Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.

Local mRNA translation in neurons has been mostly studied during axon guidance and synapse formation but not during initial neurite outgrowth. We performed a genome-wide screen for neurite-enriched mRNAs and identified an mRNA that encodes mitogen-activated protein kinase kinase 7 (MKK7), a MAP kina...

Full description

Saved in:
Bibliographic Details
Main Authors: Daniel Feltrin, Ludovico Fusco, Harald Witte, Francesca Moretti, Katrin Martin, Michel Letzelter, Erika Fluri, Peter Scheiffele, Olivier Pertz
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001439&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850190107448967168
author Daniel Feltrin
Ludovico Fusco
Harald Witte
Francesca Moretti
Katrin Martin
Michel Letzelter
Erika Fluri
Peter Scheiffele
Olivier Pertz
author_facet Daniel Feltrin
Ludovico Fusco
Harald Witte
Francesca Moretti
Katrin Martin
Michel Letzelter
Erika Fluri
Peter Scheiffele
Olivier Pertz
author_sort Daniel Feltrin
collection DOAJ
description Local mRNA translation in neurons has been mostly studied during axon guidance and synapse formation but not during initial neurite outgrowth. We performed a genome-wide screen for neurite-enriched mRNAs and identified an mRNA that encodes mitogen-activated protein kinase kinase 7 (MKK7), a MAP kinase kinase (MAPKK) for Jun kinase (JNK). We show that MKK7 mRNA localizes to the growth cone where it has the potential to be translated. MKK7 is then specifically phosphorylated in the neurite shaft, where it is part of a MAP kinase signaling module consisting of dual leucine zipper kinase (DLK), MKK7, and JNK1. This triggers Map1b phosphorylation to regulate microtubule bundling leading to neurite elongation. We propose a model in which MKK7 mRNA localization and translation in the growth cone allows for a mechanism to position JNK signaling in the neurite shaft and to specifically link it to regulation of microtubule bundling. At the same time, this uncouples activated JNK from its functions relevant to nuclear translocation and transcriptional activation.
format Article
id doaj-art-e0f85f53c3be48a79bd2cb15430d2472
institution OA Journals
issn 1544-9173
1545-7885
language English
publishDate 2012-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-e0f85f53c3be48a79bd2cb15430d24722025-08-20T02:15:24ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852012-01-011012e100143910.1371/journal.pbio.1001439Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.Daniel FeltrinLudovico FuscoHarald WitteFrancesca MorettiKatrin MartinMichel LetzelterErika FluriPeter ScheiffeleOlivier PertzLocal mRNA translation in neurons has been mostly studied during axon guidance and synapse formation but not during initial neurite outgrowth. We performed a genome-wide screen for neurite-enriched mRNAs and identified an mRNA that encodes mitogen-activated protein kinase kinase 7 (MKK7), a MAP kinase kinase (MAPKK) for Jun kinase (JNK). We show that MKK7 mRNA localizes to the growth cone where it has the potential to be translated. MKK7 is then specifically phosphorylated in the neurite shaft, where it is part of a MAP kinase signaling module consisting of dual leucine zipper kinase (DLK), MKK7, and JNK1. This triggers Map1b phosphorylation to regulate microtubule bundling leading to neurite elongation. We propose a model in which MKK7 mRNA localization and translation in the growth cone allows for a mechanism to position JNK signaling in the neurite shaft and to specifically link it to regulation of microtubule bundling. At the same time, this uncouples activated JNK from its functions relevant to nuclear translocation and transcriptional activation.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001439&type=printable
spellingShingle Daniel Feltrin
Ludovico Fusco
Harald Witte
Francesca Moretti
Katrin Martin
Michel Letzelter
Erika Fluri
Peter Scheiffele
Olivier Pertz
Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
PLoS Biology
title Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
title_full Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
title_fullStr Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
title_full_unstemmed Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
title_short Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation.
title_sort growth cone mkk7 mrna targeting regulates map1b dependent microtubule bundling to control neurite elongation
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001439&type=printable
work_keys_str_mv AT danielfeltrin growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT ludovicofusco growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT haraldwitte growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT francescamoretti growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT katrinmartin growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT michelletzelter growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT erikafluri growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT peterscheiffele growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation
AT olivierpertz growthconemkk7mrnatargetingregulatesmap1bdependentmicrotubulebundlingtocontrolneuriteelongation