evolution of paired appendages in vertebrates: T-box genes in the zebrafish , 2000, Development Genes and Evolution.

[124]  A. Burke,et al.  A new view of patterning domains in the vertebrate mesoderm. , 2003, Developmental cell.

[125]  D. Melton,et al.  Endoderm development: from patterning to organogenesis. , 2000, Trends in genetics : TIG.

[126]  Edwin S. Goodrich,et al.  Studies on the Structure and Development of Vertebrates , 1958 .

[127]  B. Thisse,et al.  Evolutionary origins of vertebrate appendicular muscle , 2000, Nature.

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

[129]  Y. Takahashi,et al.  Somitogenesis controlled by Noggin. , 1998, Developmental biology.

[130]  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.

[131]  R. Grainger,et al.  Differential cytokeratin gene expression reveals early dorsal-ventral regionalization in chick mesoderm. , 1990, Development.

[132]  M. Capecchi,et al.  Reversal of Hox1 gene subfunctionalization in the mouse. , 2006, Developmental cell.

[133]  A. Burke,et al.  The lateral somitic frontier: dorso-ventral aspects of anterio-posterior regionalization in avian embryos , 2003, Mechanisms of Development.