BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M

The activity of dynein is regulated by a number of adaptors that mediate its interaction with dynactin, effectively activating the motor complex while also connecting it to different cargos. The regulation of adaptors is consequently central to dynein physiology but remains largely unexplored. We no...

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Autores: Gallisà-Suñé, Núria, Sànchez-Fernàndez de Landa, Paula, Zimmermann, Fabian, Serna, Marina, Regué, Laura, Paz, Joel, Llorca, Óscar, Lüders, Jens, Roig, Joan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/335540
Acceso en línea:http://hdl.handle.net/10261/335540
Access Level:acceso abierto
Palabra clave:Centrosome
Dynein
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dc.title.none.fl_str_mv BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
title BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
spellingShingle BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
Gallisà-Suñé, Núria
Centrosome
Dynein
title_short BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
title_full BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
title_fullStr BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
title_full_unstemmed BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
title_sort BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and M
dc.creator.none.fl_str_mv Gallisà-Suñé, Núria
Sànchez-Fernàndez de Landa, Paula
Zimmermann, Fabian
Serna, Marina
Regué, Laura
Paz, Joel
Llorca, Óscar
Lüders, Jens
Roig, Joan
author Gallisà-Suñé, Núria
author_facet Gallisà-Suñé, Núria
Sànchez-Fernàndez de Landa, Paula
Zimmermann, Fabian
Serna, Marina
Regué, Laura
Paz, Joel
Llorca, Óscar
Lüders, Jens
Roig, Joan
author_role author
author2 Sànchez-Fernàndez de Landa, Paula
Zimmermann, Fabian
Serna, Marina
Regué, Laura
Paz, Joel
Llorca, Óscar
Lüders, Jens
Roig, Joan
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Comunidad de Madrid
Instituto de Salud Carlos III
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Centrosome
Dynein
topic Centrosome
Dynein
description The activity of dynein is regulated by a number of adaptors that mediate its interaction with dynactin, effectively activating the motor complex while also connecting it to different cargos. The regulation of adaptors is consequently central to dynein physiology but remains largely unexplored. We now describe that one of the best-known dynein adaptors, BICD2, is effectively activated through phosphorylation. In G2, phosphorylation of BICD2 by CDK1 promotes its interaction with PLK1. In turn, PLK1 phosphorylation of a single residue in the N-terminus of BICD2 results in a structural change that facilitates the interaction with dynein and dynactin, allowing the formation of active motor complexes. Moreover, modified BICD2 preferentially interacts with the nucleoporin RanBP2 once RanBP2 has been phosphorylated by CDK1. BICD2 phosphorylation is central for dynein recruitment to the nuclear envelope, centrosome tethering to the nucleus and centrosome separation in the G2 and M phases of the cell cycle. This work reveals adaptor activation through phosphorylation as crucial for the spatiotemporal regulation of dynein activity.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
2023
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/335540
url http://hdl.handle.net/10261/335540
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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instname:Consejo Superior de Investigaciones Científicas (CSIC)
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spelling BICD2 phosphorylation regulates dynein function and centrosome separation in G2 and MGallisà-Suñé, NúriaSànchez-Fernàndez de Landa, PaulaZimmermann, FabianSerna, MarinaRegué, LauraPaz, JoelLlorca, ÓscarLüders, JensRoig, JoanCentrosomeDyneinThe activity of dynein is regulated by a number of adaptors that mediate its interaction with dynactin, effectively activating the motor complex while also connecting it to different cargos. The regulation of adaptors is consequently central to dynein physiology but remains largely unexplored. We now describe that one of the best-known dynein adaptors, BICD2, is effectively activated through phosphorylation. In G2, phosphorylation of BICD2 by CDK1 promotes its interaction with PLK1. In turn, PLK1 phosphorylation of a single residue in the N-terminus of BICD2 results in a structural change that facilitates the interaction with dynein and dynactin, allowing the formation of active motor complexes. Moreover, modified BICD2 preferentially interacts with the nucleoporin RanBP2 once RanBP2 has been phosphorylated by CDK1. BICD2 phosphorylation is central for dynein recruitment to the nuclear envelope, centrosome tethering to the nucleus and centrosome separation in the G2 and M phases of the cell cycle. This work reveals adaptor activation through phosphorylation as crucial for the spatiotemporal regulation of dynein activity.J.R. and N.G.-S.work was funded by the Ministerio de Ciencia e Innovación (MICINN) and the Agencia Estatal de Investigación (AEI) from Spain (MCIN/ AEI /10.13039/501100011033/ FEDER “Una manera de hacer Europa”) through Plan Nacional de I + D grants BFU2014-58422-P, PGC2018-096307-B-I00 and PID2021-127045NB-I00 (to J.R.) and by network grant 2017 SGR 1089 (AGAUR, Generalitat de Catalunya). N.G.-S. was a recipient of FPI Fellowship BES-2015-072446 from MICINN. Work in the laboratory of J.L. was supported by grants BFU2015-69275-P (MINECO/FEDER), PGC2018-099562-B-I00 (MICINN), network grants 2017 SGR 1089 (AGAUR) and RED2018-102723-T (MICINN), and by intramural funds of IRB Barcelona, supported by CERCA (Generalitat de Catalunya). F.Z. was supported by a fellowship from the “la Caixa” Foundation (ID 100010434, fellowship code LCF/BQ/DI17/11620020) and the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no. 713673. J.P. was supported by a fellowship from MICINN (BES-2016-078003). O.L. and M.S. work was funded by the Agencia Estatal de Investigación (AEI/10.13039/501100011033), Ministerio de Ciencia e Innovación [PID2020-114429RB-I00] and by the Autonomous Region of Madrid, co-funded by the European Regional Development Fund (ERDF) [SAF2017-82632-P to O.L.]; Autonomous Region of Madrid and co-funded by the European Social Fund and the European Regional Development Fund [Y2018/BIO4747 and P2018/NMT4443 to O.L.]; CNIO is supported by the National Institute of Health Carlos III.Peer reviewedSpringer NatureMinisterio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)Ministerio de Ciencia, Innovación y Universidades (España)Comunidad de MadridInstituto de Salud Carlos IIIConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/335540reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO//BFU2014-58422-Pinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-096307-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-127045NB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2017-82632-PP2018/NMT4443/ec4Bio-CMhttp://dx.doi.org/10.1038/s41467-023-38116-1Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3355402026-05-22T06:33:51Z
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