A novel atypical sperm centriole is functional during human fertilization

Emily L Fishman,Rachel Royfman,Kyoung Jo,Calvin Simerly,Quynh P H Nguyen,Sushil Khanal,Jadranka Loncarek,Gerald Schatten,Dong Kong,Vito Mennella,Anthony R Cekic,Tomer Avidor-Reiss,Ann L Miller

doi:10.1038/s41467-018-04678-8

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.

Highlights

Human development begins with the zygote, which divides many times to produce all of the somatic cells
The dogma of centrosome reduction and previously published literature states that pericentriolar material (PCM) proteins are reduced based on the observations that γtubulin and PCNT are missing from the sperm centrosome[5]
We found that the PCM proteins γ-tubulin and PCNT were eliminated from the neck region during spermatogenesis (Supplementary Fig. 1a)

Summary

Introduction

Human development begins with the zygote, which divides many times to produce all of the somatic cells. A similar enigma existed previously in insects until it was shown that insect sperm possesses, in addition to the known centriole, a second atypical centriolar structure[14,15,16]. We follow the DC of bovine sperm into the zygote and found that it recruits PCM, forms an aster, forms a new daughter centriole, and localizes to the spindle pole, all while maintaining its attachment to the axoneme. These findings discover a novel, atypical centriole in the sperm, which functions in the zygote

Methods

Results

Conclusion