The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus

Benjamin Loppin, Emilie Bonnefoy, Caroline Anselme, Anne Laurençon, Timothy L. Karr, Pierre Couble

Research output: Contribution to journalArticle

228 Citations (Scopus)

Abstract

In sexually reproducing animals, a crucial step in zygote formation is the decondensation of the fertilizing sperm nucleus into a DNA replication-competent male pronucleus. Genome-wide nucleosome assembly on paternal DNA implies the replacement of sperm chromosomal proteins, such as protamines, by maternally provided histones. This fundamental process is specifically impaired in sésame (ssm), a unique Drosophila maternal effect mutant that prevents male pronucleus formation. Here we show that ssm is a point mutation in the Hira gene, thus demonstrating that the histone chaperone protein HIRA is required for nucleosome assembly during sperm nucleus decondensation. In vertebrates, HIRA has recently been shown to be critical for a nucleosome assembly pathway independent of DNA synthesis that specifically involves the H3.3 histone variant. We also show that nucleosomes containing H3.3, and not H3, are specifically assembled in paternal Drosophila chromatin before the first round of DNA replication. The exclusive marking of paternal chromosomes with H3.3 represents a primary epigenetic distinction between parental genomes in the zygote, and underlines an important consequence of the critical and highly specialized function of HIRA at fertilization.

Original languageEnglish (US)
Pages (from-to)1386-1390
Number of pages5
JournalNature
Volume437
Issue number7063
DOIs
StatePublished - Oct 27 2005
Externally publishedYes

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Histone Chaperones
Chromatin Assembly and Disassembly
Nucleosomes
Histones
Spermatozoa
Zygote
DNA Replication
Drosophila
Genome
Protamines
DNA
Point Mutation
Fertilization
Epigenomics
Chromatin
Vertebrates
Proteins
Chromosomes
Genes

ASJC Scopus subject areas

  • General

Cite this

Loppin, B., Bonnefoy, E., Anselme, C., Laurençon, A., Karr, T. L., & Couble, P. (2005). The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature, 437(7063), 1386-1390. https://doi.org/10.1038/nature04059

The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. / Loppin, Benjamin; Bonnefoy, Emilie; Anselme, Caroline; Laurençon, Anne; Karr, Timothy L.; Couble, Pierre.

In: Nature, Vol. 437, No. 7063, 27.10.2005, p. 1386-1390.

Research output: Contribution to journalArticle

Loppin, B, Bonnefoy, E, Anselme, C, Laurençon, A, Karr, TL & Couble, P 2005, 'The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus', Nature, vol. 437, no. 7063, pp. 1386-1390. https://doi.org/10.1038/nature04059
Loppin B, Bonnefoy E, Anselme C, Laurençon A, Karr TL, Couble P. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature. 2005 Oct 27;437(7063):1386-1390. https://doi.org/10.1038/nature04059
Loppin, Benjamin ; Bonnefoy, Emilie ; Anselme, Caroline ; Laurençon, Anne ; Karr, Timothy L. ; Couble, Pierre. / The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. In: Nature. 2005 ; Vol. 437, No. 7063. pp. 1386-1390.
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