Literature DB >> 22159579

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms.

Nagayasu Nakanishi1, Eduard Renfer, Ulrich Technau, Fabian Rentzsch.   

Abstract

As a sister group to Bilateria, Cnidaria is important for understanding early nervous system evolution. Here we examine neural development in the anthozoan cnidarian Nematostella vectensis in order to better understand whether similar developmental mechanisms are utilized to establish the strikingly different overall organization of bilaterian and cnidarian nervous systems. We generated a neuron-specific transgenic NvElav1 reporter line of N. vectensis and used it in combination with immunohistochemistry against neuropeptides, in situ hybridization and confocal microscopy to analyze nervous system formation in this cnidarian model organism in detail. We show that the development of neurons commences in the ectoderm during gastrulation and involves interkinetic nuclear migration. Transplantation experiments reveal that sensory and ganglion cells are autonomously generated by the ectoderm. In contrast to bilaterians, neurons are also generated throughout the endoderm during planula stages. Morpholino-mediated gene knockdown shows that the development of a subset of ectodermal neurons requires NvElav1, the ortholog to bilaterian neural elav1 genes. The orientation of ectodermal neurites changes during planula development from longitudinal (in early-born neurons) to transverse (in late-born neurons), whereas endodermal neurites can grow in both orientations at any stage. Our findings imply that elav1-dependent ectodermal neurogenesis evolved prior to the divergence of Cnidaria and Bilateria. Moreover, they suggest that, in contrast to bilaterians, almost the entire ectoderm and endoderm of the body column of Nematostella planulae have neurogenic potential and that the establishment of connectivity in its seemingly simple nervous system involves multiple neurite guidance systems.

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Year:  2011        PMID: 22159579     DOI: 10.1242/dev.071902

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  64 in total

Review 1.  Interkinetic nuclear migration: beyond a hallmark of neurogenesis.

Authors:  Yoichi Kosodo
Journal:  Cell Mol Life Sci       Date:  2012-03-14       Impact factor: 9.261

Review 2.  From nerve net to nerve ring, nerve cord and brain--evolution of the nervous system.

Authors:  Detlev Arendt; Maria Antonietta Tosches; Heather Marlow
Journal:  Nat Rev Neurosci       Date:  2016-01       Impact factor: 34.870

3.  Xenacoelomorpha: a case of independent nervous system centralization?

Authors:  Brenda Gavilán; Elena Perea-Atienza; Pedro Martínez
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-01-05       Impact factor: 6.237

4.  Mechanisms of cnidocyte development in the moon jellyfish Aurelia.

Authors:  David A Gold; Clive Long Fung Lau; Holly Fuong; Gregory Kao; Volker Hartenstein; David K Jacobs
Journal:  Evol Dev       Date:  2019-01-08       Impact factor: 1.930

Review 5.  Back to the Basics: Cnidarians Start to Fire.

Authors:  Thomas C G Bosch; Alexander Klimovich; Tomislav Domazet-Lošo; Stefan Gründer; Thomas W Holstein; Gáspár Jékely; David J Miller; Andrea P Murillo-Rincon; Fabian Rentzsch; Gemma S Richards; Katja Schröder; Ulrich Technau; Rafael Yuste
Journal:  Trends Neurosci       Date:  2016-12-30       Impact factor: 13.837

6.  Ecological constraints on the origin of neurones.

Authors:  Travis Monk; Michael G Paulin; Peter Green
Journal:  J Math Biol       Date:  2015-02-20       Impact factor: 2.259

Review 7.  Neuronal polarity: an evolutionary perspective.

Authors:  Melissa M Rolls; Timothy J Jegla
Journal:  J Exp Biol       Date:  2015-02-15       Impact factor: 3.312

8.  Neurogenesis in the sea urchin embryo is initiated uniquely in three domains.

Authors:  David R McClay; Esther Miranda; Stacy L Feinberg
Journal:  Development       Date:  2018-11-09       Impact factor: 6.868

Review 9.  Old cell, new trick? Cnidocytes as a model for the evolution of novelty.

Authors:  Leslie S Babonis; Mark Q Martindale
Journal:  Integr Comp Biol       Date:  2014-04-25       Impact factor: 3.326

10.  Aryl hydrocarbon receptor (AHR) in the cnidarian Nematostella vectensis: comparative expression, protein interactions, and ligand binding.

Authors:  Adam M Reitzel; Yale J Passamaneck; Sibel I Karchner; Diana G Franks; Mark Q Martindale; Ann M Tarrant; Mark E Hahn
Journal:  Dev Genes Evol       Date:  2013-11-29       Impact factor: 0.900

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