Abstract

The inheritance of the centrosome during human fertilization remains mysterious. Here we show that the sperm centrosome contains, in addition to the known typical barrel-shaped centriole (the proximal centriole, PC), a surrounding matrix (pericentriolar material, PCM), and an atypical centriole (distal centriole, DC) composed of splayed microtubules surrounding previously undescribed rods of centriole luminal proteins. The sperm centrosome is remodeled by both reduction and enrichment of specific proteins and the formation of these rods during spermatogenesis. In vivo and in vitro investigations show that the flagellum-attached, atypical DC is capable of recruiting PCM, forming a daughter centriole, and localizing to the spindle pole during mitosis. Altogether, we show that the DC is compositionally and structurally remodeled into an atypical centriole, which functions as the zygote’s second centriole. These findings now provide novel avenues for diagnostics and therapeutic strategies for male infertility, and insights into early embryo developmental defects.

Details

Title
A novel atypical sperm centriole is functional during human fertilization
Author
Fishman, Emily L 1   VIAFID ORCID Logo  ; Jo, Kyoung 1 ; Nguyen, Quynh P H 2 ; Kong, Dong 3   VIAFID ORCID Logo  ; Royfman, Rachel 1 ; Cekic, Anthony R 1 ; Khanal, Sushil 1 ; Miller, Ann L 4   VIAFID ORCID Logo  ; Simerly, Calvin 5 ; Schatten, Gerald 5 ; Loncarek, Jadranka 3 ; Mennella, Vito 2 ; Avidor-Reiss, Tomer 1 

1  Department of Biological Sciences, University of Toledo, Toledo, OH, USA 
2  Cell Biology Program, The Hospital for Sick Children, Department of Biochemistry, University of Toronto, Toronto, ON, Canada 
3  Laboratory of Protein Dynamics and Signaling, Center for Cancer Research, National Cancer Institute, Frederick, MD, USA 
4  Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI, USA 
5  Departments of Cell Biology; Obstetrics, Gynecology and Reproductive Sciences; and Bioengineering, Magee-Womens Research Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA 
Pages
1-12
Publication year
2018
Publication date
Jun 2018
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.1038/s41467-018-04678-8
ProQuest document ID
2051643951
Copyright
© 2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.