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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MDPI AG
2022-10-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/20/12113 |
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| author | Júlia Castro-Arnau François Chauvigné Joan Cerdà |
| author_facet | Júlia Castro-Arnau François Chauvigné Joan Cerdà |
| author_sort | Júlia Castro-Arnau |
| collection | DOAJ |
| 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 (<i>Sparus aurata</i>) 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 Ca<sup>2+</sup> ([Ca<sup>2+</sup>]<sub>i</sub>), but not of [K<sup>+</sup>]<sub>i</sub> or [Na<sup>+</sup>]<sub>i</sub>, 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 [Ca<sup>2+</sup>]<sub>i</sub>, [K<sup>+</sup>]<sub>i</sub> and [Na<sup>+</sup>]<sub>i</sub> in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca<sup>2+</sup> and K<sup>+</sup>. 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<sup>+</sup>-selective or Ca<sup>2+</sup>-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. |
| first_indexed | 2024-03-09T20:06:28Z |
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| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T20:06:28Z |
| publishDate | 2022-10-01 |
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| spelling | doaj.art-19e53201c8314a03a951aee1aae710882023-11-24T00:28:33ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-10-0123201211310.3390/ijms232012113Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine TeleostJúlia Castro-Arnau0François Chauvigné1Joan Cerdà2Institute of Agrifood Research and Technology (IRTA)-Institute of Biotechnology and Biomedicine (IBB), Universitat Autònoma de Barcelona, 08193 Barcelona, SpainInstitute of Marine Sciences, Spanish National Research Council (CSIC), 08003 Barcelona, SpainInstitute of Agrifood Research and Technology (IRTA)-Institute of Biotechnology and Biomedicine (IBB), Universitat Autònoma de Barcelona, 08193 Barcelona, SpainIn 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 (<i>Sparus aurata</i>) 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 Ca<sup>2+</sup> ([Ca<sup>2+</sup>]<sub>i</sub>), but not of [K<sup>+</sup>]<sub>i</sub> or [Na<sup>+</sup>]<sub>i</sub>, 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 [Ca<sup>2+</sup>]<sub>i</sub>, [K<sup>+</sup>]<sub>i</sub> and [Na<sup>+</sup>]<sub>i</sub> in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca<sup>2+</sup> and K<sup>+</sup>. 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<sup>+</sup>-selective or Ca<sup>2+</sup>-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.https://www.mdpi.com/1422-0067/23/20/12113spermatozoaionspHactivationtranscriptomeion channels |
| spellingShingle | Júlia Castro-Arnau François Chauvigné Joan Cerdà Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost International Journal of Molecular Sciences spermatozoa ions pH activation transcriptome ion channels |
| title | 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_short | 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 |
| topic | spermatozoa ions pH activation transcriptome ion channels |
| url | https://www.mdpi.com/1422-0067/23/20/12113 |
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