Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+

Autores
Gruget, Clémence; Coleman, Jeff; Bello, Oscar Daniel; Krishnakumar, Shyam S.; Perez, Eric; Rothman, James E.; Pincet, Frederic; Donaldson, Stephen H. Jr.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Synaptotagmin-1 (Syt1) is the primary calcium sensor (Ca2+ ) that mediates neurotransmitter release at the synapse. The tandem C2 domains (C2A and C2B) of Syt1 exhibit functionally critical, Ca2+ -dependent interactions with the plasma membrane. With the surface forces apparatus, we directly measure the binding energy of membrane-anchored Syt1 to an anionic membrane and find that Syt1 binds with ~6 kB T in EGTA, ~10 kB T in Mg2+ and ~18 kB T in Ca2+ . Molecular rearrangements measured during confinement are more prevalent in Ca2+ and Mg2+ and suggest that Syt1 initially binds through C2B, then reorients the C2 domains into the preferred binding configuration. These results provide energetic and mechanistic details of the Syt1 Ca2+ -activation process in synaptic transmission.
Fil: Gruget, Clémence. Ecole Normale Supérieure; Francia
Fil: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Bello, Oscar Daniel. University College London; Reino Unido. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - Mendoza. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem | Universidad Nacional de Cuyo. Facultad de Ciencias Medicas. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem.; Argentina
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos. University College London; Estados Unidos
Fil: Perez, Eric. Ecole Normale Supérieure; Francia
Fil: Rothman, James E.. University College London; Estados Unidos. University of Yale; Estados Unidos
Fil: Pincet, Frederic. Yale University. School of Medicine; Estados Unidos. Université de Recherche Paris Sciences et Lettres; Francia
Fil: Donaldson, Stephen H. Jr.. Ecole Normale Supérieure; Francia
Materia
MEMBRANE FUSION
NEUROTRANSMISSION
SYNAPTOTAGMIN
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:11336/160427
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/160427
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+Gruget, ClémenceColeman, JeffBello, Oscar DanielKrishnakumar, Shyam S.Perez, EricRothman, James E.Pincet, FredericDonaldson, Stephen H. Jr.MEMBRANE FUSIONNEUROTRANSMISSIONSYNAPTOTAGMINhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Synaptotagmin-1 (Syt1) is the primary calcium sensor (Ca2+ ) that mediates neurotransmitter release at the synapse. The tandem C2 domains (C2A and C2B) of Syt1 exhibit functionally critical, Ca2+ -dependent interactions with the plasma membrane. With the surface forces apparatus, we directly measure the binding energy of membrane-anchored Syt1 to an anionic membrane and find that Syt1 binds with ~6 kB T in EGTA, ~10 kB T in Mg2+ and ~18 kB T in Ca2+ . Molecular rearrangements measured during confinement are more prevalent in Ca2+ and Mg2+ and suggest that Syt1 initially binds through C2B, then reorients the C2 domains into the preferred binding configuration. These results provide energetic and mechanistic details of the Syt1 Ca2+ -activation process in synaptic transmission.Fil: Gruget, Clémence. Ecole Normale Supérieure; FranciaFil: Coleman, Jeff. University of Yale. School of Medicine; Estados UnidosFil: Bello, Oscar Daniel. University College London; Reino Unido. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - Mendoza. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem | Universidad Nacional de Cuyo. Facultad de Ciencias Medicas. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem.; ArgentinaFil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos. University College London; Estados UnidosFil: Perez, Eric. Ecole Normale Supérieure; FranciaFil: Rothman, James E.. University College London; Estados Unidos. University of Yale; Estados UnidosFil: Pincet, Frederic. Yale University. School of Medicine; Estados Unidos. Université de Recherche Paris Sciences et Lettres; FranciaFil: Donaldson, Stephen H. Jr.. Ecole Normale Supérieure; FranciaElsevier Science2018-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/160427Gruget, Clémence; Coleman, Jeff; Bello, Oscar Daniel; Krishnakumar, Shyam S.; Perez, Eric; et al.; Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+; Elsevier Science; FEBS Letters; 592; 9; 4-2018; 1497-15060014-5793CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://doi.wiley.com/10.1002/1873-3468.13040info:eu-repo/semantics/altIdentifier/doi/10.1002/1873-3468.13040info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:50:49Zoai:ri.conicet.gov.ar:11336/160427instacron: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 09:50:50.046CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
title Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
spellingShingle Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
Gruget, Clémence
MEMBRANE FUSION
NEUROTRANSMISSION
SYNAPTOTAGMIN
title_short Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
title_full Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
title_fullStr Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
title_full_unstemmed Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
title_sort Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+
dc.creator.none.fl_str_mv Gruget, Clémence
Coleman, Jeff
Bello, Oscar Daniel
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H. Jr.
author Gruget, Clémence
author_facet Gruget, Clémence
Coleman, Jeff
Bello, Oscar Daniel
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H. Jr.
author_role author
author2 Coleman, Jeff
Bello, Oscar Daniel
Krishnakumar, Shyam S.
Perez, Eric
Rothman, James E.
Pincet, Frederic
Donaldson, Stephen H. Jr.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv MEMBRANE FUSION
NEUROTRANSMISSION
SYNAPTOTAGMIN
topic MEMBRANE FUSION
NEUROTRANSMISSION
SYNAPTOTAGMIN
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Synaptotagmin-1 (Syt1) is the primary calcium sensor (Ca2+ ) that mediates neurotransmitter release at the synapse. The tandem C2 domains (C2A and C2B) of Syt1 exhibit functionally critical, Ca2+ -dependent interactions with the plasma membrane. With the surface forces apparatus, we directly measure the binding energy of membrane-anchored Syt1 to an anionic membrane and find that Syt1 binds with ~6 kB T in EGTA, ~10 kB T in Mg2+ and ~18 kB T in Ca2+ . Molecular rearrangements measured during confinement are more prevalent in Ca2+ and Mg2+ and suggest that Syt1 initially binds through C2B, then reorients the C2 domains into the preferred binding configuration. These results provide energetic and mechanistic details of the Syt1 Ca2+ -activation process in synaptic transmission.
Fil: Gruget, Clémence. Ecole Normale Supérieure; Francia
Fil: Coleman, Jeff. University of Yale. School of Medicine; Estados Unidos
Fil: Bello, Oscar Daniel. University College London; Reino Unido. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - Mendoza. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem | Universidad Nacional de Cuyo. Facultad de Ciencias Medicas. Instituto de Histologia y Embriologia de Mendoza Dr. Mario H. Burgos. Grupo Vinculado de Investigacion y Desarrollo Biotecnologico Aplicado Al Diagnostico Al Ihem.; Argentina
Fil: Krishnakumar, Shyam S.. University of Yale. School of Medicine; Estados Unidos. University College London; Estados Unidos
Fil: Perez, Eric. Ecole Normale Supérieure; Francia
Fil: Rothman, James E.. University College London; Estados Unidos. University of Yale; Estados Unidos
Fil: Pincet, Frederic. Yale University. School of Medicine; Estados Unidos. Université de Recherche Paris Sciences et Lettres; Francia
Fil: Donaldson, Stephen H. Jr.. Ecole Normale Supérieure; Francia
description Synaptotagmin-1 (Syt1) is the primary calcium sensor (Ca2+ ) that mediates neurotransmitter release at the synapse. The tandem C2 domains (C2A and C2B) of Syt1 exhibit functionally critical, Ca2+ -dependent interactions with the plasma membrane. With the surface forces apparatus, we directly measure the binding energy of membrane-anchored Syt1 to an anionic membrane and find that Syt1 binds with ~6 kB T in EGTA, ~10 kB T in Mg2+ and ~18 kB T in Ca2+ . Molecular rearrangements measured during confinement are more prevalent in Ca2+ and Mg2+ and suggest that Syt1 initially binds through C2B, then reorients the C2 domains into the preferred binding configuration. These results provide energetic and mechanistic details of the Syt1 Ca2+ -activation process in synaptic transmission.
publishDate 2018
dc.date.none.fl_str_mv 2018-04
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/11336/160427
Gruget, Clémence; Coleman, Jeff; Bello, Oscar Daniel; Krishnakumar, Shyam S.; Perez, Eric; et al.; Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+; Elsevier Science; FEBS Letters; 592; 9; 4-2018; 1497-1506
0014-5793
CONICET Digital
CONICET
url http://hdl.handle.net/11336/160427
identifier_str_mv Gruget, Clémence; Coleman, Jeff; Bello, Oscar Daniel; Krishnakumar, Shyam S.; Perez, Eric; et al.; Rearrangements under confinement lead to increased binding energy of Synaptotagmin-1 with anionic membranes in Mg2+ and Ca2+; Elsevier Science; FEBS Letters; 592; 9; 4-2018; 1497-1506
0014-5793
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://doi.wiley.com/10.1002/1873-3468.13040
info:eu-repo/semantics/altIdentifier/doi/10.1002/1873-3468.13040
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 Elsevier Science
publisher.none.fl_str_mv Elsevier 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
_version_ 1842269056177012736
score 13.13397

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