Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway

Autores
Bender, Crhistian Luis; Sun, Xingxing; Farooq, Muhammad; Yang, Qian; Davison, Caroline; Maroteaux, Matthieu; Huang, Yi Shuian; Ishikawa, Yoshihiro; Liu, Siqiong June
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Stress alters brain function by modifying the structure and function of neurons and astrocytes. The fine processes of astrocytes are critical for the clearance of neurotransmitters during synaptic transmission. Thus, experience-dependent remodeling of glial processes is anticipated to alter the output of neural circuits. However, the molecular mechanisms that underlie glial structural plasticity are not known. Here we show that a single exposure of male and female mice to an acute stress produced a long-lasting retraction of the lateral processes of cerebellar Bergmann glial cells. These cells express the GluA1 subunit of AMPA-type glutamate receptors, and GluA1 knockdown is known to shorten the length of glial processes. We found that stress reduced the level of GluA1 protein and AMPA receptor-mediated currents in Bergmann glial cells, and these effects were absent in mice devoid of CPEB3, a protein that binds to GluA1 mRNA and regulates GluA1 protein synthesis. Administration of a b-adrenergic receptor blocker attenuated the reduction in GluA1, and deletion of adenylate cyclase 5 prevented GluA1 suppression. Therefore, stress suppresses GluA1 protein synthesis via an adrenergic/adenylyl cyclase/CPEB3 pathway, and reduces the length of astrocyte lateral processes. Our results identify a novel mechanism for GluA1 subunit plasticity in non-neuronal cells and suggest a previously unappreciated role for AMPA receptors in stress-induced astrocytic remodeling.
Fil: Bender, Crhistian Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Farmacología Experimental de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Instituto de Farmacología Experimental de Córdoba; Argentina. State University of Louisiana; Estados Unidos
Fil: Sun, Xingxing. Huazhong University of Science & Technology; República de China. State University of Louisiana; Estados Unidos
Fil: Farooq, Muhammad. State University of Louisiana; Estados Unidos
Fil: Yang, Qian. State University of Louisiana; Estados Unidos
Fil: Davison, Caroline. State University of Louisiana; Estados Unidos
Fil: Maroteaux, Matthieu. State University of Louisiana; Estados Unidos
Fil: Huang, Yi Shuian. State University of Louisiana; Estados Unidos
Fil: Ishikawa, Yoshihiro. State University of Louisiana; Estados Unidos. Yokohama City University. Graduate School of Medicine; Japón
Fil: Liu, Siqiong June. State University of Louisiana; Estados Unidos
Materia
ADRENERGIC RECEPTORS
ASTROCYTIC REMODELING
BERGMANN GLIAL CELLS
CPEB3
GLIAL PROCESSES
GLUA1
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/141514

id CONICETDig_d2b7ce7414881d3f86e29574f99342d3
oai_identifier_str oai:ri.conicet.gov.ar:11336/141514
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathwayBender, Crhistian LuisSun, XingxingFarooq, MuhammadYang, QianDavison, CarolineMaroteaux, MatthieuHuang, Yi ShuianIshikawa, YoshihiroLiu, Siqiong JuneADRENERGIC RECEPTORSASTROCYTIC REMODELINGBERGMANN GLIAL CELLSCPEB3GLIAL PROCESSESGLUA1https://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Stress alters brain function by modifying the structure and function of neurons and astrocytes. The fine processes of astrocytes are critical for the clearance of neurotransmitters during synaptic transmission. Thus, experience-dependent remodeling of glial processes is anticipated to alter the output of neural circuits. However, the molecular mechanisms that underlie glial structural plasticity are not known. Here we show that a single exposure of male and female mice to an acute stress produced a long-lasting retraction of the lateral processes of cerebellar Bergmann glial cells. These cells express the GluA1 subunit of AMPA-type glutamate receptors, and GluA1 knockdown is known to shorten the length of glial processes. We found that stress reduced the level of GluA1 protein and AMPA receptor-mediated currents in Bergmann glial cells, and these effects were absent in mice devoid of CPEB3, a protein that binds to GluA1 mRNA and regulates GluA1 protein synthesis. Administration of a b-adrenergic receptor blocker attenuated the reduction in GluA1, and deletion of adenylate cyclase 5 prevented GluA1 suppression. Therefore, stress suppresses GluA1 protein synthesis via an adrenergic/adenylyl cyclase/CPEB3 pathway, and reduces the length of astrocyte lateral processes. Our results identify a novel mechanism for GluA1 subunit plasticity in non-neuronal cells and suggest a previously unappreciated role for AMPA receptors in stress-induced astrocytic remodeling.Fil: Bender, Crhistian Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Farmacología Experimental de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Instituto de Farmacología Experimental de Córdoba; Argentina. State University of Louisiana; Estados UnidosFil: Sun, Xingxing. Huazhong University of Science & Technology; República de China. State University of Louisiana; Estados UnidosFil: Farooq, Muhammad. State University of Louisiana; Estados UnidosFil: Yang, Qian. State University of Louisiana; Estados UnidosFil: Davison, Caroline. State University of Louisiana; Estados UnidosFil: Maroteaux, Matthieu. State University of Louisiana; Estados UnidosFil: Huang, Yi Shuian. State University of Louisiana; Estados UnidosFil: Ishikawa, Yoshihiro. State University of Louisiana; Estados Unidos. Yokohama City University. Graduate School of Medicine; JapónFil: Liu, Siqiong June. State University of Louisiana; Estados UnidosSociety for Neuroscience2020-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/141514Bender, Crhistian Luis; Sun, Xingxing; Farooq, Muhammad; Yang, Qian; Davison, Caroline; et al.; Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway; Society for Neuroscience; Journal of Neuroscience; 40; 17; 4-2020; 3374-33840270-6474CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.0013-19.2020info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/40/17/3374info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:29:28Zoai:ri.conicet.gov.ar:11336/141514instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:29:29.012CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
title Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
spellingShingle Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
Bender, Crhistian Luis
ADRENERGIC RECEPTORS
ASTROCYTIC REMODELING
BERGMANN GLIAL CELLS
CPEB3
GLIAL PROCESSES
GLUA1
title_short Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
title_full Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
title_fullStr Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
title_full_unstemmed Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
title_sort Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway
dc.creator.none.fl_str_mv Bender, Crhistian Luis
Sun, Xingxing
Farooq, Muhammad
Yang, Qian
Davison, Caroline
Maroteaux, Matthieu
Huang, Yi Shuian
Ishikawa, Yoshihiro
Liu, Siqiong June
author Bender, Crhistian Luis
author_facet Bender, Crhistian Luis
Sun, Xingxing
Farooq, Muhammad
Yang, Qian
Davison, Caroline
Maroteaux, Matthieu
Huang, Yi Shuian
Ishikawa, Yoshihiro
Liu, Siqiong June
author_role author
author2 Sun, Xingxing
Farooq, Muhammad
Yang, Qian
Davison, Caroline
Maroteaux, Matthieu
Huang, Yi Shuian
Ishikawa, Yoshihiro
Liu, Siqiong June
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ADRENERGIC RECEPTORS
ASTROCYTIC REMODELING
BERGMANN GLIAL CELLS
CPEB3
GLIAL PROCESSES
GLUA1
topic ADRENERGIC RECEPTORS
ASTROCYTIC REMODELING
BERGMANN GLIAL CELLS
CPEB3
GLIAL PROCESSES
GLUA1
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Stress alters brain function by modifying the structure and function of neurons and astrocytes. The fine processes of astrocytes are critical for the clearance of neurotransmitters during synaptic transmission. Thus, experience-dependent remodeling of glial processes is anticipated to alter the output of neural circuits. However, the molecular mechanisms that underlie glial structural plasticity are not known. Here we show that a single exposure of male and female mice to an acute stress produced a long-lasting retraction of the lateral processes of cerebellar Bergmann glial cells. These cells express the GluA1 subunit of AMPA-type glutamate receptors, and GluA1 knockdown is known to shorten the length of glial processes. We found that stress reduced the level of GluA1 protein and AMPA receptor-mediated currents in Bergmann glial cells, and these effects were absent in mice devoid of CPEB3, a protein that binds to GluA1 mRNA and regulates GluA1 protein synthesis. Administration of a b-adrenergic receptor blocker attenuated the reduction in GluA1, and deletion of adenylate cyclase 5 prevented GluA1 suppression. Therefore, stress suppresses GluA1 protein synthesis via an adrenergic/adenylyl cyclase/CPEB3 pathway, and reduces the length of astrocyte lateral processes. Our results identify a novel mechanism for GluA1 subunit plasticity in non-neuronal cells and suggest a previously unappreciated role for AMPA receptors in stress-induced astrocytic remodeling.
Fil: Bender, Crhistian Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Farmacología Experimental de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Instituto de Farmacología Experimental de Córdoba; Argentina. State University of Louisiana; Estados Unidos
Fil: Sun, Xingxing. Huazhong University of Science & Technology; República de China. State University of Louisiana; Estados Unidos
Fil: Farooq, Muhammad. State University of Louisiana; Estados Unidos
Fil: Yang, Qian. State University of Louisiana; Estados Unidos
Fil: Davison, Caroline. State University of Louisiana; Estados Unidos
Fil: Maroteaux, Matthieu. State University of Louisiana; Estados Unidos
Fil: Huang, Yi Shuian. State University of Louisiana; Estados Unidos
Fil: Ishikawa, Yoshihiro. State University of Louisiana; Estados Unidos. Yokohama City University. Graduate School of Medicine; Japón
Fil: Liu, Siqiong June. State University of Louisiana; Estados Unidos
description Stress alters brain function by modifying the structure and function of neurons and astrocytes. The fine processes of astrocytes are critical for the clearance of neurotransmitters during synaptic transmission. Thus, experience-dependent remodeling of glial processes is anticipated to alter the output of neural circuits. However, the molecular mechanisms that underlie glial structural plasticity are not known. Here we show that a single exposure of male and female mice to an acute stress produced a long-lasting retraction of the lateral processes of cerebellar Bergmann glial cells. These cells express the GluA1 subunit of AMPA-type glutamate receptors, and GluA1 knockdown is known to shorten the length of glial processes. We found that stress reduced the level of GluA1 protein and AMPA receptor-mediated currents in Bergmann glial cells, and these effects were absent in mice devoid of CPEB3, a protein that binds to GluA1 mRNA and regulates GluA1 protein synthesis. Administration of a b-adrenergic receptor blocker attenuated the reduction in GluA1, and deletion of adenylate cyclase 5 prevented GluA1 suppression. Therefore, stress suppresses GluA1 protein synthesis via an adrenergic/adenylyl cyclase/CPEB3 pathway, and reduces the length of astrocyte lateral processes. Our results identify a novel mechanism for GluA1 subunit plasticity in non-neuronal cells and suggest a previously unappreciated role for AMPA receptors in stress-induced astrocytic remodeling.
publishDate 2020
dc.date.none.fl_str_mv 2020-04
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/141514
Bender, Crhistian Luis; Sun, Xingxing; Farooq, Muhammad; Yang, Qian; Davison, Caroline; et al.; Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway; Society for Neuroscience; Journal of Neuroscience; 40; 17; 4-2020; 3374-3384
0270-6474
CONICET Digital
CONICET
url http://hdl.handle.net/11336/141514
identifier_str_mv Bender, Crhistian Luis; Sun, Xingxing; Farooq, Muhammad; Yang, Qian; Davison, Caroline; et al.; Emotional stress induces structural plasticity in Bergmann glial cells via an AC5–CPEB3–GluA1 pathway; Society for Neuroscience; Journal of Neuroscience; 40; 17; 4-2020; 3374-3384
0270-6474
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.0013-19.2020
info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/40/17/3374
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1844614301040508928
score 13.070432