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Molecular mechanisms of sperm motility are conserved in an early-branching metazoan

Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However,...

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Autores principales: Speer, Kelsey F., Allen-Waller, Luella, Novikov, Dana R., Barott, Katie L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8640785/
https://www.ncbi.nlm.nih.gov/pubmed/34810263
http://dx.doi.org/10.1073/pnas.2109993118
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author Speer, Kelsey F.
Allen-Waller, Luella
Novikov, Dana R.
Barott, Katie L.
author_facet Speer, Kelsey F.
Allen-Waller, Luella
Novikov, Dana R.
Barott, Katie L.
author_sort Speer, Kelsey F.
collection PubMed
description Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in early-branching metazoans has remained unexplored. Here, we found that elevating cytoplasmic pH induced a rapid burst of cAMP signaling and triggered the onset of motility in sperm from the reef-building coral Montipora capitata in a sAC-dependent manner. Expression of sAC in the mitochondrial-rich midpiece and flagellum of coral sperm support a dual role for this molecular pH sensor in regulating mitochondrial respiration and flagellar beating and thus motility. In addition, we found that additional members of the homologous signaling pathway described in echinoderms, both upstream and downstream of sAC, are expressed in coral sperm. These include the Na(+)/H(+) exchanger SLC9C1, protein kinase A, and the CatSper Ca(2+) channel conserved even in mammalian sperm. Indeed, the onset of motility corresponded with increased protein kinase A activity. Our discovery of this pathway in an early-branching metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize the need to better understand the role of pH-dependent signaling in the reproductive success of marine animals, particularly as climate change stressors continue to alter the physiology of corals and other marine invertebrates.
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spelling pubmed-86407852021-12-13 Molecular mechanisms of sperm motility are conserved in an early-branching metazoan Speer, Kelsey F. Allen-Waller, Luella Novikov, Dana R. Barott, Katie L. Proc Natl Acad Sci U S A Biological Sciences Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in early-branching metazoans has remained unexplored. Here, we found that elevating cytoplasmic pH induced a rapid burst of cAMP signaling and triggered the onset of motility in sperm from the reef-building coral Montipora capitata in a sAC-dependent manner. Expression of sAC in the mitochondrial-rich midpiece and flagellum of coral sperm support a dual role for this molecular pH sensor in regulating mitochondrial respiration and flagellar beating and thus motility. In addition, we found that additional members of the homologous signaling pathway described in echinoderms, both upstream and downstream of sAC, are expressed in coral sperm. These include the Na(+)/H(+) exchanger SLC9C1, protein kinase A, and the CatSper Ca(2+) channel conserved even in mammalian sperm. Indeed, the onset of motility corresponded with increased protein kinase A activity. Our discovery of this pathway in an early-branching metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize the need to better understand the role of pH-dependent signaling in the reproductive success of marine animals, particularly as climate change stressors continue to alter the physiology of corals and other marine invertebrates. National Academy of Sciences 2021-11-22 2021-11-30 /pmc/articles/PMC8640785/ /pubmed/34810263 http://dx.doi.org/10.1073/pnas.2109993118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Speer, Kelsey F.
Allen-Waller, Luella
Novikov, Dana R.
Barott, Katie L.
Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title_full Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title_fullStr Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title_full_unstemmed Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title_short Molecular mechanisms of sperm motility are conserved in an early-branching metazoan
title_sort molecular mechanisms of sperm motility are conserved in an early-branching metazoan
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8640785/
https://www.ncbi.nlm.nih.gov/pubmed/34810263
http://dx.doi.org/10.1073/pnas.2109993118
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