Advertisement
JOURNAL ARTICLES
Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic Hedgehog
J.D. Kohtz, D.P. Baker, G. Corte, G. Fishell
Development 1998 125: 5079-5089;

Summary

The cortex and basal ganglia are the major structures of the adult brain derived from the embryonic telencephalon. Two morphologically distinct regions of the basal ganglia are evident within the mature ventral telencephalon, the globus pallidus medially, and the striatum, which is positioned between the globus pallidus and the cortex. Deletion of the Sonic Hedgehog gene in mice indicates that this secreted signaling molecule is vital for the generation of both these ventral telencephalic regions. Previous experiments showed that Sonic Hedgehog induces differentiation of ventral neurons characteristic of the medial ganglionic eminence, the embryonic structure which gives rise to the globus pallidus. In this paper, we show that later in development, Sonic Hedgehog induces ventral neurons with patterns of gene expression characteristic of the lateral ganglionic eminence. This is the embryonic structure from which the striatum is derived. These results suggest that temporally regulated changes in Sonic Hedgehog responsiveness are integral in the sequential induction of basal telencephalic structures.

REFERENCES

    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. Barth K. A.,
    2. Wilson S. W.
    (1995). Expression of zebrafish nk2.2 is influenced by Sonic Hedgehog/vertebrate Hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755–1768
    OpenUrlAbstract
    1. Bayer S. A.
    (1989) Cellular aspects of brain development. Neurotoxicology 10, 307–320
    OpenUrlPubMedWeb of Science
    1. Behar T.,
    2. Ma W.,
    3. Hudson L.,
    4. Barker J. L.
    (1994) Analysis of the anatomical distribution of GAD67 mRNA encoding truncated glutamic acid decarboxylase proteins in the embryonic rat brain. Dev. Brain Res 77, 77–87
    OpenUrlCrossRefPubMed
    1. Bellusci S.,
    2. Furuta Y.,
    3. Rush M. G.,
    4. Henderson R.,
    5. Winnier G.,
    6. Hogan B. L.
    (1997) Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124, 53–63
    OpenUrlAbstract
    1. Briata P.,
    2. Di Blas E.,
    3. Gulisano M.,
    4. Mallamaci A.,
    5. Iannone R.,
    6. Boncinelli E.,
    7. Cortes G.
    (1996) EMX1 homeoprotein is expressed in cell nuclei of the developing cerebral cortex and in the axons of the olfactory sensory neurons. Mech. Dev 57, 169–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Brustle O.,
    2. Maskos U. G.,
    3. McKay R. D.
    (1995) Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron 15, 1275–1285
    OpenUrlCrossRefPubMedWeb of Science
    1. Bulfone A.,
    2. Smiga S. M.,
    3. Shimamura K.,
    4. Peterson A.,
    5. Puelles L.,
    6. Rubenstein J. L. R.
    (1995) T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15, 63–78
    OpenUrlCrossRefPubMedWeb of Science
    1. Campbell K.,
    2. Olsson M.,
    3. Bjorklund A.
    (1995) Regional incorporation and site-specific differentiation of striatal precursors transplanted to the embryonic forebrain ventricle. Neuron 15, 1259–1273
    OpenUrlCrossRefPubMedWeb of Science
    1. Chiang C.,
    2. Litingtung Y.,
    3. Lee E.,
    4. Young K. E.,
    5. Corden J. L.,
    6. Westphal H.,
    7. Beachy P. A.
    (1996) Cyclopia and defective axial patterning in mice lacking Sonic Hedgehog gene function. Nature 383, 407–413
    OpenUrlCrossRefPubMed
    1. Chomczynski P.,
    2. Sacchi N.
    (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analyt. Biochem 162, 156–159
    OpenUrlPubMedWeb of Science
    1. Couly G.,
    2. Le Douarin N. M.
    (1987) Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev. Biol 120, 198–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Dale K. J.,
    2. Vesque C.,
    3. Lints T. J.,
    4. Sampath K. T.,
    5. Furley A.,
    6. Dodd J.,
    7. Placzek M.
    (1997) Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90, 257–269
    OpenUrlCrossRefPubMedWeb of Science
    1. Diaz-Benjumea F. J.,
    2. Cohen B.,
    3. Cohen S. M.
    (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372, 175–179
    OpenUrlCrossRefPubMed
    1. Dickinson M. E.,
    2. Selleck M. A.,
    3. McMahon A. P.,
    4. Bronner-Fraser M.
    (1995) Dorsalization of the neural tube by the non-neural ectoderm. Development 121, 2099–2106
    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. Muhr J.,
    3. Placzek M.,
    4. Lints T.,
    5. Jessell T. M.,
    6. Edlund T.
    (1995) Sonic Hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81, 747–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Ericson J.,
    2. Morton S.,
    3. Kawakami A.,
    4. Roelink H.,
    5. Jessell T. M.
    (1996) Two critical periods of long-range Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661–674
    OpenUrlCrossRefPubMedWeb of Science
    1. Fishell G.
    (1995) Neural precursors adopt regional identities in response to local cues. Development 121, 803–812
    OpenUrlAbstract
    1. Fishell G.
    (1997) Regionalization in the mammalian telencephalon. Curr. Opin. Neurobiol 7, 62–69
    OpenUrlCrossRefPubMedWeb of Science
    1. Furuta Y.,
    2. Piston D. W.,
    3. Hogan B. L.
    (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203–2212
    OpenUrlAbstract
    1. Gelbart W. M.
    (1989) The decapentaplegic gene: a TGF-beta homologue controlling pattern formation in Drosophila. Development 107, 65–74
    1. Georgopoulos K.,
    2. Moore D. D.,
    3. Derfler B.
    (1992) Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science 258, 808–812
    OpenUrlAbstract/FREE Full Text
    1. Georgopoulos K.,
    2. Bigby M.,
    3. Wang J. H.,
    4. Molnar A.,
    5. Wu P.,
    6. Winandy S.,
    7. Sharpe S.
    (1994) The Ikaros gene is required for the development of all lymphoid lineages. Cell 79, 143–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Goodrich L. V.,
    2. Milenkovic L.,
    3. Higgins K. M.,
    4. Scott M. P.
    (1997) Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109–1113
    OpenUrlAbstract/FREE Full Text
    1. Hauptmann G.,
    2. Gerster T.
    (1996) Complex expression of the zp-50 pou gene in the embryonic zebrafish brain is altered by overexpression of Sonic Hedgehog. Development 122, 1769–1780
    OpenUrlAbstract
    1. Holzinger A.,
    2. Dingle S.,
    3. Bejarano P.A.,
    4. Miller M.A.,
    5. Weaver T.E.,
    6. DiLauro R.,
    7. Whitsett J.A.
    (1996) Monoclonal antibody to thyroid transcription factor-1: production, characterization, and usefulness in tumor diagnosis. Hybridoma 15, 49–53
    OpenUrlPubMedWeb of Science
    1. Hynes M.,
    2. Poulsen K.,
    3. Tessier-Lavigne M.,
    4. Rosenthal A.
    (1995) Induction of midbrain dopaminergic neurons by Sonic Hedgehog. Cell 80, 95–101
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimura S.,
    2. Hara Y.,
    3. Pineau T.,
    4. Fernandez-Salguero P.,
    5. Fox C. H.,
    6. Ward J. M.,
    7. Gonzalez F. J.
    (1996) The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10, 60–69
    OpenUrlAbstract/FREE Full Text
    1. Krauss S.,
    2. Concordet J. P.,
    3. Ingham P. W.
    (1993) A functionally conserved homolog of the Drosophila segment polarity gene hedgehog is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444
    OpenUrlCrossRefPubMedWeb of Science
    1. Lazzaro D.,
    2. Price M.,
    3. De Felice M.,
    4. Di Lauro R.
    (1991) The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113, 1093–1104
    OpenUrlAbstract
    1. Lee J.,
    2. Platt K. A.,
    3. Censullo P.,
    4. Ruiz i Altaba A.
    (1997) Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537–2552
    OpenUrlAbstract
    1. Lendahl U.,
    2. Zimmerman L. B.,
    3. McKay R. D.
    (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585–595
    OpenUrlCrossRefPubMedWeb of Science
    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. Li H.,
    2. Tierney C.,
    3. Wen L.,
    4. Wu J. Y.,
    5. Rao Y.
    (1997) A single morphogenetic field gives rise to two retina primordia under the influence of the prechordal plate. Development 124, 603–615
    OpenUrlAbstract
    1. Liem K. J.,
    2. Tremml G.,
    3. Roelink H.,
    4. Jessell T. M.
    (1995) Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969–979
    OpenUrlCrossRefPubMedWeb of Science
    1. Macdonald R.,
    2. Barth K. A.,
    3. Xu Q.,
    4. Holder N.,
    5. Mikkola I.,
    6. Wilson S.
    (1995) Midline signaling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267–3278
    OpenUrlAbstract
    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. Marti E.,
    2. Takada R.,
    3. Bumcrot D. A.,
    4. Sasaki H.,
    5. McMahon A. P.
    (1995) Distribution of Sonic Hedgehog peptides in the developing chick and mouse embryo. Development 121, 2537–2547
    OpenUrlAbstract
    1. Miao N.,
    2. Wang M.,
    3. Ott J. A.,
    4. D'Alessandro J. S.,
    5. Woolf T. M.,
    6. Bumcrot D. A.,
    7. Mahanthappa N. K.,
    8. Pang K.
    (1997) Sonic Hedgehog promotes the survival of specific CNS neuron populations and protects these cells from toxic insult in vitro. J. Neurosci 17, 5891–5899
    OpenUrlAbstract/FREE Full Text
    1. Molnar A.,
    2. Georgopoulos K.
    (1994) The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Molec. Cell. Biol 14, 8292–8303
    OpenUrlAbstract/FREE Full Text
    1. Muhr J.,
    2. Jessell T. M.,
    3. Edlund T.
    (1997) Assignment of early caudal identity to neural plate cells by a signal from caudal paraxial mesoderm. Neuron 19, 487–502
    OpenUrlCrossRefPubMedWeb of Science
    1. Northcutt R.,
    2. Kaas J.
    (1995) The emergence and evolution of mammalian neocortex. Trends Neurosci 18, 373–379
    OpenUrlCrossRefPubMedWeb of Science
    1. Panganiban G.,
    2. Sebring A.,
    3. Nagy L.,
    4. Carroll S.
    (1995) The development of crustacean limbs and the evolution of arthropods. Science 270, 1363–1366
    OpenUrlAbstract/FREE Full Text
    1. Parr B. A.,
    2. Shea M. J.,
    3. Vassileva G.,
    4. McMahon A. P.
    (1993) Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247–261
    OpenUrlAbstract
    1. Pera E. M.,
    2. Kessel M.
    (1997) Patterning of the chick forebrain anlage by the prechordal plate. Development 124, 4153–4162
    OpenUrlAbstract
    1. Placzek M.,
    2. Tessier-Lavigne M.,
    3. Yamada T.,
    4. Jessell T. M.,
    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. Placzek M.,
    2. Jessell T. M.,
    3. Dodd J.
    (1993) Induction of floor platedifferentiation by contact-dependent, homeogenetic signals. Development 117, 205–218
    OpenUrlAbstract/FREE Full Text
    1. Platt K. A.,
    2. Michaud J.,
    3. Joyner A. L.
    (1997) Expression of the mouse Gli and Ptc genes is adjacent to embryonic sources of hedgehog signals suggesting a conservation of pathways between flies and mice. Mech. Dev 62, 121–135
    OpenUrlCrossRefPubMedWeb of Science
    1. Porteus M. H.,
    2. Bulfone A.,
    3. Ciaranello R. D.,
    4. Rubenstein J. L.
    (1991) Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 7, 221–229
    OpenUrlCrossRefPubMedWeb of Science
    1. Price M.,
    2. Lazzaro D.,
    3. Pohl T.,
    4. Mattei M. G.,
    5. Ruther U.,
    6. Olivo J. C.,
    7. Duboule D.,
    8. Di Lauro R.
    (1992). Regional expression of the homeobox gene Nkx-2.2 in the developing mammalian forebrain. Neuron 8, 241–255
    OpenUrlCrossRefPubMedWeb of Science
    1. Riddle R. D.,
    2. Johnson R. L.,
    3. Laufer E.,
    4. Tabin C.
    (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416
    OpenUrlCrossRefPubMedWeb of Science
    1. Rijsewijk F.,
    2. Schuermann M.,
    3. Wagenaar E.,
    4. Parren P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Robbins D. J.,
    2. Nybakken K. E.,
    3. Kobayashi R.,
    4. Sisson J. C.,
    5. Bishop J. M.,
    6. Therond P. P.
    (1997) Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90, 225–234
    OpenUrlCrossRefPubMedWeb of Science
    1. Roelink H.,
    2. Augsberger A.,
    3. Heemskerk J.,
    4. Korzh V.,
    5. Norline S.,
    6. Ruiz i Altaba A.,
    7. Tanabe Y.,
    8. Placzek M.,
    9. Edlund T.,
    10. Jessell T. M.,
    11. Dodd J.
    (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761–775
    OpenUrlCrossRefPubMedWeb of Science
    1. Rubenstein J. L.,
    2. Martinez S.,
    3. Shimamura K.,
    4. Puelles L.
    (1994) The embryonic vertebrate forebrain: the prosomeric model. Science 266, 578–580
    OpenUrlFREE Full Text
    1. Ruiz i Altaba A.
    (1997) Catching a Gli-mpse of Hedgehog. Cell 90, 193–196
    OpenUrlCrossRefPubMed
    1. Ruiz i Altaba A.,
    2. Jessell T. M.,
    3. Roelink H.
    (1995) Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos. Mol. Cell. Neurosci 6, 106–121
    OpenUrlCrossRefPubMedWeb of Science
    1. Schaeren-Wiemers N.,
    2. Gerfin-Moser A.
    (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochem 100, 431–440
    1. Shimamura K.,
    2. Hartigan D. J.,
    3. Martinez S.,
    4. Puelles L.,
    5. Rubenstein J. L.
    (1995) Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923–3933
    OpenUrlAbstract
    1. Shimamura K.,
    2. Rubenstein J. L.
    (1997) Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709–2718
    OpenUrlAbstract
    1. Simeone A.,
    2. Acampora D.,
    3. Gulisano M.,
    4. Stornaiuolo A.,
    5. Boncinelli E.
    (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature 358, 687–690
    OpenUrlCrossRefPubMed
    1. Sisson J. C.,
    2. Ho K. S.,
    3. Suyama K.,
    4. Scott M. P.
    (1997) Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90, 235–245
    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 tumor suppressor gene patched encodes a candidate receptor for Sonic Hedgehog. Nature 384, 119–120
    OpenUrlCrossRefPubMed
    1. van Straaten H. M. W.,
    2. Hekking J. M. W.,
    3. Wiertz-Hoessels E. L.,
    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. 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-notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Pfaff S. L.,
    3. Edlund T.,
    4. Jessell T. M.
    (1993) Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673–686
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic Hedgehog
J.D. Kohtz, D.P. Baker, G. Corte, G. Fishell
Development 1998 125: 5079-5089;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights