Characterization of perinatally born glutamatergic neurons of the mouse olfactory bulb based on NeuroD6 expression reveals their resistance to sensory deprivation
During postnatal olfactory bulb (OB) neurogenesis, predetermined stem cells residing in the ventricular–subventricular zone continuously generate progenitors that migrate in the rostral migratory stream and integrate into the OB. Although the vast majority of these postnatally generated interneurons...
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Veröffentlicht in: | Journal of comparative neurology (1911) 2019-05, Vol.527 (7), p.1245-1260 |
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description | During postnatal olfactory bulb (OB) neurogenesis, predetermined stem cells residing in the ventricular–subventricular zone continuously generate progenitors that migrate in the rostral migratory stream and integrate into the OB. Although the vast majority of these postnatally generated interneurons are inhibitory, a sub‐fraction represents glutamatergic neurons that integrate into the superficial glomerular layer. In the present work, we demonstrate that the bHLH transcription factor NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxtaglomerular cells (JGCs) for the OB. Using lineage tracing combined with whole brain clearing, we provide new insight into timing of generation, morphology, and connectivity of glutamatergic JGCs. Specifically, we show that all glutamatergic JGCs send complex axons with varying projection patterns into different layers of the OB. Moreover, we find that, contrary to GABAergic OB interneurons, glutamatergic JGCs survive under sensory deprivation, indicating that inhibitory and excitatory populations are differentially susceptible to environmental stimulation.
NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxta‐glomerular neurons for the olfactory bulb. Using NeuroD6‐Cre knock‐in mice as reliable tools, we characterize their morphology and connectivity. Furthermore, by in vivo imaging, we demonstrate that glutamatergic excitatory interneurons survive under sensory deprivation. |
doi_str_mv | 10.1002/cne.24621 |
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NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxta‐glomerular neurons for the olfactory bulb. Using NeuroD6‐Cre knock‐in mice as reliable tools, we characterize their morphology and connectivity. Furthermore, by in vivo imaging, we demonstrate that glutamatergic excitatory interneurons survive under sensory deprivation.</description><identifier>ISSN: 0021-9967</identifier><identifier>ISSN: 0092-7317</identifier><identifier>EISSN: 1096-9861</identifier><identifier>EISSN: 1550-7130</identifier><identifier>DOI: 10.1002/cne.24621</identifier><identifier>PMID: 30592042</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Animal genetics ; Axons ; Genetics ; glutamatergic neurons ; Glutamatergic transmission ; Helix-loop-helix proteins (basic) ; Interneurons ; Life Sciences ; Neural networks ; Neurobiology ; NeuroD6 bHLH transcription factor ; Neurogenesis ; Neurons and Cognition ; Olfactory bulb ; postnatal neurogenesis ; RRID:AB_10013440 ; RRID:AB_1587367 ; RRID:AB_2068336 ; RRID:AB_2187539 ; RRID:AB_2200219 ; RRID:AB_2336063 ; RRID:AB_2619904 ; RRID:AB_2749806 ; RRID:AB_393778 ; RRID:AB_778267 ; RRID:AB_828390 ; RRID:AB_887877 ; RRID:IMSR_JAX:007914 ; RRID:MGI:4429523 ; RRID:MGI:5308867 ; RRID:MGI:5510844 ; RRID:SCR_001905 ; RRID:SCR_002285 ; RRID:SCR_007370 ; RRID:SCR_013672 ; Sensory deprivation ; Smell ; Stem cell transplantation ; Stem cells ; Subventricular zone ; Ventricle ; γ-Aminobutyric acid</subject><ispartof>Journal of comparative neurology (1911), 2019-05, Vol.527 (7), p.1245-1260</ispartof><rights>2018 Wiley Periodicals, Inc.</rights><rights>2019 Wiley Periodicals, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4221-5c65c0a27d45998da5246ea57930552e74e7fe793084e69bec029840b445c9163</citedby><cites>FETCH-LOGICAL-c4221-5c65c0a27d45998da5246ea57930552e74e7fe793084e69bec029840b445c9163</cites><orcidid>0000-0003-3865-4539</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcne.24621$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.24621$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30592042$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://amu.hal.science/hal-02160586$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Angelova, Alexandra</creatorcontrib><creatorcontrib>Platel, Jean‐Claude</creatorcontrib><creatorcontrib>Béclin, Christophe</creatorcontrib><creatorcontrib>Cremer, Harold</creatorcontrib><creatorcontrib>Coré, Nathalie</creatorcontrib><title>Characterization of perinatally born glutamatergic neurons of the mouse olfactory bulb based on NeuroD6 expression reveals their resistance to sensory deprivation</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>During postnatal olfactory bulb (OB) neurogenesis, predetermined stem cells residing in the ventricular–subventricular zone continuously generate progenitors that migrate in the rostral migratory stream and integrate into the OB. Although the vast majority of these postnatally generated interneurons are inhibitory, a sub‐fraction represents glutamatergic neurons that integrate into the superficial glomerular layer. In the present work, we demonstrate that the bHLH transcription factor NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxtaglomerular cells (JGCs) for the OB. Using lineage tracing combined with whole brain clearing, we provide new insight into timing of generation, morphology, and connectivity of glutamatergic JGCs. Specifically, we show that all glutamatergic JGCs send complex axons with varying projection patterns into different layers of the OB. Moreover, we find that, contrary to GABAergic OB interneurons, glutamatergic JGCs survive under sensory deprivation, indicating that inhibitory and excitatory populations are differentially susceptible to environmental stimulation.
NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxta‐glomerular neurons for the olfactory bulb. Using NeuroD6‐Cre knock‐in mice as reliable tools, we characterize their morphology and connectivity. Furthermore, by in vivo imaging, we demonstrate that glutamatergic excitatory interneurons survive under sensory deprivation.</description><subject>Animal genetics</subject><subject>Axons</subject><subject>Genetics</subject><subject>glutamatergic neurons</subject><subject>Glutamatergic transmission</subject><subject>Helix-loop-helix proteins (basic)</subject><subject>Interneurons</subject><subject>Life Sciences</subject><subject>Neural networks</subject><subject>Neurobiology</subject><subject>NeuroD6 bHLH transcription factor</subject><subject>Neurogenesis</subject><subject>Neurons and Cognition</subject><subject>Olfactory bulb</subject><subject>postnatal neurogenesis</subject><subject>RRID:AB_10013440</subject><subject>RRID:AB_1587367</subject><subject>RRID:AB_2068336</subject><subject>RRID:AB_2187539</subject><subject>RRID:AB_2200219</subject><subject>RRID:AB_2336063</subject><subject>RRID:AB_2619904</subject><subject>RRID:AB_2749806</subject><subject>RRID:AB_393778</subject><subject>RRID:AB_778267</subject><subject>RRID:AB_828390</subject><subject>RRID:AB_887877</subject><subject>RRID:IMSR_JAX:007914</subject><subject>RRID:MGI:4429523</subject><subject>RRID:MGI:5308867</subject><subject>RRID:MGI:5510844</subject><subject>RRID:SCR_001905</subject><subject>RRID:SCR_002285</subject><subject>RRID:SCR_007370</subject><subject>RRID:SCR_013672</subject><subject>Sensory deprivation</subject><subject>Smell</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Subventricular zone</subject><subject>Ventricle</subject><subject>γ-Aminobutyric acid</subject><issn>0021-9967</issn><issn>0092-7317</issn><issn>1096-9861</issn><issn>1550-7130</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp1kU1v1DAQhi0EokvhwB9AlrjAYVs764_4WC2FIq3KBc6W40y6qRx7sZMty8_hlzLpliIhcbLG88w7Hy8hrzk744xV5z7CWSVUxZ-QBWdGLU2t-FOywBxfGqP0CXlRyi1jzJhV_ZycrJg0FRPVgvxab112foTc_3RjnyJNHd1hFN3oQjjQJuVIb8I0usEhddN7GmHKKZaZHLdAhzQVoCl0KJMyVkyhoY0r0FKUu57hD4rCj12GUuYOGfbgQpmL-4xR6cvoogc6JlogllmkhV3u9_cTvSTPOsTh1cN7Sr59vPy6vlpuvnz6vL7YLL2ocE_plfTMVboV0pi6dRJPAk5qg9vKCrQA3cEc1QKUacCzytSCNUJIb7hanZL3R92tCxa7Dy4fbHK9vbrY2PkPr6mYrNWeI_vuyO5y-j5BGe3QFw8huAh4Dosk10zylUD07T_obZpyxE2QqrVmWtXib3OfUykZuscJOLOzyRZNtvcmI_vmQXFqBmgfyT-uInB-BO76AIf_K9n19eVR8jeWLbIo</recordid><startdate>20190501</startdate><enddate>20190501</enddate><creator>Angelova, Alexandra</creator><creator>Platel, Jean‐Claude</creator><creator>Béclin, Christophe</creator><creator>Cremer, Harold</creator><creator>Coré, Nathalie</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><general>John Wiley & Sons</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0003-3865-4539</orcidid></search><sort><creationdate>20190501</creationdate><title>Characterization of perinatally born glutamatergic neurons of the mouse olfactory bulb based on NeuroD6 expression reveals their resistance to sensory deprivation</title><author>Angelova, Alexandra ; Platel, Jean‐Claude ; Béclin, Christophe ; Cremer, Harold ; Coré, Nathalie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4221-5c65c0a27d45998da5246ea57930552e74e7fe793084e69bec029840b445c9163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animal genetics</topic><topic>Axons</topic><topic>Genetics</topic><topic>glutamatergic neurons</topic><topic>Glutamatergic transmission</topic><topic>Helix-loop-helix proteins (basic)</topic><topic>Interneurons</topic><topic>Life Sciences</topic><topic>Neural networks</topic><topic>Neurobiology</topic><topic>NeuroD6 bHLH transcription factor</topic><topic>Neurogenesis</topic><topic>Neurons and Cognition</topic><topic>Olfactory bulb</topic><topic>postnatal neurogenesis</topic><topic>RRID:AB_10013440</topic><topic>RRID:AB_1587367</topic><topic>RRID:AB_2068336</topic><topic>RRID:AB_2187539</topic><topic>RRID:AB_2200219</topic><topic>RRID:AB_2336063</topic><topic>RRID:AB_2619904</topic><topic>RRID:AB_2749806</topic><topic>RRID:AB_393778</topic><topic>RRID:AB_778267</topic><topic>RRID:AB_828390</topic><topic>RRID:AB_887877</topic><topic>RRID:IMSR_JAX:007914</topic><topic>RRID:MGI:4429523</topic><topic>RRID:MGI:5308867</topic><topic>RRID:MGI:5510844</topic><topic>RRID:SCR_001905</topic><topic>RRID:SCR_002285</topic><topic>RRID:SCR_007370</topic><topic>RRID:SCR_013672</topic><topic>Sensory deprivation</topic><topic>Smell</topic><topic>Stem cell transplantation</topic><topic>Stem cells</topic><topic>Subventricular zone</topic><topic>Ventricle</topic><topic>γ-Aminobutyric acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Angelova, Alexandra</creatorcontrib><creatorcontrib>Platel, Jean‐Claude</creatorcontrib><creatorcontrib>Béclin, Christophe</creatorcontrib><creatorcontrib>Cremer, Harold</creatorcontrib><creatorcontrib>Coré, Nathalie</creatorcontrib><collection>PubMed</collection><collection>CrossRef</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>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Angelova, Alexandra</au><au>Platel, Jean‐Claude</au><au>Béclin, Christophe</au><au>Cremer, Harold</au><au>Coré, Nathalie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of perinatally born glutamatergic neurons of the mouse olfactory bulb based on NeuroD6 expression reveals their resistance to sensory deprivation</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J Comp Neurol</addtitle><date>2019-05-01</date><risdate>2019</risdate><volume>527</volume><issue>7</issue><spage>1245</spage><epage>1260</epage><pages>1245-1260</pages><issn>0021-9967</issn><issn>0092-7317</issn><eissn>1096-9861</eissn><eissn>1550-7130</eissn><abstract>During postnatal olfactory bulb (OB) neurogenesis, predetermined stem cells residing in the ventricular–subventricular zone continuously generate progenitors that migrate in the rostral migratory stream and integrate into the OB. Although the vast majority of these postnatally generated interneurons are inhibitory, a sub‐fraction represents glutamatergic neurons that integrate into the superficial glomerular layer. In the present work, we demonstrate that the bHLH transcription factor NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxtaglomerular cells (JGCs) for the OB. Using lineage tracing combined with whole brain clearing, we provide new insight into timing of generation, morphology, and connectivity of glutamatergic JGCs. Specifically, we show that all glutamatergic JGCs send complex axons with varying projection patterns into different layers of the OB. Moreover, we find that, contrary to GABAergic OB interneurons, glutamatergic JGCs survive under sensory deprivation, indicating that inhibitory and excitatory populations are differentially susceptible to environmental stimulation.
NeuroD6 is specifically and transitorily expressed in the dorsal neurogenic lineage that generates glutamatergic juxta‐glomerular neurons for the olfactory bulb. Using NeuroD6‐Cre knock‐in mice as reliable tools, we characterize their morphology and connectivity. Furthermore, by in vivo imaging, we demonstrate that glutamatergic excitatory interneurons survive under sensory deprivation.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>30592042</pmid><doi>10.1002/cne.24621</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-3865-4539</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animal genetics Axons Genetics glutamatergic neurons Glutamatergic transmission Helix-loop-helix proteins (basic) Interneurons Life Sciences Neural networks Neurobiology NeuroD6 bHLH transcription factor Neurogenesis Neurons and Cognition Olfactory bulb postnatal neurogenesis RRID:AB_10013440 RRID:AB_1587367 RRID:AB_2068336 RRID:AB_2187539 RRID:AB_2200219 RRID:AB_2336063 RRID:AB_2619904 RRID:AB_2749806 RRID:AB_393778 RRID:AB_778267 RRID:AB_828390 RRID:AB_887877 RRID:IMSR_JAX:007914 RRID:MGI:4429523 RRID:MGI:5308867 RRID:MGI:5510844 RRID:SCR_001905 RRID:SCR_002285 RRID:SCR_007370 RRID:SCR_013672 Sensory deprivation Smell Stem cell transplantation Stem cells Subventricular zone Ventricle γ-Aminobutyric acid |
title | Characterization of perinatally born glutamatergic neurons of the mouse olfactory bulb based on NeuroD6 expression reveals their resistance to sensory deprivation |
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