miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation

Autores
Bernardi, Yanel Elina; Sanchez Vasquez, Estefania; Márquez, Rocío Belén; Piacentino, Michael L.; Urrutia, Hugo; Rossi, Izadora; Alcântara Saraiva, Karina L.; Pereira Neves, Antonio; Ramirez, Marcel I.; Bronner, Marianne E.; de Miguel, Natalia; Strobl Mazulla, Pablo Hernan
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
While interactions between neural crest and placode cells are critical for the proper formation of the trigeminal ganglion, the mechanisms underlying this process remain largely uncharacterized. Here, by using chick embryos, we show that the microRNA (miR)-203, whose epigenetic repression is required for neural crest migration, is reactivated in coalescing and condensing trigeminal ganglion cells. Overexpression of miR-203 induces ectopic coalescence of neural crest cells and increases ganglion size. By employing cell-specific electroporations for either miR-203 sponging or genomic editing using CRISPR/Cas9, we elucidated that neural crest cells serve as the source, while placode cells serve as the site of action for miR-203 in trigeminal ganglion condensation. Demonstrating intercellular communication, overexpression of miR-203 in the neural crest in vitro or in vivo represses an miR-responsive sensor in placode cells. Moreover, neural crest-secreted extracellular vesicles (EVs), visualized using pHluorin-CD63 vector, become incorporated into the cytoplasm of placode cells. Finally, RT-PCR analysis shows that small EVs isolated from condensing trigeminal ganglia are selectively loaded with miR-203. Together, our findings reveal a critical role in vivo for neural crest-placode communication mediated by sEVs and their selective microRNA cargo for proper trigeminal ganglion formation.
Fil: Bernardi, Yanel Elina. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Sanchez Vasquez, Estefania. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Márquez, Rocío Belén. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Piacentino, Michael L.. California Institute of Technology; Estados Unidos
Fil: Urrutia, Hugo. California Institute of Technology; Estados Unidos
Fil: Rossi, Izadora. California Institute of Technology; Estados Unidos
Fil: Alcântara Saraiva, Karina L.. California Institute of Technology; Estados Unidos
Fil: Pereira Neves, Antonio. California Institute of Technology; Estados Unidos
Fil: Ramirez, Marcel I.. California Institute of Technology; Estados Unidos
Fil: Bronner, Marianne E.. California Institute of Technology; Estados Unidos
Fil: de Miguel, Natalia. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Strobl Mazulla, Pablo Hernan. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Materia
sEVs
miRNAs
neural crest
placode
trigeminal ganglion
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:11336/253553
Acceder
id CONICETDig_7f5db4b71618d7ed8ac3fcda4a0655b4
oai_identifier_str oai:ri.conicet.gov.ar:11336/253553
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formationBernardi, Yanel ElinaSanchez Vasquez, EstefaniaMárquez, Rocío BelénPiacentino, Michael L.Urrutia, HugoRossi, IzadoraAlcântara Saraiva, Karina L.Pereira Neves, AntonioRamirez, Marcel I.Bronner, Marianne E.de Miguel, NataliaStrobl Mazulla, Pablo HernansEVsmiRNAsneural crestplacodetrigeminal ganglionhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1While interactions between neural crest and placode cells are critical for the proper formation of the trigeminal ganglion, the mechanisms underlying this process remain largely uncharacterized. Here, by using chick embryos, we show that the microRNA (miR)-203, whose epigenetic repression is required for neural crest migration, is reactivated in coalescing and condensing trigeminal ganglion cells. Overexpression of miR-203 induces ectopic coalescence of neural crest cells and increases ganglion size. By employing cell-specific electroporations for either miR-203 sponging or genomic editing using CRISPR/Cas9, we elucidated that neural crest cells serve as the source, while placode cells serve as the site of action for miR-203 in trigeminal ganglion condensation. Demonstrating intercellular communication, overexpression of miR-203 in the neural crest in vitro or in vivo represses an miR-responsive sensor in placode cells. Moreover, neural crest-secreted extracellular vesicles (EVs), visualized using pHluorin-CD63 vector, become incorporated into the cytoplasm of placode cells. Finally, RT-PCR analysis shows that small EVs isolated from condensing trigeminal ganglia are selectively loaded with miR-203. Together, our findings reveal a critical role in vivo for neural crest-placode communication mediated by sEVs and their selective microRNA cargo for proper trigeminal ganglion formation.Fil: Bernardi, Yanel Elina. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; ArgentinaFil: Sanchez Vasquez, Estefania. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; ArgentinaFil: Márquez, Rocío Belén. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; ArgentinaFil: Piacentino, Michael L.. California Institute of Technology; Estados UnidosFil: Urrutia, Hugo. California Institute of Technology; Estados UnidosFil: Rossi, Izadora. California Institute of Technology; Estados UnidosFil: Alcântara Saraiva, Karina L.. California Institute of Technology; Estados UnidosFil: Pereira Neves, Antonio. California Institute of Technology; Estados UnidosFil: Ramirez, Marcel I.. California Institute of Technology; Estados UnidosFil: Bronner, Marianne E.. California Institute of Technology; Estados UnidosFil: de Miguel, Natalia. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; ArgentinaFil: Strobl Mazulla, Pablo Hernan. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; ArgentinaPublic Library of Science2024-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/253553Bernardi, Yanel Elina; Sanchez Vasquez, Estefania; Márquez, Rocío Belén; Piacentino, Michael L.; Urrutia, Hugo; et al.; miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation; Public Library of Science; PLOS Biology; 22; 7; 7-2024; 1-211545-7885CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://dx.plos.org/10.1371/journal.pbio.3002074info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pbio.3002074info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:43:25Zoai:ri.conicet.gov.ar:11336/253553instacron: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:34982025-09-03 09:43:25.781CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
title miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
spellingShingle miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
Bernardi, Yanel Elina
sEVs
miRNAs
neural crest
placode
trigeminal ganglion
title_short miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
title_full miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
title_fullStr miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
title_full_unstemmed miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
title_sort miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
dc.creator.none.fl_str_mv Bernardi, Yanel Elina
Sanchez Vasquez, Estefania
Márquez, Rocío Belén
Piacentino, Michael L.
Urrutia, Hugo
Rossi, Izadora
Alcântara Saraiva, Karina L.
Pereira Neves, Antonio
Ramirez, Marcel I.
Bronner, Marianne E.
de Miguel, Natalia
Strobl Mazulla, Pablo Hernan
author Bernardi, Yanel Elina
author_facet Bernardi, Yanel Elina
Sanchez Vasquez, Estefania
Márquez, Rocío Belén
Piacentino, Michael L.
Urrutia, Hugo
Rossi, Izadora
Alcântara Saraiva, Karina L.
Pereira Neves, Antonio
Ramirez, Marcel I.
Bronner, Marianne E.
de Miguel, Natalia
Strobl Mazulla, Pablo Hernan
author_role author
author2 Sanchez Vasquez, Estefania
Márquez, Rocío Belén
Piacentino, Michael L.
Urrutia, Hugo
Rossi, Izadora
Alcântara Saraiva, Karina L.
Pereira Neves, Antonio
Ramirez, Marcel I.
Bronner, Marianne E.
de Miguel, Natalia
Strobl Mazulla, Pablo Hernan
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv sEVs
miRNAs
neural crest
placode
trigeminal ganglion
topic sEVs
miRNAs
neural crest
placode
trigeminal ganglion
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv While interactions between neural crest and placode cells are critical for the proper formation of the trigeminal ganglion, the mechanisms underlying this process remain largely uncharacterized. Here, by using chick embryos, we show that the microRNA (miR)-203, whose epigenetic repression is required for neural crest migration, is reactivated in coalescing and condensing trigeminal ganglion cells. Overexpression of miR-203 induces ectopic coalescence of neural crest cells and increases ganglion size. By employing cell-specific electroporations for either miR-203 sponging or genomic editing using CRISPR/Cas9, we elucidated that neural crest cells serve as the source, while placode cells serve as the site of action for miR-203 in trigeminal ganglion condensation. Demonstrating intercellular communication, overexpression of miR-203 in the neural crest in vitro or in vivo represses an miR-responsive sensor in placode cells. Moreover, neural crest-secreted extracellular vesicles (EVs), visualized using pHluorin-CD63 vector, become incorporated into the cytoplasm of placode cells. Finally, RT-PCR analysis shows that small EVs isolated from condensing trigeminal ganglia are selectively loaded with miR-203. Together, our findings reveal a critical role in vivo for neural crest-placode communication mediated by sEVs and their selective microRNA cargo for proper trigeminal ganglion formation.
Fil: Bernardi, Yanel Elina. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Sanchez Vasquez, Estefania. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Márquez, Rocío Belén. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Piacentino, Michael L.. California Institute of Technology; Estados Unidos
Fil: Urrutia, Hugo. California Institute of Technology; Estados Unidos
Fil: Rossi, Izadora. California Institute of Technology; Estados Unidos
Fil: Alcântara Saraiva, Karina L.. California Institute of Technology; Estados Unidos
Fil: Pereira Neves, Antonio. California Institute of Technology; Estados Unidos
Fil: Ramirez, Marcel I.. California Institute of Technology; Estados Unidos
Fil: Bronner, Marianne E.. California Institute of Technology; Estados Unidos
Fil: de Miguel, Natalia. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
Fil: Strobl Mazulla, Pablo Hernan. Universidad Nacional de San Martin. Instituto Tecnologico de Chascomus. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - la Plata. Instituto Tecnologico de Chascomus.; Argentina
description While interactions between neural crest and placode cells are critical for the proper formation of the trigeminal ganglion, the mechanisms underlying this process remain largely uncharacterized. Here, by using chick embryos, we show that the microRNA (miR)-203, whose epigenetic repression is required for neural crest migration, is reactivated in coalescing and condensing trigeminal ganglion cells. Overexpression of miR-203 induces ectopic coalescence of neural crest cells and increases ganglion size. By employing cell-specific electroporations for either miR-203 sponging or genomic editing using CRISPR/Cas9, we elucidated that neural crest cells serve as the source, while placode cells serve as the site of action for miR-203 in trigeminal ganglion condensation. Demonstrating intercellular communication, overexpression of miR-203 in the neural crest in vitro or in vivo represses an miR-responsive sensor in placode cells. Moreover, neural crest-secreted extracellular vesicles (EVs), visualized using pHluorin-CD63 vector, become incorporated into the cytoplasm of placode cells. Finally, RT-PCR analysis shows that small EVs isolated from condensing trigeminal ganglia are selectively loaded with miR-203. Together, our findings reveal a critical role in vivo for neural crest-placode communication mediated by sEVs and their selective microRNA cargo for proper trigeminal ganglion formation.
publishDate 2024
dc.date.none.fl_str_mv 2024-07
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/11336/253553
Bernardi, Yanel Elina; Sanchez Vasquez, Estefania; Márquez, Rocío Belén; Piacentino, Michael L.; Urrutia, Hugo; et al.; miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation; Public Library of Science; PLOS Biology; 22; 7; 7-2024; 1-21
1545-7885
CONICET Digital
CONICET
url http://hdl.handle.net/11336/253553
identifier_str_mv Bernardi, Yanel Elina; Sanchez Vasquez, Estefania; Márquez, Rocío Belén; Piacentino, Michael L.; Urrutia, Hugo; et al.; miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation; Public Library of Science; PLOS Biology; 22; 7; 7-2024; 1-21
1545-7885
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://dx.plos.org/10.1371/journal.pbio.3002074
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pbio.3002074
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
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
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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score 12.885934

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