Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles

17 p.-10 fig.

Detalhes bibliográficos
Autores: González-Jiménez, Patricia, Duarte, Sofia, Martínez, Alma E., Navarro-Carrasco, Elena, Lalioti, Vasiliky S., Pajares, María Ángeles, Pérez-Sala, Dolores
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:dnet:digitalcsic_::aa801169b601424e61e89beb09ba55dd
Acesso em linha:http://hdl.handle.net/10261/310976
Access Level:acceso abierto
Palavra-chave:Protein lipoxidation
Electrophiles and oxidants
Vimentin-actin interplayIntermediate filaments
Actin stress fibers
Cysteine modification
Posttranslational modification
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network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
title Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
spellingShingle Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
González-Jiménez, Patricia
Protein lipoxidation
Electrophiles and oxidants
Vimentin-actin interplayIntermediate filaments
Actin stress fibers
Cysteine modification
Posttranslational modification
title_short Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
title_full Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
title_fullStr Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
title_full_unstemmed Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
title_sort Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophiles
dc.creator.none.fl_str_mv González-Jiménez, Patricia
Duarte, Sofia
Martínez, Alma E.
Navarro-Carrasco, Elena
Lalioti, Vasiliky S.
Pajares, María Ángeles
Pérez-Sala, Dolores
author González-Jiménez, Patricia
author_facet González-Jiménez, Patricia
Duarte, Sofia
Martínez, Alma E.
Navarro-Carrasco, Elena
Lalioti, Vasiliky S.
Pajares, María Ángeles
Pérez-Sala, Dolores
author_role author
author2 Duarte, Sofia
Martínez, Alma E.
Navarro-Carrasco, Elena
Lalioti, Vasiliky S.
Pajares, María Ángeles
Pérez-Sala, Dolores
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Instituto de Salud Carlos III
European Commission
González-Jiménez, Patricia [0000-0002-7588-2779]
Duarte, Sofia [0000-0001-5081-6989]
Martínez, Alma E. [0000-0002-6712-7079]
Navarro-Carrasco, Elena [0000-0002-1533-8210]
Lalioti, Vasiliky S. [0000-0002-4273-6126]
Pajares, María A. [0000-0002-4714-9051]
Pérez-Sala, Dolores [0000-0003-0600-665X]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Protein lipoxidation
Electrophiles and oxidants
Vimentin-actin interplayIntermediate filaments
Actin stress fibers
Cysteine modification
Posttranslational modification
topic Protein lipoxidation
Electrophiles and oxidants
Vimentin-actin interplayIntermediate filaments
Actin stress fibers
Cysteine modification
Posttranslational modification
description 17 p.-10 fig.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
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/10261/310976
url http://hdl.handle.net/10261/310976
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097624-B-I00
info:eu-repo/grantAgreement/EC/H2020/675132
https://doi.org/10.1016/j.redox.2023.102756
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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
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spelling Vimentin single cysteine residue acts as a tunable sensor for network organization and as a key for actin remodeling in response to oxidants and electrophilesGonzález-Jiménez, PatriciaDuarte, SofiaMartínez, Alma E.Navarro-Carrasco, ElenaLalioti, Vasiliky S.Pajares, María ÁngelesPérez-Sala, DoloresProtein lipoxidationElectrophiles and oxidantsVimentin-actin interplayIntermediate filamentsActin stress fibersCysteine modificationPosttranslational modification17 p.-10 fig.Cysteine residues can undergo multiple posttranslational modifications with diverse functional consequences, potentially behaving as tunable sensors. The intermediate filament protein vimentin has important implications in pathophysiology, including cancer progression, infection, and fibrosis, and maintains a close interplay with other cytoskeletal structures, such as actin filaments and microtubules. We previously showed that the single vimentin cysteine, C328, is a key target for oxidants and electrophiles. Here, we demonstrate that structurally diverse cysteine-reactive agents, including electrophilic mediators, oxidants and drug-related compounds, disrupt the vimentin network eliciting morphologically distinct reorganizations. As most of these agents display broad reactivity, we pinpointed the importance of C328 by confirming that local perturbations introduced through mutagenesis provoke structure-dependent vimentin rearrangements. Thus, GFP-vimentin wild type (wt) forms squiggles and short filaments in vimentin-deficient cells, the C328F, C328W, and C328H mutants generate diverse filamentous assemblies, and the C328A and C328D constructs fail to elongate yielding dots. Remarkably, vimentin C328H structures resemble the wt, but are strongly resistant to electrophile-elicited disruption. Therefore, the C328H mutant allows elucidating whether cysteine-dependent vimentin reorganization influences other cellular responses to reactive agents. Electrophiles such as 1,4-dinitro-1H-imidazole and 4-hydroxynonenal induce robust actin stress fibers in cells expressing vimentin wt. Strikingly, under these conditions, vimentin C328H expression blunts electrophile-elicited stress fiber formation, apparently acting upstream of RhoA. Analysis of additional vimentin C328 mutants shows that electrophile-sensitive and assembly-defective vimentin variants permit induction of stress fibers by reactive species, whereas electrophile-resistant filamentous vimentin structures prevent it. Together, our results suggest that vimentin acts as a break for actin stress fibers formation, which would be released by C328-aided disruption, thus allowing full actin remodeling in response to oxidants and electrophiles. These observations postulate C328 as a “sensor” transducing structurally diverse modifications into fine-tuned vimentin network rearrangements, and a gatekeeper for certain electrophiles in the interplay with actin.This work was supported by Grants RTI2018-097624-B-I00 and PID2021-126827OB-I00, funded by MCIN/AEI/10.13039/501100011033 and ERDF, “A way of making Europe”; RETIC Aradyal RD16/0006/0021 from ISCIII, cofunded by ERDF; European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie Grant agreement no. 675132 “Masstrplan”; PGJ is the recipient of a predoctoral contract PRE2019-088194, from MCIN/AEI/10.13039/501100011033 and ESF, “Investing in your future”, Spain. AEM is the recipient of a postdoctoral contract from the Juan de la Cierva Program, FJC2021-047028-I, funded by MCIN/AEI/10.13039/501100011033 and by European Union NextGenerationEU/PRTRPeer reviewedElsevierMinisterio de Ciencia e Innovación (España)Instituto de Salud Carlos IIIEuropean CommissionGonzález-Jiménez, Patricia [0000-0002-7588-2779]Duarte, Sofia [0000-0001-5081-6989]Martínez, Alma E. [0000-0002-6712-7079]Navarro-Carrasco, Elena [0000-0002-1533-8210]Lalioti, Vasiliky S. [0000-0002-4273-6126]Pajares, María A. [0000-0002-4714-9051]Pérez-Sala, Dolores [0000-0003-0600-665X]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/310976reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097624-B-I00info:eu-repo/grantAgreement/EC/H2020/675132https://doi.org/10.1016/j.redox.2023.102756Síinfo:eu-repo/semantics/openAccessoai:dnet:digitalcsic_::aa801169b601424e61e89beb09ba55dd2026-05-22T06:33:51Z
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