Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs

After insemination, a subpopulation of sperm reaches the oviducts and binds to isthmic epithelial cells to form a “sperm reservoir”. Our objective was to explore the role of annexin A5 (ANXA5), a protein that binds with high affinity to phosphatidylserine (PS), in the formation of the sperm reservoi...

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Main Authors: Lorraine Schmaltz, Elie Barakat, Renaud Fleurot, Rustem Uzbekov, Karine Reynaud, Ludivine Laffont, Guillaume Tsikis, Isabelle Mérour, Pascal Mermillod, Marie Saint-Dizier
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:European Journal of Cell Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S0171933524000888
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author Lorraine Schmaltz
Elie Barakat
Renaud Fleurot
Rustem Uzbekov
Karine Reynaud
Ludivine Laffont
Guillaume Tsikis
Isabelle Mérour
Pascal Mermillod
Marie Saint-Dizier
author_facet Lorraine Schmaltz
Elie Barakat
Renaud Fleurot
Rustem Uzbekov
Karine Reynaud
Ludivine Laffont
Guillaume Tsikis
Isabelle Mérour
Pascal Mermillod
Marie Saint-Dizier
author_sort Lorraine Schmaltz
collection DOAJ
description After insemination, a subpopulation of sperm reaches the oviducts and binds to isthmic epithelial cells to form a “sperm reservoir”. Our objective was to explore the role of annexin A5 (ANXA5), a protein that binds with high affinity to phosphatidylserine (PS), in the formation of the sperm reservoir in pigs.Phosphatidylserine was detected on the head of approximately 10 % of boar sperm at ejaculation. Porcine ANXA5 was immunodetected with a strong signal on luminal cilia in the isthmus and in derived isthmic epithelial spheroids (IES). Exogenous PS between 0.01 and 0.1 µg/mL and recombinant porcine ANXA5 (rpANXA5) above 0.1 µg/mL inhibited sperm binding to IES without reducing sperm motility. Pre-incubation of sperm, but not IES, with rpANXA5 inhibited sperm binding to IES. Under capacitating conditions, the proportion of live sperm with head PS exposure and the ability of sperm to bind to rpANXA5 and IES cilia increased within 30 min. Conversely, the acrosome reaction decreased the ability of sperm to bind rpANXA5 and prevented sperm binding to IES.In conclusion, sperm membrane remodelling during capacitation enhanced head PS exposure in motile sperm, resulting in increased interaction with ciliary ANXA5 on isthmic epithelial spheroids. These findings support a role for PS-ANXA5 interaction in the formation of the sperm reservoir in mammalian females.
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spelling doaj-art-83cc889e9376471191ef09828166b41f2025-01-23T05:26:15ZengElsevierEuropean Journal of Cell Biology0171-93352025-03-011041151471Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigsLorraine Schmaltz0Elie Barakat1Renaud Fleurot2Rustem Uzbekov3Karine Reynaud4Ludivine Laffont5Guillaume Tsikis6Isabelle Mérour7Pascal Mermillod8Marie Saint-Dizier9INRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceLaboratory of Cell Biology and Electron Microscopy, University of Tours, Tours, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceYXIA, St-Gilles, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, FranceINRAE, CNRS, University of Tours, Physiologie de la Reproduction et des comportements, Center INRAE Val-de-Loire, Nouzilly, France; Corresponding author.After insemination, a subpopulation of sperm reaches the oviducts and binds to isthmic epithelial cells to form a “sperm reservoir”. Our objective was to explore the role of annexin A5 (ANXA5), a protein that binds with high affinity to phosphatidylserine (PS), in the formation of the sperm reservoir in pigs.Phosphatidylserine was detected on the head of approximately 10 % of boar sperm at ejaculation. Porcine ANXA5 was immunodetected with a strong signal on luminal cilia in the isthmus and in derived isthmic epithelial spheroids (IES). Exogenous PS between 0.01 and 0.1 µg/mL and recombinant porcine ANXA5 (rpANXA5) above 0.1 µg/mL inhibited sperm binding to IES without reducing sperm motility. Pre-incubation of sperm, but not IES, with rpANXA5 inhibited sperm binding to IES. Under capacitating conditions, the proportion of live sperm with head PS exposure and the ability of sperm to bind to rpANXA5 and IES cilia increased within 30 min. Conversely, the acrosome reaction decreased the ability of sperm to bind rpANXA5 and prevented sperm binding to IES.In conclusion, sperm membrane remodelling during capacitation enhanced head PS exposure in motile sperm, resulting in increased interaction with ciliary ANXA5 on isthmic epithelial spheroids. These findings support a role for PS-ANXA5 interaction in the formation of the sperm reservoir in mammalian females.http://www.sciencedirect.com/science/article/pii/S0171933524000888SpermatozoaOviductPhosphatidylserineAnnexin A5CapacitationSperm storage
spellingShingle Lorraine Schmaltz
Elie Barakat
Renaud Fleurot
Rustem Uzbekov
Karine Reynaud
Ludivine Laffont
Guillaume Tsikis
Isabelle Mérour
Pascal Mermillod
Marie Saint-Dizier
Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
European Journal of Cell Biology
Spermatozoa
Oviduct
Phosphatidylserine
Annexin A5
Capacitation
Sperm storage
title Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
title_full Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
title_fullStr Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
title_full_unstemmed Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
title_short Phosphatidylserine on sperm head interact with Annexin A5 on oviduct luminal cilia to form a sperm reservoir in pigs
title_sort phosphatidylserine on sperm head interact with annexin a5 on oviduct luminal cilia to form a sperm reservoir in pigs
topic Spermatozoa
Oviduct
Phosphatidylserine
Annexin A5
Capacitation
Sperm storage
url http://www.sciencedirect.com/science/article/pii/S0171933524000888
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