A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa
The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular con...
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Online Access: | https://hdl.handle.net/11250/2992229 https://doi.org/10.1073/pnas.2019346118 |
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ftimr:oai:imr.brage.unit.no:11250/2992229 2023-05-15T15:32:28+02:00 A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa Chauvigné, Francois Ducat, Carla Ferré, Alba Hansen, Tom Johnny Carrascal, Montserrat Abián, Joaquín Finn, Roderick Nigel Cerdà, Joan 2021 application/pdf https://hdl.handle.net/11250/2992229 https://doi.org/10.1073/pnas.2019346118 eng eng Norges forskningsråd: 254872 Norges forskningsråd: 294768 Proceedings of the National Academy of Sciences of the United States of America. 2021, 118 (10), 1-12. urn:issn:0027-8424 https://hdl.handle.net/11250/2992229 https://doi.org/10.1073/pnas.2019346118 cristin:1931752 1-12 118 Proceedings of the National Academy of Sciences of the United States of America 10 Peer reviewed Journal article 2021 ftimr https://doi.org/10.1073/pnas.2019346118 2022-04-27T22:40:17Z The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate H2O2 efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish (Danio rerio) and the Atlantic salmon (Salmo salar), in which spermatozoa are activated in freshwater, an intracellular Ca2+-signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (Sparus aurata), in which spermatozoa activation occurs in seawater, a cross-talk between Ca2+- and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection. publishedVersion Article in Journal/Newspaper Atlantic salmon Salmo salar Institute for Marine Research: Brage IMR Proceedings of the National Academy of Sciences 118 10 |
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Open Polar |
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Institute for Marine Research: Brage IMR |
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language |
English |
description |
The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate H2O2 efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish (Danio rerio) and the Atlantic salmon (Salmo salar), in which spermatozoa are activated in freshwater, an intracellular Ca2+-signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (Sparus aurata), in which spermatozoa activation occurs in seawater, a cross-talk between Ca2+- and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection. publishedVersion |
format |
Article in Journal/Newspaper |
author |
Chauvigné, Francois Ducat, Carla Ferré, Alba Hansen, Tom Johnny Carrascal, Montserrat Abián, Joaquín Finn, Roderick Nigel Cerdà, Joan |
spellingShingle |
Chauvigné, Francois Ducat, Carla Ferré, Alba Hansen, Tom Johnny Carrascal, Montserrat Abián, Joaquín Finn, Roderick Nigel Cerdà, Joan A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
author_facet |
Chauvigné, Francois Ducat, Carla Ferré, Alba Hansen, Tom Johnny Carrascal, Montserrat Abián, Joaquín Finn, Roderick Nigel Cerdà, Joan |
author_sort |
Chauvigné, Francois |
title |
A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
title_short |
A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
title_full |
A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
title_fullStr |
A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
title_full_unstemmed |
A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
title_sort |
multiplier peroxiporin signal transduction pathway powers piscine spermatozoa |
publishDate |
2021 |
url |
https://hdl.handle.net/11250/2992229 https://doi.org/10.1073/pnas.2019346118 |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_source |
1-12 118 Proceedings of the National Academy of Sciences of the United States of America 10 |
op_relation |
Norges forskningsråd: 254872 Norges forskningsråd: 294768 Proceedings of the National Academy of Sciences of the United States of America. 2021, 118 (10), 1-12. urn:issn:0027-8424 https://hdl.handle.net/11250/2992229 https://doi.org/10.1073/pnas.2019346118 cristin:1931752 |
op_doi |
https://doi.org/10.1073/pnas.2019346118 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
118 |
container_issue |
10 |
_version_ |
1766362970274660352 |