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JOURNAL ARTICLES
A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve
V.A. Wallace, M.C. Raff
Development 1999 126: 2901-2909;

Summary

Retinal ganglion cell (RGC) axons have been shown to stimulate the proliferation of astrocytes in the developing rodent optic nerve, but the signals that mediate this effect have not been identified. The following findings suggest that Sonic hedgehog (Shh) is one of the signals. (1) RGCs express both Shh mRNA and protein, whereas the optic nerve contains the protein but not the mRNA. (2) Astrocytes and their precursors in the developing optic nerve express the Hedgehog (Hh) receptor gene Patched (Ptc), suggesting that they are being signalled by an Hh protein. (3) Ptc expression in the nerve is greatly decreased by either nerve transection or by treatment with neutralizing anti-Shh antibodies, suggesting that it depends on axon-derived Shh. (4) Astrocyte proliferation in the developing nerve is reduced by treatment with anti-Shh antibodies, suggesting that Shh normally helps stimulate this proliferation.

Reference

    1. Alcedo J.,
    2. Ayzenzon M.,
    3. Von Ohlen T.,
    4. Noll M.,
    5. Hooper J. E.
    (1996) The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86, 221–232
    OpenUrlCrossRefPubMedWeb of Science
    1. Barres B.,
    2. Hart I.,
    3. Coles H.,
    4. Burne J.,
    5. Voyvodic J.,
    6. Richardson W.,
    7. Raff M.
    (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Barres B.,
    2. Jacobson M.,
    3. Schmid R.,
    4. Sendtner M.,
    5. Raff M.
    (1993) Does oligodendrocyte survival depend on axons?. Curr. Biol 3, 489–497
    1. Barres B.,
    2. Raff M.
    (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361, 258–260
    OpenUrlCrossRefPubMedWeb of Science
    1. Bellusci S.,
    2. Furuta Y.,
    3. Rush M.,
    4. Henderson R.,
    5. Winnier G.,
    6. Hogan B.
    (1997) Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124, 53–63
    OpenUrlAbstract
    1. Bumcrot D. A.,
    2. Takada R.,
    3. McMahon A. P.
    (1995) Proteolytic processing yields two secreted forms of sonic hedgehog. Mol. Cell Biol 15, 2294–230
    OpenUrlAbstract/FREE Full Text
    1. Burne J. F.,
    2. Raff M. C.
    (1997) Retinal ganglion cell axons drive the proliferation of astrocytes in the developing rodent optic nerve. Neuron 18, 223–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Burne J. F.,
    2. Staple J. K.,
    3. Raff M. C.
    (1996) Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J. Neurosci 16, 2064–2073
    OpenUrlAbstract/FREE Full Text
    1. Concordet J. P.,
    2. Lewis K. E.,
    3. Moore J. W.,
    4. Goodrich L. V.,
    5. Johnson R. L.,
    6. Scott M. P.,
    7. Ingham P. W.
    (1996) Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835–2846
    OpenUrlAbstract
    1. de Iongh R.,
    2. McAvoy J. W.
    (1992) Distribution of acidic and basic fibroblast growth factors (FGF) in the foetal rat eye: implications for lens development. Growth Factors 6, 159–177
    OpenUrlPubMed
    1. DeBlock M.,
    2. Debrouwer D.
    (1993) RNA-RNA in situ hybridization using digoxigenin-labeled probes: the use of high molecular weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitroblue tetrazolium. Analyt. Chem 216, 88–89
    OpenUrl
    1. DeLong G. R.,
    2. Sidman R. L.
    (1962) Effects of eye remonal at birth on histogenesis of the mouse superior colliculus: an autoradiographic analysis with tritiated thymidine. J. Comp. Neurol 118, 205–224
    1. Duprez D.,
    2. Fournier-Thibault C.,
    3. Douarin N.
    (1998) Sonic Hedgehog induces proliferation of committed skeletal muscle cells in the chick limb. Development 125, 495–505
    OpenUrlAbstract
    1. Echelard Y.,
    2. Epstein D. J.,
    3. St-Jacques B.,
    4. Shen L.,
    5. Mohler J.,
    6. McMahon J. A.,
    7. McMahon A. P.
    (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430
    OpenUrlCrossRefPubMedWeb of Science
    1. Ericson J.,
    2. Morton S.,
    3. Kawakami A.,
    4. Roelink H.,
    5. Jessell T. M.
    (1996) Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661–673
    OpenUrlCrossRefPubMedWeb of Science
    1. Fan C.-M.,
    2. Porter J. A.,
    3. Chiang D. T.,
    4. Beachy P. A.,
    5. Tessier-Lavigne M.
    (1995) Long-range sclerotome induction by sonic hedgehog: Direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81, 457–465
    OpenUrlCrossRefPubMedWeb of Science
    1. Fan H.,
    2. Oro A. E.,
    3. Scott M. P.,
    4. Khavari P. A.
    (1997) Induction ofbasal cell carcinoma features in transgenic human skin expressing sonic hedgehog. Nat. Med 3, 788–792
    OpenUrlCrossRefPubMedWeb of Science
    1. Goodrich L. V.,
    2. Johnson R. L.,
    3. Milenkovic L.,
    4. McMahon J. A.,
    5. Scott M. P.
    (1996) Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 10, 301–312
    OpenUrlAbstract/FREE Full Text
    1. Goodrich L. V.,
    2. Scott M. P.
    (1998) Hedgehog and patched in neural development and disease. Neuron 21, 1243–1257
    OpenUrlCrossRefPubMedWeb of Science
    1. Hammerschmidt M.,
    2. Brook A.,
    3. McMahon A. P.
    (1997) The world according to hedgehog. Trends Genet 13, 14–21
    OpenUrlCrossRefPubMedWeb of Science
    1. Huang Z.,
    2. Kunes S.
    (1996) Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86, 411–422
    OpenUrlCrossRefPubMedWeb of Science
    1. Huang Z.,
    2. Kunes S.
    (1998) Signals transmitted along retinal axons in Drosophila: Hedgehog signal reception and the cell circuitry of lamina cartridge assembly. Development 125, 3753–3764
    OpenUrlAbstract
    1. Huang Z.,
    2. Shilo B. Z.,
    3. Kunes S.
    (1998) A retinal axon fascicle uses spitz, an EGF receptor ligand, to construct a synaptic cartridge in the brain of Drosophila. Cell 95, 693–703
    OpenUrlCrossRefPubMedWeb of Science
    1. Jensen A. M.,
    2. Wallace V. A.
    (1997) Expression of Sonic hedgehog and its putative role as a precursor cell mitogen in the developing mouse retina. Development 124, 363–371
    OpenUrlAbstract
    1. Lee J. J.,
    2. Ekker S. C.,
    3. von Kessler D. P.,
    4. Porter J. A.,
    5. Sun B. I.,
    6. Beachy P. A.
    (1994) Autoproteolysis in hedgehog protein biogenesis. Science 266, 1528–1537
    OpenUrlAbstract/FREE Full Text
    1. Levine E. M.,
    2. Roelink H.,
    3. Turner J.,
    4. Reh T. A.
    (1997) Sonic hedgehog promotes rod photoreceptor differentiation in mammalian retinal cells in vitro. J. Neurosci 17, 6277–6288
    OpenUrlAbstract/FREE Full Text
    1. Macdonald R.,
    2. Scholes J.,
    3. Strahle U.,
    4. Brennan C.,
    5. Holder N.,
    6. Brand M.,
    7. Wilson S. W.
    (1997) The Pax protein Noi is required for commissural axon pathway formation in the rostral forebrain. Development 124, 2397–408
    OpenUrlAbstract
    1. Magaud J. P.,
    2. Sargent I.,
    3. Clarke P. J.,
    4. Ffrench M.,
    5. Rimokh R.,
    6. Mason D. Y.
    (1989) Double immunocytochemical labeling of cell and tissue samples with monoclonal anti-bromodeoxyuridine. J. Histochem. Cytochem 37, 1517–1527
    OpenUrlAbstract/FREE Full Text
    1. Marigo V.,
    2. Davey R. A.,
    3. Zuo Y.,
    4. Cunningham J. M.,
    5. Tabin C. J.
    (1996) Biochemical evidence that patched is the Hedgehog receptor. Nature 384, 176–179
    OpenUrlCrossRefPubMed
    1. Marigo V.,
    2. Scott M. P.,
    3. Johnson R. L.,
    4. Goodrich L. V.,
    5. Tabin C. J.
    (1996) Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122, 1225–1233
    OpenUrlAbstract
    1. Mi H.,
    2. Barres B. A.
    (1999) Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 19, 1049–1061
    OpenUrlAbstract/FREE Full Text
    1. Miyake A.,
    2. Hattori Y.,
    3. Ohta M.,
    4. Itoh N.
    (1996) Rat oligodendrocytes and astrocytes preferentially express fibroblast growth factor receptor-2 and-3 mRNAs. J. Neurosci. Res 45, 534–541
    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 Pax2 during murine neurogenesis. Development 109, 797–809
    OpenUrlAbstract/FREE Full Text
    1. Ono K.,
    2. Yasui Y.,
    3. Rutishauser U.,
    4. Miller R. H.
    (1997) Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve. Neuron 19, 283–292
    OpenUrlCrossRefPubMedWeb of Science
    1. Oro A. E.,
    2. Higgins K. M.,
    3. Hu Z.,
    4. Bonifas J. M.,
    5. Epstein E. H.,
    6. Scott M. P.
    (1997) Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 276, 817–821
    OpenUrlAbstract/FREE Full Text
    1. Otteson D. C.,
    2. Shelden E.,
    3. Jones J. M.,
    4. Kameoka J.,
    5. Hitchcock P. F.
    (1998) Pax2 expression and retinal morphogenesis in the normal and Krd mouse. Dev. Biol 193, 209–224
    OpenUrlCrossRefPubMedWeb of Science
    1. Pepinsky R. B.,
    2. Zeng C.,
    3. Wen D.,
    4. Rayhorn P.,
    5. Baker D. P.,
    6. Williams K. P.,
    7. Bixler S. A.,
    8. Ambrose C. M.,
    9. Garber E. A.,
    10. Miatkowski K.,
    11. Taylor F. R.,
    12. Wang E. A.,
    13. Galdes A.
    (1998) Identification of a palmitic acid-modified form of human Sonic hedgehog. J Biol Chem 273, 14037–14045
    OpenUrlAbstract/FREE Full Text
    1. Porter J. A.,
    2. Ekker S. C.,
    3. Park W. J.,
    4. von Kessler D. P.,
    5. Young K. E.,
    6. Chen C. H.,
    7. Ma Y.,
    8. Woods A. S.,
    9. Cotter R. J.,
    10. Koonin E. V.,
    11. Beachy P. A.
    (1996) Hedgehog patterning activity: role of a lipophilic modification mediated by the carboxy-terminal autoprocessing domain. Cell 86, 21–34
    OpenUrlCrossRefPubMedWeb of Science
    1. Porter J. A.,
    2. von Kessler D. P.,
    3. Ekker S. C.,
    4. Young K. E.,
    5. Lee J. J.,
    6. Moses K.,
    7. Beachy P. A.
    (1995) The product of hedgehogautoproteolytic cleavage active in local and long-range signalling. Nature 374, 363–366
    OpenUrlCrossRefPubMedWeb of Science
    1. Porter J. A.,
    2. Young K. E.,
    3. Beachy P. A.
    (1996) Cholesterol modification of hedgehog signaling proteins in animal development. Science 274, 255–259
    OpenUrlAbstract/FREE Full Text
    1. Pringle N. P.,
    2. Mudhar H. S.,
    3. Collarini E. J.,
    4. Richardson W. D.
    (1992) PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115, 535–551
    OpenUrlAbstract
    1. Shi J.,
    2. Marinovich A.,
    3. Barres B. A.
    (1998) Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. J Neurosci 18, 4627–4636
    OpenUrlAbstract/FREE Full Text
    1. Silver J.,
    2. Robb R. M.
    (1979) Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Dev. Biol 68, 175–190
    OpenUrlCrossRefPubMedWeb of Science
    1. Skoff R. P.,
    2. Price D. L.,
    3. Stocks A.
    (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. I. Cell proliferation. J Comp. Neurol 169, 291–312
    OpenUrlCrossRefPubMedWeb of Science
    1. Skoff R. P.,
    2. Price D. L.,
    3. Stocks A.
    (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin. J. Comp. Neurol 169, 313–334
    OpenUrlCrossRefPubMedWeb of Science
    1. Small R. K.,
    2. Riddle P.,
    3. Noble M.
    (1987) Evidence for migration of oligodendrocyte—type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328, 155–157
    OpenUrlCrossRefPubMedWeb of Science
    1. Stone D. M.,
    2. Hynes M.,
    3. Armanini M.,
    4. Swanson T. A.,
    5. Gu Q.,
    6. Johnson R. L.,
    7. Scott M. P.,
    8. Pennica D.,
    9. Goddard A.,
    10. Phillips H.,
    11. Noll M.,
    12. Hooper J. E.,
    13. de Sauvage F.,
    14. Rosenthal A.
    (1996) The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384, 129–134
    OpenUrlCrossRefPubMedWeb of Science
    1. Takabatake T.,
    2. Ogawa M.,
    3. Takahashi T. C.,
    4. Mizuno M.,
    5. Okamoto M.,
    6. Takeshima K.
    (1997) Hedgehog and patched gene expression in adult ocular tissues. FEBS Lett 410, 485–489
    OpenUrlCrossRefPubMedWeb of Science
    1. Traiffort E.,
    2. Charytoniuk D. A.,
    3. Faure H.,
    4. Ruat M.
    (1998) Regional distribution of Sonic hedgehog, Patched and Smoothened mRNA in the adult rat brain. J. Neurochem 70, 1327–1330
    OpenUrlPubMedWeb of Science
    1. Ulshafer R. J.,
    2. Clavert A.
    (1979) Cell death and optic fiber penetration in the optic stalk of the chick. J. Morphol 162, 67–76
    OpenUrlCrossRefPubMed
    1. van den Heuvel M.,
    2. Ingham P. W.
    (1996) smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382, 547–551
    OpenUrlCrossRefPubMedWeb of Science
    1. Wallace V. A.
    (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Current Biology 9, 445–448
    OpenUrlCrossRefPubMedWeb of Science
    1. Wang S.,
    2. Sdrulla A. D.,
    3. diSibio G.,
    4. Bush G.,
    5. Nofziger D.,
    6. Hicks C.,
    7. Weinmaster G.,
    8. Barres B. A.
    (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63–75
    OpenUrlCrossRefPubMedWeb of Science
    1. Wechsler-Reya R. J. S. M. P.
    (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 22, 103–114
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve
V.A. Wallace, M.C. Raff
Development 1999 126: 2901-2909;
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