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Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization

Human sperm compete for fertilization. Here, we find that human sperm, unexpectedly, cooperate under conditions mimicking the viscosity contrasts in the female reproductive tract. Sperm attach at the head region to migrate as a cooperative group upon transit into and through a high viscosity medium...

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Autores principales: Xiao, Sa, Riordon, Jason, Lagunov, Alex, Ghaffarzadeh, Mahta, Hannam, Thomas, Nosrati, Reza, Sinton, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10164193/
https://www.ncbi.nlm.nih.gov/pubmed/37149719
http://dx.doi.org/10.1038/s42003-023-04875-2
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author Xiao, Sa
Riordon, Jason
Lagunov, Alex
Ghaffarzadeh, Mahta
Hannam, Thomas
Nosrati, Reza
Sinton, David
author_facet Xiao, Sa
Riordon, Jason
Lagunov, Alex
Ghaffarzadeh, Mahta
Hannam, Thomas
Nosrati, Reza
Sinton, David
author_sort Xiao, Sa
collection PubMed
description Human sperm compete for fertilization. Here, we find that human sperm, unexpectedly, cooperate under conditions mimicking the viscosity contrasts in the female reproductive tract. Sperm attach at the head region to migrate as a cooperative group upon transit into and through a high viscosity medium (15-100 cP) from low viscosity seminal fluid. Sperm groups benefit from higher swimming velocity, exceeding that of individual sperm by over 50%. We find that sperm associated with a group possess high DNA integrity (7% fragmentation index) – a stark contrast to individual sperm exhibiting low DNA integrity (> 50% fragmentation index) – and feature membrane decapacitation factors that mediate sperm attachment to form the group. Cooperative behaviour becomes less prevalent upon capacitation and groups tend to disband as the surrounding viscosity reduces. When sperm from different male sources are present, related sperm preferentially form groups and achieve greater swimming velocity, while unrelated sperm are slowed by their involvement in a group. These findings reveal cooperation as a selective mode of human sperm motion – sperm with high DNA integrity cooperate to transit the highly viscous regions in the female tract and outcompete rival sperm for fertilization – and provide insight into cooperation-based sperm selection strategies for assisted reproduction.
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spelling pubmed-101641932023-05-08 Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization Xiao, Sa Riordon, Jason Lagunov, Alex Ghaffarzadeh, Mahta Hannam, Thomas Nosrati, Reza Sinton, David Commun Biol Article Human sperm compete for fertilization. Here, we find that human sperm, unexpectedly, cooperate under conditions mimicking the viscosity contrasts in the female reproductive tract. Sperm attach at the head region to migrate as a cooperative group upon transit into and through a high viscosity medium (15-100 cP) from low viscosity seminal fluid. Sperm groups benefit from higher swimming velocity, exceeding that of individual sperm by over 50%. We find that sperm associated with a group possess high DNA integrity (7% fragmentation index) – a stark contrast to individual sperm exhibiting low DNA integrity (> 50% fragmentation index) – and feature membrane decapacitation factors that mediate sperm attachment to form the group. Cooperative behaviour becomes less prevalent upon capacitation and groups tend to disband as the surrounding viscosity reduces. When sperm from different male sources are present, related sperm preferentially form groups and achieve greater swimming velocity, while unrelated sperm are slowed by their involvement in a group. These findings reveal cooperation as a selective mode of human sperm motion – sperm with high DNA integrity cooperate to transit the highly viscous regions in the female tract and outcompete rival sperm for fertilization – and provide insight into cooperation-based sperm selection strategies for assisted reproduction. Nature Publishing Group UK 2023-05-06 /pmc/articles/PMC10164193/ /pubmed/37149719 http://dx.doi.org/10.1038/s42003-023-04875-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Xiao, Sa
Riordon, Jason
Lagunov, Alex
Ghaffarzadeh, Mahta
Hannam, Thomas
Nosrati, Reza
Sinton, David
Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title_full Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title_fullStr Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title_full_unstemmed Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title_short Human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
title_sort human sperm cooperate to transit highly viscous regions on the competitive pathway to fertilization
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10164193/
https://www.ncbi.nlm.nih.gov/pubmed/37149719
http://dx.doi.org/10.1038/s42003-023-04875-2
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