Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission

Dynamin 1 (Dyn1) GTPase, a principal driver of membrane fission during synaptic endocytosis, self-assembles into short mechanoactive helices cleaving the necks of endocytic vesicles. While structural information about Dyn1 helix is abundant, little is known about the nanoscale dynamics of the helica...

Descripción completa

Detalles Bibliográficos
Autores: Zhang, Yuliang, Lillo, Javier Vera, Mohamed Abdelrasoul, Mahmoud Shaaban, Wang, Yaqing, Arrasate, Pedro, Frolov, Vadim A., Noy, Aleksandr
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/388553
Acceso en línea:http://hdl.handle.net/10261/388553
https://api.elsevier.com/content/abstract/scopus_id/85211058585
Access Level:acceso abierto
Palabra clave:Dynamin
High-speed atomic force microscopy
Membrane fission
Membrane remodeling
id ES_2f3cfa7bcc9b93a3941cdb0447658f3f
oai_identifier_str oai:digital.csic.es:10261/388553
network_acronym_str ES
network_name_str España
repository_id_str
spelling Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fissionZhang, YuliangLillo, Javier VeraMohamed Abdelrasoul, Mahmoud ShaabanWang, YaqingArrasate, PedroFrolov, Vadim A.Noy, AleksandrDynaminHigh-speed atomic force microscopyMembrane fissionMembrane remodelingDynamin 1 (Dyn1) GTPase, a principal driver of membrane fission during synaptic endocytosis, self-assembles into short mechanoactive helices cleaving the necks of endocytic vesicles. While structural information about Dyn1 helix is abundant, little is known about the nanoscale dynamics of the helical scaffolding at the moment of fission, complicating mechanistic understanding of Dyn1 action. To address the role of the helix dynamics in fission, we used High-Speed Atomic Force Microscopy (HS-AFM) and fluorescence microscopy to track and compare the spatiotemporal characteristics of the helices formed by wild-type Dyn1 and its K44A mutant impaired in GTP hydrolysis on minimal lipid membrane templates. In the absence of nucleotide, membrane-bound WTDyn1 and K44ADyn1 self-assembled into tubular protein scaffolding of similar diameter encaging the lipid bilayer. In both cases, the GTP addition caused scaffold constriction coupled with formation of 20 to 30 nm nanogaps in the protein coverage. While both proteins reached scaffold diameters characteristic for membrane superconstriction causing fission, the fission was detected only with WTDyn1. We associated the fission activity with the dynamic evolution of the nanogaps: K44ADyn1 gaps were static, while WTDyn1 gaps actively evolved via repetitive nonaxisymmetric constriction-bending deformations caused by localized GTP hydrolysis. Modeling of the deformations implicated filament twist as an additional deformation mode which combines with superconstriction to facilitate membrane fission. Our results thus show that the dynamics of the Dyn1 helical scaffold goes beyond radial constriction and involves nonaxisymmetric deformations, where filament twist emerges as a critical driver of membrane fission.Research reported in this publication was supported by the National Institute of General Medicine of the NIH under award number R01GM121725. Work at the Molecular Foundry was supported by the Office of Science, Office of Basic Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. The experiments on the fluorescence microscopy analysis of the effects of K44A mutations were partially supported by the Basque Government grant IT1625-22.Peer reviewedNational Academy of Sciences (U.S.)National Institutes of Health (US)Department of Energy (US)Eusko JaurlaritzaZhang, Yuliang [0000-0002-9413-0900]Frolov, Vadim A. [0000-0002-0653-5669]Noy, Aleksandr [0000-0003-4924-2652]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/388553https://api.elsevier.com/content/abstract/scopus_id/85211058585reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésNoy, Aleksandr; Mohamed, Mahmoud Shaaban; Wang, Yaqing; Zhang, Yuliang; Frolov, Vadim A.; Vera, Javier; 2024; Data from: Nanoscale twisting dynamics of Dynamin1 helices reveals GTP-driven reassembly coupled to membrane fission [Dataset]; Figshare; https://doi.org/10.6084/m9.figshare.24759666.v1http://dx.doi.org/10.1073/pnas.2321514121Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3885532026-05-22T06:33:51Z
dc.title.none.fl_str_mv Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
title Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
spellingShingle Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
Zhang, Yuliang
Dynamin
High-speed atomic force microscopy
Membrane fission
Membrane remodeling
title_short Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
title_full Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
title_fullStr Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
title_full_unstemmed Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
title_sort Nanoscale dynamics of Dynamin 1 helices reveals squeeze-twist deformation mode critical for membrane fission
dc.creator.none.fl_str_mv Zhang, Yuliang
Lillo, Javier Vera
Mohamed Abdelrasoul, Mahmoud Shaaban
Wang, Yaqing
Arrasate, Pedro
Frolov, Vadim A.
Noy, Aleksandr
author Zhang, Yuliang
author_facet Zhang, Yuliang
Lillo, Javier Vera
Mohamed Abdelrasoul, Mahmoud Shaaban
Wang, Yaqing
Arrasate, Pedro
Frolov, Vadim A.
Noy, Aleksandr
author_role author
author2 Lillo, Javier Vera
Mohamed Abdelrasoul, Mahmoud Shaaban
Wang, Yaqing
Arrasate, Pedro
Frolov, Vadim A.
Noy, Aleksandr
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Institutes of Health (US)
Department of Energy (US)
Eusko Jaurlaritza
Zhang, Yuliang [0000-0002-9413-0900]
Frolov, Vadim A. [0000-0002-0653-5669]
Noy, Aleksandr [0000-0003-4924-2652]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Dynamin
High-speed atomic force microscopy
Membrane fission
Membrane remodeling
topic Dynamin
High-speed atomic force microscopy
Membrane fission
Membrane remodeling
description Dynamin 1 (Dyn1) GTPase, a principal driver of membrane fission during synaptic endocytosis, self-assembles into short mechanoactive helices cleaving the necks of endocytic vesicles. While structural information about Dyn1 helix is abundant, little is known about the nanoscale dynamics of the helical scaffolding at the moment of fission, complicating mechanistic understanding of Dyn1 action. To address the role of the helix dynamics in fission, we used High-Speed Atomic Force Microscopy (HS-AFM) and fluorescence microscopy to track and compare the spatiotemporal characteristics of the helices formed by wild-type Dyn1 and its K44A mutant impaired in GTP hydrolysis on minimal lipid membrane templates. In the absence of nucleotide, membrane-bound WTDyn1 and K44ADyn1 self-assembled into tubular protein scaffolding of similar diameter encaging the lipid bilayer. In both cases, the GTP addition caused scaffold constriction coupled with formation of 20 to 30 nm nanogaps in the protein coverage. While both proteins reached scaffold diameters characteristic for membrane superconstriction causing fission, the fission was detected only with WTDyn1. We associated the fission activity with the dynamic evolution of the nanogaps: K44ADyn1 gaps were static, while WTDyn1 gaps actively evolved via repetitive nonaxisymmetric constriction-bending deformations caused by localized GTP hydrolysis. Modeling of the deformations implicated filament twist as an additional deformation mode which combines with superconstriction to facilitate membrane fission. Our results thus show that the dynamics of the Dyn1 helical scaffold goes beyond radial constriction and involves nonaxisymmetric deformations, where filament twist emerges as a critical driver of membrane fission.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/388553
https://api.elsevier.com/content/abstract/scopus_id/85211058585
url http://hdl.handle.net/10261/388553
https://api.elsevier.com/content/abstract/scopus_id/85211058585
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Noy, Aleksandr; Mohamed, Mahmoud Shaaban; Wang, Yaqing; Zhang, Yuliang; Frolov, Vadim A.; Vera, Javier; 2024; Data from: Nanoscale twisting dynamics of Dynamin1 helices reveals GTP-driven reassembly coupled to membrane fission [Dataset]; Figshare; https://doi.org/10.6084/m9.figshare.24759666.v1
http://dx.doi.org/10.1073/pnas.2321514121
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences (U.S.)
publisher.none.fl_str_mv National Academy of Sciences (U.S.)
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869405464599461888
score 15.811543

Similares en LA Referencia