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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/141514
Ver los metadatos del registro completo
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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 |
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1844614301040508928 |
score |
13.070432 |