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Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation

The functional maturation of spermatozoa that is necessary to achieve fertilization occurs as these cells transit through the epididymis, a highly specialized region of the male reproductive tract. A defining feature of this maturation process is that it occurs in the complete absence of nuclear gen...

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Autores principales: Nixon, Brett, De Iuliis, Geoffry N., Hart, Hanah M., Zhou, Wei, Mathe, Andrea, Bernstein, Ilana R., Anderson, Amanda L., Stanger, Simone J., Skerrett-Byrne, David A., Jamaluddin, M. Fairuz B., Almazi, Juhura G., Bromfield, Elizabeth G., Larsen, Martin R., Dun, Matthew D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Biochemistry and Molecular Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6427233/
https://www.ncbi.nlm.nih.gov/pubmed/30213844
http://dx.doi.org/10.1074/mcp.RA118.000946
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author Nixon, Brett
De Iuliis, Geoffry N.
Hart, Hanah M.
Zhou, Wei
Mathe, Andrea
Bernstein, Ilana R.
Anderson, Amanda L.
Stanger, Simone J.
Skerrett-Byrne, David A.
Jamaluddin, M. Fairuz B.
Almazi, Juhura G.
Bromfield, Elizabeth G.
Larsen, Martin R.
Dun, Matthew D.
author_facet Nixon, Brett
De Iuliis, Geoffry N.
Hart, Hanah M.
Zhou, Wei
Mathe, Andrea
Bernstein, Ilana R.
Anderson, Amanda L.
Stanger, Simone J.
Skerrett-Byrne, David A.
Jamaluddin, M. Fairuz B.
Almazi, Juhura G.
Bromfield, Elizabeth G.
Larsen, Martin R.
Dun, Matthew D.
author_sort Nixon, Brett
collection PubMed
description The functional maturation of spermatozoa that is necessary to achieve fertilization occurs as these cells transit through the epididymis, a highly specialized region of the male reproductive tract. A defining feature of this maturation process is that it occurs in the complete absence of nuclear gene transcription or de novo, protein translation in the spermatozoa. Rather, it is driven by sequential interactions between spermatozoa and the complex external milieu in which they are bathed within lumen of the epididymal tubule. A feature of this dynamic microenvironment are epididymosomes, small membrane encapsulated vesicles that are secreted from the epididymal soma. Herein, we report comparative proteomic profiling of epididymosomes isolated from different segments of the mouse epididymis using multiplexed tandem mass tag (TMT) based quantification coupled with high resolution LC-MS/MS. A total of 1640 epididymosome proteins were identified and quantified via this proteomic method. Notably, this analysis revealed pronounced segment-to-segment variation in the encapsulated epididymosome proteome. Thus, 146 proteins were identified as being differentially accumulated between caput and corpus epididymosomes, and a further 344 were differentially accumulated between corpus and cauda epididymosomes (i.e., fold change of ≤ −1.5 or ≥ 1.5; p, < 0.05). Application of gene ontology annotation revealed a substantial portion of the epididymosome proteins mapped to the cellular component of extracellular exosome and to the biological processes of transport, oxidation-reduction, and metabolism. Additional annotation of the subset of epididymosome proteins that have not previously been identified in exosomes revealed enrichment of categories associated with the acquisition of sperm function (e.g., fertilization and binding to the zona pellucida). In tandem with our demonstration that epididymosomes are able to convey protein cargo to the head of maturing spermatozoa, these data emphasize the fundamental importance of epididymosomes as key elements of the epididymal microenvironment responsible for coordinating post-testicular sperm maturation.
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spelling pubmed-64272332019-03-22 Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation Nixon, Brett De Iuliis, Geoffry N. Hart, Hanah M. Zhou, Wei Mathe, Andrea Bernstein, Ilana R. Anderson, Amanda L. Stanger, Simone J. Skerrett-Byrne, David A. Jamaluddin, M. Fairuz B. Almazi, Juhura G. Bromfield, Elizabeth G. Larsen, Martin R. Dun, Matthew D. Mol Cell Proteomics Research The functional maturation of spermatozoa that is necessary to achieve fertilization occurs as these cells transit through the epididymis, a highly specialized region of the male reproductive tract. A defining feature of this maturation process is that it occurs in the complete absence of nuclear gene transcription or de novo, protein translation in the spermatozoa. Rather, it is driven by sequential interactions between spermatozoa and the complex external milieu in which they are bathed within lumen of the epididymal tubule. A feature of this dynamic microenvironment are epididymosomes, small membrane encapsulated vesicles that are secreted from the epididymal soma. Herein, we report comparative proteomic profiling of epididymosomes isolated from different segments of the mouse epididymis using multiplexed tandem mass tag (TMT) based quantification coupled with high resolution LC-MS/MS. A total of 1640 epididymosome proteins were identified and quantified via this proteomic method. Notably, this analysis revealed pronounced segment-to-segment variation in the encapsulated epididymosome proteome. Thus, 146 proteins were identified as being differentially accumulated between caput and corpus epididymosomes, and a further 344 were differentially accumulated between corpus and cauda epididymosomes (i.e., fold change of ≤ −1.5 or ≥ 1.5; p, < 0.05). Application of gene ontology annotation revealed a substantial portion of the epididymosome proteins mapped to the cellular component of extracellular exosome and to the biological processes of transport, oxidation-reduction, and metabolism. Additional annotation of the subset of epididymosome proteins that have not previously been identified in exosomes revealed enrichment of categories associated with the acquisition of sperm function (e.g., fertilization and binding to the zona pellucida). In tandem with our demonstration that epididymosomes are able to convey protein cargo to the head of maturing spermatozoa, these data emphasize the fundamental importance of epididymosomes as key elements of the epididymal microenvironment responsible for coordinating post-testicular sperm maturation. The American Society for Biochemistry and Molecular Biology 2019-03-15 2018-09-13 /pmc/articles/PMC6427233/ /pubmed/30213844 http://dx.doi.org/10.1074/mcp.RA118.000946 Text en © 2019 Nixon et al. Published by The American Society for Biochemistry and Molecular Biology, Inc. Author's Choice,—Final version open access under the terms of the Creative Commons CC-BY license (http://creativecommons.org/licenses/by/4.0) .
spellingShingle Research
Nixon, Brett
De Iuliis, Geoffry N.
Hart, Hanah M.
Zhou, Wei
Mathe, Andrea
Bernstein, Ilana R.
Anderson, Amanda L.
Stanger, Simone J.
Skerrett-Byrne, David A.
Jamaluddin, M. Fairuz B.
Almazi, Juhura G.
Bromfield, Elizabeth G.
Larsen, Martin R.
Dun, Matthew D.
Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title_full Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title_fullStr Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title_full_unstemmed Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title_short Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation
title_sort proteomic profiling of mouse epididymosomes reveals their contributions to post-testicular sperm maturation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6427233/
https://www.ncbi.nlm.nih.gov/pubmed/30213844
http://dx.doi.org/10.1074/mcp.RA118.000946
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