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JOURNAL ARTICLES
Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes
A.S. Fernandez, C. Pieau, J. Reperant, E. Boncinelli, M. Wassef
Development 1998 125: 2099-2111;

Summary

Homologies between vertebrate forebrain subdivisions are still uncertain. In particular the identification of homologs of the mammalian neocortex or the dorsal ventricular ridge (DVR) of birds and reptiles is still a matter of dispute. To get insight about the organization of the primordia of the main telencephalic subdivisions along the anteroposterior axis of the neural tube, a fate map of the dorsal prosencephalon was obtained in avian chimeras at the 8- to 9-somite stage. At this stage, the primordia of the pallium, DVR and striatum were located on the dorsal aspect of the prosencephalon and ordered caudorostrally along the longitudinal axis of the brain. Expression of homeobox-containing genes of the Emx, Dlx and Pax families were used as markers of anteroposterior developmental subdivisions of the forebrain in mouse, chick, turtle and frog. Their expression domains delineated three main telencephalic subdivisions in all species at the onset of neurogenesis: the pallial, intermediate and striatal neuroepithelial domains. The fate of the intermediate subdivisions diverged, however, between species at later stages of development. Homologies between forebrain subdivisions are proposed based on the conservation and divergence of these gene expression patterns.

REFERENCES

    1. Altman J.,
    2. Bayer S. A.
    (1995). Atlas of Prenatal Rat Brain Development. Boca Raton: CRC Press.
    1. Alvarez-Bolado G.,
    2. Rosenfeld M. G.,
    3. Swanson L. W.
    (1995). Model of forebrain regionalization based on spatiotemporal patterns of POU-III homeobox gene expression, birthdates, and morphological features. J. Comp. Neurol 355, 237–295.
    OpenUrlCrossRefPubMedWeb of Science
    1. Anderson S. A.,
    2. Qiu M.,
    3. Bulfone A.,
    4. Eisenstat D. D.,
    5. Meneses J.,
    6. Pedersen R.,
    7. Rubenstein J. L.
    (1997). Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27–37.
    OpenUrlAbstract/FREE Full Text
    1. Anderson S. A.,
    2. Eisenstat D. D.,
    3. Shi L.,
    4. Rubenstein J. L. R.
    (1997). Interneuron migration from the basal forebrain to the neocortex: Dependence on Dlx genes. Science 278, 474–476.
    OpenUrlAbstract/FREE Full Text
    1. Asano M.,
    2. Emori Y.,
    3. Saigo K.,
    4. Shiokawa K.
    (1992). Isolation and characterization of a Xenopus cDNA which encodes a homeodomain highly homologous to Drosophila Distal-less. J. Biol. Chem. 267, 5044–5047.
    OpenUrlCrossRefPubMedWeb of Science
    1. Balaban E.,
    2. Teillet M. A.,
    3. Le Douarin N.
    (1988). Application of the quail-chick chimera system to the study of brain development and behavior. Science 241, 1339–1342.
    OpenUrlPubMedWeb of Science
    1. Bally-Cuif L.,
    2. Wassef M.
    (1994). Ectopic induction and reorganization of Wnt-1 expression in quail/chick chimeras. Development 120, 3379–3394.
    OpenUrlAbstract
    1. Boncinelli E.,
    2. Gulisano M.,
    3. Broccoli V.
    (1993). Emx and Otx homeobox genes in the developing mouse brain. J. Neurobiol 24, 1356–1366.
    OpenUrlCrossRefPubMedWeb of Science
    1. Bruce L. L.,
    2. Neary T. J.
    (1995). The limbic system of tetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behav. Evol 46, 224–234.
    OpenUrlCrossRefPubMed
    1. Bulfone A.,
    2. Puelles L.,
    3. Porteus M. H.,
    4. Frohman M. A.,
    5. Martin G. R.,
    6. Rubenstein J. L. R.
    (1993). Spatially restricted expression of Dlx-1, Dlx −2 (Tes-1), Gbx-2 and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci 13, 3155–3172.
    OpenUrlCrossRefPubMed
    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.
    OpenUrlCrossRef
    1. Butler A. B.
    (1994). The evolution of the dorsal pallium in the telencephalon of amniotes: cladistic analysis and a new hypothesis. Brain Res. Rev 19, 66–101.
    OpenUrlCrossRef
    1. Carroll S. B.
    (1995). Homeotic genes and the evolution of arthropodes and chordates. Nature 376, 479–485.
    OpenUrlCrossRefPubMedWeb of Science
    1. Caviness V. S., Jr
    (1982). Neocortical histogenesis in normal and reeler mice: a developmental study based upon (3H) thymidine autoradiography. Dev. Brain Res 4, 293–302.
    OpenUrlCrossRefPubMedWeb of Science
    1. Caviness V. S., Jr,
    2. Takahashi T.,
    3. Nowakowski R. S.
    (1995). Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model. Trends Genet 18, 379–.
    OpenUrlAbstract/FREE Full Text
    1. Cordes S. P.,
    2. Barsh G. S.
    (1994). The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025–1034.
    OpenUrlCrossRefPubMedWeb of Science
    1. Couly G. F.,
    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. De Carlos J. A.,
    2. Lopez-Mascaraque L.,
    3. Valverde F.
    (1996). Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci 16, 6146–6156.
    OpenUrlCrossRefPubMed
    1. Dirksen M.-L.,
    2. Mathers P.,
    3. Jamrich M.
    (1993). Expression of a Xenopus distal-less related gene involved in forebrain and cranio-facial development. Mech. Dev 41, 121–128.
    OpenUrlPubMed
    1. Eagleson G. W.,
    2. Harris W. A.
    (1990). Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol 21, 427–440.
    OpenUrlAbstract/FREE Full Text
    1. Eagleson G. W.,
    2. Ferreiro B.,
    3. Harris W. A.
    (1995). Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain. J. Neurobiol 28, 146–158.
    OpenUrlCrossRefPubMedWeb of Science
    1. Filimonoff I. N.
    (1964). Homologies of the cerebral formations of mammals and reptiles. J. Hirnforsch 7, 229–251.
    OpenUrlCrossRefPubMedWeb of Science
    1. Finlay B. L.,
    2. Darlington R. B.
    (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584.
    OpenUrlCrossRefPubMedWeb of Science
    1. Goffinet A. M.,
    2. Daumerie Ch.,
    3. Langerwerf B.,
    4. Pieau C.
    (1986). Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J. Comp. Neurol 243, 106–116.
    OpenUrlCrossRefPubMedWeb of Science
    1. Gulisano M.,
    2. Broccoli V.,
    3. Pardini C.,
    4. Boncinelli E.
    (1996). Emx 1 and Emx 2 show different patterns of expression during proliferation and differentiation of the developing cerebral cortex in the mouse. Eur. J. Neurosci 8, 1037–1050.
    OpenUrlCrossRefWeb of Science
    1. Hamburger V.,
    2. Hamilton H.
    (1951). A series of normal stages in the development of the chick embryo. J. Morphol 88, 49–92.
    OpenUrlPubMedWeb of Science
    1. Hauptmann G.,
    2. Gerster T.
    (1994). Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet 10, 266–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Herrick C. J.
    (1948). The Brain of the Tiger Salamander Chicago: University of Chicago Press.
    1. Karten H. J.
    (1969). The organization of the avian telencephalon and some speculations on the phylogenyof the amniote telencephalon. Ann. NY Acad. Sci 167, 164–179.
    OpenUrlPubMedWeb of Science
    1. Karten H. J.
    (1991). Homology and evolutionary origins of the neocortex. Brain Behav. Evol 38, 264–272.
    OpenUrlAbstract
    1. Finlay B. L.,
    2. Innocenti G.,
    3. Scheich H.
    1. Lohman A. H. M.,
    2. Smeets W. J. A. J.
    (1991). The dorsal ventricular ridge and cortex of reptiles in historical and phylogenetic perspective. In The Neocortex: Ontogeny and Phylogeny. (ed. Finlay B. L., Innocenti G., Scheich H.). pp. 59–74. New York: Plenum.
    1. MacLean P. D.
    (1990). The Triune Brain in Evolution. New York: Plenum Press.
    1. Marin F.,
    2. Puelles L.
    (1995). Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur. J. Neurosci 7, 1714–1738.
    OpenUrlCrossRefPubMedWeb of Science
    1. McKay I. J.,
    2. Muchamore I.,
    3. Krumlauf R.,
    4. Maden M.,
    5. Lumsden A.,
    6. Lewis J.
    (1994). The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199–2211.
    OpenUrlCrossRefPubMedWeb of Science
    1. Medina L.,
    2. Reiner A.
    (1995). Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. Brain Behav. Evol 46, 235–258.
    OpenUrlAbstract
    1. Moens C. B.,
    2. Yan Y. L.,
    3. Appel B.,
    4. Force A. G.,
    5. Kimmel C. B.
    (1996). valentino a zebrafish gene required for normal hindbrain segmentation. Development 122, 3981–3990.
    OpenUrlCrossRefPubMedWeb of Science
    1. Morasso M. I.,
    2. Mahon K. A.,
    3. Sargent T. D.
    (1995). A Xenopus distal-less gene in transgenic mice: conserved regulation in distal limb epidermis and other sites of epithelial-mesenchymal interaction. Proc. Natl. Acad. Sci. USA 92, 3968–3972.
    OpenUrlAbstract
    1. Morita T.,
    2. Nitta H.,
    3. Kiyama Y.,
    4. Mori H.,
    5. Mishina M.
    (1995). Differential expression of two zebrafish Emx homeoprotein mRNAs in the developing brain. Neurosci. Lett 198, 131–134.
    OpenUrlCrossRefPubMed
    1. Nieuwkoop P. D.,
    2. Faber J.
    (1956). Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company.
    1. Northcutt R. G.
    (1981). Evolution of the telencephalon in nonmammals. Ann. Rev. Neurosci 4, 301–350.
    OpenUrlCrossRefPubMedWeb of Science
    1. Northcutt R. G.,
    2. Kaas J.
    (1995). The emergence and evolution of mammalian neocortex. Trends Neurosci 18, 373–379.
    OpenUrlCrossRef
    1. Papalopulu N.,
    2. Kintner C.
    (1993). Xenopus distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development 117, 961–975.
    OpenUrlCrossRefPubMedWeb of Science
    1. Patarnello T.,
    2. Bargelloni L.,
    3. Boncinelli E.,
    4. Spada F.,
    5. Pannese M.,
    6. Broccoli V.
    (1997). Evolution of Emx genes and brain development in vertebrates. Proc. Royal Soc. B. (in press).
    1. Pieau C.,
    2. Dorizzi M.
    (1981). Determination of temperature sensitive stages for sexual differentiation of the gonads in embryos of the turtle Emys orbicularis. J. Morphol. 170, 373–382.
    OpenUrlCrossRefPubMedWeb of Science
    1. Porteus M. H.,
    2. Bulfone A.,
    3. Ciaranello R. D.,
    4. Rubenstein J. L. R.
    (1991). Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 7, 221–229.
    OpenUrlAbstract
    1. Porteus M. H.,
    2. Bulfone A.,
    3. Liu J.-K.,
    4. Puelles L.,
    5. Lo L.-C.,
    6. Rubenstein J. L. R.
    (1994). DLX-2, MASH-1, and MAP-2 expression and bromodoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci 14, 6370–6383.
    OpenUrlAbstract/FREE Full Text
    1. Price M.,
    2. Lemaistre M.,
    3. Pischetola M.,
    4. Di Lauro R.,
    5. Duboule D.
    (1991). A mouse gene related to Distal-Less shows a restricted expression in the developing forebrain. Nature 351, 748–751.
    OpenUrlCrossRefPubMedWeb of Science
    1. Puelles L.,
    2. Rubenstein J. L.
    (1993). Expression patterns of homeoboxand other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16, 472–479.
    OpenUrlCrossRefPubMed
    1. Puelles L.
    (1995). A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav. Evol 46, 319–337.
    OpenUrlPubMedWeb of Science
    1. Reiner A.,
    2. Brauth S. E.,
    3. Karten H. J.
    (1984). Evolution of the amniote basal ganglia. Trends Neurosci 7, 320–325.
    OpenUrlAbstract/FREE Full Text
    1. Robinson G. W.,
    2. Mahon K. A.
    (1994). Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech. Dev 48, 199–215.
    OpenUrl
    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.
    OpenUrlPubMed
    1. Schneider-Maunoury S.,
    2. Seitanidou T.,
    3. Charnay P.,
    4. Lumsden A.
    (1993). Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75, 1199–1214.
    OpenUrlAbstract/FREE Full Text
    1. Schneider-Maunoury S.,
    2. Topilko P.,
    3. Seitandou T.,
    4. Levi G.,
    5. Cohen-Tannoudji M.,
    6. Pournin S.,
    7. Babinet C.,
    8. Charnay P.
    (1997). Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215–1226.
    OpenUrlAbstract
    1. Shimamoto T.,
    2. Nakamura S.,
    3. Bollekens J.,
    4. Ruddle F. H.,
    5. Takeshita K.
    (1997). Inhibition of DLX-7 homeobox gene causes decreased expression of GATA-1 and c-myc genes and apoptosis. Proc. Natl. Acad. Sci. USA 94, 3245–3249.
    OpenUrlAbstract
    1. Shimamura K.,
    2. Martinez S.,
    3. Puelles L.,
    4. Rubenstein J. L. R.
    (1997). Patterns of gene expression in the neural plate and neural tube subdivide the embryonic forebrain into transverse and longitudinal domains. Dev Neurosci 19, 88–96.
    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.
    OpenUrlCrossRefPubMedWeb of Science
    1. Simeone A.,
    2. Gulisano M.,
    3. Acampora D.,
    4. Stornaiuolo A.,
    5. Rambaldi M.,
    6. Boncinelli E.
    (1992). Two vertebrate homeobox genes related to the Drosophila Empty Spiracles gene are expressed in the embryonic cerebral cortex. EMBO J 11, 2541–2550.
    OpenUrlPubMedWeb of Science
    1. Simeone A.,
    2. Acampora D.,
    3. Pannese M.,
    4. D'Esposito M.,
    5. Stornaiuolo A.,
    6. Gulisano M.,
    7. Mallamaci A.,
    8. Kastury K.,
    9. Druck T.,
    10. Huebner K.,
    11. Boncinelli E.
    (1994). Cloning and characterization of two members of the vertebrate Dlx gene family. Proc. Natl. Acad. Sci. USA 91, 2250–2254.
    OpenUrlCrossRefPubMedWeb of Science
    1. Smart I. H. M.,
    2. McSherry G. M.
    (1982). Growth patterns in the lateral wall of the mouse telencephalon. II. Histological changes during and subsequent to the period of isocortical neuron production. J. Anat 134, 4415–442.
    OpenUrlCrossRefPubMed
    1. Smeets W. J.,
    2. Gonzalez A.
    (1994). Sensorimotor integration in the brain of reptiles. Eur. J. Morphol 32, 299–302.
    OpenUrlCrossRefPubMedWeb of Science
    1. Stock D. W.,
    2. Ellies D. L.,
    3. Zhao Z.,
    4. Ekker M.,
    5. Ruddle F. H.,
    6. Weiss K. M.
    (1996). The evolution of the vertebrate Dlx gene family. Proc. Natl. Acad. Sci. USA 93, 10858–10863.
    OpenUrlAbstract
    1. Stoykova A.,
    2. Gruss P.
    (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci 14, 1395–1412.
    OpenUrlCrossRefPubMedWeb of Science
    1. Stoykova A.,
    2. Fritsch R.,
    3. Walther C.,
    4. Gruss P.
    (1996). Forebrain patterning defects in Small eye mutant mice. Development 122, 3453–3465.
    OpenUrlAbstract
    1. Stoykova A.,
    2. Götz M.,
    3. Gruss P.,
    4. Price J.
    (1997). Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124, 3765–3777.
    1. Striedter G. F.,
    2. Beydler S.
    (1997). Distribution of radial glia in the developing telencephalon of chicks. J. Comp. Neurol 387, 399–420.
    1. Striedter G. F.
    (1997). The telencephalon of tetrapods in evolution. Brain Behav. Evol 49, 179–213.
    1. Tsai H. M.,
    2. Garber B. B.,
    3. Larramendi L. M. H.
    (1981). 3H-thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo. I. Neuronal birthdates of telencephalic compartments in situ. J. Comp. Neurol 198, 275–292.
    1. Tsai H. M.,
    2. Garber B. B.,
    3. Larramendi L. M. H.
    (1981). 3H-thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo. II. Dynamics of neuronal migration, displacement and aggregation. J. Comp. Neurol 198, 293–306.
    1. Turque N.,
    2. Plaza S.,
    3. Radvanyi F.,
    4. Carriere C.,
    5. Saule S.
    (1994). Pax-QNR/ Pax-6, a paired box-and homeobox-containing gene expressed in neurons, is also expressed in pancreatic endocrine cells. Mol. Endocrinol 8, 929–938.
    1. Ulinski P. S.
    (1983). Dorsal Ventricular Ridge. A Treatise on Forebrain Organization in Reptiles and Birds. New York, John Wiley.
    1. Walther C.,
    2. Gruss P.
    (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435–1449.
    1. Wilkinson D.G.
    (1992). In: In Situ Hybridization: a Practical Approach, Wilkinson DG ed. (Oxford: IRL Press) pp. 75–83.
    1. Xuan S.,
    2. Baptista C. A.,
    3. Balas G.,
    4. Tao W.,
    5. Soares V. C.,
    6. Lai E.
    (1995). Winged helix trannscription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14, 1141–1152.
    1. Yoshida M.,
    2. Suda Y.,
    3. Matsuo I.,
    4. Miyamoto N.,
    5. Takeda N.,
    6. Kuratani S.,
    7. Aizawa S.
    (1997). Emx 1 and Emx 2 functions in development of dorsal telencephalon. Development 124, 101–111.
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JOURNAL ARTICLES
Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes
A.S. Fernandez, C. Pieau, J. Reperant, E. Boncinelli, M. Wassef
Development 1998 125: 2099-2111;
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