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1878-108X3382010AugTrends in neurosciencesTrends NeurosciBuilding a bridal chamber: development of the thalamus.373380373-8010.1016/j.tins.2010.05.003The thalamus is a central brain region that plays a crucial role in distributing incoming sensory information to appropriate regions of the cortex. The thalamus develops in the posterior part of the embryonic forebrain, where early cell fate decisions are controlled by a local signaling center - the mid-diencephalic organizer - which forms at the boundary between prospective prethalamus and thalamus. In this review we discuss recent observations of early thalamic development in zebrafish, chick, and mouse embryos, that reveal a conserved set of interactions between homeodomain transcription factors. These interactions position the organizer along the neuraxis. The most prominent of the organizer's signals, Sonic hedgehog, is necessary for conferring regional identity on the prethalamus and thalamus and for patterning their differentiation.Crown Copyright 2010. Published by Elsevier Ltd. All rights reserved.ScholppSteffenSKarlsruhe Institute of Technology, Institute for Toxicology and Genetics, 76021 Karlsruhe, Germany.LumsdenAndrewAengG0601064MRC_Medical Research CouncilUnited KingdomG0901899MRC_Medical Research CouncilUnited KingdomWT_Wellcome TrustUnited KingdomJournal ArticleResearch Support, Non-U.S. Gov'tReview20100611
EnglandTrends Neurosci78086160166-22360Transcription FactorsIMAnimalsBody PatterninggeneticsCell DifferentiationgeneticsCell MovementgeneticsChick EmbryoGene Expression Regulation, DevelopmentalMiceSignal TransductiongeneticsThalamusembryologymetabolismTranscription FactorsgeneticsmetabolismZebrafish2010211201051920105202010615602010615602010111360201081ppublish20541814PMC295431310.1016/j.tins.2010.05.003S0166-2236(10)00077-9Jones E.G. Cambridge University Press; 2007. The Thalamus.Crick F., Koch C. A framework for consciousness. Nat. Neurosci. 2003;6:119–126.12555104Kuhlenbeck H. The ontogenetic development of diencephalic centers in the bird's brain (chick) and comparison with the reptilian and mammalian diencephalon. J. Comp. Neurol. 1937;66:23–75.Zeltser L.M. A new developmental compartment in the forebrain regulated by Lunatic fringe. Nat. Neurosci. 2001;4:683–684.11426219Vieira C. Thalamic development induced by Shh in the chick embryo. Dev. Biol. 2005;284:351–363.16026780Guinazu M.F. Tissue interactions in the developing chick diencephalon. Neural Dev. 2007;2:25.PMC221752517999760Kobayashi D. Early subdivisions in the neural plate define distinct competence for inductive signals. Development. 2002;129:83–93.11782403Hirata T. Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development. 2006;133:3993–4004.16971467Lecaudey V. Expression of the zebrafish Iroquois genes during early nervous system formation and patterning. J. Comp. Neurol. 2005;492:289–302.16217788Lagutin O.V. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 2003;17:368–379.PMC19598912569128Scholpp S. Otx1l, Otx2 and Irx1b establish and position the ZLI in the diencephalon. Development. 2007;134:3167–3176.PMC711606817670791Lavado A. Six3 inactivation causes progressive caudalization and aberrant patterning of the mammalian diencephalon. Development. 2008;135:441–450.18094027Hashimoto H. Expression of the zinc finger gene fez-like in zebrafish forebrain. Mech. Dev. 2000;97:191–195.11025224Matsuo-Takasaki M. Cloning and expression of a novel zinc finger gene, Fez, transcribed in the forebrain of Xenopus and mouse embryos. Mech. Dev. 2000;93:201–204.10781957Jeong J.Y. Patterning the zebrafish diencephalon by the conserved zinc-finger protein Fezl. Development. 2007;134:127–136.17164418Acampora D. Genetic control of brain morphogenesis through Otx gene dosage requirement. Development. 1997;124:3639–3650.9342056Staudt N., Houart C. The prethalamus is established during gastrulation and influences diencephalic regionalization. PLoS Biol. 2007;5:e69.PMC180848617341136Larsen C.W. Boundary formation and compartition in the avian diencephalon. J. Neurosci. 2001;21:4699–4711.PMC676234311425897Varga Z.M. Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development. 2001;128:3497–3509.11566855Zeltser L.M. Shh-dependent formation of the ZLI is opposed by signals from the dorsal diencephalon. Development. 2005;132:2023–2033.15788458Jeong Y. A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development. 2006;133:761–772.16407397Ertzer R. Cooperation of sonic hedgehog enhancers in midline expression. Dev. Biol. 2007;301:578–589.17157288Scholpp S. Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development. 2006;133:855–864.16452095Schier A.F. Mutations affecting the development of the embryonic zebrafish brain. Development. 1996;123:165–178.9007238Chambers D. RALDH-independent generation of retinoic acid during vertebrate embryogenesis by CYP1B1. Development. 2007;134:1369–1383.17329364Kiecker C., Lumsden A. Compartments and their boundaries in vertebrate brain development. Nat. Rev. Neurosci. 2005;6:553–564.15959467Pratt T. A role for Pax6 in the normal development of dorsal thalamus and its cortical connections. Development. 2000;127:5167–5178.11060242Osorio J. Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeodomain, Pax and hedgehog genes. Dev. Biol. 2005;288:100–112.16289025Barth K.A., Wilson S.W. 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. 1995;121:1755–1768.7600991Ruiz i Altaba A. Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development. 1998;125:2203–2212.9584120Puelles L., Martinez-de-la-Torre M. Autoradiographic and Golgi study on the early development of n. isthmi principalis and adjacent grisea in the chick embryo: a tridimensional viewpoint. Anat. Embryol. (Berl) 1987;176:19–34.3605646Shimamura K. Longitudinal organization of the anterior neural plate and neural tube. Development. 1995;121:3923–3933.8575293Shimamura K., Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development. 1997;124:2709–2718.9226442Kiecker C., Lumsden A. Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat. Neurosci. 2004;7:1242–1249.15494730Vue T.Y. Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J. Neurosci. 2009;29:4484–4497.PMC271884919357274Kiecker C., Niehrs C. A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development. 2001;128:4189–4201.11684656Rhinn M. Positioning of the midbrain-hindbrain boundary organizer through global posteriorization of the neuroectoderm mediated by Wnt8 signaling. Development. 2005;132:1261–1272.15703279Gomez-Skarmeta J.L., Modolell J. Iroquois genes: genomic organization and function in vertebrate neural development. Curr. Opin. Genet. Dev. 2002;12:403–408.12100884Vue T.Y. Characterization of progenitor domains in the developing mouse thalamus. J. Comp. Neurol. 2007;505:73–91.17729296Scholpp S. Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc. Natl. Acad. Sci. U. S. A. 2009;106:19895–19900.PMC277570319903880Wall D.S. Progenitor cell proliferation in the retina is dependent on Notch-independent Sonic hedgehog/Hes1 activity. J. Cell Biol. 2009;184:101–112.PMC261508719124651Puelles E. Otx2 controls identity and fate of glutamatergic progenitors of the thalamus by repressing GABAergic differentiation. J. Neurosci. 2006;26:5955–5964.PMC667521016738237Kriks S. Gsh2 is required for the repression of Ngn1 and specification of dorsal interneuron fate in the spinal cord. Development. 2005;132:2991–3002.15930101Mizuguchi R. Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat. Neurosci. 2006;9:770–778.16715081Hashimoto-Torii K. Differential activities of Sonic hedgehog mediated by Gli transcription factors define distinct neuronal subtypes in the dorsal thalamus. Mech. Dev. 2003;120:1097–1111.14568100Szabo N.E. The role of Sonic hedgehog of neural origin in thalamic differentiation in the mouse. J. Neurosci. 2009;29:2453–2466.PMC666623919244520Mercier P. Expression pattern of two otx genes suggests a role in specifying anterior body structures in zebrafish. Int. J. Dev. Biol. 1995;39:559–573.8619954Bosse A. Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech. Dev. 1997;69:169–181.9486539Echelard Y. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993;75:1417–1430.7916661Lo L.C. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev. 1991;5:1524–1537.1909283Andrews G.L. Dlx transcription factors regulate differentiation of dopaminergic neurons of the ventral thalamus. Mol. Cell Neurosci. 2003;23:107–120.12799141Ma Q. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 1996;87:43–52.8858147Bulfone A. 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. 1993;13:3155–3172.PMC65766887687285Bally-Cuif L. c-otx2 is expressed in two different phases of gastrulation and is sensitive to retinoic acid treatment in chick embryo. Mech. Dev. 1995;49:49–63.7748789Jasoni C.L. A chicken achaete-scute homolog (CASH-1) is expressed in a temporally and spatially discrete manner in the developing nervous system. Development. 1994;120:769–783.7600956Perez S.E. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development. 1999;126:1715–1728.10079233Itoh M. A role for iro1 and iro7 in the establishment of an anteroposterior compartment of the ectoderm adjacent to the midbrain-hindbrain boundary. Development. 2002;129:2317–2327.11973265Allende M.L., Weinberg E.S. The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev. Biol. 1994;166:509–530.7813774Akimenko M.A. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 1994;14:3475–3486.PMC65769617911517Korzh V. Expression of zebrafish bHLH genes ngn1 and nrd defines distinct stages of neural differentiation. Dev. Dyn. 1998;213:92–104.9733104Rhinn M. Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech. Dev. 2003;120:919–936.12963112Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000;1:20–29.11262869Briscoe J., Novitch B.G. Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008;363:57–70.PMC260548617282991Dessaud E. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature. 2007;450:717–720.18046410Chen L. Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus. Development. 2009;136:1317–1326.PMC268746319279136Murray K.D. Nucleus- and cell-specific gene expression in monkey thalamus. Proc. Natl. Acad. Sci. U. S. A. 2007;104:1989–1994.PMC178390317261798Quinlan R. Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev. 2009;4:35.PMC275702319732418Salinas P.C., Nusse R. Regional expression of the Wnt-3 gene in the developing mouse forebrain in relationship to diencephalic neuromeres. Mech. Dev. 1992;39:151–160.1363370Garcia-Lopez R. Fate map of the diencephalon and the zona limitans at the 10-somites stage in chick embryos. Dev. Biol. 2004;268:514–530.15063186Braun M.M. Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development. 2003;130:5579–5587.14522868Peng G., Westerfield M. Lhx5 promotes forebrain development and activates transcription of secreted Wnt antagonists. Development. 2006;133:3191–3200.16854974Zhou C.J. Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J. Neurosci. 2004;24:7632–7639.PMC672961515342729Ishibashi M., McMahon A.P. A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development. 2002;129:4807–4819.12361972Miyake A. Fgf19 regulated by Hh signaling is required for zebrafish forebrain development. Dev. Biol. 2005;288:259–275.16256099Gimeno L., Martinez S. Expression of chick Fgf19 and mouse Fgf15 orthologs is regulated in the developing brain by Fgf8 and Shh. Dev. Dyn. 2007;236:2285–2297.17654705Walshe J., Mason I. Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development. 2003;130:4337–4349.12900450Kataoka A., Shimogori T. Fgf8 controls regional identity in the developing thalamus. Development. 2008;135:2873–2881.18653561Martinez-Ferre A., Martinez S. The development of the thalamic motor learning area is regulated by Fgf8 expression. J. Neurosci. 2009;29:13389–13400.PMC666520319846726Regan J.C. An Fgf8-dependent bistable cell migratory event establishes CNS asymmetry. Neuron. 2009;61:27–34.PMC279041219146810Nakagawa Y., O’Leary D.D. Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. J. Neurosci. 2001;21:2711–2725.PMC676251811306624Bachy I. The LIM-homeodomain gene family in the developing Xenopus brain: conservation and divergences with the mouse related to the evolution of the forebrain. J. Neurosci. 2001;21:7620–7629.PMC676290211567052Holland L.Z., Holland N.D. Chordate origins of the vertebrate central nervous system. Curr. Opin. NeuroBiol. 1999;9:596–602.10508734Wada H., Satoh N. Patterning the protochordate neural tube. Curr. Opin. NeuroBiol. 2001;11:16–21.11179867Lowe C.J. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell. 2003;113:853–865.12837244Takatori N. Expression of hedgehog genes in Ciona intestinalis embryos. Mech. Dev. 2002;116:235–238.12128232Shimeld S.M. The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog. Dev. Genes Evol. 1999;209:40–47.9914417Holland L.Z. Characterization and developmental expression of AmphiNk2-2, an NK2 class homeobox gene from Amphioxus (Phylum Chordata; Subphylum Cephalochordata) Dev. Genes Evol. 1998;208:100–105.9569351Langeland J.A. An amphioxus LIM-homeobox gene, AmphiLim1/5, expressed early in the invaginating organizer region and later in differentiating cells of the kidney and central nervous system. Int. J. Biol. Sci. 2006;2:110–116.PMC145843316763670Guerin A. Neurodevelopment genes in lampreys reveal trends for forebrain evolution in craniates. PLoS One. 2009;4:e5374.PMC267140119399187Lumsden A. Motorizing the spinal cord. Cell. 1991;64:471–473.1991316Jeong J.Y. Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl. Proc. Natl. Acad. Sci. U. S. A. 2006;103:5143–5148.PMC145880816549779Tomsa J.M., Langeland J.A. Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev. Biol. 1999;207:26–37.10049562Lowe C.J. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 2006;4:e291.PMC155192616933975Matsumoto K. The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat. Neurosci. 2004;7:605–612.15133517