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

Alexander V. Emelyanov, Joshua Rabbani, Monika Mehta, Elena Vershilova, Michael C. Keogh, Dmitry V. Fyodorov

Research output: Contribution to journalArticlepeer-review

14 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)2027-2040
Number of pages14
JournalGenes and Development
Volume28
Issue number18
DOIs
StatePublished - Sep 15 2014

Keywords

  • Chromatin Assembly
  • Fertilization
  • Histone chaperones
  • Male pronucleus
  • Protamines
  • Sperm chromatin remodeling

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology

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