Loading…

Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration

As an essential step for brain morphogenesis, neurons migrate via mechanical interactions with components of their environment such as neighboring cells and the extracellular matrix. However, the molecular mechanism by which neurons exert forces on their environment during migration remains poorly u...

Full description

Saved in:
Bibliographic Details
Published in:Cell reports (Cambridge) 2018-10, Vol.25 (3), p.624-639.e6
Main Authors: Minegishi, Takunori, Uesugi, Yasuyuki, Kaneko, Naoko, Yoshida, Wataru, Sawamoto, Kazunobu, Inagaki, Naoyuki
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33
cites cdi_FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33
container_end_page 639.e6
container_issue 3
container_start_page 624
container_title Cell reports (Cambridge)
container_volume 25
creator Minegishi, Takunori
Uesugi, Yasuyuki
Kaneko, Naoko
Yoshida, Wataru
Sawamoto, Kazunobu
Inagaki, Naoyuki
description As an essential step for brain morphogenesis, neurons migrate via mechanical interactions with components of their environment such as neighboring cells and the extracellular matrix. However, the molecular mechanism by which neurons exert forces on their environment during migration remains poorly understood. Here, we show that shootin1b is expressed in migrating mouse olfactory interneurons and accumulates at their leading process growth cone. We demonstrate that shootin1b, by binding to cortactin and L1-CAM, couples F-actin retrograde flow and the adhesive substrate as a clutch molecule. Shootin1b-mediated clutch coupling at the growth cone generates traction force on the substrate, thereby promoting leading process extension and subsequent somal translocation of olfactory interneurons. Furthermore, loss of shootin1 causes abnormal positioning of the interneurons and dysgenesis of the olfactory bulb. Our findings indicate that shootin1b plays a key role in force-driven leading process extension, which propels the migration of olfactory interneurons during olfactory bulb formation. [Display omitted] •Shootin1b accumulates at the leading process growth cone of olfactory interneurons•Shootin1b couples F-actin retrograde flow and cell adhesions as a clutch molecule•The shootin1b-mediated clutch coupling generates force for neuronal migration•Loss of shootin1 inhibits rostral migration of olfactory interneurons in the brain Minegishi et al. use gene knockout, protein interaction assays, force microscopy, speckle imaging, and migration assays to analyze the molecular mechanics driving neuronal migration in vivo. Their data demonstrate that shootin1b mediates a mechanical clutch to produce force for the migration of olfactory interneurons in the brain.
doi_str_mv 10.1016/j.celrep.2018.09.068
format article
fullrecord <record><control><sourceid>pubmed_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_7efeb1673dd5422ca437164cfb0ebaae</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S2211124718315286</els_id><doaj_id>oai_doaj_org_article_7efeb1673dd5422ca437164cfb0ebaae</doaj_id><sourcerecordid>30332643</sourcerecordid><originalsourceid>FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33</originalsourceid><addsrcrecordid>eNp9kNtKxDAQhoMoKqtvINIX2JpJ0rS5EWTxBJ5AvQ45TN0stVnSruDbG62KV-ZiMiT__0_yEXIEtAQK8mRVOuwSrktGoSmpKqlstsg-YwBzYKLe_tPvkcNhWNG8JAVQYpfscco5k4Lvk7vHZYxj6MEWt-iDGXEoTG7d0vTBma5YdJvRLYsxFg8p-o3D4iKmXNuYijvcpNhn0W14SWYMsT8gO63pBjz83mfk-eL8aXE1v7m_vF6c3cxdVcE4F4YZJaznvnaCMycbSRufa6Vko_INeLRKVIZWtLJC2kYIxfNfODBQnvMZuZ5yfTQrvU7h1aR3HU3QXwcxvWiTxuA61DW2aEHW3PtKMOaM4DVI4VpL0RqDOUtMWS7FYUjY_uYB1Z-09UpPtPUnbU2VzrSz7XiyrTf2Ff2v6YdtFpxOAswg3gImPbiAvcuYE7oxvzT8P-EDW8GQbA</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration</title><source>BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS</source><creator>Minegishi, Takunori ; Uesugi, Yasuyuki ; Kaneko, Naoko ; Yoshida, Wataru ; Sawamoto, Kazunobu ; Inagaki, Naoyuki</creator><creatorcontrib>Minegishi, Takunori ; Uesugi, Yasuyuki ; Kaneko, Naoko ; Yoshida, Wataru ; Sawamoto, Kazunobu ; Inagaki, Naoyuki</creatorcontrib><description>As an essential step for brain morphogenesis, neurons migrate via mechanical interactions with components of their environment such as neighboring cells and the extracellular matrix. However, the molecular mechanism by which neurons exert forces on their environment during migration remains poorly understood. Here, we show that shootin1b is expressed in migrating mouse olfactory interneurons and accumulates at their leading process growth cone. We demonstrate that shootin1b, by binding to cortactin and L1-CAM, couples F-actin retrograde flow and the adhesive substrate as a clutch molecule. Shootin1b-mediated clutch coupling at the growth cone generates traction force on the substrate, thereby promoting leading process extension and subsequent somal translocation of olfactory interneurons. Furthermore, loss of shootin1 causes abnormal positioning of the interneurons and dysgenesis of the olfactory bulb. Our findings indicate that shootin1b plays a key role in force-driven leading process extension, which propels the migration of olfactory interneurons during olfactory bulb formation. [Display omitted] •Shootin1b accumulates at the leading process growth cone of olfactory interneurons•Shootin1b couples F-actin retrograde flow and cell adhesions as a clutch molecule•The shootin1b-mediated clutch coupling generates force for neuronal migration•Loss of shootin1 inhibits rostral migration of olfactory interneurons in the brain Minegishi et al. use gene knockout, protein interaction assays, force microscopy, speckle imaging, and migration assays to analyze the molecular mechanics driving neuronal migration in vivo. Their data demonstrate that shootin1b mediates a mechanical clutch to produce force for the migration of olfactory interneurons in the brain.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2018.09.068</identifier><identifier>PMID: 30332643</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Actins - metabolism ; Animals ; Brain - cytology ; Brain - physiology ; Cell Adhesion ; Cell Movement ; Cells, Cultured ; clutch molecule ; Female ; growth cone ; Growth Cones - physiology ; interneuron ; Interneurons - cytology ; Interneurons - physiology ; L1-CAM ; leading process ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Inbred ICR ; Mice, Knockout ; Nerve Tissue Proteins - physiology ; neuronal migration ; olfactory bulb ; Olfactory Bulb - cytology ; Olfactory Bulb - physiology ; Rats, Wistar ; shootin1</subject><ispartof>Cell reports (Cambridge), 2018-10, Vol.25 (3), p.624-639.e6</ispartof><rights>2018 The Authors</rights><rights>Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33</citedby><cites>FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30332643$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Minegishi, Takunori</creatorcontrib><creatorcontrib>Uesugi, Yasuyuki</creatorcontrib><creatorcontrib>Kaneko, Naoko</creatorcontrib><creatorcontrib>Yoshida, Wataru</creatorcontrib><creatorcontrib>Sawamoto, Kazunobu</creatorcontrib><creatorcontrib>Inagaki, Naoyuki</creatorcontrib><title>Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>As an essential step for brain morphogenesis, neurons migrate via mechanical interactions with components of their environment such as neighboring cells and the extracellular matrix. However, the molecular mechanism by which neurons exert forces on their environment during migration remains poorly understood. Here, we show that shootin1b is expressed in migrating mouse olfactory interneurons and accumulates at their leading process growth cone. We demonstrate that shootin1b, by binding to cortactin and L1-CAM, couples F-actin retrograde flow and the adhesive substrate as a clutch molecule. Shootin1b-mediated clutch coupling at the growth cone generates traction force on the substrate, thereby promoting leading process extension and subsequent somal translocation of olfactory interneurons. Furthermore, loss of shootin1 causes abnormal positioning of the interneurons and dysgenesis of the olfactory bulb. Our findings indicate that shootin1b plays a key role in force-driven leading process extension, which propels the migration of olfactory interneurons during olfactory bulb formation. [Display omitted] •Shootin1b accumulates at the leading process growth cone of olfactory interneurons•Shootin1b couples F-actin retrograde flow and cell adhesions as a clutch molecule•The shootin1b-mediated clutch coupling generates force for neuronal migration•Loss of shootin1 inhibits rostral migration of olfactory interneurons in the brain Minegishi et al. use gene knockout, protein interaction assays, force microscopy, speckle imaging, and migration assays to analyze the molecular mechanics driving neuronal migration in vivo. Their data demonstrate that shootin1b mediates a mechanical clutch to produce force for the migration of olfactory interneurons in the brain.</description><subject>Actins - metabolism</subject><subject>Animals</subject><subject>Brain - cytology</subject><subject>Brain - physiology</subject><subject>Cell Adhesion</subject><subject>Cell Movement</subject><subject>Cells, Cultured</subject><subject>clutch molecule</subject><subject>Female</subject><subject>growth cone</subject><subject>Growth Cones - physiology</subject><subject>interneuron</subject><subject>Interneurons - cytology</subject><subject>Interneurons - physiology</subject><subject>L1-CAM</subject><subject>leading process</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Inbred ICR</subject><subject>Mice, Knockout</subject><subject>Nerve Tissue Proteins - physiology</subject><subject>neuronal migration</subject><subject>olfactory bulb</subject><subject>Olfactory Bulb - cytology</subject><subject>Olfactory Bulb - physiology</subject><subject>Rats, Wistar</subject><subject>shootin1</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9kNtKxDAQhoMoKqtvINIX2JpJ0rS5EWTxBJ5AvQ45TN0stVnSruDbG62KV-ZiMiT__0_yEXIEtAQK8mRVOuwSrktGoSmpKqlstsg-YwBzYKLe_tPvkcNhWNG8JAVQYpfscco5k4Lvk7vHZYxj6MEWt-iDGXEoTG7d0vTBma5YdJvRLYsxFg8p-o3D4iKmXNuYijvcpNhn0W14SWYMsT8gO63pBjz83mfk-eL8aXE1v7m_vF6c3cxdVcE4F4YZJaznvnaCMycbSRufa6Vko_INeLRKVIZWtLJC2kYIxfNfODBQnvMZuZ5yfTQrvU7h1aR3HU3QXwcxvWiTxuA61DW2aEHW3PtKMOaM4DVI4VpL0RqDOUtMWS7FYUjY_uYB1Z-09UpPtPUnbU2VzrSz7XiyrTf2Ff2v6YdtFpxOAswg3gImPbiAvcuYE7oxvzT8P-EDW8GQbA</recordid><startdate>20181016</startdate><enddate>20181016</enddate><creator>Minegishi, Takunori</creator><creator>Uesugi, Yasuyuki</creator><creator>Kaneko, Naoko</creator><creator>Yoshida, Wataru</creator><creator>Sawamoto, Kazunobu</creator><creator>Inagaki, Naoyuki</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>DOA</scope></search><sort><creationdate>20181016</creationdate><title>Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration</title><author>Minegishi, Takunori ; Uesugi, Yasuyuki ; Kaneko, Naoko ; Yoshida, Wataru ; Sawamoto, Kazunobu ; Inagaki, Naoyuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Actins - metabolism</topic><topic>Animals</topic><topic>Brain - cytology</topic><topic>Brain - physiology</topic><topic>Cell Adhesion</topic><topic>Cell Movement</topic><topic>Cells, Cultured</topic><topic>clutch molecule</topic><topic>Female</topic><topic>growth cone</topic><topic>Growth Cones - physiology</topic><topic>interneuron</topic><topic>Interneurons - cytology</topic><topic>Interneurons - physiology</topic><topic>L1-CAM</topic><topic>leading process</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Inbred ICR</topic><topic>Mice, Knockout</topic><topic>Nerve Tissue Proteins - physiology</topic><topic>neuronal migration</topic><topic>olfactory bulb</topic><topic>Olfactory Bulb - cytology</topic><topic>Olfactory Bulb - physiology</topic><topic>Rats, Wistar</topic><topic>shootin1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Minegishi, Takunori</creatorcontrib><creatorcontrib>Uesugi, Yasuyuki</creatorcontrib><creatorcontrib>Kaneko, Naoko</creatorcontrib><creatorcontrib>Yoshida, Wataru</creatorcontrib><creatorcontrib>Sawamoto, Kazunobu</creatorcontrib><creatorcontrib>Inagaki, Naoyuki</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Minegishi, Takunori</au><au>Uesugi, Yasuyuki</au><au>Kaneko, Naoko</au><au>Yoshida, Wataru</au><au>Sawamoto, Kazunobu</au><au>Inagaki, Naoyuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2018-10-16</date><risdate>2018</risdate><volume>25</volume><issue>3</issue><spage>624</spage><epage>639.e6</epage><pages>624-639.e6</pages><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>As an essential step for brain morphogenesis, neurons migrate via mechanical interactions with components of their environment such as neighboring cells and the extracellular matrix. However, the molecular mechanism by which neurons exert forces on their environment during migration remains poorly understood. Here, we show that shootin1b is expressed in migrating mouse olfactory interneurons and accumulates at their leading process growth cone. We demonstrate that shootin1b, by binding to cortactin and L1-CAM, couples F-actin retrograde flow and the adhesive substrate as a clutch molecule. Shootin1b-mediated clutch coupling at the growth cone generates traction force on the substrate, thereby promoting leading process extension and subsequent somal translocation of olfactory interneurons. Furthermore, loss of shootin1 causes abnormal positioning of the interneurons and dysgenesis of the olfactory bulb. Our findings indicate that shootin1b plays a key role in force-driven leading process extension, which propels the migration of olfactory interneurons during olfactory bulb formation. [Display omitted] •Shootin1b accumulates at the leading process growth cone of olfactory interneurons•Shootin1b couples F-actin retrograde flow and cell adhesions as a clutch molecule•The shootin1b-mediated clutch coupling generates force for neuronal migration•Loss of shootin1 inhibits rostral migration of olfactory interneurons in the brain Minegishi et al. use gene knockout, protein interaction assays, force microscopy, speckle imaging, and migration assays to analyze the molecular mechanics driving neuronal migration in vivo. Their data demonstrate that shootin1b mediates a mechanical clutch to produce force for the migration of olfactory interneurons in the brain.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30332643</pmid><doi>10.1016/j.celrep.2018.09.068</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2211-1247
ispartof Cell reports (Cambridge), 2018-10, Vol.25 (3), p.624-639.e6
issn 2211-1247
2211-1247
language eng
recordid cdi_doaj_primary_oai_doaj_org_article_7efeb1673dd5422ca437164cfb0ebaae
source BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS
subjects Actins - metabolism
Animals
Brain - cytology
Brain - physiology
Cell Adhesion
Cell Movement
Cells, Cultured
clutch molecule
Female
growth cone
Growth Cones - physiology
interneuron
Interneurons - cytology
Interneurons - physiology
L1-CAM
leading process
Male
Mice
Mice, Inbred C57BL
Mice, Inbred ICR
Mice, Knockout
Nerve Tissue Proteins - physiology
neuronal migration
olfactory bulb
Olfactory Bulb - cytology
Olfactory Bulb - physiology
Rats, Wistar
shootin1
title Shootin1b Mediates a Mechanical Clutch to Produce Force for Neuronal Migration
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T07%3A08%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-pubmed_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Shootin1b%20Mediates%20a%20Mechanical%20Clutch%20to%20Produce%20Force%20for%20Neuronal%20Migration&rft.jtitle=Cell%20reports%20(Cambridge)&rft.au=Minegishi,%20Takunori&rft.date=2018-10-16&rft.volume=25&rft.issue=3&rft.spage=624&rft.epage=639.e6&rft.pages=624-639.e6&rft.issn=2211-1247&rft.eissn=2211-1247&rft_id=info:doi/10.1016/j.celrep.2018.09.068&rft_dat=%3Cpubmed_doaj_%3E30332643%3C/pubmed_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c551t-4a2a94bd3d7c432c68608d6865968994b1deb945a0505b46b8449324731219d33%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_id=info:pmid/30332643&rfr_iscdi=true