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      Mutual repression between Gbx2 and Otx2 in sensory placodes reveals a general mechanism for ectodermal patterning

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          Abstract

          In the vertebrate head, central and peripheral components of the sensory nervous system have different embryonic origins, the neural plate and sensory placodes. This raises the question of how they develop in register to form functional sense organs and sensory circuits. Here we show that mutual repression between the homeobox transcription factors Gbx2 and Otx2 patterns the placode territory by influencing regional identity and by segregating inner ear and trigeminal progenitors. Activation of Otx2 targets is necessary for anterior olfactory, lens and trigeminal character, while Gbx2 function is required for the formation of the posterior otic placode. Thus, like in the neural plate antagonistic interaction between Otx2 and Gbx2 establishes positional information thus providing a general mechanism for rostro-caudal patterning of the ectoderm. Our findings support the idea that the Otx/Gbx boundary has an ancient evolutionary origin to which different modules were recruited to specify cells of different fates.

          Highlights

          ► Otx2 and Gbx2 segregate placode progenitors of different fates. ► Otx2 and Gbx2 mutually repress each other. ► Otx2 target activation is required for olfactory, lens and trigeminal specification. ► Gbx2 is required for otic placode specification.

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          In situ hybridization: an improved whole-mount method for Xenopus embryos.

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            Early steps in the development of the forebrain.

            The tremendous complexity of the adult forebrain makes it a challenging task to elucidate how this structure forms during embryonic development. Nevertheless, we are beginning to understand how a simple epithelial sheet of ectoderm gives rise to the labyrinthine network of cells that constitutes the functional forebrain. Here, we discuss early events in forebrain development--those that lead to the establishment of the anterior neural plate and the regional subdivision of this territory into the different domains of the prospective forebrain.
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              Specification of the neural crest occurs during gastrulation and requires Pax7.

              The neural crest is a stem population critical for development of the vertebrate craniofacial skeleton and peripheral ganglia. Neural crest cells originate along the border between the neural plate and epidermis, migrate extensively and generate numerous derivatives, including neurons and glia of the peripheral nervous system, melanocytes, bone and cartilage of the head skeleton. Impaired neural crest development is associated with human defects, including cleft palate. Classically, the neural crest has been thought to form by interactions at the border between neural and non-neural ectoderm or mesoderm, and defined factors such as bone morphogenetic proteins (BMPs) and Wnt proteins have been postulated as neural crest-inducers. Although competence to induce crest cells declines after stage 10 (ref. 14), little is known about when neural crest induction begins in vivo. Here we report that neural crest induction is underway during gastrulation and well before proper neural plate appearance. We show that a restricted region of chick epiblast (stage 3-4) is specified to generate neural crest cells when explanted under non-inducing conditions. This region expresses the transcription factor Pax7 by stage 4 + and later contributes to neural folds and migrating neural crest. In chicken embryos, Pax7 is required for neural crest formation in vivo, because blocking its translation inhibits expression of the neural crest markers Slug, Sox9, Sox10 and HNK-1. Our results indicate that neural crest specification initiates earlier than previously assumed, independently of mesodermal and neural tissues, and that Pax7 has a crucial function during neural crest development.
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                Author and article information

                Journal
                Dev Biol
                Dev. Biol
                Developmental Biology
                Elsevier
                0012-1606
                1095-564X
                01 July 2012
                01 July 2012
                : 367-540
                : 1-7
                : 55-65
                Affiliations
                [a ]Department of Craniofacial Development, King's College London, Guy's Campus, Tower Wing Floor 27, London SE1 9RT, UK
                [b ]Department of Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK
                Author notes
                [* ]Corresponding author. Fax: +44 20 7188 1674. andrea.streit@ 123456kcl.ac.uk
                Article
                YDBIO5705
                10.1016/j.ydbio.2012.04.025
                3384001
                22564795
                0c583a31-dce7-4774-b3ff-c04ee4a6062c
                © 2012 Elsevier Inc.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 12 March 2012
                : 13 April 2012
                : 17 April 2012
                Categories
                Article

                Developmental biology
                trigeminal,placodes,xenopus,chick,eye,cranial ganglia,ear,fate map
                Developmental biology
                trigeminal, placodes, xenopus, chick, eye, cranial ganglia, ear, fate map

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