Neurog1 and Neurog2 control two waves of neuronal differentiation in the piriform cortex
The three-layered piriform cortex, an integral part of the olfactory system, processes odor information relayed by olfactory bulb mitral cells. Specifically, mitral cell axons form the lateral olfactory tract (LOT) by targeting lateral olfactory tract (lot) guidepost cells in the piriform cortex. Wh...
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creator | Dixit, Rajiv Wilkinson, Grey Cancino, Gonzalo I Shaker, Tarek Adnani, Lata Li, Saiqun Dennis, Daniel Kurrasch, Deborah Chan, Jennifer A Olson, Eric C Kaplan, David R Zimmer, Céline Schuurmans, Carol |
description | The three-layered piriform cortex, an integral part of the olfactory system, processes odor information relayed by olfactory bulb mitral cells. Specifically, mitral cell axons form the lateral olfactory tract (LOT) by targeting lateral olfactory tract (lot) guidepost cells in the piriform cortex. While lot cells and other piriform cortical neurons share a pallial origin, the factors that specify their precise phenotypes are poorly understood. Here we show that in mouse, the proneural genes Neurog1 and Neurog2 are coexpressed in the ventral pallium, a progenitor pool that first gives rise to Cajal-Retzius (CR) cells, which populate layer I of all cortical domains, and later to layer II/III neurons of the piriform cortex. Using loss-of-function and gain-of-function approaches, we find that Neurog1 has a unique early role in reducing CR cell neurogenesis by tempering Neurog2's proneural activity. In addition, Neurog1 and Neurog2 have redundant functions in the ventral pallium, acting in two phases to first specify a CR cell fate and later to specify layer II/III piriform cortex neuronal identities. In the early phase, Neurog1 and Neurog2 are also required for lot cell differentiation, which we reveal are a subset of CR neurons, the loss of which prevents mitral cell axon innervation and LOT formation. Consequently, mutation of Trp73, a CR-specific cortical gene, results in lot cell and LOT axon displacement. Neurog1 and Neurog2 thus have unique and redundant functions in the piriform cortex, controlling the timing of differentiation of early-born CR/lot cells and specifying the identities of later-born layer II/III neurons. |
doi_str_mv | 10.1523/JNEUROSCI.0614-13.2014 |
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Specifically, mitral cell axons form the lateral olfactory tract (LOT) by targeting lateral olfactory tract (lot) guidepost cells in the piriform cortex. While lot cells and other piriform cortical neurons share a pallial origin, the factors that specify their precise phenotypes are poorly understood. Here we show that in mouse, the proneural genes Neurog1 and Neurog2 are coexpressed in the ventral pallium, a progenitor pool that first gives rise to Cajal-Retzius (CR) cells, which populate layer I of all cortical domains, and later to layer II/III neurons of the piriform cortex. Using loss-of-function and gain-of-function approaches, we find that Neurog1 has a unique early role in reducing CR cell neurogenesis by tempering Neurog2's proneural activity. In addition, Neurog1 and Neurog2 have redundant functions in the ventral pallium, acting in two phases to first specify a CR cell fate and later to specify layer II/III piriform cortex neuronal identities. In the early phase, Neurog1 and Neurog2 are also required for lot cell differentiation, which we reveal are a subset of CR neurons, the loss of which prevents mitral cell axon innervation and LOT formation. Consequently, mutation of Trp73, a CR-specific cortical gene, results in lot cell and LOT axon displacement. 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Specifically, mitral cell axons form the lateral olfactory tract (LOT) by targeting lateral olfactory tract (lot) guidepost cells in the piriform cortex. While lot cells and other piriform cortical neurons share a pallial origin, the factors that specify their precise phenotypes are poorly understood. Here we show that in mouse, the proneural genes Neurog1 and Neurog2 are coexpressed in the ventral pallium, a progenitor pool that first gives rise to Cajal-Retzius (CR) cells, which populate layer I of all cortical domains, and later to layer II/III neurons of the piriform cortex. Using loss-of-function and gain-of-function approaches, we find that Neurog1 has a unique early role in reducing CR cell neurogenesis by tempering Neurog2's proneural activity. In addition, Neurog1 and Neurog2 have redundant functions in the ventral pallium, acting in two phases to first specify a CR cell fate and later to specify layer II/III piriform cortex neuronal identities. In the early phase, Neurog1 and Neurog2 are also required for lot cell differentiation, which we reveal are a subset of CR neurons, the loss of which prevents mitral cell axon innervation and LOT formation. Consequently, mutation of Trp73, a CR-specific cortical gene, results in lot cell and LOT axon displacement. Neurog1 and Neurog2 thus have unique and redundant functions in the piriform cortex, controlling the timing of differentiation of early-born CR/lot cells and specifying the identities of later-born layer II/III neurons.</description><subject>Animals</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Cell Differentiation - physiology</subject><subject>Cerebral Cortex - cytology</subject><subject>Cerebral Cortex - embryology</subject><subject>Cerebral Cortex - metabolism</subject><subject>Electroporation</subject><subject>Embryo, Mammalian</subject><subject>Female</subject><subject>Immunohistochemistry</subject><subject>In Situ Hybridization</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Mutant Strains</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neural Stem Cells - metabolism</subject><subject>Neurogenesis - physiology</subject><subject>Neurons - cytology</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkV1LIzEUhoO4aLf6FySX3kz3nCSTmbkRpPiJKOxW8C6kmUQj06QmU939906pFr3aq3Pg_eAkDyFHCBMsGf91fXt2__vuz_RqAhJFgXzCAMUOGQ1qUzABuEtGwCoopKjEPvmZ8zMAVIDVHtlnQgDHko_Iw61dpfiIVIeWbnZGTQx9ih3t3yJ906820-hoWItBd7T1ztlkQ-9172OgPtD-ydKlT97FtBjSqbd_D8gPp7tsDz_mmMzOz2bTy-Lm7uJqenpTGFGyvigbC8AbDZq3jvG2MqWcC-QAUjpjUBgoWyslmNq1beM4nzvUonalqGph-ZicbGqXq_nCtmY4K-lOLZNf6PRPRe3VdyX4J_UYX9VQWaOoh4Ljj4IUX1Y292rhs7Fdp4ONq6ywZlVdD58l_28VDVQoWFMOVrmxmhRzTtZtL0JQa4BqC1CtASrkag1wCB59fc829kmMvwPlY5k4</recordid><startdate>20140108</startdate><enddate>20140108</enddate><creator>Dixit, Rajiv</creator><creator>Wilkinson, Grey</creator><creator>Cancino, Gonzalo I</creator><creator>Shaker, Tarek</creator><creator>Adnani, Lata</creator><creator>Li, Saiqun</creator><creator>Dennis, Daniel</creator><creator>Kurrasch, Deborah</creator><creator>Chan, Jennifer A</creator><creator>Olson, Eric C</creator><creator>Kaplan, David R</creator><creator>Zimmer, Céline</creator><creator>Schuurmans, Carol</creator><general>Society for Neuroscience</general><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>7X8</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20140108</creationdate><title>Neurog1 and Neurog2 control two waves of neuronal differentiation in the piriform cortex</title><author>Dixit, Rajiv ; Wilkinson, Grey ; Cancino, Gonzalo I ; Shaker, Tarek ; Adnani, Lata ; Li, Saiqun ; Dennis, Daniel ; Kurrasch, Deborah ; Chan, Jennifer A ; Olson, Eric C ; Kaplan, David R ; Zimmer, Céline ; Schuurmans, Carol</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c452t-59e0039a0a3df23d7c56b4130066fcc14c05de660c8fdd9f33bf1a48f54784e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Cell Differentiation - physiology</topic><topic>Cerebral Cortex - cytology</topic><topic>Cerebral Cortex - embryology</topic><topic>Cerebral Cortex - metabolism</topic><topic>Electroporation</topic><topic>Embryo, Mammalian</topic><topic>Female</topic><topic>Immunohistochemistry</topic><topic>In Situ Hybridization</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Mutant Strains</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neural Stem Cells - metabolism</topic><topic>Neurogenesis - physiology</topic><topic>Neurons - cytology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dixit, Rajiv</creatorcontrib><creatorcontrib>Wilkinson, Grey</creatorcontrib><creatorcontrib>Cancino, Gonzalo I</creatorcontrib><creatorcontrib>Shaker, Tarek</creatorcontrib><creatorcontrib>Adnani, Lata</creatorcontrib><creatorcontrib>Li, Saiqun</creatorcontrib><creatorcontrib>Dennis, Daniel</creatorcontrib><creatorcontrib>Kurrasch, Deborah</creatorcontrib><creatorcontrib>Chan, Jennifer A</creatorcontrib><creatorcontrib>Olson, Eric C</creatorcontrib><creatorcontrib>Kaplan, David R</creatorcontrib><creatorcontrib>Zimmer, Céline</creatorcontrib><creatorcontrib>Schuurmans, Carol</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dixit, Rajiv</au><au>Wilkinson, Grey</au><au>Cancino, Gonzalo I</au><au>Shaker, Tarek</au><au>Adnani, Lata</au><au>Li, Saiqun</au><au>Dennis, Daniel</au><au>Kurrasch, Deborah</au><au>Chan, Jennifer A</au><au>Olson, Eric C</au><au>Kaplan, David R</au><au>Zimmer, Céline</au><au>Schuurmans, Carol</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neurog1 and Neurog2 control two waves of neuronal differentiation in the piriform cortex</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2014-01-08</date><risdate>2014</risdate><volume>34</volume><issue>2</issue><spage>539</spage><epage>553</epage><pages>539-553</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>The three-layered piriform cortex, an integral part of the olfactory system, processes odor information relayed by olfactory bulb mitral cells. Specifically, mitral cell axons form the lateral olfactory tract (LOT) by targeting lateral olfactory tract (lot) guidepost cells in the piriform cortex. While lot cells and other piriform cortical neurons share a pallial origin, the factors that specify their precise phenotypes are poorly understood. Here we show that in mouse, the proneural genes Neurog1 and Neurog2 are coexpressed in the ventral pallium, a progenitor pool that first gives rise to Cajal-Retzius (CR) cells, which populate layer I of all cortical domains, and later to layer II/III neurons of the piriform cortex. Using loss-of-function and gain-of-function approaches, we find that Neurog1 has a unique early role in reducing CR cell neurogenesis by tempering Neurog2's proneural activity. In addition, Neurog1 and Neurog2 have redundant functions in the ventral pallium, acting in two phases to first specify a CR cell fate and later to specify layer II/III piriform cortex neuronal identities. In the early phase, Neurog1 and Neurog2 are also required for lot cell differentiation, which we reveal are a subset of CR neurons, the loss of which prevents mitral cell axon innervation and LOT formation. Consequently, mutation of Trp73, a CR-specific cortical gene, results in lot cell and LOT axon displacement. Neurog1 and Neurog2 thus have unique and redundant functions in the piriform cortex, controlling the timing of differentiation of early-born CR/lot cells and specifying the identities of later-born layer II/III neurons.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>24403153</pmid><doi>10.1523/JNEUROSCI.0614-13.2014</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Basic Helix-Loop-Helix Transcription Factors - metabolism Cell Differentiation - physiology Cerebral Cortex - cytology Cerebral Cortex - embryology Cerebral Cortex - metabolism Electroporation Embryo, Mammalian Female Immunohistochemistry In Situ Hybridization Male Mice Mice, Mutant Strains Nerve Tissue Proteins - metabolism Neural Stem Cells - metabolism Neurogenesis - physiology Neurons - cytology |
title | Neurog1 and Neurog2 control two waves of neuronal differentiation in the piriform cortex |
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