Cargando…

Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization

Nuclear DNA in the male gamete of sexually reproducing animals is organized as sperm chromatin compacted primarily by sperm-specific protamines. Fertilization leads to sperm chromatin remodeling, during which protamines are expelled and replaced by histones. Despite our increased understanding of th...

Descripción completa

Detalles Bibliográficos
Autores principales: Emelyanov, Alexander V., Rabbani, Joshua, Mehta, Monika, Vershilova, Elena, Keogh, Michael C., Fyodorov, Dmitry V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4173154/
https://www.ncbi.nlm.nih.gov/pubmed/25228646
http://dx.doi.org/10.1101/gad.248583.114
_version_ 1782336140493193216
author Emelyanov, Alexander V.
Rabbani, Joshua
Mehta, Monika
Vershilova, Elena
Keogh, Michael C.
Fyodorov, Dmitry V.
author_facet Emelyanov, Alexander V.
Rabbani, Joshua
Mehta, Monika
Vershilova, Elena
Keogh, Michael C.
Fyodorov, Dmitry V.
author_sort Emelyanov, Alexander V.
collection PubMed
description Nuclear DNA in the male gamete of sexually reproducing animals is organized as sperm chromatin compacted primarily by sperm-specific protamines. Fertilization leads to sperm chromatin remodeling, during which protamines are expelled and replaced by histones. Despite our increased understanding of the factors that mediate nucleosome assembly in the nascent male pronucleus, the machinery for protamine removal remains largely unknown. Here we identify four Drosophila protamine chaperones that mediate the dissociation of protamine–DNA complexes: NAP-1, NLP, and nucleophosmin are previously characterized histone chaperones, and TAP/p32 has no known function in chromatin metabolism. We show that TAP/p32 is required for the removal of Drosophila protamine B in vitro, whereas NAP-1, NLP, and Nph share roles in the removal of protamine A. Embryos from P32-null females show defective formation of the male pronucleus in vivo. TAP/p32, similar to NAP-1, NLP, and Nph, facilitates nucleosome assembly in vitro and is therefore a histone chaperone. Furthermore, mutants of P32, Nlp, and Nph exhibit synthetic-lethal genetic interactions. In summary, we identified factors mediating protamine removal from DNA and reconstituted in a defined system the process of sperm chromatin remodeling that exchanges protamines for histones to form the nucleosome-based chromatin characteristic of somatic cells.
format Online
Article
Text
id pubmed-4173154
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher Cold Spring Harbor Laboratory Press
record_format MEDLINE/PubMed
spelling pubmed-41731542015-03-15 Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization Emelyanov, Alexander V. Rabbani, Joshua Mehta, Monika Vershilova, Elena Keogh, Michael C. Fyodorov, Dmitry V. Genes Dev Research Paper Nuclear DNA in the male gamete of sexually reproducing animals is organized as sperm chromatin compacted primarily by sperm-specific protamines. Fertilization leads to sperm chromatin remodeling, during which protamines are expelled and replaced by histones. Despite our increased understanding of the factors that mediate nucleosome assembly in the nascent male pronucleus, the machinery for protamine removal remains largely unknown. Here we identify four Drosophila protamine chaperones that mediate the dissociation of protamine–DNA complexes: NAP-1, NLP, and nucleophosmin are previously characterized histone chaperones, and TAP/p32 has no known function in chromatin metabolism. We show that TAP/p32 is required for the removal of Drosophila protamine B in vitro, whereas NAP-1, NLP, and Nph share roles in the removal of protamine A. Embryos from P32-null females show defective formation of the male pronucleus in vivo. TAP/p32, similar to NAP-1, NLP, and Nph, facilitates nucleosome assembly in vitro and is therefore a histone chaperone. Furthermore, mutants of P32, Nlp, and Nph exhibit synthetic-lethal genetic interactions. In summary, we identified factors mediating protamine removal from DNA and reconstituted in a defined system the process of sperm chromatin remodeling that exchanges protamines for histones to form the nucleosome-based chromatin characteristic of somatic cells. Cold Spring Harbor Laboratory Press 2014-09-15 /pmc/articles/PMC4173154/ /pubmed/25228646 http://dx.doi.org/10.1101/gad.248583.114 Text en © 2014 Emelyanov et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research Paper
Emelyanov, Alexander V.
Rabbani, Joshua
Mehta, Monika
Vershilova, Elena
Keogh, Michael C.
Fyodorov, Dmitry V.
Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title_full Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title_fullStr Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title_full_unstemmed Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title_short Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization
title_sort drosophila tap/p32 is a core histone chaperone that cooperates with nap-1, nlp, and nucleophosmin in sperm chromatin remodeling during fertilization
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4173154/
https://www.ncbi.nlm.nih.gov/pubmed/25228646
http://dx.doi.org/10.1101/gad.248583.114
work_keys_str_mv AT emelyanovalexanderv drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization
AT rabbanijoshua drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization
AT mehtamonika drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization
AT vershilovaelena drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization
AT keoghmichaelc drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization
AT fyodorovdmitryv drosophilatapp32isacorehistonechaperonethatcooperateswithnap1nlpandnucleophosmininspermchromatinremodelingduringfertilization