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...
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| Veröffentlicht in: | PLoS biology 2012-12, Vol.10 (12), p.e1001439-e1001439 |
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| creator | Feltrin, Daniel Fusco, Ludovico Witte, Harald Moretti, Francesca Martin, Katrin Letzelter, Michel Fluri, Erika Scheiffele, Peter Pertz, Olivier |
| 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. |
| doi_str_mv | 10.1371/journal.pbio.1001439 |
| format | Article |
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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.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.1001439</identifier><identifier>PMID: 23226105</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3' Untranslated Regions - genetics ; Animals ; Base Sequence ; Biology ; Cell Differentiation ; Cell Line ; Cells ; Genetic aspects ; Genetic translation ; Genome - genetics ; Growth Cones - enzymology ; Health aspects ; Hippocampus - cytology ; JNK Mitogen-Activated Protein Kinases - metabolism ; Kinases ; MAP Kinase Kinase 7 - metabolism ; MAP Kinase Signaling System ; Messenger RNA ; Mice ; Microtubule-Associated Proteins - metabolism ; Microtubules - metabolism ; Mitogen-activated protein kinases ; Models, Biological ; Neural transmission ; Neurites - enzymology ; Neurites - metabolism ; Neurons ; Phosphorylation ; Phosphothreonine - metabolism ; Physiological aspects ; Protein Biosynthesis ; Proteins ; Reproducibility of Results ; RNA Transport ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Time Factors</subject><ispartof>PLoS biology, 2012-12, Vol.10 (12), p.e1001439-e1001439</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Feltrin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Feltrin D, Fusco L, Witte H, Moretti F, Martin K, et al. (2012) Growth Cone MKK7 mRNA Targeting Regulates MAP1b-Dependent Microtubule Bundling to Control Neurite Elongation. 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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.</description><subject>3' Untranslated Regions - genetics</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Biology</subject><subject>Cell Differentiation</subject><subject>Cell Line</subject><subject>Cells</subject><subject>Genetic aspects</subject><subject>Genetic translation</subject><subject>Genome - genetics</subject><subject>Growth Cones - enzymology</subject><subject>Health aspects</subject><subject>Hippocampus - cytology</subject><subject>JNK Mitogen-Activated Protein Kinases - metabolism</subject><subject>Kinases</subject><subject>MAP Kinase Kinase 7 - metabolism</subject><subject>MAP Kinase Signaling System</subject><subject>Messenger RNA</subject><subject>Mice</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Microtubules - metabolism</subject><subject>Mitogen-activated protein kinases</subject><subject>Models, Biological</subject><subject>Neural transmission</subject><subject>Neurites - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Feltrin, Daniel</au><au>Fusco, Ludovico</au><au>Witte, Harald</au><au>Moretti, Francesca</au><au>Martin, Katrin</au><au>Letzelter, Michel</au><au>Fluri, Erika</au><au>Scheiffele, Peter</au><au>Pertz, Olivier</au><au>Holt, Christine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2012-12-01</date><risdate>2012</risdate><volume>10</volume><issue>12</issue><spage>e1001439</spage><epage>e1001439</epage><pages>e1001439-e1001439</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23226105</pmid><doi>10.1371/journal.pbio.1001439</doi><oa>free_for_read</oa></addata></record> |
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| subjects | 3' Untranslated Regions - genetics Animals Base Sequence Biology Cell Differentiation Cell Line Cells Genetic aspects Genetic translation Genome - genetics Growth Cones - enzymology Health aspects Hippocampus - cytology JNK Mitogen-Activated Protein Kinases - metabolism Kinases MAP Kinase Kinase 7 - metabolism MAP Kinase Signaling System Messenger RNA Mice Microtubule-Associated Proteins - metabolism Microtubules - metabolism Mitogen-activated protein kinases Models, Biological Neural transmission Neurites - enzymology Neurites - metabolism Neurons Phosphorylation Phosphothreonine - metabolism Physiological aspects Protein Biosynthesis Proteins Reproducibility of Results RNA Transport RNA, Messenger - genetics RNA, Messenger - metabolism Time Factors |
| title | Growth cone MKK7 mRNA targeting regulates MAP1b-dependent microtubule bundling to control neurite elongation |
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