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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 (dis...

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Autores principales: 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, Avidor-Reiss, Tomer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5992222/
https://www.ncbi.nlm.nih.gov/pubmed/29880810
http://dx.doi.org/10.1038/s41467-018-04678-8
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author 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
Avidor-Reiss, Tomer
author_facet 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
Avidor-Reiss, Tomer
author_sort Fishman, Emily L.
collection PubMed
description 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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spelling pubmed-59922222018-06-11 A novel atypical sperm centriole is functional during human fertilization 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 Avidor-Reiss, Tomer Nat Commun Article 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. Nature Publishing Group UK 2018-06-07 /pmc/articles/PMC5992222/ /pubmed/29880810 http://dx.doi.org/10.1038/s41467-018-04678-8 Text en © The Author(s) 2018 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/.
spellingShingle Article
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
Avidor-Reiss, Tomer
A novel atypical sperm centriole is functional during human fertilization
title A novel atypical sperm centriole is functional during human fertilization
title_full A novel atypical sperm centriole is functional during human fertilization
title_fullStr A novel atypical sperm centriole is functional during human fertilization
title_full_unstemmed A novel atypical sperm centriole is functional during human fertilization
title_short A novel atypical sperm centriole is functional during human fertilization
title_sort novel atypical sperm centriole is functional during human fertilization
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5992222/
https://www.ncbi.nlm.nih.gov/pubmed/29880810
http://dx.doi.org/10.1038/s41467-018-04678-8
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