VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.

Neuritogenesis is a critical early step in the development and maturation of neurons and neuronal circuits. While extracellular directional cues are known to specify the site and orientation of nascent neurite formation in vivo, little is known about the genetic pathways that block inappropriate neu...

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Main Authors: Leticia Sanchez-Alvarez, Jiravat Visanuvimol, Andrea McEwan, Anna Su, Janice H Imai, Antonio Colavita
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-09-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3164692?pdf=render
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spelling doaj-4062dd55cc334f0ab969c483533439b52020-11-25T02:01:21ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042011-09-0179e100225710.1371/journal.pgen.1002257VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.Leticia Sanchez-AlvarezJiravat VisanuvimolAndrea McEwanAnna SuJanice H ImaiAntonio ColavitaNeuritogenesis is a critical early step in the development and maturation of neurons and neuronal circuits. While extracellular directional cues are known to specify the site and orientation of nascent neurite formation in vivo, little is known about the genetic pathways that block inappropriate neurite emergence in order to maintain proper neuronal polarity. Here we report that the Caenorhabditis elegans orthologues of Van Gogh (vang-1), Prickle (prkl-1), and Dishevelled (dsh-1), core components of planar cell polarity (PCP) signaling, are required in a subset of peripheral motor neurons to restrict neurite emergence to a specific organ axis. In loss-of-function mutants, neurons display supernumerary neurites that extend inappropriately along the orthogonal anteroposterior (A/P) body axis. We show that autonomous and non-autonomous gene activities are required early and persistently to inhibit the formation or consolidation of growth cone protrusions directed away from organ precursor cells. Furthermore, prkl-1 overexpression is sufficient to suppress neurite formation and reorient neuronal polarity in a vang-1- and dsh-1-dependent manner. Our findings suggest a novel role for a PCP-like pathway in maintaining polarized neuronal morphology by inhibiting neuronal responses to extrinsic or intrinsic cues that would otherwise promote extraneous neurite formation.http://europepmc.org/articles/PMC3164692?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Leticia Sanchez-Alvarez
Jiravat Visanuvimol
Andrea McEwan
Anna Su
Janice H Imai
Antonio Colavita
spellingShingle Leticia Sanchez-Alvarez
Jiravat Visanuvimol
Andrea McEwan
Anna Su
Janice H Imai
Antonio Colavita
VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
PLoS Genetics
author_facet Leticia Sanchez-Alvarez
Jiravat Visanuvimol
Andrea McEwan
Anna Su
Janice H Imai
Antonio Colavita
author_sort Leticia Sanchez-Alvarez
title VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
title_short VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
title_full VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
title_fullStr VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
title_full_unstemmed VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans.
title_sort vang-1 and prkl-1 cooperate to negatively regulate neurite formation in caenorhabditis elegans.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2011-09-01
description Neuritogenesis is a critical early step in the development and maturation of neurons and neuronal circuits. While extracellular directional cues are known to specify the site and orientation of nascent neurite formation in vivo, little is known about the genetic pathways that block inappropriate neurite emergence in order to maintain proper neuronal polarity. Here we report that the Caenorhabditis elegans orthologues of Van Gogh (vang-1), Prickle (prkl-1), and Dishevelled (dsh-1), core components of planar cell polarity (PCP) signaling, are required in a subset of peripheral motor neurons to restrict neurite emergence to a specific organ axis. In loss-of-function mutants, neurons display supernumerary neurites that extend inappropriately along the orthogonal anteroposterior (A/P) body axis. We show that autonomous and non-autonomous gene activities are required early and persistently to inhibit the formation or consolidation of growth cone protrusions directed away from organ precursor cells. Furthermore, prkl-1 overexpression is sufficient to suppress neurite formation and reorient neuronal polarity in a vang-1- and dsh-1-dependent manner. Our findings suggest a novel role for a PCP-like pathway in maintaining polarized neuronal morphology by inhibiting neuronal responses to extrinsic or intrinsic cues that would otherwise promote extraneous neurite formation.
url http://europepmc.org/articles/PMC3164692?pdf=render
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