Ring-like oligomers of synaptotagmins and related C2 domain proteins

Autores
Zanetti, Maria Natalia; Bello, Oscar Daniel; Wang, Jing; Coleman, Jeff; Cai, Yiying; Sindelar, Charles V.; Rothman, James E.; Krishnakumar, Shyam S.
Año de publicación
2016
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
We recently reported that the C2AB portion of Synaptotagmin 1 (Syt1) could selfassemble into Ca2+-sensitive ring-like oligomers on membranes, which could potentially regulate neurotransmitter release. Here we report that analogous ring-like oligomers assemble from the C2AB domains of other Syt isoforms (Syt2, Syt7, Syt9) as well as related C2 domain containing protein, Doc2B and extended Synaptotagmins (E-Syts). Evidently, circular oligomerization is a general and conserved structural aspect of many C2 domain proteins, including Synaptotagmins. Further, using electron microscopy combined with targeted mutations, we show that under physiologically relevant conditions, both the Syt1 ring assembly and its rapid disruption by Ca2+ involve the well-established functional surfaces on the C2B domain that are important for synaptic transmission. Our data suggests that ring formation may be triggered at an early step in synaptic vesicle docking and positions Syt1 to synchronize neurotransmitter release to Ca2+ influx.
Fil: Zanetti, Maria Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; Argentina
Fil: Bello, Oscar Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; Argentina
Fil: Wang, Jing. University of Yale. School of Medicine; Estados Unidos
Fil: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Cai, Yiying. University of Yale. School of Medicine; Estados Unidos
Fil: Sindelar, Charles V.. University of Yale. School of Medicine; Estados Unidos
Fil: Rothman, James E.. University of Yale. School of Medicine; Estados Unidos
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos
Materia
Biophisics
Neuroscience
Membrane fusion
Estructural biology
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/183138
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/183138
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Ring-like oligomers of synaptotagmins and related C2 domain proteinsZanetti, Maria NataliaBello, Oscar DanielWang, JingColeman, JeffCai, YiyingSindelar, Charles V.Rothman, James E.Krishnakumar, Shyam S.BiophisicsNeuroscienceMembrane fusionEstructural biologyhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1We recently reported that the C2AB portion of Synaptotagmin 1 (Syt1) could selfassemble into Ca2+-sensitive ring-like oligomers on membranes, which could potentially regulate neurotransmitter release. Here we report that analogous ring-like oligomers assemble from the C2AB domains of other Syt isoforms (Syt2, Syt7, Syt9) as well as related C2 domain containing protein, Doc2B and extended Synaptotagmins (E-Syts). Evidently, circular oligomerization is a general and conserved structural aspect of many C2 domain proteins, including Synaptotagmins. Further, using electron microscopy combined with targeted mutations, we show that under physiologically relevant conditions, both the Syt1 ring assembly and its rapid disruption by Ca2+ involve the well-established functional surfaces on the C2B domain that are important for synaptic transmission. Our data suggests that ring formation may be triggered at an early step in synaptic vesicle docking and positions Syt1 to synchronize neurotransmitter release to Ca2+ influx.Fil: Zanetti, Maria Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; ArgentinaFil: Bello, Oscar Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; ArgentinaFil: Wang, Jing. University of Yale. School of Medicine; Estados UnidosFil: Coleman, Jeff. University of Yale. School of Medicine; Estados UnidosFil: Cai, Yiying. University of Yale. School of Medicine; Estados UnidosFil: Sindelar, Charles V.. University of Yale. School of Medicine; Estados UnidosFil: Rothman, James E.. University of Yale. School of Medicine; Estados UnidosFil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados UnidoseLife Sciences Publications2016-07info: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/11336/183138Zanetti, Maria Natalia; Bello, Oscar Daniel; Wang, Jing; Coleman, Jeff; Cai, Yiying; et al.; Ring-like oligomers of synaptotagmins and related C2 domain proteins; eLife Sciences Publications; eLife; 5; 7-2016; 1-152050-084XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/17262info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.17262info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:07:42Zoai:ri.conicet.gov.ar:11336/183138instacron: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:34982025-10-22 11:07:42.974CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Ring-like oligomers of synaptotagmins and related C2 domain proteins
title Ring-like oligomers of synaptotagmins and related C2 domain proteins
spellingShingle Ring-like oligomers of synaptotagmins and related C2 domain proteins
Zanetti, Maria Natalia
Biophisics
Neuroscience
Membrane fusion
Estructural biology
title_short Ring-like oligomers of synaptotagmins and related C2 domain proteins
title_full Ring-like oligomers of synaptotagmins and related C2 domain proteins
title_fullStr Ring-like oligomers of synaptotagmins and related C2 domain proteins
title_full_unstemmed Ring-like oligomers of synaptotagmins and related C2 domain proteins
title_sort Ring-like oligomers of synaptotagmins and related C2 domain proteins
dc.creator.none.fl_str_mv Zanetti, Maria Natalia
Bello, Oscar Daniel
Wang, Jing
Coleman, Jeff
Cai, Yiying
Sindelar, Charles V.
Rothman, James E.
Krishnakumar, Shyam S.
author Zanetti, Maria Natalia
author_facet Zanetti, Maria Natalia
Bello, Oscar Daniel
Wang, Jing
Coleman, Jeff
Cai, Yiying
Sindelar, Charles V.
Rothman, James E.
Krishnakumar, Shyam S.
author_role author
author2 Bello, Oscar Daniel
Wang, Jing
Coleman, Jeff
Cai, Yiying
Sindelar, Charles V.
Rothman, James E.
Krishnakumar, Shyam S.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Biophisics
Neuroscience
Membrane fusion
Estructural biology
topic Biophisics
Neuroscience
Membrane fusion
Estructural biology
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv We recently reported that the C2AB portion of Synaptotagmin 1 (Syt1) could selfassemble into Ca2+-sensitive ring-like oligomers on membranes, which could potentially regulate neurotransmitter release. Here we report that analogous ring-like oligomers assemble from the C2AB domains of other Syt isoforms (Syt2, Syt7, Syt9) as well as related C2 domain containing protein, Doc2B and extended Synaptotagmins (E-Syts). Evidently, circular oligomerization is a general and conserved structural aspect of many C2 domain proteins, including Synaptotagmins. Further, using electron microscopy combined with targeted mutations, we show that under physiologically relevant conditions, both the Syt1 ring assembly and its rapid disruption by Ca2+ involve the well-established functional surfaces on the C2B domain that are important for synaptic transmission. Our data suggests that ring formation may be triggered at an early step in synaptic vesicle docking and positions Syt1 to synchronize neurotransmitter release to Ca2+ influx.
Fil: Zanetti, Maria Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; Argentina
Fil: Bello, Oscar Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Instituto de Histología y Embriología de Mendoza Dr. Mario H. Burgos; Argentina
Fil: Wang, Jing. University of Yale. School of Medicine; Estados Unidos
Fil: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Cai, Yiying. University of Yale. School of Medicine; Estados Unidos
Fil: Sindelar, Charles V.. University of Yale. School of Medicine; Estados Unidos
Fil: Rothman, James E.. University of Yale. School of Medicine; Estados Unidos
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos
description We recently reported that the C2AB portion of Synaptotagmin 1 (Syt1) could selfassemble into Ca2+-sensitive ring-like oligomers on membranes, which could potentially regulate neurotransmitter release. Here we report that analogous ring-like oligomers assemble from the C2AB domains of other Syt isoforms (Syt2, Syt7, Syt9) as well as related C2 domain containing protein, Doc2B and extended Synaptotagmins (E-Syts). Evidently, circular oligomerization is a general and conserved structural aspect of many C2 domain proteins, including Synaptotagmins. Further, using electron microscopy combined with targeted mutations, we show that under physiologically relevant conditions, both the Syt1 ring assembly and its rapid disruption by Ca2+ involve the well-established functional surfaces on the C2B domain that are important for synaptic transmission. Our data suggests that ring formation may be triggered at an early step in synaptic vesicle docking and positions Syt1 to synchronize neurotransmitter release to Ca2+ influx.
publishDate 2016
dc.date.none.fl_str_mv 2016-07
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/11336/183138
Zanetti, Maria Natalia; Bello, Oscar Daniel; Wang, Jing; Coleman, Jeff; Cai, Yiying; et al.; Ring-like oligomers of synaptotagmins and related C2 domain proteins; eLife Sciences Publications; eLife; 5; 7-2016; 1-15
2050-084X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/183138
identifier_str_mv Zanetti, Maria Natalia; Bello, Oscar Daniel; Wang, Jing; Coleman, Jeff; Cai, Yiying; et al.; Ring-like oligomers of synaptotagmins and related C2 domain proteins; eLife Sciences Publications; eLife; 5; 7-2016; 1-15
2050-084X
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://elifesciences.org/articles/17262
info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.17262
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications
publisher.none.fl_str_mv eLife Sciences Publications
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_ 1846781396545175552
score 12.982451

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