Literature DB >> 31881199

Developmental origin of peripheral ciliary band neurons in the sea urchin embryo.

Leslie A Slota1, Esther Miranda1, Brianna Peskin1, David R McClay2.   

Abstract

In the sea urchin larva, most neurons lie within an ectodermal region called the ciliary band. Our understanding of the mechanisms of specification and patterning of these peripheral ciliary band neurons is incomplete. Here, we first examine the gene regulatory landscape from which this population of neural progenitors arise in the neuroectoderm. We show that ciliary band neural progenitors first appear in a bilaterally symmetric pattern on the lateral edges of chordin expression in the neuroectoderm. Later in development, these progenitors appear in a salt-and-pepper pattern in the ciliary band where they express soxC, and prox, which are markers of neural specification, and begin to express synaptotagminB, a marker of differentiated neurons. We show that the ciliary band expresses the acid sensing ion channel gene asicl, which suggests that ciliary band neurons control the larva's ability to discern touch sensitivity. Using a chemical inhibitor of MAPK signaling, we show that this signaling pathway is required for proper specification and patterning of ciliary band neurons. Using live imaging, we show that these neural progenitors undergo small distance migrations in the embryo. We then show that the normal swimming behavior of the larvae is compromised if the neurogenesis pathway is perturbed. The developmental sequence of ciliary band neurons is very similar to that of neural crest-derived sensory neurons in vertebrates and may provide insights into the evolution of sensory neurons in deuterostomes.
Copyright © 2019 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Ciliary band; Neurogenin; Neuronal progenitor; Peripheral neurons; Sea urchin

Mesh:

Substances:

Year:  2019        PMID: 31881199      PMCID: PMC7080585          DOI: 10.1016/j.ydbio.2019.12.011

Source DB:  PubMed          Journal:  Dev Biol        ISSN: 0012-1606            Impact factor:   3.582


  31 in total

1.  Sea urchin neural development and the metazoan paradigm of neurogenesis.

Authors:  Robert D Burke; Daniel J Moller; Oliver A Krupke; Valerie J Taylor
Journal:  Genesis       Date:  2014-03       Impact factor: 2.487

2.  A Raf/MEK/ERK signaling pathway is required for development of the sea urchin embryo micromere lineage through phosphorylation of the transcription factor Ets.

Authors:  Eric Röttinger; Lydia Besnardeau; Thierry Lepage
Journal:  Development       Date:  2004-03       Impact factor: 6.868

3.  Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos.

Authors:  Shunsuke Yaguchi; Junko Yaguchi; Robert D Burke
Journal:  Development       Date:  2006-05-10       Impact factor: 6.868

4.  Time and extent of ciliary response to particles in a non-filtering feeding mechanism.

Authors:  Richard R Strathmann
Journal:  Biol Bull       Date:  2007-04       Impact factor: 1.818

5.  The sea urchin animal pole domain is a Six3-dependent neurogenic patterning center.

Authors:  Zheng Wei; Junko Yaguchi; Shunsuke Yaguchi; Robert C Angerer; Lynne M Angerer
Journal:  Development       Date:  2009-04       Impact factor: 6.868

Review 6.  The evolutionary origin of the vertebrate neural crest and its developmental gene regulatory network--insights from amphioxus.

Authors:  Jr-Kai Sky Yu
Journal:  Zoology (Jena)       Date:  2009-11-24       Impact factor: 2.240

7.  Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo.

Authors:  Junko Yaguchi; Lynne M Angerer; Kazuo Inaba; Shunsuke Yaguchi
Journal:  Dev Biol       Date:  2011-12-22       Impact factor: 3.582

8.  Chordin is required for neural but not axial development in sea urchin embryos.

Authors:  Cynthia A Bradham; Catherine Oikonomou; Alexander Kühn; Amanda B Core; Joshua W Modell; David R McClay; Albert J Poustka
Journal:  Dev Biol       Date:  2009-01-29       Impact factor: 3.582

9.  Identification of neural transcription factors required for the differentiation of three neuronal subtypes in the sea urchin embryo.

Authors:  Leslie A Slota; David R McClay
Journal:  Dev Biol       Date:  2018-01-10       Impact factor: 3.582

10.  Migratory neuronal progenitors arise from the neural plate borders in tunicates.

Authors:  Alberto Stolfi; Kerrianne Ryan; Ian A Meinertzhagen; Lionel Christiaen
Journal:  Nature       Date:  2015-10-28       Impact factor: 49.962

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  3 in total

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Authors:  Megan L Martik; Marianne E Bronner
Journal:  Nat Rev Neurosci       Date:  2021-09-01       Impact factor: 34.870

2.  Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome.

Authors:  Periklis Paganos; Danila Voronov; Jacob M Musser; Detlev Arendt; Maria Ina Arnone
Journal:  Elife       Date:  2021-11-25       Impact factor: 8.140

Review 3.  The Use of Larval Sea Stars and Sea Urchins in the Discovery of Shared Mechanisms of Metazoan Whole-Body Regeneration.

Authors:  Andrew Wolff; Veronica Hinman
Journal:  Genes (Basel)       Date:  2021-07-13       Impact factor: 4.096

  3 in total

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