A role for SOX 1 in neural determination

l In vertebrates, the delineation of the neural plate from a region of the primitive ectoderm is accompanied by the onset of specific gene expression which in turn promotes the formation of the nervous system. Here we show that SOX1, an HMG-box protein related to SRY, is one of the earliest transcription factors to be expressed in ectodermal cells committed to the neural fate: the onset of expression of SOX1 appears to coincide with the induction of neural ectoderm. We demonstrate a role for SOX1 in neural determination and differentiation using an inducible expression P19 cell system as an in vitro model of neurogenesis. Misexpression of SOX1 can substitute for the requirement of retinoic acid to impart neural fate to competent ectodermal P19 cells. Using a series of antigenic markers which identify early neural cell types in combination with BrdU labeling, we demonstrate a temporal and spatial correlation between the differentiation of cell types along the dorsoventral axis of the neural tube and the downregulation of SOX1 expression. SOX1, therefore, defines the dividing neural precursors of the embryonic central nervous system (CNS).

[1]  R. Lovell-Badge,et al.  Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. , 1998, Genes & development.

[2]  C. Hudson,et al.  Xsox17α and -β Mediate Endoderm Formation in Xenopus , 1997, Cell.

[3]  P. Sharpe,et al.  Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue , 1997, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  R. Lovell-Badge,et al.  Sox genes find their feet. , 1997, Current opinion in genetics & development.

[5]  R. Lovell-Badge,et al.  Preventing the loss of competence for neural induction: HGF/SF, L5 and Sox-2. , 1997, Development.

[6]  Donald M. Bell,et al.  SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. , 1997, Developmental biology.

[7]  R. Kageyama,et al.  Conversion of ectoderm into a neural fate by ATH‐3, a vertebrate basic helix–loop–helix gene homologous to Drosophila proneural gene atonal , 1997, The EMBO journal.

[8]  David J. Anderson,et al.  X-MyT1, a Xenopus C2HC-Type Zinc Finger Protein with a Regulatory Function in Neuronal Differentiation , 1996, Cell.

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

[10]  Johan Ericson,et al.  Two Critical Periods of Sonic Hedgehog Signaling Required for the Specification of Motor Neuron Identity , 1996, Cell.

[11]  T. Jessell,et al.  Diversity and Pattern in the Developing Spinal Cord , 1996, Science.

[12]  M. Ashburner,et al.  The Dichaete gene of Drosophila melanogaster encodes a SOX-domain protein required for embryonic segmentation. , 1996, Development.

[13]  J. Nambu,et al.  The Drosophila fish-hook gene encodes a HMG domain protein essential for segmentation and CNS development. , 1996, Development.

[14]  David J. Anderson,et al.  Identification of neurogenin, a Vertebrate Neuronal Determination Gene , 1996, Cell.

[15]  S. Vriz,et al.  Zygotic expression of the zebrafish Sox-19, an HMG box-containing gene, suggests an involvement in central nervous system development. , 1996, Brain research. Molecular brain research.

[16]  M. Segal,et al.  Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro , 1996, Mechanisms of Development.

[17]  P. Goodfellow,et al.  Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds , 1996, Nature Genetics.

[18]  A. Sinclair,et al.  A male-specific role for SOX9 in vertebrate sex determination. , 1996, Development.

[19]  P. Tam,et al.  The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. , 1996, Developmental biology.

[20]  A. Chitnis,et al.  Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos. , 1996, Development.

[21]  Gerd Scherer,et al.  Sex reversal by loss of the C–terminal transactivation domain of human SOX9 , 1996, Nature Genetics.

[22]  Y. Kanai,et al.  Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis , 1996, The Journal of cell biology.

[23]  A. Cumano,et al.  Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4 , 1996, Nature.

[24]  P. Goodfellow,et al.  A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. , 1996, Development.

[25]  T. Jessell,et al.  Requirement for LIM Homeobox Gene Isl1 in Motor Neuron Generation Reveals a Motor Neuron– Dependent Step in Interneuron Differentiation , 1996, Cell.

[26]  R. Lovell-Badge,et al.  The molecular genetics of Sry and its role in mammalian sex determination. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  J. W. Foster,et al.  Mutations in SOX9, the gene responsible for Campomelic dysplasia and autosomal sex reversal. , 1995, American journal of human genetics.

[28]  N. Corbi,et al.  Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. , 1995, Genes & development.

[29]  S. Mcconnell,et al.  Constructing the cerebral cortex: Neurogenesis and fate determination , 1995, Neuron.

[30]  R. Lovell-Badge,et al.  The genes for a spliceosome protein (SAP62) and the anti-Müllerian hormone (AMH) are contiguous. , 1995, Human molecular genetics.

[31]  David A. Case,et al.  Structural basis for DNA bending by the architectural transcription factor LEF-1 , 1995, Nature.

[32]  G. Muscat,et al.  Trans-activation and DNA-binding properties of the transcription factor, Sox-18. , 1995, Nucleic acids research.

[33]  R. Lovell-Badge,et al.  Involvement of SOX proteins in lens‐specific activation of crystallin genes. , 1995, The EMBO journal.

[34]  A. Gronenborn,et al.  Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex , 1995, Cell.

[35]  H. Weintraub,et al.  Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. , 1995, Science.

[36]  D. Gottlieb,et al.  Embryonic stem cells express neuronal properties in vitro. , 1995, Developmental biology.

[37]  R. Lovell-Badge,et al.  The zebrafish Zf-Sox 19 protein: a novel member of the Sox family which reveals highly conserved motifs outside of the DNA-binding domain. , 1995, Gene.

[38]  E. Cartwright,et al.  Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development , 1995, Mechanisms of Development.

[39]  Sahar Mansour,et al.  Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene , 1994, Nature.

[40]  W. Harris,et al.  XASH genes promote neurogenesis in Xenopus embryos. , 1994, Development.

[41]  R. Harland.  Neural induction in Xenopus. , 1994, Current opinion in genetics & development.

[42]  P. Goodfellow,et al.  Definition of a consensus DNA binding site for SRY. , 1994, Nucleic acids research.

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

[44]  P. Tam,et al.  Gastrulation in the mouse embryo: Ultrastructural and molecular aspects of germ layer morphogenesis , 1993, Microscopy research and technique.

[45]  H. Clevers,et al.  Sox‐4, an Sry‐like HMG box protein, is a transcriptional activator in lymphocytes. , 1993, The EMBO journal.

[46]  J. Campos-Ortega.  Mechanisms of early neurogenesis in Drosophila melanogaster. , 1993, Journal of neurobiology.

[47]  Peter Goodfellow,et al.  Circular transcripts of the testis-determining gene Sry in adult mouse testis , 1993, Cell.

[48]  H C Clevers,et al.  The murine Sox-4 protein is encoded on a single exon. , 1993, Nucleic acids research.

[49]  M. McBurney,et al.  P19 embryonal carcinoma cells. , 1993, The International journal of developmental biology.

[50]  P. Koopman,et al.  Seven new members of the Sox gene family expressed during mouse development. , 1993, Nucleic acids research.

[51]  P. Sharpe,et al.  PCR amplification of SRY-related gene sequences reveals evolutionary conservation of the SRY-box motif. , 1993, PCR methods and applications.

[52]  P N Goodfellow,et al.  SRY, like HMG1, recognizes sharp angles in DNA. , 1992, The EMBO journal.

[53]  H. Clevers,et al.  Sequence‐specific interaction of the HMG box proteins TCF‐1 and SRY occurs within the minor groove of a Watson‐Crick double helix. , 1992, The EMBO journal.

[54]  A. Ashworth,et al.  A conserved family of genes related to the testis determining gene, SRY. , 1992, Nucleic acids research.

[55]  Rudolf Grosschedl,et al.  The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures , 1992, Cell.

[56]  E. D. De Robertis,et al.  Neural induction and regionalisation in the chick embryo. , 1992, Development.

[57]  R. Pedersen,et al.  Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. , 1991, Development.

[58]  S. Mcconnell,et al.  Cell cycle dependence of laminar determination in developing neocortex , 1991 .

[59]  T. Jessell,et al.  Control of cell pattern in the developing nervous system: Polarizing activity of the floor plate and notochord , 1991, Cell.

[60]  Robin Lovell-Badge,et al.  A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif , 1990, Nature.

[61]  Peter Goodfellow,et al.  A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes , 1990, Nature.

[62]  R. McKay.  The origins of cellular diversity in the mammalian central nervous system , 1989, Cell.

[63]  J. Craig,et al.  The int-1 proto-oncogene is transcriptionally activated during neuroectodermal differentiation of P19 mouse embryonal carcinoma cells. , 1989, Oncogene.

[64]  P. Gruss,et al.  Expression of homeobox gene Hox 1.1 during mouse embryogenesis. , 1988, Development.

[65]  J. Campos-Ortega.  Genetics of early neurogenesis in Drosophila melanogaster , 1985, Trends in Neurosciences.

[66]  J. Altman,et al.  The development of the rat spinal cord. , 1984, Advances in anatomy, embryology, and cell biology.

[67]  M. McBurney,et al.  Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells , 1982, The Journal of cell biology.

[68]  R. Poelmann.  Differential mitosis and degeneration patterns in relation to the alterations in the shape of the embryonic ectoderm of early post-implantation mouse embryos. , 1980, Journal of embryology and experimental morphology.

[69]  M. Snow.  Gastrulation in the mouse: Growth and regionalization of the epiblast , 1977 .

[70]  S. Fujita.  The matrix cell and cytogenesis in the developing central nervous system , 1963, The Journal of comparative neurology.

[71]  F. C. Sauer.  Mitosis in the neural tube , 1935 .

[72]  Parsons Mj.  Functional analysis of Sox3 : an x-linked, sry related gene. , 1997 .

[73]  Andy Greenfield,et al.  The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos , 1995, Nature Genetics.

[74]  P. Tam,et al.  Neuroectodermal fate of epiblast cells in the distal region of the mouse egg cylinder: implication for body plan organization during early embryogenesis. , 1995, Development.

[75]  A. Ruiz i Altaba.  Pattern formation in the vertebrate neural plate. , 1994, Trends in neurosciences.

[76]  T. Jessell,et al.  Induction of floor plate differentiation by contact-dependent, homeogenetic signals. , 1993, Development.

[77]  T. Saito,et al.  Induction and repression of mammalian achaete-scute homologue (MASH) gene expression during neuronal differentiation of P19 embryonal carcinoma cells. , 1992, Development.