Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis

Mammalian spermatogenesis is associated with the transient appearance of condensed mitochondria, a singularity of germ cells with unknown function. Using proteomic analysis, respirometry, and electron microscopy with tomography, we studied the development of condensed mitochondria. Condensed mitocho...

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Main Authors: Mindong Ren, Yang Xu, Colin K. L. Phoon, Hediye Erdjument-Bromage, Thomas A. Neubert, Sujith Rajan, M. Mahmood Hussain, Michael Schlame
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2022.867175/full
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author Mindong Ren
Mindong Ren
Yang Xu
Colin K. L. Phoon
Hediye Erdjument-Bromage
Hediye Erdjument-Bromage
Thomas A. Neubert
Thomas A. Neubert
Sujith Rajan
M. Mahmood Hussain
Michael Schlame
Michael Schlame
author_facet Mindong Ren
Mindong Ren
Yang Xu
Colin K. L. Phoon
Hediye Erdjument-Bromage
Hediye Erdjument-Bromage
Thomas A. Neubert
Thomas A. Neubert
Sujith Rajan
M. Mahmood Hussain
Michael Schlame
Michael Schlame
author_sort Mindong Ren
collection DOAJ
description Mammalian spermatogenesis is associated with the transient appearance of condensed mitochondria, a singularity of germ cells with unknown function. Using proteomic analysis, respirometry, and electron microscopy with tomography, we studied the development of condensed mitochondria. Condensed mitochondria arose from orthodox mitochondria during meiosis by progressive contraction of the matrix space, which was accompanied by an initial expansion and a subsequent reduction of the surface area of the inner membrane. Compared to orthodox mitochondria, condensed mitochondria respired more actively, had a higher concentration of respiratory enzymes and supercomplexes, and contained more proteins involved in protein import and expression. After the completion of meiosis, the abundance of condensed mitochondria declined, which coincided with the onset of the biogenesis of acrosomes. Immuno-electron microscopy and the analysis of sub-cellular fractions suggested that condensed mitochondria or their fragments were translocated into the lumen of the acrosome. Thus, it seems condensed mitochondria are formed from orthodox mitochondria by extensive transformations in order to support the formation of the acrosomal matrix.
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spelling doaj.art-ebb66ead9f3f46589f2f54c0efc831952022-12-22T00:17:54ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-04-011010.3389/fcell.2022.867175867175Condensed Mitochondria Assemble Into the Acrosomal Matrix During SpermiogenesisMindong Ren0Mindong Ren1Yang Xu2Colin K. L. Phoon3Hediye Erdjument-Bromage4Hediye Erdjument-Bromage5Thomas A. Neubert6Thomas A. Neubert7Sujith Rajan8M. Mahmood Hussain9Michael Schlame10Michael Schlame11Departments of Anesthesiology, New York, NY, United StatesDepartment of Cell Biology, New York, NY, United StatesDepartments of Anesthesiology, New York, NY, United StatesDepartment of Pediatrics, New York, NY, United StatesDepartment of Cell Biology, New York, NY, United StatesKimmel Center for Biology and Medicine at the Skirball Institute, New York University School of Medicine, New York, NY, United StatesDepartment of Cell Biology, New York, NY, United StatesKimmel Center for Biology and Medicine at the Skirball Institute, New York University School of Medicine, New York, NY, United StatesDepartment of Foundations of Medicine, NYU Long Island School of Medicine, Mineola, NY, United StatesDepartment of Foundations of Medicine, NYU Long Island School of Medicine, Mineola, NY, United StatesDepartments of Anesthesiology, New York, NY, United StatesDepartment of Cell Biology, New York, NY, United StatesMammalian spermatogenesis is associated with the transient appearance of condensed mitochondria, a singularity of germ cells with unknown function. Using proteomic analysis, respirometry, and electron microscopy with tomography, we studied the development of condensed mitochondria. Condensed mitochondria arose from orthodox mitochondria during meiosis by progressive contraction of the matrix space, which was accompanied by an initial expansion and a subsequent reduction of the surface area of the inner membrane. Compared to orthodox mitochondria, condensed mitochondria respired more actively, had a higher concentration of respiratory enzymes and supercomplexes, and contained more proteins involved in protein import and expression. After the completion of meiosis, the abundance of condensed mitochondria declined, which coincided with the onset of the biogenesis of acrosomes. Immuno-electron microscopy and the analysis of sub-cellular fractions suggested that condensed mitochondria or their fragments were translocated into the lumen of the acrosome. Thus, it seems condensed mitochondria are formed from orthodox mitochondria by extensive transformations in order to support the formation of the acrosomal matrix.https://www.frontiersin.org/articles/10.3389/fcell.2022.867175/fullacrosomecristaemitochondriaspermatogenesisspermiogenensis
spellingShingle Mindong Ren
Mindong Ren
Yang Xu
Colin K. L. Phoon
Hediye Erdjument-Bromage
Hediye Erdjument-Bromage
Thomas A. Neubert
Thomas A. Neubert
Sujith Rajan
M. Mahmood Hussain
Michael Schlame
Michael Schlame
Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
Frontiers in Cell and Developmental Biology
acrosome
cristae
mitochondria
spermatogenesis
spermiogenensis
title Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
title_full Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
title_fullStr Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
title_full_unstemmed Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
title_short Condensed Mitochondria Assemble Into the Acrosomal Matrix During Spermiogenesis
title_sort condensed mitochondria assemble into the acrosomal matrix during spermiogenesis
topic acrosome
cristae
mitochondria
spermatogenesis
spermiogenensis
url https://www.frontiersin.org/articles/10.3389/fcell.2022.867175/full
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