FGF receptor signalling is required to maintain neural progenitors during Hensen's node progression

Previous analyses of labelled clones of cells within the developing nervous system of the mouse have indicated that descendants are initially dispersed rostrocaudally followed by more local proliferation, which is consistent with the progressing node's contributing descendants from a resident population of progenitor cells as it advances caudally. Here we electroporated an expression vector encoding green fluorescent protein into the chicken embryo near Hensen's node to test and confirm the pattern inferred in the mouse. This provides a model in which a proliferative stem zone is maintained in the node by a localized signal; those cells that are displaced out of the stem zone go on to contribute to the growing axis. To test whether fibroblast growth factor (FGF) signalling could be involved in the maintenance of the stem zone, we co-electroporated a dominant-negative FGF receptor with a lineage marker, and found that it markedly alters the elongation of the spinal cord primordium. The results indicate that FGF receptor signalling promotes the continuous development of the posterior nervous system by maintaining presumptive neural progenitors in the region near Hensen's node. This offers a potential explanation for the mixed findings on FGF in the growth and patterning of the embryonic axis.

[1]  R. Harland,et al.  Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. , 1995, Development.

[2]  T Yamada,et al.  Caudalization by the amphibian organizer: brachyury, convergent extension and retinoic acid. , 1994, Development.

[3]  J. Shih,et al.  The cellular basis of the convergence and extension of the Xenopus neural plate , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  F M Watt,et al.  Out of Eden: stem cells and their niches. , 2000, Science.

[5]  J. Slack,et al.  eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. , 1996, Development.

[6]  C. Kimmel,et al.  Cell cycles and clonal strings during formation of the zebrafish central nervous system. , 1994, Development.

[7]  M. Stark,et al.  Timing and cell interactions underlying neural induction in the chick embryo. , 1999, Development.

[8]  J. Slack,et al.  The role of fibroblast growth factors in early Xenopus development. , 1994, Biochemical Society symposium.

[9]  S. Fraser,et al.  Specification of the hindbrain fate in the zebrafish. , 1998, Developmental biology.

[10]  R. Beddington.  Induction of a second neural axis by the mouse node. , 1994, Development.

[11]  W. S. Miller.  The blood and lymph vessels of the lung of necturus maculatus , 1905 .

[12]  S. Fraser,et al.  Specification of the zebrafish nervous system by nonaxial signals. , 1997, Science.

[13]  P. Tam,et al.  Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. , 1999, Developmental biology.

[14]  R. Beddington,et al.  Axis Development and Early Asymmetry in Mammals , 1999, Cell.

[15]  T. Bouwmeester,et al.  Vertebrate head induction by anterior primitive endoderm , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

[16]  L. Niswander,et al.  Requirement for BMP Signaling in Interdigital Apoptosis and Scale Formation , 1996, Science.

[17]  S. Sokol,et al.  FGF is required for posterior neural patterning but not for neural induction. , 1999, Developmental biology.

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

[19]  L. Mathis,et al.  Different clonal dispersion in the rostral and caudal mouse central nervous system. , 2000, Development.

[20]  K. Storey,et al.  Axial mesendoderm refines rostrocaudal pattern in the chick nervous system. , 1999, Development.

[21]  I. Álvarez,et al.  Patterns of neurepithelial cell rearrangement during avian neurulation are determined prior to notochordal inductive interactions. , 1991, Developmental Biology.

[22]  T. Doniach.  Basic FGF as an inducer of anteroposterior neural pattern , 1995, Cell.

[23]  Y. Hatada,et al.  A fate map of the epiblast of the early chick embryo. , 1994, Development.

[24]  R. Keller,et al.  Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. , 1988, Development.

[25]  S. Fraser,et al.  Neural crest cell dynamics revealed by time-lapse video microscopy of whole embryo chick explant cultures. , 1998, Developmental biology.

[26]  J. Rossant,et al.  Expression of the fibroblast growth factor receptor FGFR-1/flg during gastrulation and segmentation in the mouse embryo. , 1992, Developmental biology.

[27]  H. Okamoto,et al.  bFGF as a possible morphogen for the anteroposterior axis of the central nervous system in Xenopus. , 1995, Development.

[28]  Scott E. Fraser,et al.  Imaging Cells in the Developing Nervous System with Retrovirus Expressing Modified Green Fluorescent Protein , 1999, Experimental Neurology.

[29]  T. Mizuno,et al.  Initial anteroposterior pattern of the zebrafish central nervous system is determined by differential competence of the epiblast. , 1998, Development.

[30]  C. M. Sargent,et al.  Early posterior neural tissue is induced by FGF in the chick embryo. , 1998, Development.

[31]  P. Charnay,et al.  Successive patterns of clonal cell dispersion in relation to neuromeric subdivision in the mouse neuroepithelium. , 1999, Development.

[32]  E. Sanders,et al.  Formation and Differentiation of Early Embryonic Mesoderm , 1992, NATO ASI Series.

[33]  Andrew Lumsden,et al.  Patterning the Vertebrate Neuraxis , 1996, Science.

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

[35]  J. Yates,et al.  Stable replication of plasmids derived from Epstein–Barr virus in various mammalian cells , 1985, Nature.

[36]  I. Álvarez,et al.  Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. , 1989, Development.

[37]  E. D. De Robertis,et al.  A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls. , 1996, Development.

[38]  R. Krumlauf,et al.  ‘Shocking’ developments in chick embryology: electroporation and in ovo gene expression , 1999, Nature Cell Biology.

[39]  A. Hemmati-Brivanlou,et al.  Caudalization of neural fate by tissue recombination and bFGF. , 1995, Development.

[40]  J. Shih,et al.  Planar induction of convergence and extension of the neural plate by the organizer of Xenopus , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  G. Schoenwolf.  Observations on closure of the neuropores in the chick embryo. , 1979, The American journal of anatomy.

[42]  W. Harris,et al.  Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. , 1990, Journal of neurobiology.

[43]  W. Saurin,et al.  Evidence in the mouse for self-renewing stem cells in the formation of a segmented longitudinal structure, the myotome. , 1996, Development.

[44]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[45]  K. Kroll,et al.  Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. , 1996, Development.

[46]  K. Storey,et al.  A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates , 2000, Current Biology.

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

[48]  C. Stern,et al.  Fates and migratory routes of primitive streak cells in the chick embryo. , 1996, Development.

[49]  H. Ueno,et al.  A truncated form of fibroblast growth factor receptor 1 inhibits signal transduction by multiple types of fibroblast growth factor receptor. , 1992, The Journal of biological chemistry.

[50]  C. Stern,et al.  Evidence for Stem Cells in the Mesoderm of Hensen’s Node and Their Role in Embryonic Pattern Formation , 1992 .

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

[52]  A. Durston,et al.  Neural induction and patterning in embryos deficient in FGF signaling. , 1997, The International journal of developmental biology.

[53]  M. Kirschner,et al.  Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in xenopus embryos , 1991, Cell.

[54]  S. Fraser,et al.  In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. , 2000, Development.

[55]  J H Lewis,et al.  cash4, a novel achaete-scute homolog induced by Hensen's node during generation of the posterior nervous system. , 1997, Genes & development.