Primary body axes of vertebrates: Generation of a near‐Cartesian coordinate system and the role of Spemann‐type organizer

A rationale for the complex‐appearing generation of the primary body axes in vertebrates can be obtained if this process is divided into two parts. First, an ancestral system is responsible for the anteroposterior (AP) patterning of the brain and the positioning of the heart. The blastopore (marginal zone) acts as a source region that generates primary AP‐positional information for the brain, a process that is largely independent of the organizer. This evolutionary old system was once organizing the single axis of radial–symmetric ancestors. Second, the trunk is assumed to be an evolutionary later addition. The AP organization of the trunk depends on a time‐controlled posterior transformation in which an oscillation plays a crucial role. This oscillation also leads to the repetitive nature of the trunk pattern as seen in somites or segments. The function of the Spemann‐type organizer is not to specify the dorsoventral (DV) positional information directly but to initiate the formation of a stripe‐shaped midline organizer, realized with different structures in the brain and in the trunk (prechordal plate vs. notochord). The distance of the cells to this midline (rather than to the organizer) is crucial for the DV specification. The basically different modes of axes formation in vertebrates and insects is proposed to have their origin in the initial positioning of the mesoderm. Only in vertebrates the mesoderm is initiated in a ring at a posterior position. Thus, only in vertebrates complex tissue movements are required to transform the ring‐shaped posterior mesoderm into the rod‐shaped axial structures. Developmental Dynamics 235:2907–2919, 2006. © 2006 Wiley‐Liss, Inc.

[1]  S. Roth,et al.  Dorsoventral Axis Formation in the Drosophila Embryo—Shaping and Transducing a Morphogen Gradient , 2005, Current Biology.

[2]  Robert A. Drewell,et al.  Transcription defines the embryonic domains of cis-regulatory activity at the Drosophila bithorax complex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Niehrs Regionally specific induction by the Spemann–Mangold organizer , 2004, Nature Reviews Genetics.

[4]  Wolfgang Driever,et al.  Repressor activity of Headless/Tcf3 is essential for vertebrate head formation , 2000, Nature.

[5]  J. Gerhart Changing the axis changes the perspective , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[6]  A. Glinka,et al.  The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning. , 2000, Development.

[7]  M. Sheets,et al.  Heading in a new direction: implications of the revised fate map for understanding Xenopus laevis development. , 2006, Developmental biology.

[8]  C. Niehrs,et al.  An ancient Wnt-Dickkopf antagonism in Hydra , 2006, Development.

[9]  Jacqueline Deschamps,et al.  Head-tail patterning of the vertebrate embryo: one, two or many unresolved problems? , 2006, The International journal of developmental biology.

[10]  H. Spemann,et al.  Über den Anteil von Implantat und Wirtskeim an der Orientierung und Beschaffenheit der induzierten Embryonalanlage , 1931, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

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

[12]  R. Krumlauf,et al.  Initiation of Rhombomeric Hoxb4 Expression Requires Induction by Somites and a Retinoid Pathway , 1998, Neuron.

[13]  L. Solnica-Krezel Conserved Patterns of Cell Movements during Vertebrate Gastrulation , 2005, Current Biology.

[14]  H. Reichert,et al.  An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila , 2003, Development.

[15]  William C. Smith,et al.  Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos , 1992, Cell.

[16]  A. Durston,et al.  The initiation of Hox gene expression in Xenopus laevis is controlled by Brachyury and BMP-4. , 2004, Developmental biology.

[17]  C. Niehrs,et al.  The role of prechordal mesendoderm in neural patterning , 2001, Current Opinion in Neurobiology.

[18]  H. Bode,et al.  Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra. , 1999, Development.

[19]  E. Robertis,et al.  Embryonic Dorsal-Ventral Signaling: Secreted Frizzled-Related Proteins as Inhibitors of Tolloid Proteinases , 2006, Cell.

[20]  W. Talbot,et al.  Nodal signaling patterns the organizer. , 2000, Development.

[21]  T. Lints,et al.  XNkx-2.5, a Xenopus gene related to Nkx-2.5 and tinman: evidence for a conserved role in cardiac development. , 1994, Developmental biology.

[22]  F. Luyten,et al.  Frzb, a Secreted Protein Expressed in the Spemann Organizer, Binds and Inhibits Wnt-8 , 1997, Cell.

[23]  J. van Nes,et al.  Developmental regulation of the Hox genes during axial morphogenesis in the mouse , 2005, Development.

[24]  E. Robertis,et al.  Regulation of ADMP and BMP2/4/7 at Opposite Embryonic Poles Generates a Self-Regulating Morphogenetic Field , 2005, Cell.

[25]  D. Arendt,et al.  Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs , 1999, Mechanisms of Development.

[26]  R. Moon,et al.  Two tcf3 genes cooperate to pattern the zebrafish brain , 2003, Development.

[27]  Ethel Nicholson Browne,et al.  The production of new hydranths in Hydra by the insertion of small grafts , 1909 .

[28]  S P Allen,et al.  Somite number and vertebrate evolution. , 1998, Development.

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

[30]  H. Reichert,et al.  The urbilaterian brain: developmental insights into the evolutionary origin of the brain in insects and vertebrates. , 2003, Arthropod structure & development.

[31]  G. Schoenwolf,et al.  De novo induction of the organizer and formation of the primitive streak in an experimental model of notochord reconstitution in avian embryos. , 1998, Development.

[32]  C. Stern Initial patterning of the central nervous system: How many organizers? , 2001, Nature Reviews Neuroscience.

[33]  J. Gerhart,et al.  Planar induction of anteroposterior pattern in the developing central nervous system of Xenopus laevis. , 1992, Science.

[34]  C. Kimmel,et al.  Origin and organization of the zebrafish fate map. , 1990, Development.

[35]  B. Thisse,et al.  The molecular nature of the zebrafish tail organizer , 2003, Nature.

[36]  M. Oelgeschläger,et al.  The establishment of spemann's organizer and patterning of the vertebrate embryo , 2000, Nature Reviews Genetics.

[37]  E. Lander,et al.  Anteroposterior Patterning in Hemichordates and the Origins of the Chordate Nervous System , 2003, Cell.

[38]  W. Driever,et al.  Axis-inducing activities and cell fates of the zebrafish organizer. , 2000, Development.

[39]  M. Maden Retinoid signalling in the development of the central nervous system , 2002, Nature Reviews Neuroscience.

[40]  S. Fraser,et al.  Order and coherence in the fate map of the zebrafish nervous system. , 1995, Development.

[41]  E. Sánchez-Herrero,et al.  Genetic and molecular characterization of a novel iab-8 regulatory domain in the Abdominal-B gene of Drosophila melanogaster. , 2002, Development.

[42]  C. Niehrs,et al.  Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction , 1998, Nature.

[43]  C. Waddington,et al.  Studies on the Nature of the Amphibian Organization Centre. III.--The Activation of the Evocator , 1936 .

[44]  A. R. I. Altaba Planar and vertical signals in the induction and patterning of the Xenopus nervous system , 1992 .

[45]  Ken W. Y. Cho,et al.  Interaction of goosecoid and brachyury in Xenopus mesoderm patterning , 1997, Mechanisms of Development.

[46]  H. Meinhardt Models of biological pattern formation , 1982 .

[47]  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.

[48]  S. Gaunt,et al.  Temporal colinearity in expression of anterior hox genes in developing chick embryos , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[49]  D. Duboule,et al.  Organizing Axes in Time and Space; 25 Years of Colinear Tinkering , 2003, Science.

[50]  Lewis Wolpert,et al.  Principles of Development , 1997 .

[51]  H. Meinhardt,et al.  Pattern formation by local self-activation and lateral inhibition. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[52]  L. Gräper Die Primitiventwicklung des Hühnchens nach stereokinematographischen Untersuchungen, kontrolliert durch vitale Farbmarkierung und verglichen mit der Entwicklung anderer Wirbeltiere , 1929, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[53]  Christian Wehrle,et al.  Wnt3a plays a major role in the segmentation clock controlling somitogenesis. , 2003, Developmental cell.

[54]  M. Maden Retinoic acid and limb regeneration--a personal view. , 2002, The International journal of developmental biology.

[55]  P. Nieuwkoop The formation of the mesoderm in urodelean amphibians VI. The self-organizing capacity of the induced meso-endoderm , 1992, Roux's archives of developmental biology.

[56]  Kentaro Kato,et al.  Expression of a novel aristaless related homeobox gene ‘Arx’ in the vertebrate telencephalon, diencephalon and floor plate , 1997, Mechanisms of Development.

[57]  A. Lumsden Segmentation and compartition in the early avian hindbrain , 2004, Mechanisms of Development.

[58]  E. D. De Robertis,et al.  Dorsal-ventral patterning and neural induction in Xenopus embryos. , 2004, Annual review of cell and developmental biology.

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

[60]  P. Nieuwkoop Activation and organization of the central nervous system in amphibians. Part II. Differentiation and organization , 1952 .

[61]  E. D. De Robertis,et al.  Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos , 2005, Development.

[62]  Hans Clevers,et al.  XTcf-3 Transcription Factor Mediates β-Catenin-Induced Axis Formation in Xenopus Embryos , 1996, Cell.

[63]  R. Moon,et al.  Wnt signaling: why is everything so negative? , 1998, Current opinion in cell biology.

[64]  M. D. Stokes,et al.  Three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) associated with the tail bud: the evolution of somitogenesis in chordates. , 2001, Developmental biology.

[65]  D. Kessler,et al.  Goosecoid promotes head organizer activity by direct repression of Xwnt8 in Spemann's organizer. , 2001, Development.

[66]  C. Niehrs,et al.  A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. , 2001, Development.

[67]  H. Meinhardt Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. , 1989, Development.

[68]  Hans Meinhardt,et al.  Different strategies for midline formation in bilaterians , 2004, Nature Reviews Neuroscience.

[69]  M. Kessel,et al.  The avian organizer. , 2001, The International journal of developmental biology.

[70]  M. Sheets,et al.  Rethinking axial patterning in amphibians , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[71]  B. Gumbiner,et al.  Induction of the primary dorsalizing center in Xenopus by the Wnt/GSK/beta-catenin signaling pathway, but not by Vg1, Activin or Noggin. , 1997, Development.

[72]  T. Bouwmeester,et al.  Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer , 1996, Nature.

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

[74]  J. Cooke,et al.  The chick Brachyury gene: developmental expression pattern and response to axial induction by localized activin. , 1995, Developmental biology.

[75]  Hans Meinhardt,et al.  The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[76]  A. Schier,et al.  Lefty Proteins Are Long-Range Inhibitors of Squint-Mediated Nodal Signaling , 2002, Current Biology.

[77]  H. Spemann,et al.  über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren , 1924, Archiv für mikroskopische Anatomie und Entwicklungsmechanik.

[78]  H. Bode,et al.  HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. , 2000, Development.

[79]  C. Niehrs,et al.  Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus , 1997, Nature.

[80]  P. Nieuwkoop,et al.  The formation of the mesoderm in urodelean amphibians , 1973, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[81]  B. Schierwater,et al.  Axial Patterning and Diversification in the Cnidaria Predate the Hox System , 2006, Current Biology.

[82]  H. Haas,et al.  Integrative mechanisms in development of the early chick blastoderm. I. Regulative potentiality of separated parts , 1960 .

[83]  Christoph M. Happel,et al.  WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra , 2000, Nature.

[84]  M. Martindale The evolution of metazoan axial properties , 2005, Nature Reviews Genetics.

[85]  T. Jessell,et al.  Progressive induction of caudal neural character by graded Wnt signaling , 2002, Nature Neuroscience.

[86]  H. Meinhardt,et al.  Organizer and axes formation as a self-organizing process. , 2001, The International journal of developmental biology.

[87]  G. Schoenwolf,et al.  Getting organized: new insights into the organizer of higher vertebrates. , 1998, Current topics in developmental biology.

[88]  L. Holland,et al.  Developmental expression of AmphiWnt1, an amphioxus gene in the Wnt1/wingless subfamily , 2000, Development Genes and Evolution.

[89]  E. Ober,et al.  Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish. , 1999, Developmental biology.

[90]  H. Meinhardt,et al.  Space-dependent cell determination under the control of morphogen gradient. , 1978, Journal of theoretical biology.

[91]  P. Tam,et al.  Anterior patterning by synergistic activity of the early gastrula organizer and the anterior germ layer tissues of the mouse embryo. , 1999, Development.

[92]  M. Schummer,et al.  Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Z. Lele,et al.  Zebrafish admp is required to restrict the size of the organizer and to promote posterior and ventral development , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[94]  H. Oda,et al.  Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning , 2006, Development.

[95]  R. Beddington,et al.  Anterior patterning in mouse. , 1998, Trends in genetics : TIG.

[96]  T. Hirano,et al.  Zebrafish Dkk1 functions in forebrain specification and axial mesendoderm formation. , 2000, Developmental biology.

[97]  Tadahiro Iimura,et al.  Onset of the segmentation clock in the chick embryo: evidence for oscillations in the somite precursors in the primitive streak. , 2002, Development.

[98]  M. Kessel,et al.  Gastrulation and homeobox genes in chick embryos , 1997, Mechanisms of Development.

[99]  Alexander F Schier,et al.  Molecular genetics of axis formation in zebrafish. , 2005, Annual review of genetics.

[100]  C. Niehrs,et al.  Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. , 1997, Development.

[101]  P. Nieuwkoop,et al.  Activation and organization of the central nervous system in amphibians. Part III. Synthesis of a new working hypothesis , 1952 .

[102]  Elliot M. Meyerowitz,et al.  MscS-like Proteins Control Plastid Size and Shape in Arabidopsis thaliana , 2006, Current Biology.

[103]  H. Bode,et al.  HyBra1, a Brachyury homologue, acts during head formation in Hydra. , 1999, Development.

[104]  H. Bode,et al.  CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. , 1996, Developmental biology.

[105]  Hiroshi Shimizu,et al.  Peduncle of Hydra and the heart of higher organisms share a common ancestral origin , 2003, Genesis.

[106]  L. Holland,et al.  Nuclear β‐catenin promotes non‐neural ectoderm and posterior cell fates in amphioxus embryos , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[107]  M. Sieweke,et al.  Defined concentrations of a posteriorizing signal are critical for MafB/Kreisler segmental expression in the hindbrain. , 1998, Development.

[108]  H. Bode,et al.  CnOtx, a member of the Otx gene family, has a role in cell movement in hydra. , 1999, Developmental biology.

[109]  H. Oda,et al.  Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells , 2003, Development.

[110]  M. Krinks,et al.  Anti-dorsalizing morphogenetic protein is a novel TGF-beta homolog expressed in the Spemann organizer. , 1995, Development.

[111]  Cornelis J Weijer,et al.  Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. , 2002, Developmental cell.

[112]  Allan Bradley,et al.  Requirement for Wnt3 in vertebrate axis formation , 1999, Nature Genetics.

[113]  Denis Duboule,et al.  Localized and Transient Transcription of Hox Genes Suggests a Link between Patterning and the Segmentation Clock , 2001, Cell.

[114]  A. Brivanlou,et al.  Early posterior/ventral fate specification in the vertebrate embryo. , 2001, Developmental biology.

[115]  Ray Keller,et al.  Cell migration during gastrulation. , 2005, Current opinion in cell biology.

[116]  M. Kessel,et al.  Nuclear beta-catenin and the development of bilateral symmetry in normal and LiCl-exposed chick embryos. , 1999, Development.

[117]  D. Arendt,et al.  Inversion of dorsoventral axis? , 1994, Nature.

[118]  L. Davidson,et al.  BMP antagonism by Spemann's organizer regulates rostral-caudal fate of mesoderm. , 2004, Developmental biology.

[119]  Hans Meinhardt,et al.  Models of Segmentation , 1986 .

[120]  J. Gerhart,et al.  Formation and function of Spemann's organizer. , 1997, Annual review of cell and developmental biology.

[121]  H. Lenhoff Ethel Browne, Hans Spemann, and the Discovery of the Organizer Phenomenon. , 1991, The Biological bulletin.

[122]  R. Moon,et al.  Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. , 1993, Genes & development.