Cartography of hevin-expressing cells in the adult brain reveals prominent expression in astrocytes and parvalbumin neurons
Hevin, also known as SPARC-like 1, is a member of the secreted protein acidic and rich in cysteine family of matricellular proteins, which has been implicated in neuronal migration and synaptogenesis during development. Unlike previously characterized matricellular proteins, hevin remains strongly e...
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| Veröffentlicht in: | Brain Structure and Function 2019-04, Vol.224 (3), p.1219-1244 |
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| creator | Mongrédien, Raphaële Erdozain, Amaia M. Dumas, Sylvie Cutando, Laura del Moral, Amaia Nuñez Puighermanal, Emma Rezai Amin, Sara Giros, Bruno Valjent, Emmanuel Meana, J. Javier Gautron, Sophie Callado, Luis F. Fabre, Véronique Vialou, Vincent |
| description | Hevin, also known as SPARC-like 1, is a member of the secreted protein acidic and rich in cysteine family of matricellular proteins, which has been implicated in neuronal migration and synaptogenesis during development. Unlike previously characterized matricellular proteins, hevin remains strongly expressed in the adult brain in both astrocytes and neurons, but its precise pattern of expression is unknown. The present study provides the first systematic description of hevin mRNA distribution in the adult mouse brain. Using isotopic in situ hybridization, we showed that hevin is strongly expressed in the cortex, hippocampus, basal ganglia complex, diverse thalamic nuclei and brainstem motor nuclei. To identify the cellular phenotype of hevin-expressing cells, we used double fluorescent in situ hybridization in mouse and human adult brains. In the mouse, hevin mRNA was found in the majority of astrocytes but also in specific neuronal populations. Hevin was expressed in almost all parvalbumin-positive projection neurons and local interneurons. In addition, hevin mRNA was found in: (1) subsets of other inhibitory GABAergic neuronal subtypes, including calbindin, cholecystokinin, neuropeptide Y, and somatostatin-positive neurons; (2) subsets of glutamatergic neurons, identified by the expression of the vesicular glutamate transporters VGLUT1 and VGLUT2; and (3) the majority of cholinergic neurons from motor nuclei. Hevin mRNA was absent from all monoaminergic neurons and cholinergic neurons of the ascending pathway. A similar cellular profile of expression was observed in human, with expression of hevin in parvalbumin interneurons and astrocytes in the cortex and caudate nucleus as well as in cortical glutamatergic neurons. Furthermore, hevin transcript was enriched in ribosomes of astrocytes and parvalbumin neurons providing a direct evidence of hevin mRNAs translation in these cell types. This study reveals the unique and complex expression profile of the matricellular protein hevin in the adult brain. This distribution is compatible with a role of hevin in astrocytic-mediated adult synaptic plasticity and in the regulation of network activity mediated by parvalbumin-expressing neurons. |
| doi_str_mv | 10.1007/s00429-019-01831-x |
| format | Article |
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Javier ; Gautron, Sophie ; Callado, Luis F. ; Fabre, Véronique ; Vialou, Vincent</creator><creatorcontrib>Mongrédien, Raphaële ; Erdozain, Amaia M. ; Dumas, Sylvie ; Cutando, Laura ; del Moral, Amaia Nuñez ; Puighermanal, Emma ; Rezai Amin, Sara ; Giros, Bruno ; Valjent, Emmanuel ; Meana, J. Javier ; Gautron, Sophie ; Callado, Luis F. ; Fabre, Véronique ; Vialou, Vincent</creatorcontrib><description>Hevin, also known as SPARC-like 1, is a member of the secreted protein acidic and rich in cysteine family of matricellular proteins, which has been implicated in neuronal migration and synaptogenesis during development. Unlike previously characterized matricellular proteins, hevin remains strongly expressed in the adult brain in both astrocytes and neurons, but its precise pattern of expression is unknown. The present study provides the first systematic description of hevin mRNA distribution in the adult mouse brain. Using isotopic in situ hybridization, we showed that hevin is strongly expressed in the cortex, hippocampus, basal ganglia complex, diverse thalamic nuclei and brainstem motor nuclei. To identify the cellular phenotype of hevin-expressing cells, we used double fluorescent in situ hybridization in mouse and human adult brains. In the mouse, hevin mRNA was found in the majority of astrocytes but also in specific neuronal populations. Hevin was expressed in almost all parvalbumin-positive projection neurons and local interneurons. In addition, hevin mRNA was found in: (1) subsets of other inhibitory GABAergic neuronal subtypes, including calbindin, cholecystokinin, neuropeptide Y, and somatostatin-positive neurons; (2) subsets of glutamatergic neurons, identified by the expression of the vesicular glutamate transporters VGLUT1 and VGLUT2; and (3) the majority of cholinergic neurons from motor nuclei. Hevin mRNA was absent from all monoaminergic neurons and cholinergic neurons of the ascending pathway. A similar cellular profile of expression was observed in human, with expression of hevin in parvalbumin interneurons and astrocytes in the cortex and caudate nucleus as well as in cortical glutamatergic neurons. Furthermore, hevin transcript was enriched in ribosomes of astrocytes and parvalbumin neurons providing a direct evidence of hevin mRNAs translation in these cell types. This study reveals the unique and complex expression profile of the matricellular protein hevin in the adult brain. This distribution is compatible with a role of hevin in astrocytic-mediated adult synaptic plasticity and in the regulation of network activity mediated by parvalbumin-expressing neurons.</description><identifier>ISSN: 1863-2653</identifier><identifier>EISSN: 1863-2661</identifier><identifier>EISSN: 0340-2061</identifier><identifier>DOI: 10.1007/s00429-019-01831-x</identifier><identifier>PMID: 30656447</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Astrocytes ; Basal ganglia ; Biomedical and Life Sciences ; Biomedicine ; Brain ; Brain stem ; Calbindin ; Caudate nucleus ; Cell Biology ; Cell migration ; Cholecystokinin ; Cortex ; Fluorescence in situ hybridization ; Glutamatergic transmission ; Interneurons ; Life Sciences ; Motor nuclei ; Neurology ; Neurons and Cognition ; Neuropeptide Y ; Neurosciences ; Original Article ; Osteonectin ; Parvalbumin ; Phenotypes ; Ribosomes ; Synaptic plasticity ; Synaptogenesis ; Thalamus ; Transcription</subject><ispartof>Brain Structure and Function, 2019-04, Vol.224 (3), p.1219-1244</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2019</rights><rights>Brain Structure and Function is a copyright of Springer, (2019). All Rights Reserved.</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-c456t-ef2c2b489808f355fd968de83a8092419bfa21253f747fec97effd9b830239223</citedby><cites>FETCH-LOGICAL-c456t-ef2c2b489808f355fd968de83a8092419bfa21253f747fec97effd9b830239223</cites><orcidid>0000-0003-4271-9104 ; 0000-0002-7913-6714 ; 0000-0001-5876-9822 ; 0000-0002-4510-7640 ; 0000-0002-8212-751X ; 0000-0003-0207-9122 ; 0000-0001-9941-012X ; 0000-0002-1034-606X ; 0000-0002-0176-4550</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00429-019-01831-x$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00429-019-01831-x$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27923,27924,41487,42556,51318</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30656447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://inserm.hal.science/inserm-02008003$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Mongrédien, Raphaële</creatorcontrib><creatorcontrib>Erdozain, Amaia M.</creatorcontrib><creatorcontrib>Dumas, Sylvie</creatorcontrib><creatorcontrib>Cutando, Laura</creatorcontrib><creatorcontrib>del Moral, Amaia Nuñez</creatorcontrib><creatorcontrib>Puighermanal, Emma</creatorcontrib><creatorcontrib>Rezai Amin, Sara</creatorcontrib><creatorcontrib>Giros, Bruno</creatorcontrib><creatorcontrib>Valjent, Emmanuel</creatorcontrib><creatorcontrib>Meana, J. Javier</creatorcontrib><creatorcontrib>Gautron, Sophie</creatorcontrib><creatorcontrib>Callado, Luis F.</creatorcontrib><creatorcontrib>Fabre, Véronique</creatorcontrib><creatorcontrib>Vialou, Vincent</creatorcontrib><title>Cartography of hevin-expressing cells in the adult brain reveals prominent expression in astrocytes and parvalbumin neurons</title><title>Brain Structure and Function</title><addtitle>Brain Struct Funct</addtitle><addtitle>Brain Struct Funct</addtitle><description>Hevin, also known as SPARC-like 1, is a member of the secreted protein acidic and rich in cysteine family of matricellular proteins, which has been implicated in neuronal migration and synaptogenesis during development. Unlike previously characterized matricellular proteins, hevin remains strongly expressed in the adult brain in both astrocytes and neurons, but its precise pattern of expression is unknown. The present study provides the first systematic description of hevin mRNA distribution in the adult mouse brain. Using isotopic in situ hybridization, we showed that hevin is strongly expressed in the cortex, hippocampus, basal ganglia complex, diverse thalamic nuclei and brainstem motor nuclei. To identify the cellular phenotype of hevin-expressing cells, we used double fluorescent in situ hybridization in mouse and human adult brains. In the mouse, hevin mRNA was found in the majority of astrocytes but also in specific neuronal populations. Hevin was expressed in almost all parvalbumin-positive projection neurons and local interneurons. In addition, hevin mRNA was found in: (1) subsets of other inhibitory GABAergic neuronal subtypes, including calbindin, cholecystokinin, neuropeptide Y, and somatostatin-positive neurons; (2) subsets of glutamatergic neurons, identified by the expression of the vesicular glutamate transporters VGLUT1 and VGLUT2; and (3) the majority of cholinergic neurons from motor nuclei. Hevin mRNA was absent from all monoaminergic neurons and cholinergic neurons of the ascending pathway. A similar cellular profile of expression was observed in human, with expression of hevin in parvalbumin interneurons and astrocytes in the cortex and caudate nucleus as well as in cortical glutamatergic neurons. Furthermore, hevin transcript was enriched in ribosomes of astrocytes and parvalbumin neurons providing a direct evidence of hevin mRNAs translation in these cell types. This study reveals the unique and complex expression profile of the matricellular protein hevin in the adult brain. This distribution is compatible with a role of hevin in astrocytic-mediated adult synaptic plasticity and in the regulation of network activity mediated by parvalbumin-expressing neurons.</description><subject>Astrocytes</subject><subject>Basal ganglia</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Brain stem</subject><subject>Calbindin</subject><subject>Caudate nucleus</subject><subject>Cell Biology</subject><subject>Cell migration</subject><subject>Cholecystokinin</subject><subject>Cortex</subject><subject>Fluorescence in situ hybridization</subject><subject>Glutamatergic transmission</subject><subject>Interneurons</subject><subject>Life Sciences</subject><subject>Motor nuclei</subject><subject>Neurology</subject><subject>Neurons and Cognition</subject><subject>Neuropeptide Y</subject><subject>Neurosciences</subject><subject>Original Article</subject><subject>Osteonectin</subject><subject>Parvalbumin</subject><subject>Phenotypes</subject><subject>Ribosomes</subject><subject>Synaptic plasticity</subject><subject>Synaptogenesis</subject><subject>Thalamus</subject><subject>Transcription</subject><issn>1863-2653</issn><issn>1863-2661</issn><issn>0340-2061</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kUFv1DAQhSNERUvhD3BAlrhwIGVsJ459rFZAkVbiUs6Wk4x3UyV2sJPVrvjzOE27SBw4WLY133vj8cuydxRuKED1OQIUTOVAlyU5zY8vsisqBc-ZEPTl-Vzyy-x1jA8ApZJUvcouOYhSFEV1lf3emDD5XTDj_kS8JXs8dC7H4xgwxs7tSIN9H0nnyLRHYtq5n0gdTLoHPKBJpTH4oXPoJvKs8m7hTZyCb04TRmJcS0YTDqav58QSh3PwLr7JLmxywLdP-3X28-uX-81dvv3x7fvmdps3RSmmHC1rWF1IJUFaXpa2VUK2KLmRoFhBVW0No6zktioqi42q0CamlhwYV4zx6-zT6rs3vR5DN5hw0t50-u52qzsXMQwaGIAE4IcF_7jiabJfM8ZJD11cvsE49HPUjFaKKyigSuiHf9AHPweXhkmUkEAFVIshW6km-BgD2vMjKOglSb0mqVOS-jFJfUyi90_Wcz1ge5Y8R5cAvgIxldwOw9_e_7H9A0luqxQ</recordid><startdate>20190401</startdate><enddate>20190401</enddate><creator>Mongrédien, Raphaële</creator><creator>Erdozain, Amaia M.</creator><creator>Dumas, Sylvie</creator><creator>Cutando, Laura</creator><creator>del Moral, Amaia Nuñez</creator><creator>Puighermanal, Emma</creator><creator>Rezai Amin, Sara</creator><creator>Giros, Bruno</creator><creator>Valjent, Emmanuel</creator><creator>Meana, J. 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Unlike previously characterized matricellular proteins, hevin remains strongly expressed in the adult brain in both astrocytes and neurons, but its precise pattern of expression is unknown. The present study provides the first systematic description of hevin mRNA distribution in the adult mouse brain. Using isotopic in situ hybridization, we showed that hevin is strongly expressed in the cortex, hippocampus, basal ganglia complex, diverse thalamic nuclei and brainstem motor nuclei. To identify the cellular phenotype of hevin-expressing cells, we used double fluorescent in situ hybridization in mouse and human adult brains. In the mouse, hevin mRNA was found in the majority of astrocytes but also in specific neuronal populations. Hevin was expressed in almost all parvalbumin-positive projection neurons and local interneurons. In addition, hevin mRNA was found in: (1) subsets of other inhibitory GABAergic neuronal subtypes, including calbindin, cholecystokinin, neuropeptide Y, and somatostatin-positive neurons; (2) subsets of glutamatergic neurons, identified by the expression of the vesicular glutamate transporters VGLUT1 and VGLUT2; and (3) the majority of cholinergic neurons from motor nuclei. Hevin mRNA was absent from all monoaminergic neurons and cholinergic neurons of the ascending pathway. A similar cellular profile of expression was observed in human, with expression of hevin in parvalbumin interneurons and astrocytes in the cortex and caudate nucleus as well as in cortical glutamatergic neurons. Furthermore, hevin transcript was enriched in ribosomes of astrocytes and parvalbumin neurons providing a direct evidence of hevin mRNAs translation in these cell types. This study reveals the unique and complex expression profile of the matricellular protein hevin in the adult brain. 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| fulltext | fulltext |
| identifier | ISSN: 1863-2653 |
| ispartof | Brain Structure and Function, 2019-04, Vol.224 (3), p.1219-1244 |
| issn | 1863-2653 1863-2661 0340-2061 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_inserm_02008003v2 |
| source | SpringerLink Journals - AutoHoldings |
| subjects | Astrocytes Basal ganglia Biomedical and Life Sciences Biomedicine Brain Brain stem Calbindin Caudate nucleus Cell Biology Cell migration Cholecystokinin Cortex Fluorescence in situ hybridization Glutamatergic transmission Interneurons Life Sciences Motor nuclei Neurology Neurons and Cognition Neuropeptide Y Neurosciences Original Article Osteonectin Parvalbumin Phenotypes Ribosomes Synaptic plasticity Synaptogenesis Thalamus Transcription |
| title | Cartography of hevin-expressing cells in the adult brain reveals prominent expression in astrocytes and parvalbumin neurons |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-12T10%3A33%3A57IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Cartography%20of%20hevin-expressing%20cells%20in%20the%20adult%20brain%20reveals%20prominent%20expression%20in%20astrocytes%20and%20parvalbumin%20neurons&rft.jtitle=Brain%20Structure%20and%20Function&rft.au=Mongr%C3%A9dien,%20Rapha%C3%ABle&rft.date=2019-04-01&rft.volume=224&rft.issue=3&rft.spage=1219&rft.epage=1244&rft.pages=1219-1244&rft.issn=1863-2653&rft.eissn=1863-2661&rft_id=info:doi/10.1007/s00429-019-01831-x&rft_dat=%3Cproquest_hal_p%3E2179390407%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2168016072&rft_id=info:pmid/30656447&rfr_iscdi=true |