Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost

In oviparous marine fishes, the hyperosmotic induction of sperm motility in seawater (SW) is well established, however, the potential function of ion channels in the maintenance of post activated spermatozoon swimming performance remains largely unknown. Here, we investigated the influence of ion ch...

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Detalhes bibliográficos
Autores: Castro Arnau, Júlia, Chauvigné, François, Cerdà, Joan
Formato: artículo
Fecha de publicación:2022
País:España
Recursos:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
Repositorio:IRTA Pubpro. Open Digital Archive
OAI Identifier:oai:repositori.irta.cat:20.500.12327/1957
Acesso em linha:http://hdl.handle.net/20.500.12327/1957
https://doi.org/10.3390/ijms232012113
Access Level:acceso abierto
Palavra-chave:637
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spelling Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine TeleostCastro Arnau, JúliaChauvigné, FrançoisCerdà, Joan637In oviparous marine fishes, the hyperosmotic induction of sperm motility in seawater (SW) is well established, however, the potential function of ion channels in the maintenance of post activated spermatozoon swimming performance remains largely unknown. Here, we investigated the influence of ion channels on the spermatozoon swimming parameters using the gilthead seabream (Sparus aurata) as a model for modern marine teleosts. Our data show that the SW-induced activation of seabream sperm motility requires three concomitant processes, the hyperosmotic shock, an ion-flux independent increase of the intracellular concentration of Ca2+ ([Ca2+]i), but not of [K+]i or [Na+]i, and the alkalization of the cytosol. The combination of all three processes is obligatory to trigger flagellar beating. However, the time-course monitoring of sperm motion kinetics and changes in the [Ca2+]i, [K+]i and [Na+]i in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca2+ and K+. A meta-analysis of a seabream sperm transcriptome uncovered the expression of multiple ion channels, some of which were immunolocalized in the head and/or tail of the spermatozoon. Selective pharmacological inhibition of these ion channel families impaired the long-term motility, progressivity, and velocity of SW-activated spermatozoa. The data further revealed that some antagonists of K+-selective or Ca2+-selective channels, as well as of stretch-activated and mechanosensitive channels, altered the trajectory of spermatozoa, suggesting that these ion channels are likely involved in the control of the swimming pattern of the post activated spermatozoon. These combined findings provide new insight into the signaling pathways regulating spermatozoon activation and swimming performance in marine fishes.info:eu-repo/semantics/publishedVersionMDPIProducció AnimalAqüicultura202220222022info:eu-repo/semantics/article25application/pdfhttp://hdl.handle.net/20.500.12327/1957https://doi.org/10.3390/ijms232012113reponame:IRTA Pubpro. Open Digital Archiveinstname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)InglésInternational Journal of Molecular SciencesMINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORINAttribution 4.0 Internationalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.irta.cat:20.500.12327/19572026-06-16T08:51:17Z
dc.title.none.fl_str_mv Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
title Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
spellingShingle Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
Castro Arnau, Júlia
637
title_short Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
title_full Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
title_fullStr Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
title_full_unstemmed Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
title_sort Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost
dc.creator.none.fl_str_mv Castro Arnau, Júlia
Chauvigné, François
Cerdà, Joan
author Castro Arnau, Júlia
author_facet Castro Arnau, Júlia
Chauvigné, François
Cerdà, Joan
author_role author
author2 Chauvigné, François
Cerdà, Joan
author2_role author
author
dc.contributor.none.fl_str_mv Producció Animal
Aqüicultura
dc.subject.none.fl_str_mv 637
topic 637
description In oviparous marine fishes, the hyperosmotic induction of sperm motility in seawater (SW) is well established, however, the potential function of ion channels in the maintenance of post activated spermatozoon swimming performance remains largely unknown. Here, we investigated the influence of ion channels on the spermatozoon swimming parameters using the gilthead seabream (Sparus aurata) as a model for modern marine teleosts. Our data show that the SW-induced activation of seabream sperm motility requires three concomitant processes, the hyperosmotic shock, an ion-flux independent increase of the intracellular concentration of Ca2+ ([Ca2+]i), but not of [K+]i or [Na+]i, and the alkalization of the cytosol. The combination of all three processes is obligatory to trigger flagellar beating. However, the time-course monitoring of sperm motion kinetics and changes in the [Ca2+]i, [K+]i and [Na+]i in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca2+ and K+. A meta-analysis of a seabream sperm transcriptome uncovered the expression of multiple ion channels, some of which were immunolocalized in the head and/or tail of the spermatozoon. Selective pharmacological inhibition of these ion channel families impaired the long-term motility, progressivity, and velocity of SW-activated spermatozoa. The data further revealed that some antagonists of K+-selective or Ca2+-selective channels, as well as of stretch-activated and mechanosensitive channels, altered the trajectory of spermatozoa, suggesting that these ion channels are likely involved in the control of the swimming pattern of the post activated spermatozoon. These combined findings provide new insight into the signaling pathways regulating spermatozoon activation and swimming performance in marine fishes.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12327/1957
https://doi.org/10.3390/ijms232012113
url http://hdl.handle.net/20.500.12327/1957
https://doi.org/10.3390/ijms232012113
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv International Journal of Molecular Sciences
MINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORIN
dc.rights.none.fl_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 25
application/pdf
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
dc.source.none.fl_str_mv reponame:IRTA Pubpro. Open Digital Archive
instname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
instname_str Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
reponame_str IRTA Pubpro. Open Digital Archive
collection IRTA Pubpro. Open Digital Archive
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,301629

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