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JOURNAL ARTICLES
Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord
M.D. Goulding, A. Lumsden, P. Gruss
Development 1993 117: 1001-1016;

Summary

Members of the paired box (Pax) gene family are expressed in discrete regions of the developing central nervous system, suggesting a role in neural patterning. In this study, we describe the isolation of the chicken homologues of Pax-3 and Pax-6. Both genes are very highly conserved and share extensive homology with the mouse Pax-3 and Pax-6 genes. Pax-3 is expressed in the primitive streak and in two bands of cells at the lateral extremity of the neural plate. In the spinal cord, Pax-6 is expressed later than Pax-3 with the first detectable expression preceding closure of the neural tube. When the neural tube closes, transcripts of both genes become dorsoventrally restricted in the undifferentiated mitotic neuroepithelium. We show that the removal of the notochord, or implantation of an additional notochord, dramatically alter the dorsoventral (DV) expression patterns of Pax-3 and Pax-6. These manipulations suggest that signals from the notochord and floor plate regulate the establishment of the dorsoventrally restricted expression domains of Pax-3 and Pax-6 in the spinal cord. The rapid changes to Pax gene expression that occur in neural progenitor cells following the grafting of an ectopic notochord suggest that changes to Pax gene expression are an early effect of the notochord on spinal cord patterning.

REFERENCES

    1. Adams B.,
    2. Doefler P.,
    3. Aguzzi A.,
    4. Kozmik Z.,
    5. Urbanek P.,
    6. Maurer-Fogy I.,
    7. Busslinger M.
    (1992) Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS and adult testis. Genes Dev 6, 1589–1607
    OpenUrlAbstract/FREE Full Text
    1. Anderson D.
    (1989) The neural crest lineage problem: neuropoeisis?. Neuron 3, 1–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Auerbach R.
    (1954) Analysis of the the developmental effects of a lethal mutation in the house mouse. J. Exp. Zool 127, 305–329
    OpenUrlCrossRefWeb of Science
    1. Balling R.,
    2. Deutsch U.,
    3. Gruss P.
    (1988) Undulated, a mutation affecting the development of the mouse skeleton, has a point mutation in the paired box of Pax-1. Cell 55, 531–535
    OpenUrlCrossRefPubMedWeb of Science
    1. Burns F. R.,
    2. von Kannen S.,
    3. Guy L.,
    4. Raper J. A.,
    5. Kamholz J.,
    6. Chang S.
    (1991) DM-GRASP, a novel immunoglobulin superfamily axonal surface protein that supports neurite extension. Neuron 7, 209–220
    OpenUrlCrossRefPubMedWeb of Science
    1. Burri M.,
    2. Tromvoukis Y.,
    3. Bopp D.,
    4. Frigerio G.,
    5. Noll M.
    (1989) Conservation of the paired domain in metazoans and its structure in three isolated human genes. EMBO J 8, 1183–1190
    OpenUrlPubMedWeb of Science
    1. Chalepakis G.,
    2. Fritsch R.,
    3. Fickenscher H.,
    4. Deutsch U.,
    5. Goulding M.,
    6. Gruss P.
    (1991) The molecular basis of the undulated/Pax-1 mutation. Cell 66, 873–884
    OpenUrlCrossRefPubMedWeb of Science
    1. Charlebois T. S.,
    2. Spencer D. H.,
    3. Tarkington S. K.,
    4. Henry J. J.,
    5. Grainger R. M.
    (1990) Isolation of a chick cytokeratin cDNA clone indicative of regional specialization in early embryonic ectoderm. Development 108, 33–45
    OpenUrlAbstract
    1. Clarke J. D. W.,
    2. Holder N.,
    3. Soffe S. R.,
    4. Storm-Mathisen J.
    (1991) Neuro-anatomical and functional analysis of neural tube formation in notochordless Xenopus embryos; laterality of ventral spinal cord is lost. Development 112, 499–516
    OpenUrlAbstract
    1. Deutsch U.,
    2. Dressler G. R.,
    3. Gruss P.
    (1988) Pax-1, a member of a paired box homologous murine gene family is expressed in segmenting structures during development. Cell 53, 617–625
    OpenUrlCrossRefPubMedWeb of Science
    1. Dodd J.,
    2. Morton S. B.,
    3. Karagogeos D.,
    4. Yamamoto M.,
    5. Jessell T. M.
    (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1, 105–116
    OpenUrlCrossRefPubMedWeb of Science
    1. Epstein D. J.,
    2. Vekemans M.,
    3. Gros P.
    (1991) Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67, 767–774
    OpenUrlCrossRefPubMedWeb of Science
    1. Ericson J.,
    2. Thor S.,
    3. Edlund T.,
    4. Jessell T. M.,
    5. Yamada T.
    (1992) Early stages of motor neuron differentiation revealed by expression of homoeobox gene Islet-1. Science 256, 1555–1560
    OpenUrlAbstract/FREE Full Text
    1. Goulding M. D.,
    2. Chalepakis G.,
    3. Deutsch U.,
    4. Erselius J. R.,
    5. Gruss P.
    (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10, 5–.
    OpenUrl
    1. Gruneburg H.
    (1950) Genetical studies on the skeleton of the mouse II. Undulated and its modifiers. J. Genet 52, 142–173
    OpenUrl
    1. Hamburger V.
    (1948) The mitotic patterns in the spinal cord of the chickembryo and their relationship to histogenic processes. J. Comp. Neurol 88, 221–284
    OpenUrlCrossRef
    1. Hamburger V.,
    2. Hamilton H.
    (1951) A series of normal stages in the development of the chick embryo. J. Morph 88, 49–92
    OpenUrlCrossRefWeb of Science
    1. Hill R. E.,
    2. Favor J.,
    3. Hogan B. L. M.,
    4. Ton C. C.,
    5. Saunders G. F.,
    6. Hanson I. M.,
    7. Prosser J.,
    8. Jordan T.,
    9. Hastie N. D.,
    10. van Heyningen V.
    (1991) Mouse Small eye results from mutations in a paired-like homoeobox-containing gene. Nature 354, 522–525
    OpenUrlCrossRefPubMed
    1. Hogan B. L. M.,
    2. Horsburgh G.,
    3. Cohen J.,
    4. Hetherington C. M.,
    5. Fischer G.,
    6. Lyon M.
    (1986) Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J. Embryol. Exp. Morph 97, 95–110
    OpenUrlPubMedWeb of Science
    1. Holley J. A.
    (1982) Early development of the circumferential axonal pathway in mouse and chick spinal cord. J. Comp. Neurol 205, 371–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Hollyday M.,
    2. Hamburger V.
    (1977) An autoradiographic study of the lateral motor column in the chick embryo. Brain Res 132, 197–208
    OpenUrlCrossRefPubMedWeb of Science
    1. Jostes B.,
    2. Walther C.,
    3. Gruss P.
    (1991) The murine paired box gene, Pax-7, is expressed specifically during the development of the nervous and muscular systems. Mech. Dev 33, 27–38
    1. Kitchin I. C.
    (1949) The effects of notochordectomy in Amblystoma mexicanum. J. Exp. Zool 112, 393–415
    1. Krauss S.,
    2. Johanson T.,
    3. Korzh V.,
    4. Moens U.,
    5. Ericson J. U.,
    6. Fjose A.
    (1991) Zebrafish pax[zf-a]: a paired box-containing gene expressed in the neural tube. EMBO. J 10, 3609–3619
    OpenUrlPubMedWeb of Science
    1. Krauss S.,
    2. Johanson T.,
    3. Korzh V.,
    4. Fjose A.
    (1991) Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113, 1193–1206
    OpenUrlAbstract
    1. Langman J.,
    2. Haden C.
    (1970) Formation and migration of neuroblasts in the spinal cord of the chick embryo. J. Comp. Neurol 138, 419–432
    OpenUrlCrossRefPubMedWeb of Science
    1. McConnell J.-A.,
    2. Sechrist J. W.
    (1980) Identification of early neurons in the brain stem and spinal cord: An autoradiographic study in the chick. J. Comp. Neurol 192, 769–783
    OpenUrlCrossRefPubMedWeb of Science
    1. Moase C. E.,
    2. Trasler D. G.
    (1989) Spinal ganglia reduction in splotch delayed neural tube defect mutants. Teratology 42, 171–182
    1. Moase C. E.,
    2. Trasler D. G.
    (1990) Delayed neural crest cell emigration from Sp and Spd mouse neural tube explants. Teratology 42, 171–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Nornes H. O.,
    2. Das G. D.
    (1974) Temporal pattern of neurogenesis in spinal cord of rat: An autoradiographic study. Brain Res 73, 121–138
    OpenUrlCrossRefPubMedWeb of Science
    1. Nornes H. O.,
    2. Dressler G. R.,
    3. Knapik E. W.,
    4. Deutsch U.,
    5. Gruss P.
    (1990) Spatially and temporally restricted expression of Pax 2 during murine neurogenesis. Development 109, 797–809
    OpenUrlAbstract/FREE Full Text
    1. Plachov D.,
    2. Chowdhury K.,
    3. Walther C.,
    4. Simon D.,
    5. Guenet J.-L.,
    6. Gruss P.
    (1990) Pax 8, a murine paired box gene expressed in the developing excretory system and thyroid gland. Development 110, 643–651
    OpenUrlAbstract/FREE Full Text
    1. Placzek M.,
    2. Tessier-Lavigne M.,
    3. Yamada T.,
    4. Jessell T.,
    5. Dodd J.
    (1990) Mesodermal control of neural cell identity: Floor plate induction by the notochord. Science 250, 985–988
    OpenUrlAbstract/FREE Full Text
    1. Pueschel A.,
    2. Gruss P.,
    3. Westerfeld M.
    (1992) Sequence and expression pattern of Pax-6 are highly conserved between zebrafish and mice. Development 114, 643–651
    OpenUrlAbstract
    1. Ruiz i Altaba A.
    (1992) Planar and vertical signals in the induction and patterning of the Xenopus nervous system. Development 115, 67–80
    OpenUrlAbstract
    1. Sanger F.,
    2. Nicklen S.,
    3. Coulson A. R.
    (1977) DNA sequencing with chain termination inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467
    OpenUrlAbstract/FREE Full Text
    1. Tanaka H.,
    2. Obata K.
    (1984) Developmental changes in unique cell surface antigens of the chick embryo spinal motor neurons and ganglion cells. Dev. Biol 106, 26–37
    OpenUrlCrossRefPubMedWeb of Science
    1. Tessier-Lavigne M.,
    2. Placzek M.,
    3. Lumsden A. G. S.,
    4. Dodd J.,
    5. Jessell T.
    (1988) Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336, 775–778
    OpenUrlCrossRefPubMed
    1. Treisman J.,
    2. Gönczy P.,
    3. Vashishtha M.,
    4. Harris E.,
    5. Desplan C.
    (1989) A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59, 553–562
    OpenUrlCrossRefPubMedWeb of Science
    1. Treisman J.,
    2. Harris E.,
    3. Desplan C.
    (1991) The paired box encodes a second DNA-binding domain in the paired homeo domain protein. Genes Dev 5, 594–604
    OpenUrlAbstract/FREE Full Text
    1. van Straaten H. W. M.,
    2. Hekking J. W. M.
    (1991) Development of the floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo. Anat. Embryol 184, 55–63
    OpenUrlCrossRefPubMed
    1. van Straaten H. W. M.,
    2. Hekking J. W. M.,
    3. Wiertz-Hoessels E. J. L. M.,
    4. Thors. F.,
    5. Drukker J.
    (1988) Effect of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo. Anat. Embryol 177, 317–324
    OpenUrlCrossRefPubMed
    1. van Straaten H. W. M.,
    2. Hekking J. W. M.,
    3. Thors F.,
    4. Wiertz-Hoessels E. L. J. M.,
    5. Drukker J.
    (1985) Induction of an additional floor plate in the neural tube. Acta Morphol. Neerl. Scand 23, 91–97
    OpenUrlPubMedWeb of Science
    1. Walther C.,
    2. Gruss P.
    (1991) Pax-6, a murine paired box gene is expressed in the developing CNS. Development 113, 1435–1449
    OpenUrlAbstract
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessell T. M.
    (1991) Control of cell pattern in the developing nervous system: Polarizing activity of the floor plate and notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord
M.D. Goulding, A. Lumsden, P. Gruss
Development 1993 117: 1001-1016;
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