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A novel atypical sperm centriole is functional during human fertilization

A novel atypical sperm centriole is functional during human fertilization
A novel atypical sperm centriole is functional during human fertilization

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.

Animals, Cattle, Cell Cycle Proteins/metabolism, Cell Line, Tumor, Centrioles/physiology, Congenital Abnormalities/etiology, Embryonic Development/physiology, Female, Fertilization/physiology, Fertilization in Vitro, Flagella/physiology, Humans, Infertility, Male/etiology, Male, Microscopy, Electron, Microtubules/physiology, Mitosis/physiology, Spermatogenesis/physiology, Spermatozoa/cytology, Testis/cytology, Tubulin/metabolism, Xenopus laevis, Zygote/cytology
2041-1723
Fishman, Emily L
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Jo, Kyoung
9b1b6471-238d-4339-9e94-881725b48780
Nguyen, Quynh P H
e887b852-af09-46a2-9d21-7786d9884b88
Kong, Dong
e8bc4dbb-b121-4943-91e1-d33713aefdf4
Royfman, Rachel
c36e403c-580c-4438-8bc7-64b3ff9a19ba
Cekic, Anthony R
d4ee7432-3916-4e7f-a327-bc7d5be8c18f
Khanal, Sushil
21d38080-2baf-4fa3-ba27-f3638a18837b
Miller, Ann L
58857949-8661-4959-904a-ee0737ec8b0c
Simerly, Calvin
c845732a-b2f5-4d15-82dd-fdad6249ddb8
Schatten, Gerald
c0183bae-3cfa-49d8-8e14-08a1753fe815
Loncarek, Jadranka
84457114-5482-4c7e-bb0f-aac7a1172e23
Mennella, Vito
43c60e29-c0a7-4ab8-8e5c-fcb59f70a28a
Avidor-Reiss, Tomer
ad760347-f82b-46b6-8ef6-bd1f407acfd5
Fishman, Emily L
24e63f01-115e-4cea-ac4a-ccd09532dd6f
Jo, Kyoung
9b1b6471-238d-4339-9e94-881725b48780
Nguyen, Quynh P H
e887b852-af09-46a2-9d21-7786d9884b88
Kong, Dong
e8bc4dbb-b121-4943-91e1-d33713aefdf4
Royfman, Rachel
c36e403c-580c-4438-8bc7-64b3ff9a19ba
Cekic, Anthony R
d4ee7432-3916-4e7f-a327-bc7d5be8c18f
Khanal, Sushil
21d38080-2baf-4fa3-ba27-f3638a18837b
Miller, Ann L
58857949-8661-4959-904a-ee0737ec8b0c
Simerly, Calvin
c845732a-b2f5-4d15-82dd-fdad6249ddb8
Schatten, Gerald
c0183bae-3cfa-49d8-8e14-08a1753fe815
Loncarek, Jadranka
84457114-5482-4c7e-bb0f-aac7a1172e23
Mennella, Vito
43c60e29-c0a7-4ab8-8e5c-fcb59f70a28a
Avidor-Reiss, Tomer
ad760347-f82b-46b6-8ef6-bd1f407acfd5

Fishman, Emily L, Jo, Kyoung, Nguyen, Quynh P H, Kong, Dong, Royfman, Rachel, Cekic, Anthony R, Khanal, Sushil, Miller, Ann L, Simerly, Calvin, Schatten, Gerald, Loncarek, Jadranka, Mennella, Vito and Avidor-Reiss, Tomer (2018) A novel atypical sperm centriole is functional during human fertilization. Nature Communications, 9 (1), [2210]. (doi:10.1038/s41467-018-04678-8).

Record type: Article

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.

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centriole is functional during human fertilization - Version of Record
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Accepted/In Press date: 1 January 2018
e-pub ahead of print date: 7 June 2018
Published date: 7 June 2018
Keywords: Animals, Cattle, Cell Cycle Proteins/metabolism, Cell Line, Tumor, Centrioles/physiology, Congenital Abnormalities/etiology, Embryonic Development/physiology, Female, Fertilization/physiology, Fertilization in Vitro, Flagella/physiology, Humans, Infertility, Male/etiology, Male, Microscopy, Electron, Microtubules/physiology, Mitosis/physiology, Spermatogenesis/physiology, Spermatozoa/cytology, Testis/cytology, Tubulin/metabolism, Xenopus laevis, Zygote/cytology

Identifiers

Local EPrints ID: 434161
URI: http://eprints.soton.ac.uk/id/eprint/434161
ISSN: 2041-1723
PURE UUID: e8ea0677-3e9f-431d-bf8e-c900bb38e039
ORCID for Vito Mennella: ORCID iD orcid.org/0000-0002-4842-9012

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Date deposited: 13 Sep 2019 16:30
Last modified: 16 Mar 2024 04:03

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Contributors

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

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