A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality

Autores
Ricardi, Martiniano María; Wallmeroth, Niklas; Cermesoni, Cecilia; Mehlhorn, Dietmar Gerald; Richter, Sandra; Zhang, Lei; Mittendorf, Josephine; Godehardt, Ingeborg; Berendzen, Kenneth Wayne; von Roepenack Lahaye, Edda; Stierhof, York Dieter; Lipka, Volker; Jürgens, Gerd; Grefen, Christopher
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The final step in secretion is membrane fusion facilitated by SNARE proteins that reside in opposite membranes. The formation of a trans-SNARE complex between one R and three Q coiled-coiled SNARE domains drives the final approach of the membranes providing the mechanical energy for fusion. Biological control of this mechanism is exerted by additional domains within some SNAREs. For example, the N-terminal Longin domain (LD) of R-SNAREs (also called Vesicle-associated membrane proteins, VAMPs) can fold back onto the SNARE domain blocking interaction with other cognate SNAREs. The LD may also determine the subcellular localization via interaction with other trafficking-related proteins. Here, we provide cell-biological and genetic evidence that phosphorylation of the Tyrosine57 residue regulates the functionality of VAMP721. We found that an aspartate mutation mimics phosphorylation, leading to protein instability and subsequent degradation in lytic vacuoles. The mutant SNARE also fails to rescue the defects of vamp721vamp722 loss-of-function lines in spite of its wildtype-like localization within the secretory pathway and the ability to interact with cognate SNARE partners. Most importantly, it imposes a dominant negative phenotype interfering with root growth, normal secretion and cytokinesis in wildtype plants generating large aggregates that mainly contain secretory vesicles. Non-phosphorylatable VAMP721Y57F needs higher gene dosage to rescue double mutants in comparison to native VAMP721 underpinning that phosphorylation modulates SNARE function. We propose a model where short-lived phosphorylation of Y57 serves as a regulatory step to control VAMP721 activity, favoring its open state and interaction with cognate partners to ultimately drive membrane fusion.
Fil: Ricardi, Martiniano María. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Ruhr Universität Bochum; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; Argentina
Fil: Wallmeroth, Niklas. Eberhard Karls Universität Tübingen; Alemania
Fil: Cermesoni, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; Argentina
Fil: Mehlhorn, Dietmar Gerald. Ruhr Universität Bochum; Alemania
Fil: Richter, Sandra. Eberhard Karls Universität Tübingen; Alemania
Fil: Zhang, Lei. Ruhr Universität Bochum; Alemania
Fil: Mittendorf, Josephine. Universität Göttingen; Alemania
Fil: Godehardt, Ingeborg. Ruhr Universität Bochum; Alemania
Fil: Berendzen, Kenneth Wayne. Eberhard Karls Universität Tübingen; Alemania
Fil: von Roepenack Lahaye, Edda. Eberhard Karls Universität Tübingen; Alemania
Fil: Stierhof, York Dieter. Eberhard Karls Universität Tübingen; Alemania
Fil: Lipka, Volker. Universität Göttingen; Alemania
Fil: Jürgens, Gerd. Eberhard Karls Universität Tübingen; Alemania
Fil: Grefen, Christopher. Ruhr Universität Bochum; Alemania
Materia
CYTOKINESIS
EXOCYTOSIS
MEMBRANE
PHOSPHORYLATION
SECRETORY PATHWAY
SNARES
VESICLE FUSION
VESICLE TRAFFICKING
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/228566
Acceder
id CONICETDig_24d9ccef64b99d5e1818ffe22b3fdc11
oai_identifier_str oai:ri.conicet.gov.ar:11336/228566
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionalityRicardi, Martiniano MaríaWallmeroth, NiklasCermesoni, CeciliaMehlhorn, Dietmar GeraldRichter, SandraZhang, LeiMittendorf, JosephineGodehardt, IngeborgBerendzen, Kenneth Waynevon Roepenack Lahaye, EddaStierhof, York DieterLipka, VolkerJürgens, GerdGrefen, ChristopherCYTOKINESISEXOCYTOSISMEMBRANEPHOSPHORYLATIONSECRETORY PATHWAYSNARESVESICLE FUSIONVESICLE TRAFFICKINGhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The final step in secretion is membrane fusion facilitated by SNARE proteins that reside in opposite membranes. The formation of a trans-SNARE complex between one R and three Q coiled-coiled SNARE domains drives the final approach of the membranes providing the mechanical energy for fusion. Biological control of this mechanism is exerted by additional domains within some SNAREs. For example, the N-terminal Longin domain (LD) of R-SNAREs (also called Vesicle-associated membrane proteins, VAMPs) can fold back onto the SNARE domain blocking interaction with other cognate SNAREs. The LD may also determine the subcellular localization via interaction with other trafficking-related proteins. Here, we provide cell-biological and genetic evidence that phosphorylation of the Tyrosine57 residue regulates the functionality of VAMP721. We found that an aspartate mutation mimics phosphorylation, leading to protein instability and subsequent degradation in lytic vacuoles. The mutant SNARE also fails to rescue the defects of vamp721vamp722 loss-of-function lines in spite of its wildtype-like localization within the secretory pathway and the ability to interact with cognate SNARE partners. Most importantly, it imposes a dominant negative phenotype interfering with root growth, normal secretion and cytokinesis in wildtype plants generating large aggregates that mainly contain secretory vesicles. Non-phosphorylatable VAMP721Y57F needs higher gene dosage to rescue double mutants in comparison to native VAMP721 underpinning that phosphorylation modulates SNARE function. We propose a model where short-lived phosphorylation of Y57 serves as a regulatory step to control VAMP721 activity, favoring its open state and interaction with cognate partners to ultimately drive membrane fusion.Fil: Ricardi, Martiniano María. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Ruhr Universität Bochum; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; ArgentinaFil: Wallmeroth, Niklas. Eberhard Karls Universität Tübingen; AlemaniaFil: Cermesoni, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; ArgentinaFil: Mehlhorn, Dietmar Gerald. Ruhr Universität Bochum; AlemaniaFil: Richter, Sandra. Eberhard Karls Universität Tübingen; AlemaniaFil: Zhang, Lei. Ruhr Universität Bochum; AlemaniaFil: Mittendorf, Josephine. Universität Göttingen; AlemaniaFil: Godehardt, Ingeborg. Ruhr Universität Bochum; AlemaniaFil: Berendzen, Kenneth Wayne. Eberhard Karls Universität Tübingen; AlemaniaFil: von Roepenack Lahaye, Edda. Eberhard Karls Universität Tübingen; AlemaniaFil: Stierhof, York Dieter. Eberhard Karls Universität Tübingen; AlemaniaFil: Lipka, Volker. Universität Göttingen; AlemaniaFil: Jürgens, Gerd. Eberhard Karls Universität Tübingen; AlemaniaFil: Grefen, Christopher. Ruhr Universität Bochum; AlemaniaWiley Blackwell Publishing, Inc2023-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/228566Ricardi, Martiniano María; Wallmeroth, Niklas; Cermesoni, Cecilia; Mehlhorn, Dietmar Gerald; Richter, Sandra; et al.; A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality; Wiley Blackwell Publishing, Inc; Plant Journal; 116; 6; 12-2023; 1633-16510960-7412CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/tpj.16451info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1111/tpj.16451info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:24:37Zoai:ri.conicet.gov.ar:11336/228566instacron: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:34982025-09-10 13:24:38.012CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
title A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
spellingShingle A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
Ricardi, Martiniano María
CYTOKINESIS
EXOCYTOSIS
MEMBRANE
PHOSPHORYLATION
SECRETORY PATHWAY
SNARES
VESICLE FUSION
VESICLE TRAFFICKING
title_short A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
title_full A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
title_fullStr A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
title_full_unstemmed A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
title_sort A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality
dc.creator.none.fl_str_mv Ricardi, Martiniano María
Wallmeroth, Niklas
Cermesoni, Cecilia
Mehlhorn, Dietmar Gerald
Richter, Sandra
Zhang, Lei
Mittendorf, Josephine
Godehardt, Ingeborg
Berendzen, Kenneth Wayne
von Roepenack Lahaye, Edda
Stierhof, York Dieter
Lipka, Volker
Jürgens, Gerd
Grefen, Christopher
author Ricardi, Martiniano María
author_facet Ricardi, Martiniano María
Wallmeroth, Niklas
Cermesoni, Cecilia
Mehlhorn, Dietmar Gerald
Richter, Sandra
Zhang, Lei
Mittendorf, Josephine
Godehardt, Ingeborg
Berendzen, Kenneth Wayne
von Roepenack Lahaye, Edda
Stierhof, York Dieter
Lipka, Volker
Jürgens, Gerd
Grefen, Christopher
author_role author
author2 Wallmeroth, Niklas
Cermesoni, Cecilia
Mehlhorn, Dietmar Gerald
Richter, Sandra
Zhang, Lei
Mittendorf, Josephine
Godehardt, Ingeborg
Berendzen, Kenneth Wayne
von Roepenack Lahaye, Edda
Stierhof, York Dieter
Lipka, Volker
Jürgens, Gerd
Grefen, Christopher
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CYTOKINESIS
EXOCYTOSIS
MEMBRANE
PHOSPHORYLATION
SECRETORY PATHWAY
SNARES
VESICLE FUSION
VESICLE TRAFFICKING
topic CYTOKINESIS
EXOCYTOSIS
MEMBRANE
PHOSPHORYLATION
SECRETORY PATHWAY
SNARES
VESICLE FUSION
VESICLE TRAFFICKING
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The final step in secretion is membrane fusion facilitated by SNARE proteins that reside in opposite membranes. The formation of a trans-SNARE complex between one R and three Q coiled-coiled SNARE domains drives the final approach of the membranes providing the mechanical energy for fusion. Biological control of this mechanism is exerted by additional domains within some SNAREs. For example, the N-terminal Longin domain (LD) of R-SNAREs (also called Vesicle-associated membrane proteins, VAMPs) can fold back onto the SNARE domain blocking interaction with other cognate SNAREs. The LD may also determine the subcellular localization via interaction with other trafficking-related proteins. Here, we provide cell-biological and genetic evidence that phosphorylation of the Tyrosine57 residue regulates the functionality of VAMP721. We found that an aspartate mutation mimics phosphorylation, leading to protein instability and subsequent degradation in lytic vacuoles. The mutant SNARE also fails to rescue the defects of vamp721vamp722 loss-of-function lines in spite of its wildtype-like localization within the secretory pathway and the ability to interact with cognate SNARE partners. Most importantly, it imposes a dominant negative phenotype interfering with root growth, normal secretion and cytokinesis in wildtype plants generating large aggregates that mainly contain secretory vesicles. Non-phosphorylatable VAMP721Y57F needs higher gene dosage to rescue double mutants in comparison to native VAMP721 underpinning that phosphorylation modulates SNARE function. We propose a model where short-lived phosphorylation of Y57 serves as a regulatory step to control VAMP721 activity, favoring its open state and interaction with cognate partners to ultimately drive membrane fusion.
Fil: Ricardi, Martiniano María. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Ruhr Universität Bochum; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; Argentina
Fil: Wallmeroth, Niklas. Eberhard Karls Universität Tübingen; Alemania
Fil: Cermesoni, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular. Laboratorio de Fisiología y Biología Molecular; Argentina
Fil: Mehlhorn, Dietmar Gerald. Ruhr Universität Bochum; Alemania
Fil: Richter, Sandra. Eberhard Karls Universität Tübingen; Alemania
Fil: Zhang, Lei. Ruhr Universität Bochum; Alemania
Fil: Mittendorf, Josephine. Universität Göttingen; Alemania
Fil: Godehardt, Ingeborg. Ruhr Universität Bochum; Alemania
Fil: Berendzen, Kenneth Wayne. Eberhard Karls Universität Tübingen; Alemania
Fil: von Roepenack Lahaye, Edda. Eberhard Karls Universität Tübingen; Alemania
Fil: Stierhof, York Dieter. Eberhard Karls Universität Tübingen; Alemania
Fil: Lipka, Volker. Universität Göttingen; Alemania
Fil: Jürgens, Gerd. Eberhard Karls Universität Tübingen; Alemania
Fil: Grefen, Christopher. Ruhr Universität Bochum; Alemania
description The final step in secretion is membrane fusion facilitated by SNARE proteins that reside in opposite membranes. The formation of a trans-SNARE complex between one R and three Q coiled-coiled SNARE domains drives the final approach of the membranes providing the mechanical energy for fusion. Biological control of this mechanism is exerted by additional domains within some SNAREs. For example, the N-terminal Longin domain (LD) of R-SNAREs (also called Vesicle-associated membrane proteins, VAMPs) can fold back onto the SNARE domain blocking interaction with other cognate SNAREs. The LD may also determine the subcellular localization via interaction with other trafficking-related proteins. Here, we provide cell-biological and genetic evidence that phosphorylation of the Tyrosine57 residue regulates the functionality of VAMP721. We found that an aspartate mutation mimics phosphorylation, leading to protein instability and subsequent degradation in lytic vacuoles. The mutant SNARE also fails to rescue the defects of vamp721vamp722 loss-of-function lines in spite of its wildtype-like localization within the secretory pathway and the ability to interact with cognate SNARE partners. Most importantly, it imposes a dominant negative phenotype interfering with root growth, normal secretion and cytokinesis in wildtype plants generating large aggregates that mainly contain secretory vesicles. Non-phosphorylatable VAMP721Y57F needs higher gene dosage to rescue double mutants in comparison to native VAMP721 underpinning that phosphorylation modulates SNARE function. We propose a model where short-lived phosphorylation of Y57 serves as a regulatory step to control VAMP721 activity, favoring its open state and interaction with cognate partners to ultimately drive membrane fusion.
publishDate 2023
dc.date.none.fl_str_mv 2023-12
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/11336/228566
Ricardi, Martiniano María; Wallmeroth, Niklas; Cermesoni, Cecilia; Mehlhorn, Dietmar Gerald; Richter, Sandra; et al.; A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality; Wiley Blackwell Publishing, Inc; Plant Journal; 116; 6; 12-2023; 1633-1651
0960-7412
CONICET Digital
CONICET
url http://hdl.handle.net/11336/228566
identifier_str_mv Ricardi, Martiniano María; Wallmeroth, Niklas; Cermesoni, Cecilia; Mehlhorn, Dietmar Gerald; Richter, Sandra; et al.; A tyrosine phospho-switch within the Longin domain of VAMP721 modulates SNARE functionality; Wiley Blackwell Publishing, Inc; Plant Journal; 116; 6; 12-2023; 1633-1651
0960-7412
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1111/tpj.16451
info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1111/tpj.16451
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
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 12.48226

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