Directed Migration of Cortical Interneurons Depends on the Cell-Autonomous Action of Sip1
GABAergic interneurons mainly originate in the medial ganglionic eminence (MGE) of the embryonic ventral telencephalon (VT) and migrate tangentially to the cortex, guided by membrane-bound and secreted factors. We found that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2013-01, Vol.77 (1), p.70-82 |
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| creator | van den Berghe, Veronique Stappers, Elke Vandesande, Bram Dimidschstein, Jordane Kroes, Roel Francis, Annick Conidi, Andrea Lesage, Flore Dries, Ruben Cazzola, Silvia Berx, Geert Kessaris, Nicoletta Vanderhaeghen, Pierre van IJcken, Wilfred Grosveld, Frank G. Goossens, Steven Haigh, Jody J. Fishell, Gord Goffinet, André Aerts, Stein Huylebroeck, Danny Seuntjens, Eve |
| description | GABAergic interneurons mainly originate in the medial ganglionic eminence (MGE) of the embryonic ventral telencephalon (VT) and migrate tangentially to the cortex, guided by membrane-bound and secreted factors. We found that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, is required for their proper differentiation and correct guidance. The majority of Sip1 knockout interneurons fail to migrate to the neocortex and stall in the VT. RNA sequencing reveals that Sip1 knockout interneurons do not acquire a fully mature cortical interneuron identity and contain increased levels of the repulsive receptor Unc5b. Focal electroporation of Unc5b-encoding vectors in the MGE of wild-type brain slices disturbs migration to the neocortex, whereas reducing Unc5b levels in Sip1 knockout slices and brains rescues the migration defect. Our results reveal that Sip1, through tuning of Unc5b levels, is essential for cortical interneuron guidance.
► Sip1 is crucial for directed cortical interneuron migration ► RNA sequencing identifies Sip1-dependent differentiation and guidance factors ► Sip1 is essential to constrain the expression level of Unc5b in the MGE ► Tuning of Unc5b expression level regulates the direction of interneuron migration
Van den Berghe et al. demonstrate that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, controls their differentiation and directed migration. Through regulating Unc5b expression, Sip1 contributes to efficient guided migration during brain development in the embryo. |
| doi_str_mv | 10.1016/j.neuron.2012.11.009 |
| format | Article |
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► Sip1 is crucial for directed cortical interneuron migration ► RNA sequencing identifies Sip1-dependent differentiation and guidance factors ► Sip1 is essential to constrain the expression level of Unc5b in the MGE ► Tuning of Unc5b expression level regulates the direction of interneuron migration
Van den Berghe et al. demonstrate that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, controls their differentiation and directed migration. Through regulating Unc5b expression, Sip1 contributes to efficient guided migration during brain development in the embryo.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2012.11.009</identifier><identifier>PMID: 23312517</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Brain slice preparation ; Cell Movement - physiology ; Cerebral Cortex - cytology ; Cerebral Cortex - growth & development ; Gene Knockout Techniques ; Interneurons - physiology ; Mice ; Mice, Transgenic ; Migration ; Neocortex - cytology ; Neocortex - growth & development ; Nerve Tissue Proteins - deficiency ; Nerve Tissue Proteins - genetics ; Netrin Receptors ; Neurons ; Organ Culture Techniques ; Receptors, Cell Surface - deficiency ; Receptors, Cell Surface - genetics ; Rodents ; Telencephalon - cytology ; Telencephalon - growth & development ; Transcription factors</subject><ispartof>Neuron (Cambridge, Mass.), 2013-01, Vol.77 (1), p.70-82</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Jan 9, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c535t-96b4b9b7c72600a47cf45d3acd1496197cc121462d76b8a14597b82c546a3f2c3</citedby><cites>FETCH-LOGICAL-c535t-96b4b9b7c72600a47cf45d3acd1496197cc121462d76b8a14597b82c546a3f2c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0896627312010008$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23312517$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van den Berghe, Veronique</creatorcontrib><creatorcontrib>Stappers, Elke</creatorcontrib><creatorcontrib>Vandesande, Bram</creatorcontrib><creatorcontrib>Dimidschstein, Jordane</creatorcontrib><creatorcontrib>Kroes, Roel</creatorcontrib><creatorcontrib>Francis, Annick</creatorcontrib><creatorcontrib>Conidi, Andrea</creatorcontrib><creatorcontrib>Lesage, Flore</creatorcontrib><creatorcontrib>Dries, Ruben</creatorcontrib><creatorcontrib>Cazzola, Silvia</creatorcontrib><creatorcontrib>Berx, Geert</creatorcontrib><creatorcontrib>Kessaris, Nicoletta</creatorcontrib><creatorcontrib>Vanderhaeghen, Pierre</creatorcontrib><creatorcontrib>van IJcken, Wilfred</creatorcontrib><creatorcontrib>Grosveld, Frank G.</creatorcontrib><creatorcontrib>Goossens, Steven</creatorcontrib><creatorcontrib>Haigh, Jody J.</creatorcontrib><creatorcontrib>Fishell, Gord</creatorcontrib><creatorcontrib>Goffinet, André</creatorcontrib><creatorcontrib>Aerts, Stein</creatorcontrib><creatorcontrib>Huylebroeck, Danny</creatorcontrib><creatorcontrib>Seuntjens, Eve</creatorcontrib><title>Directed Migration of Cortical Interneurons Depends on the Cell-Autonomous Action of Sip1</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>GABAergic interneurons mainly originate in the medial ganglionic eminence (MGE) of the embryonic ventral telencephalon (VT) and migrate tangentially to the cortex, guided by membrane-bound and secreted factors. We found that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, is required for their proper differentiation and correct guidance. The majority of Sip1 knockout interneurons fail to migrate to the neocortex and stall in the VT. RNA sequencing reveals that Sip1 knockout interneurons do not acquire a fully mature cortical interneuron identity and contain increased levels of the repulsive receptor Unc5b. Focal electroporation of Unc5b-encoding vectors in the MGE of wild-type brain slices disturbs migration to the neocortex, whereas reducing Unc5b levels in Sip1 knockout slices and brains rescues the migration defect. Our results reveal that Sip1, through tuning of Unc5b levels, is essential for cortical interneuron guidance.
► Sip1 is crucial for directed cortical interneuron migration ► RNA sequencing identifies Sip1-dependent differentiation and guidance factors ► Sip1 is essential to constrain the expression level of Unc5b in the MGE ► Tuning of Unc5b expression level regulates the direction of interneuron migration
Van den Berghe et al. demonstrate that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, controls their differentiation and directed migration. Through regulating Unc5b expression, Sip1 contributes to efficient guided migration during brain development in the embryo.</description><subject>Animals</subject><subject>Brain slice preparation</subject><subject>Cell Movement - physiology</subject><subject>Cerebral Cortex - cytology</subject><subject>Cerebral Cortex - growth & development</subject><subject>Gene Knockout Techniques</subject><subject>Interneurons - physiology</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Migration</subject><subject>Neocortex - cytology</subject><subject>Neocortex - growth & development</subject><subject>Nerve Tissue Proteins - deficiency</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Netrin Receptors</subject><subject>Neurons</subject><subject>Organ Culture Techniques</subject><subject>Receptors, Cell Surface - deficiency</subject><subject>Receptors, Cell Surface - genetics</subject><subject>Rodents</subject><subject>Telencephalon - cytology</subject><subject>Telencephalon - growth & development</subject><subject>Transcription factors</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU9v1DAQxa0KRJfCN6iqSFy4JHhsx44vlVZb_lQq4tBy4GQ5zoR6tWtv7QSJb4-XtBw4IE5z-b2ZN-8Rcg60AQry3bYJOKcYGkaBNQANpfqErIBqVQvQ-hlZ0U7LWjLFT8nLnLeUgmg1vCCnjHNgLagV-XblE7oJh-qz_57s5GOo4lhtYpq8s7vqOkyYlkO5usIDhiFXhZnusdrgblev5ymGuI9zrtbuSX7rD_CKPB_tLuPrx3lGvn54f7f5VN98-Xi9Wd_UruXtVGvZi173yikmKbVCuVG0A7duAKElaOUcMBCSDUr2nT1-oPqOuVZIy0fm-Bl5u-w9pPgwY57M3mdXrNmAxZUB1rVAaQfqP1DFhe40lwV98xe6jXMK5REDUhTnJT5WKLFQLsWcE47mkPzepp8GqDm2ZLZmCc8cWzIAprRUZBePy-d-j8Mf0VMtBbhcACzB_fCYTHYeg8Phd1tmiP7fF34BOaui7g</recordid><startdate>20130109</startdate><enddate>20130109</enddate><creator>van den Berghe, Veronique</creator><creator>Stappers, Elke</creator><creator>Vandesande, Bram</creator><creator>Dimidschstein, Jordane</creator><creator>Kroes, Roel</creator><creator>Francis, Annick</creator><creator>Conidi, Andrea</creator><creator>Lesage, Flore</creator><creator>Dries, Ruben</creator><creator>Cazzola, Silvia</creator><creator>Berx, Geert</creator><creator>Kessaris, Nicoletta</creator><creator>Vanderhaeghen, Pierre</creator><creator>van IJcken, Wilfred</creator><creator>Grosveld, Frank G.</creator><creator>Goossens, Steven</creator><creator>Haigh, Jody J.</creator><creator>Fishell, Gord</creator><creator>Goffinet, André</creator><creator>Aerts, Stein</creator><creator>Huylebroeck, Danny</creator><creator>Seuntjens, Eve</creator><general>Elsevier Inc</general><general>Elsevier Limited</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20130109</creationdate><title>Directed Migration of Cortical Interneurons Depends on the Cell-Autonomous Action of Sip1</title><author>van den Berghe, Veronique ; Stappers, Elke ; Vandesande, Bram ; Dimidschstein, Jordane ; Kroes, Roel ; Francis, Annick ; Conidi, Andrea ; Lesage, Flore ; Dries, Ruben ; Cazzola, Silvia ; Berx, Geert ; Kessaris, Nicoletta ; Vanderhaeghen, Pierre ; van IJcken, Wilfred ; Grosveld, Frank G. ; Goossens, Steven ; Haigh, Jody J. ; Fishell, Gord ; Goffinet, André ; Aerts, Stein ; Huylebroeck, Danny ; Seuntjens, Eve</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c535t-96b4b9b7c72600a47cf45d3acd1496197cc121462d76b8a14597b82c546a3f2c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Brain slice preparation</topic><topic>Cell Movement - physiology</topic><topic>Cerebral Cortex - cytology</topic><topic>Cerebral Cortex - growth & development</topic><topic>Gene Knockout Techniques</topic><topic>Interneurons - physiology</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Migration</topic><topic>Neocortex - cytology</topic><topic>Neocortex - growth & development</topic><topic>Nerve Tissue Proteins - deficiency</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Netrin Receptors</topic><topic>Neurons</topic><topic>Organ Culture Techniques</topic><topic>Receptors, Cell Surface - deficiency</topic><topic>Receptors, Cell Surface - genetics</topic><topic>Rodents</topic><topic>Telencephalon - cytology</topic><topic>Telencephalon - growth & development</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van den Berghe, Veronique</creatorcontrib><creatorcontrib>Stappers, Elke</creatorcontrib><creatorcontrib>Vandesande, Bram</creatorcontrib><creatorcontrib>Dimidschstein, Jordane</creatorcontrib><creatorcontrib>Kroes, Roel</creatorcontrib><creatorcontrib>Francis, Annick</creatorcontrib><creatorcontrib>Conidi, Andrea</creatorcontrib><creatorcontrib>Lesage, Flore</creatorcontrib><creatorcontrib>Dries, Ruben</creatorcontrib><creatorcontrib>Cazzola, Silvia</creatorcontrib><creatorcontrib>Berx, Geert</creatorcontrib><creatorcontrib>Kessaris, Nicoletta</creatorcontrib><creatorcontrib>Vanderhaeghen, Pierre</creatorcontrib><creatorcontrib>van IJcken, Wilfred</creatorcontrib><creatorcontrib>Grosveld, Frank G.</creatorcontrib><creatorcontrib>Goossens, Steven</creatorcontrib><creatorcontrib>Haigh, Jody J.</creatorcontrib><creatorcontrib>Fishell, Gord</creatorcontrib><creatorcontrib>Goffinet, André</creatorcontrib><creatorcontrib>Aerts, Stein</creatorcontrib><creatorcontrib>Huylebroeck, Danny</creatorcontrib><creatorcontrib>Seuntjens, Eve</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>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van den Berghe, Veronique</au><au>Stappers, Elke</au><au>Vandesande, Bram</au><au>Dimidschstein, Jordane</au><au>Kroes, Roel</au><au>Francis, Annick</au><au>Conidi, Andrea</au><au>Lesage, Flore</au><au>Dries, Ruben</au><au>Cazzola, Silvia</au><au>Berx, Geert</au><au>Kessaris, Nicoletta</au><au>Vanderhaeghen, Pierre</au><au>van IJcken, Wilfred</au><au>Grosveld, Frank G.</au><au>Goossens, Steven</au><au>Haigh, Jody J.</au><au>Fishell, Gord</au><au>Goffinet, André</au><au>Aerts, Stein</au><au>Huylebroeck, Danny</au><au>Seuntjens, Eve</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Directed Migration of Cortical Interneurons Depends on the Cell-Autonomous Action of Sip1</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2013-01-09</date><risdate>2013</risdate><volume>77</volume><issue>1</issue><spage>70</spage><epage>82</epage><pages>70-82</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>GABAergic interneurons mainly originate in the medial ganglionic eminence (MGE) of the embryonic ventral telencephalon (VT) and migrate tangentially to the cortex, guided by membrane-bound and secreted factors. We found that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, is required for their proper differentiation and correct guidance. The majority of Sip1 knockout interneurons fail to migrate to the neocortex and stall in the VT. RNA sequencing reveals that Sip1 knockout interneurons do not acquire a fully mature cortical interneuron identity and contain increased levels of the repulsive receptor Unc5b. Focal electroporation of Unc5b-encoding vectors in the MGE of wild-type brain slices disturbs migration to the neocortex, whereas reducing Unc5b levels in Sip1 knockout slices and brains rescues the migration defect. Our results reveal that Sip1, through tuning of Unc5b levels, is essential for cortical interneuron guidance.
► Sip1 is crucial for directed cortical interneuron migration ► RNA sequencing identifies Sip1-dependent differentiation and guidance factors ► Sip1 is essential to constrain the expression level of Unc5b in the MGE ► Tuning of Unc5b expression level regulates the direction of interneuron migration
Van den Berghe et al. demonstrate that Sip1 (Zfhx1b, Zeb2), a transcription factor enriched in migrating cortical interneurons, controls their differentiation and directed migration. Through regulating Unc5b expression, Sip1 contributes to efficient guided migration during brain development in the embryo.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23312517</pmid><doi>10.1016/j.neuron.2012.11.009</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Brain slice preparation Cell Movement - physiology Cerebral Cortex - cytology Cerebral Cortex - growth & development Gene Knockout Techniques Interneurons - physiology Mice Mice, Transgenic Migration Neocortex - cytology Neocortex - growth & development Nerve Tissue Proteins - deficiency Nerve Tissue Proteins - genetics Netrin Receptors Neurons Organ Culture Techniques Receptors, Cell Surface - deficiency Receptors, Cell Surface - genetics Rodents Telencephalon - cytology Telencephalon - growth & development Transcription factors |
| title | Directed Migration of Cortical Interneurons Depends on the Cell-Autonomous Action of Sip1 |
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