Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa

22 pages, 10 figures, supplementary material https://doi.org/10.1007/s00018-024-05341-w.-- Data availability: Data from this study, including raw data tables, alignments, and uncropped gels and blots, are available in the Supplementary material

Detalles Bibliográficos
Autores: Castro-Arnau, Júlia, Chauvigné, François, Toft-Bertelsen, Trine L., Finn, Roderick N., MacAulay, Nanna, Cerdà, Joan
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:10261/364665
Acceso en línea:http://hdl.handle.net/10261/364665
Access Level:acceso abierto
Palabra clave:Fish
Sperm
Aquaporin
Regulatory volume increase
Ion channel
Motility
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
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spelling Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoaCastro-Arnau, JúliaChauvigné, FrançoisToft-Bertelsen, Trine L.Finn, Roderick N.MacAulay, NannaCerdà, JoanFishSpermAquaporinRegulatory volume increaseIon channelMotilityhttp://metadata.un.org/sdg/14Conserve and sustainably use the oceans, seas and marine resources for sustainable development22 pages, 10 figures, supplementary material https://doi.org/10.1007/s00018-024-05341-w.-- Data availability: Data from this study, including raw data tables, alignments, and uncropped gels and blots, are available in the Supplementary materialVolume regulation is essential for cell homeostasis and physiological function. Amongst the sensory molecules that have been associated with volume regulation is the transient receptor potential vanilloid 4 (TRPV4), which is a non-selective cation channel that in conjunction with aquaporins, typically controls regulatory volume decrease (RVD). Here we show that the interaction between orthologous AQP4 (Aqp4a) and TRPV4 (Trpv4) is important for regulatory volume increase (RVI) in post-activated marine fish spermatozoa under high osmotic stress. Based upon electrophysiological, volumetric, and in vivo and ex vivo functional experiments using the pharmacological and immunological inhibition of Aqp4a and Trpv4 our model suggests that upon ejaculation and exposure to the hypertonic seawater, spermatozoon shrinkage is initially mediated by water efflux through Aqp1aa in the flagellar tail. The shrinkage results in an increase in intracellular Ca2+ concentration, and the activation of sperm motility and a Na+/K+/2Cl− (NKCC1) cotransporter. The activity of NKCC1 is required for the initiation of cell swelling, which secondarily activates the Aqp4a-Trpv4 complex to facilitate the influx of water via Aqp4a-M43 and Ca2+ via Trpv4 and L-type channels for the mediation of RVI. The inhibitory experiments show that blocking of each of these events prevents either shrinkage or RVI. Our data thus reveal that post-activated marine fish spermatozoa are capable of initiating RVI under a high hypertonic stress, which is essential for the maintenance of sperm motilityOpen Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This work was supported by the Spanish Ministry of Science and Innovation (MCIN/AEI/MCIN/AEI/10.13039/501100011033) and FEDER “A way of making Europe”, European Union, Grant no. AGL2016-76802-R (to J.C.), and the Catalan Government Grant 2021 SGR 00068 (to J.C). J.C.-A. was supported by a predoctoral (BES-2017-080778) contract from Spanish MCIN. This work also acknowledges the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S) funded by AEI 10.13039/501100011033Peer reviewedSpringerConsejo Superior de Investigaciones Científicas (España)Agencia Estatal de Investigación (España)European CommissionMinisterio de Ciencia e Innovación (España)Ministerio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/364665reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO//76802https://doi.org/10.1007/s00018-024-05341-wSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3646652026-05-22T06:33:51Z
dc.title.none.fl_str_mv Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
title Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
spellingShingle Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
Castro-Arnau, Júlia
Fish
Sperm
Aquaporin
Regulatory volume increase
Ion channel
Motility
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
title_short Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
title_full Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
title_fullStr Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
title_full_unstemmed Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
title_sort Aqp4a and Trpv4 mediate regulatory cell volume increase for swimming maintenance of marine fish spermatozoa
dc.creator.none.fl_str_mv Castro-Arnau, Júlia
Chauvigné, François
Toft-Bertelsen, Trine L.
Finn, Roderick N.
MacAulay, Nanna
Cerdà, Joan
author Castro-Arnau, Júlia
author_facet Castro-Arnau, Júlia
Chauvigné, François
Toft-Bertelsen, Trine L.
Finn, Roderick N.
MacAulay, Nanna
Cerdà, Joan
author_role author
author2 Chauvigné, François
Toft-Bertelsen, Trine L.
Finn, Roderick N.
MacAulay, Nanna
Cerdà, Joan
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Consejo Superior de Investigaciones Científicas (España)
Agencia Estatal de Investigación (España)
European Commission
Ministerio de Ciencia e Innovación (España)
Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Fish
Sperm
Aquaporin
Regulatory volume increase
Ion channel
Motility
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
topic Fish
Sperm
Aquaporin
Regulatory volume increase
Ion channel
Motility
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
description 22 pages, 10 figures, supplementary material https://doi.org/10.1007/s00018-024-05341-w.-- Data availability: Data from this study, including raw data tables, alignments, and uncropped gels and blots, are available in the Supplementary material
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
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/10261/364665
url http://hdl.handle.net/10261/364665
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO//76802
https://doi.org/10.1007/s00018-024-05341-w
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
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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score 15,812429

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