Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain

Autores
Gruget, Clémence; Bello, Oscar Daniel; Coleman, Jeff; Krishnakumar, Shyam S.; Perez, Eric; Rothman, James E.; Pincet, Frederic; Donaldson, Stephen H.
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Synaptotagmin interaction with anionic lipid (phosphatidylserine/phosphatidylinositol) containing membranes, both in the absence and presence of calcium ions (Ca2+), is critical to its central role in orchestrating neurotransmitter release. The molecular surfaces involved, namely the conserved polylysine motif in the C2B domain and Ca2+-binding aliphatic loops on both C2A and C2B domains, are known. Here we use surface force apparatus combined with systematic mutational analysis of the functional surfaces to directly measure Syt1-membrane interaction and fully map the site-binding energetics of Syt1 both in the absence and presence of Ca2+. By correlating energetics data with the molecular rearrangements measured during confinement, we find that both C2 domains cooperate in membrane binding, with the C2B domain functioning as the main energetic driver, and the C2A domain acting as a facilitator.
Fil: Gruget, Clémence. Ecole Normale Supérieure; Francia
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: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos
Fil: Perez, Eric. Ecole Normale Supérieure; Francia
Fil: Rothman, James E.. University of Yale. School of Medicine; Estados Unidos
Fil: Pincet, Frederic. Ecole Normale Supérieure; Francia. University of Yale. School of Medicine; Estados Unidos
Fil: Donaldson, Stephen H.. Ecole Normale Supérieure; Francia
Materia
EXOCYTOSIS
MOLECULAR
CONFORMATION
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:11336/141422
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domainGruget, ClémenceBello, Oscar DanielColeman, JeffKrishnakumar, Shyam S.Perez, EricRothman, James E.Pincet, FredericDonaldson, Stephen H.EXOCYTOSISMOLECULARCONFORMATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Synaptotagmin interaction with anionic lipid (phosphatidylserine/phosphatidylinositol) containing membranes, both in the absence and presence of calcium ions (Ca2+), is critical to its central role in orchestrating neurotransmitter release. The molecular surfaces involved, namely the conserved polylysine motif in the C2B domain and Ca2+-binding aliphatic loops on both C2A and C2B domains, are known. Here we use surface force apparatus combined with systematic mutational analysis of the functional surfaces to directly measure Syt1-membrane interaction and fully map the site-binding energetics of Syt1 both in the absence and presence of Ca2+. By correlating energetics data with the molecular rearrangements measured during confinement, we find that both C2 domains cooperate in membrane binding, with the C2B domain functioning as the main energetic driver, and the C2A domain acting as a facilitator.Fil: Gruget, Clémence. Ecole Normale Supérieure; FranciaFil: 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: Coleman, Jeff. University of Yale. School of Medicine; Estados UnidosFil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados UnidosFil: Perez, Eric. Ecole Normale Supérieure; FranciaFil: Rothman, James E.. University of Yale. School of Medicine; Estados UnidosFil: Pincet, Frederic. Ecole Normale Supérieure; Francia. University of Yale. School of Medicine; Estados UnidosFil: Donaldson, Stephen H.. Ecole Normale Supérieure; FranciaNature2020-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/141422Gruget, Clémence; Bello, Oscar Daniel; Coleman, Jeff; Krishnakumar, Shyam S.; Perez, Eric; et al.; Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain; Nature; Scientific Reports; 10; 1; 10-2020; 1-102045-2322CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://www.nature.com/articles/s41598-020-74923-yinfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-020-74923-yinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:15:26Zoai:ri.conicet.gov.ar:11336/141422instacron: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 10:15:26.434CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
title Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
spellingShingle Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
Gruget, Clémence
EXOCYTOSIS
MOLECULAR
CONFORMATION
title_short Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
title_full Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
title_fullStr Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
title_full_unstemmed Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
title_sort Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain
dc.creator.none.fl_str_mv Gruget, Clémence
Bello, Oscar Daniel
Coleman, Jeff
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H.
author Gruget, Clémence
author_facet Gruget, Clémence
Bello, Oscar Daniel
Coleman, Jeff
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H.
author_role author
author2 Bello, Oscar Daniel
Coleman, Jeff
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv EXOCYTOSIS
MOLECULAR
CONFORMATION
topic EXOCYTOSIS
MOLECULAR
CONFORMATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Synaptotagmin interaction with anionic lipid (phosphatidylserine/phosphatidylinositol) containing membranes, both in the absence and presence of calcium ions (Ca2+), is critical to its central role in orchestrating neurotransmitter release. The molecular surfaces involved, namely the conserved polylysine motif in the C2B domain and Ca2+-binding aliphatic loops on both C2A and C2B domains, are known. Here we use surface force apparatus combined with systematic mutational analysis of the functional surfaces to directly measure Syt1-membrane interaction and fully map the site-binding energetics of Syt1 both in the absence and presence of Ca2+. By correlating energetics data with the molecular rearrangements measured during confinement, we find that both C2 domains cooperate in membrane binding, with the C2B domain functioning as the main energetic driver, and the C2A domain acting as a facilitator.
Fil: Gruget, Clémence. Ecole Normale Supérieure; Francia
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: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos
Fil: Perez, Eric. Ecole Normale Supérieure; Francia
Fil: Rothman, James E.. University of Yale. School of Medicine; Estados Unidos
Fil: Pincet, Frederic. Ecole Normale Supérieure; Francia. University of Yale. School of Medicine; Estados Unidos
Fil: Donaldson, Stephen H.. Ecole Normale Supérieure; Francia
description Synaptotagmin interaction with anionic lipid (phosphatidylserine/phosphatidylinositol) containing membranes, both in the absence and presence of calcium ions (Ca2+), is critical to its central role in orchestrating neurotransmitter release. The molecular surfaces involved, namely the conserved polylysine motif in the C2B domain and Ca2+-binding aliphatic loops on both C2A and C2B domains, are known. Here we use surface force apparatus combined with systematic mutational analysis of the functional surfaces to directly measure Syt1-membrane interaction and fully map the site-binding energetics of Syt1 both in the absence and presence of Ca2+. By correlating energetics data with the molecular rearrangements measured during confinement, we find that both C2 domains cooperate in membrane binding, with the C2B domain functioning as the main energetic driver, and the C2A domain acting as a facilitator.
publishDate 2020
dc.date.none.fl_str_mv 2020-10
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/11336/141422
Gruget, Clémence; Bello, Oscar Daniel; Coleman, Jeff; Krishnakumar, Shyam S.; Perez, Eric; et al.; Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain; Nature; Scientific Reports; 10; 1; 10-2020; 1-10
2045-2322
CONICET Digital
CONICET
url http://hdl.handle.net/11336/141422
identifier_str_mv Gruget, Clémence; Bello, Oscar Daniel; Coleman, Jeff; Krishnakumar, Shyam S.; Perez, Eric; et al.; Synaptotagmin-1 membrane binding is driven by the C2B domain and assisted cooperatively by the C2A domain; Nature; Scientific Reports; 10; 1; 10-2020; 1-10
2045-2322
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://www.nature.com/articles/s41598-020-74923-y
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-020-74923-y
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
dc.publisher.none.fl_str_mv Nature
publisher.none.fl_str_mv Nature
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_ 1844614090577674240
score 13.070432

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