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Cooperation-based sperm clusters mediate sperm oviduct entry and fertilization

Qu, Yongcun and Chen, Qi and Guo, Shanshan and Ma, Chiyuan and Lu, Yonggang and Shi, Junchao and Liu, Shichao and Zhou, Tong and Noda, Taichi and Qian, Jingjing and Zhang, Liwen and Zhu, Xili and Lei, Xiaohua and Cao, Yujing and Li, Wei and Li, Wei and Plachta, Nicolas and Matzuk, Martin M. and Ikawa, Masahito and Duan, Enkui and Zhang, Ying and Wang, Hongmei (2021) Cooperation-based sperm clusters mediate sperm oviduct entry and fertilization. Protein and Cell . ISSN 1674-800X. (In Press) https://resolver.caltech.edu/CaltechAUTHORS:20201021-072733806

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Abstract

Sperm cooperation has been observed in multiple species (Pizzari and Foster, 2008), yet its existence and benefit for reproductive success in mammals remains underexplored. Here, combining tissue-clearing with deep three-dimensional (3D) imaging, we demonstrate that postcopulatory mouse sperm congregate into unidirectional sperm cooperative clusters at the utero-tubal junction (UTJ), a key physical barrier for passage into the oviduct. Reducing sperm number in male mice by unilateral vasoligation (Uni-Vas) or busulfan-treatment impairs sperm cluster formation and oviduct entry. Interestingly, Tex101−/− male mouse produce normal sperm number, motility and morphology, yet their sperm cannot form clusters and fail to pass through the UTJ, which is at least in part due to the altered tail beating pattern of the Tex101 null sperm. Moreover, Tex101 null sperm’s defect in oviduct entry cannot be rescued by the presence of wild-type (WT) sperm in the same uteri by sequential mating, suggesting sperm cooperative cluster as an essential behavior contributing to male fertility.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1007/s13238-021-00825-yDOIArticle
https://doi.org/10.1101/2020.10.18.344275DOIDiscussion Paper
ORCID:
AuthorORCID
Chen, Qi0000-0001-6353-9589
Li, Wei0000-0002-6235-0749
Li, Wei0000-0001-7864-404X
Plachta, Nicolas0000-0002-5035-7425
Ikawa, Masahito0000-0001-9859-6217
Zhang, Ying0000-0003-4082-5026
Additional Information:© The Author(s) 2021. 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. Accepted 12 January 2021; Published 01 March 2021. This work was supported by the National Key Research and Development Program of China (2018YFC1004500 to YZ, 2019YFA0802600 to YZ, 2016YFA0500903 to ED, 2017YFC1001401 to ED, 2015CB943003 to YZ), the Strategic Priority Research Program of the CAS (XDA16020700 to HW) National Basic Research Program of China (81490742 to ED), National Natural Science Foundation of China (81490741 to HW, 31671201 to YZ, 31671568 to ED), Youth Innovation Promotion Association, CAS (Grant No. 2016081 to YZ). The Eunice Kennedy Shriver National Institute of Child Health and Human Development (grants HD088412 and P01HD087157) supports our studies of UTJ migration defects in mouse models. We thank Shiwen Li for the help of image processing. Yongcun Qu, Qi Chen, Shanshan Guo, Chiyuan Ma, Yonggang Lu, Junchao Shi, Shichao Liu, Tong Zhou, Taichi Noda, Jingjing Qian, Liwen Zhang, Xili Zhu, Xiaohua Lei, Yujing Cao, Wei Li, Wei Li, Nicolas Plachta, Martin M. Matzuk, Masahito Ikawa, Enkui Duan, Ying Zhang, Hongmei Wang declare that they have no conflict of interest. All animal studies were carried out under protocols approved by the Animal Care and Use Committee of Institute of Zoology, Chinese Academy of Sciences. Yongcun Qu, Qi Chen and Shanshan Guo have contributed equally contributed to this work.
Funders:
Funding AgencyGrant Number
National Key Research and Development Program of China2018YFC1004500
National Key Research and Development Program of China2019YFA0802600
National Key Research and Development Program of China2016YFA0500903
National Key Research and Development Program of China2017YFC1001401
National Key Research and Development Program of China2015CB943003
Chinese Academy of SciencesXDA16020700
National Basic Research Program of China81490742
National Natural Science Foundation of China81490741
National Natural Science Foundation of China31671201
National Natural Science Foundation of China31671568
Chinese Academy of Sciences2016081
NIHHD088412
NIH P01HD087157
Record Number:CaltechAUTHORS:20201021-072733806
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201021-072733806
Official Citation:Qu, Y., Chen, Q., Guo, S. et al. Cooperation-based sperm clusters mediate sperm oviduct entry and fertilization. Protein Cell (2021). https://doi.org/10.1007/s13238-021-00825-y
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106176
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Oct 2020 16:55
Last Modified:10 Mar 2021 17:42

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