Early teleostean basal ganglia development visualized by Zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression

We examined the brain expression patterns of zebrafish genes Lhx6, Lhx7, Dlx2a, GAD67, and Tbr2/eomesa; except for GAD67, expression domains are restricted to the forebrain. In particular, a distribution of transcripts in the early zebrafish telencephalon comparable to that of tetrapods is revealed. Expression domains of Lhx6 and Lhx7 are restricted to a ventral subdivision (Sdv) of the precommissural dorsal subpallium, interpreted here as the homologue of the mammalian medial ganglionic eminence (the adult pallidum in mammals). In contrast, there is no such expression in the dorsal subdivision (Sdd) of the dorsal subpallium, interpreted here as the homologue of the mammalian lateral ganglionic eminence (the adult caudatoputamen in mammals). The Lhx6 and Lhx7 genes are furthermore expressed in the zebrafish ventral subpallium (Sv, septum), and in the supra‐/postcommissurally lying posterior subdivision of the dorsal subpallium (Sdp; possible homologue of the subpallial amygdala). Also in support of this comparative interpretation, Dlx2a is generally expressed in all of the subpallium, including the ventricular zones of (all three subvidisions of) the dorsal as well as of the ventral subpallium. In contrast, Tbr2 is expressed in all of the zebrafish pallium and in a restricted zone of the ventral subpallium, comparable to the known restricted septal expression in mammals. The telencephalic expression of GAD67 largely coincides with that of Dlx2a. However, GAD67‐positive cells migrate (radially) into postmitotic zones of the peripheral subpallium (as does Dlx2a and Lhx6) as well as (tangentially) into pallial zones (as does Dlx2a, but not Lhx6). J. Comp. Neurol. 507:1245–1257, 2008. © 2008 Wiley‐Liss, Inc.

[1]  N. Moreno,et al.  Development of the vomeronasal amygdala in anuran amphibians: Hodological, neurochemical, and gene expression characterization , 2007, The Journal of comparative neurology.

[2]  L. Zon,et al.  Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis , 2007, Nature.

[3]  Laure Bally-Cuif,et al.  The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. , 2006, Methods.

[4]  J. Sire,et al.  Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): Differential involvement in the visceral skeleton and braincase , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[5]  S. Rétaux,et al.  GABAergic specification in the basal forebrain is controlled by the LIM-hd factor Lhx7. , 2006, Developmental biology.

[6]  R. Northcutt Connections of the lateral and medial divisions of the goldfish telencephalic pallium , 2006, The Journal of comparative neurology.

[7]  M. Wullimann,et al.  A phylotypic stage in vertebrate brain development: GABA cell patterns in zebrafish compared with mouse , 2006, The Journal of comparative neurology.

[8]  A. Rubinstein,et al.  Neuroprotection of MPTP-induced toxicity in zebrafish dopaminergic neurons. , 2005, Brain research. Molecular brain research.

[9]  M. Wullimann,et al.  Atlas of Early Zebrafish Brain Development: A Tool for Molecular Neurogenetics , 2005 .

[10]  V. Korzh,et al.  Zebrafish embryos are susceptible to the dopaminergic neurotoxin MPTP , 2005, The European journal of neuroscience.

[11]  C. Englund,et al.  Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex , 2005, The Journal of Neuroscience.

[12]  E. Rink,et al.  The too few mutant selectively affects subgroups of monoaminergic neurons in the zebrafish forebrain , 2004, Neuroscience.

[13]  J. Fetcho,et al.  Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish , 2004, The Journal of comparative neurology.

[14]  J. Fetcho,et al.  Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish , 2004, The Journal of comparative neurology.

[15]  Su Guo,et al.  Sensitivity of zebrafish to environmental toxins implicated in Parkinson's disease. , 2004, Neurotoxicology and teratology.

[16]  B. Draper,et al.  Fgf signaling is required for zebrafish tooth development. , 2004, Developmental biology.

[17]  M. Wullimann,et al.  Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior , 2004, The Journal of comparative neurology.

[18]  Philippe Vernier,et al.  The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio , 2004, Brain Research.

[19]  S. Guo,et al.  Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish? , 2004, Genes, brain, and behavior.

[20]  M. Wullimann,et al.  Identification and morphogenesis of the eminentia thalami in the zebrafish , 2004, The Journal of comparative neurology.

[21]  S. Anderson,et al.  Origins of Cortical Interneuron Subtypes , 2004, The Journal of Neuroscience.

[22]  E. G. Jones,et al.  Two epochs in the development of γ‐aminobutyric acidergic neurons in the ferret thalamus , 2003 .

[23]  Oscar Marín,et al.  The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Leonard I. Zon,et al.  Cancer genetics and drug discovery in the zebrafish , 2003, Nature Reviews Cancer.

[25]  M. Wullimann,et al.  Anatomy of neurogenesis in the early zebrafish brain. , 2003, Brain research. Developmental brain research.

[26]  G. Fishell,et al.  The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations , 2002, Nature Neuroscience.

[27]  J. Rubenstein,et al.  Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. , 2002, Development.

[28]  M. Wullimann,et al.  Expression of Zash-1a in the postembryonic zebrafish brain allows comparison to mouse Mash1 domains. , 2002, Brain research. Gene expression patterns.

[29]  J. Rubenstein,et al.  Developmental functions of the Distal-less/Dlx homeobox genes. , 2002, Development.

[30]  M. Wullimann,et al.  BrdU-, neuroD (nrd)- and Hu-studies reveal unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain , 2002, Mechanisms of Development.

[31]  M. Wullimann,et al.  Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study. , 2002, Brain research. Developmental brain research.

[32]  François Guillemot,et al.  Proneural genes and the specification of neural cell types , 2002, Nature Reviews Neuroscience.

[33]  M. Wullimann,et al.  The teleostean forebrain: a comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization , 2002, Brain Research Bulletin.

[34]  C. Schuurmans,et al.  Molecular mechanisms underlying cell fate specification in the developing telencephalon , 2002, Current Opinion in Neurobiology.

[35]  O. Marín,et al.  A long, remarkable journey: Tangential migration in the telencephalon , 2001, Nature Reviews Neuroscience.

[36]  John E. Dowling,et al.  Behavioral screening for cocaine sensitivity in mutagenized zebrafish , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Wolfgang Driever,et al.  Dopamine transporter expression distinguishes dopaminergic neurons from other catecholaminergic neurons in the developing zebrafish embryo , 2001, Mechanisms of Development.

[38]  M. Wullimann,et al.  The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum) , 2001, Brain Research.

[39]  E. Mugnaini,et al.  Domain‐restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos , 2000, The Journal of comparative neurology.

[40]  M. Fishman,et al.  Genetics of heart development. , 2000, Trends in genetics : TIG.

[41]  J. Rubenstein,et al.  Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx‐2, Emx‐1, Nkx‐2.1, Pax‐6, and Tbr‐1 , 2000, The Journal of comparative neurology.

[42]  S. Anderson,et al.  Origin and Molecular Specification of Striatal Interneurons , 2000, The Journal of Neuroscience.

[43]  P. Vernier,et al.  Distribution of the mRNA encoding the four dopamine D1 receptor subtypes in the brain of the european eel (Anguilla anguilla): Comparative approach to the function of D1 receptors in vertebrates , 2000, The Journal of comparative neurology.

[44]  M. Ekker,et al.  A Highly Conserved Enhancer in the Dlx5/Dlx6Intergenic Region is the Site of Cross-Regulatory Interactions betweenDlx Genes in the Embryonic Forebrain , 2000, The Journal of Neuroscience.

[45]  S. Anderson,et al.  DLX‐1, DLX‐2, and DLX‐5 expression define distinct stages of basal forebrain differentiation , 1999, The Journal of comparative neurology.

[46]  O. Marín,et al.  Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. , 1999, Development.

[47]  A. Ballabio,et al.  Expression pattern of the Tbr2 (Eomesodermin) gene during mouse and chick brain development , 1999, Mechanisms of Development.

[48]  W. Driever,et al.  Mutations in the zebrafish unmask shared regulatory pathways controlling the development of catecholaminergic neurons. , 1999, Developmental biology.

[49]  F. Guillemot,et al.  Mash1 regulates neurogenesis in the ventral telencephalon. , 1999, Development.

[50]  M. Besson,et al.  Lhx9: A Novel LIM-Homeodomain Gene Expressed in the Developing Forebrain , 1999, The Journal of Neuroscience.

[51]  W. Smeets,et al.  Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians , 1998, Trends in Neurosciences.

[52]  P. Sharpe,et al.  Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. , 1998, Development.

[53]  Leyuan Shi,et al.  Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. , 1997, Science.

[54]  S. Anderson,et al.  Mutations of the Homeobox Genes Dlx-1 and Dlx-2 Disrupt the Striatal Subventricular Zone and Differentiation of Late Born Striatal Neurons , 1997, Neuron.

[55]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[56]  W. Harris,et al.  Xotch inhibits cell differentiation in the xenopus retina , 1995, Neuron.

[57]  M. Westerfield,et al.  Combinatorial expression of three zebrafish genes related to distal- less: part of a homeobox gene code for the head , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  R. Northcutt,et al.  An immunohistochemical study of the telencephalon of the senegal bichir (Polypterus senegalus) , 1992, The Journal of comparative neurology.

[59]  D. Kimelman,et al.  Overlapping expression of zebrafish T-brain-1 and eomesodermin during forebrain development , 2001, Mechanisms of Development.

[60]  S. Sharma,et al.  Distribution of substance P‐like immunoreactivity in the goldfish brain , 1989, The Journal of comparative neurology.

[61]  R. Northcutt,et al.  New Observations on the Organization and Evolution of the Telencephalon of Actinopterygian Fishes , 1980 .