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H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A.

ABSTRACT: We have isolated from a subtractive cDNA library of Xenopus laevis a novel transcript, H2A.ZI, which belongs to the H2A.Z variant gene family. Characterization of its expression during oogenesis and development shows significant differences from the expression of the core histone H2A. First, H2A.ZI mRNA is mainly detected only during oogenesis and after the midblastula transition, whereas H2A is constitutively expressed, at much higher levels, throughout embryonic growth. Second, in contrast with H2A, the variant H2A.ZI is polyadenylated during development. Third, expression of H2A.ZI is uncoupled from the S phase after gastrula, whereas synthesis of the core histone H2A mRNA is tightly controlled to DNA replication. Interestingly, H2A.ZI is less charged in the N-terminal tail which is crucial for chromatin-mediated repression. The characteristics of H2A.ZI suggest that its incorporation into nucleosomes would lead to a chromatin structure more competent for gene expression during development.

SUBMITTER: Iouzalen N

PROVIDER: S-EPMC146197 | biostudies-other | 1996 Oct

REPOSITORIES: biostudies-other

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H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A.

Iouzalen N N Moreau J J Méchali M M

Nucleic acids research 19961001 20

We have isolated from a subtractive cDNA library of Xenopus laevis a novel transcript, H2A.ZI, which belongs to the H2A.Z variant gene family. Characterization of its expression during oogenesis and development shows significant differences from the expression of the core histone H2A. First, H2A.ZI mRNA is mainly detected only during oogenesis and after the midblastula transition, whereas H2A is constitutively expressed, at much higher levels, throughout embryonic growth. Second, in contrast wit ...[more]

PMID: 8918796

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Project description:BackgroundStored, soluble histones in eggs are essential for early development, in particular during the maternally controlled early cell cycles in the absence of transcription. Histone post-translational modifications (PTMs) direct and regulate chromatin-templated transactions, so understanding the nature and function of pre-deposition maternal histones is essential to deciphering mechanisms of regulation of development, chromatin assembly, and transcription. Little is known about histone H2A pre-deposition modifications nor known about the transitions that occur upon the onset of zygotic control of the cell cycle and transcription at the mid-blastula transition (MBT).ResultsWe isolated histones from staged Xenopus laevis oocytes, eggs, embryos, and assembled pronuclei to identify changes in histone H2A modifications prior to deposition and in chromatin. Soluble and chromatin-bound histones from eggs and embryos demonstrated distinct patterns of maternal and zygotic H2A PTMs, with significant pre-deposition quantities of S1ph and R3me1, and R3me2s. We observed the first functional distinction between H2A and H4 S1 phosphorylation, as we showed that H2A and H2A.X-F (also known as H2A.X.3) serine 1 (S1) is phosphorylated concomitant with germinal vesicle breakdown (GVBD) while H4 serine 1 phosphorylation occurs post-MBT. In egg extract H2A/H4 S1 phosphorylation is independent of the cell cycle, chromatin assembly, and DNA replication. H2AS1ph is highly enriched on blastula chromatin during repression of zygotic gene expression while H4S1ph is correlated with the beginning of maternal gene expression and the lengthening of the cell cycle, consistent with distinct biological roles for H2A and H4 S1 phosphorylation. We isolated soluble H2A and H2A.X-F from the egg and chromatin-bound in pronuclei and analyzed them by mass spectrometry analysis to quantitatively determine abundances of S1ph and R3 methylation. We show that H2A and H4 S1ph, R3me1 and R3me2s are enriched on nucleosomes containing both active and repressive histone PTMs in human A549 cells and Xenopus embryos.ConclusionsSignificantly, we demonstrated that H2A phosphorylation and H4 arginine methylation form a new class of bona fide pre-deposition modifications in the vertebrate embryo. We show that S1ph and R3me containing chromatin domains are not correlated with H3 regulatory PTMs, suggesting a unique role for phosphorylation and arginine methylation.

Project description:Herpes simplex virus 1 (HSV-1) transcription is restricted in latently infected neurons and the genomes are in mostly silenced chromatin, whereas all viral genes are transcribed in lytically infected cells, in which the genomes are dynamically chromatinized. Epigenetic regulation modulates HSV-1 transcription during lytic, latent, and reactivating infections but the precise mechanisms are not fully defined. Nucleosomes are dynamic: they slide, breathe, assemble, and disassemble. We and others have proposed that the most dynamic HSV-1 chromatin is transcriptionally competent, whereas the least dynamic is silenced. However, the mechanisms yielding the unusually dynamic viral chromatin remain unknown. Histone variants affect nucleosome dynamics. The dynamics of H2A, H2A.X, and macroH2A were enhanced in infected cells, whereas those of H2A.B were uniquely decreased. We constructed stably transduced cells expressing tagged histone H2A, H2A.B, macroH2A, or H2B, which assembles the H2A/H2B nucleosome dimers with all H2A variants. All H2A variants, as well as ectopic and endogenous H2B were assembled into HSV-1 chromatin evenly throughout the genome but canonical H2A was relatively depleted whereas H2A.B was enriched, particularly in the most dynamic viral chromatin. When viral transcription and DNA replication were restricted, H2A.B became as depleted from the viral chromatin through the entire genome as H2A. We propose that lytic HSV-1 nucleosomes are enriched in the dynamic variant H2A.B/H2B dimers to promote HSV-1 chromatin dynamics and transcriptional competency and conclude that the dynamics of HSV-1 chromatin are determined in part by the H2A variants.ImportanceHerpes simplex virus 1 (HSV-1) transcription is epigenetically regulated during latent and lytic infections, and epigenetic inhibitors have been proposed as potential antiviral drugs to modulate latency and reactivation. However, the detailed epigenetic mechanisms of regulation of HSV-1 transcription have not been fully characterized and may differ from those regulating cellular transcription. Whereas lytic HSV-1 chromatin is unusually dynamic, latent silenced HSV-1 chromatin is not. The mechanisms resulting in the unique dynamics of the lytic chromatin remain unknown. Here we identify the enrichment of the highly dynamic histone 2A variant H2A in the most dynamic viral chromatin, which provides a mechanistic understanding of its unique dynamics. Future work to identify the mechanisms of enrichment in H2A.B on the viral chromatin may identify novel druggable epigenetic regulators that modulate HSV-1 latency and reactivation.

Dataset Information

H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A.

Publications

H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A.

Similar Datasets

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