Literature DB >> 17301244

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation.

Patrick R H Steinmetz1, Fabiola Zelada-Gonzáles, Carola Burgtorf, Joachim Wittbrodt, Detlev Arendt.   

Abstract

During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball- into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.

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Year:  2007        PMID: 17301244      PMCID: PMC1815249          DOI: 10.1073/pnas.0606589104

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  43 in total

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Journal:  Mech Dev       Date:  1996-02       Impact factor: 1.882

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Journal:  Development       Date:  1990-04       Impact factor: 6.868

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  20 in total

1.  Hedgehog signaling regulates segment formation in the annelid Platynereis.

Authors:  Nicolas Dray; Kristin Tessmar-Raible; Martine Le Gouar; Laura Vibert; Foteini Christodoulou; Katharina Schipany; Aurélien Guillou; Juliane Zantke; Heidi Snyman; Julien Béhague; Michel Vervoort; Detlev Arendt; Guillaume Balavoine
Journal:  Science       Date:  2010-07-16       Impact factor: 47.728

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

Review 3.  Acoel development supports a simple planula-like urbilaterian.

Authors:  Andreas Hejnol; Mark Q Martindale
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2008-04-27       Impact factor: 6.237

4.  Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra.

Authors:  Isabelle Philipp; Roland Aufschnaiter; Suat Ozbek; Stefanie Pontasch; Marcell Jenewein; Hiroshi Watanabe; Fabian Rentzsch; Thomas W Holstein; Bert Hobmayer
Journal:  Proc Natl Acad Sci U S A       Date:  2009-02-23       Impact factor: 11.205

5.  Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii.

Authors:  Adrien Demilly; Patrick Steinmetz; Eve Gazave; Lauriane Marchand; Michel Vervoort
Journal:  Nat Commun       Date:  2013       Impact factor: 14.919

6.  Fate map and morphogenesis of presumptive neural crest and dorsal neural tube.

Authors:  Akouavi M Ezin; Scott E Fraser; Marianne Bronner-Fraser
Journal:  Dev Biol       Date:  2009-03-28       Impact factor: 3.582

7.  Six3 demarcates the anterior-most developing brain region in bilaterian animals.

Authors:  Patrick Rh Steinmetz; Rolf Urbach; Nico Posnien; Joakim Eriksson; Roman P Kostyuchenko; Carlo Brena; Keren Guy; Michael Akam; Gregor Bucher; Detlev Arendt
Journal:  Evodevo       Date:  2010-12-29       Impact factor: 2.250

8.  The normal development of Platynereis dumerilii (Nereididae, Annelida).

Authors:  Antje Hl Fischer; Thorsten Henrich; Detlev Arendt
Journal:  Front Zool       Date:  2010-12-30       Impact factor: 3.172

9.  Large-scale clonal analysis reveals unexpected complexity in surface ectoderm morphogenesis.

Authors:  Anne-Cécile Petit; Jean-François Nicolas
Journal:  PLoS One       Date:  2009-02-06       Impact factor: 3.240

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Authors:  Ben Steventon; Roberto Mayor; Andrea Streit
Journal:  Dev Biol       Date:  2012-04-28       Impact factor: 3.582

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