XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly

Junhong Han, Hui Zhang, Honglian Zhang, Zhiquan Wang, Hui Zhou, Zhiguo Zhang

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

Summary Nucleosome assembly following DNA replication and gene transcription is important to maintain genome stability and epigenetic information. Newly synthesized histones H3-H4 first bind histone chaperone Asf1 and are then transferred to other chaperones for nucleosome assembly. However, it is unknown how H3-H4 is transferred from the Asf1-H3-H4 complex to other chaperones because Asf1 binds H3-H4 with high affinity. Here, we show that yeast Rtt101Mms1 E3 ubiquitin ligase preferentially binds and ubiquitylates new histone H3 acetylated at lysine 56. Inactivation of Rtt101 or mutating H3 lysine residues ubiquitylated by the Rtt101Mms1 ligase impairs nucleosome assembly and promotes Asf1-H3 interactions. Similar phenotypes occur in human cells in which the ortholog of Rtt101Mms1, Cul4ADDB1, is depleted. These results indicate that the transfer of H3-H4 from the Asf1-H3-H4 complex to other histone chaperones is regulated by a conserved E3 ligase and provide evidence for crosstalk between histone acetylation and ubiquitylation in nucleosome assembly.

Original languageEnglish (US)
JournalCell
Volume155
Issue number4
DOIs
StatePublished - Nov 7 2013

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Ubiquitin-Protein Ligases
Nucleosomes
Histones
Histone Chaperones
Hand
Lysine
Genes
Acetylation
Genomic Instability
Ubiquitination
Transcription
Ligases
Crosstalk
DNA Replication
Epigenomics
Yeast
Yeasts
Cells
Phenotype
DNA

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly. / Han, Junhong; Zhang, Hui; Zhang, Honglian; Wang, Zhiquan; Zhou, Hui; Zhang, Zhiguo.

In: Cell, Vol. 155, No. 4, 07.11.2013.

Research output: Contribution to journalArticle

Han, J, Zhang, H, Zhang, H, Wang, Z, Zhou, H & Zhang, Z 2013, 'XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly', Cell, vol. 155, no. 4. https://doi.org/10.1016/j.cell.2013.10.014
Han, Junhong ; Zhang, Hui ; Zhang, Honglian ; Wang, Zhiquan ; Zhou, Hui ; Zhang, Zhiguo. / XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly. In: Cell. 2013 ; Vol. 155, No. 4.
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AU - Zhang, Zhiguo

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AB - Summary Nucleosome assembly following DNA replication and gene transcription is important to maintain genome stability and epigenetic information. Newly synthesized histones H3-H4 first bind histone chaperone Asf1 and are then transferred to other chaperones for nucleosome assembly. However, it is unknown how H3-H4 is transferred from the Asf1-H3-H4 complex to other chaperones because Asf1 binds H3-H4 with high affinity. Here, we show that yeast Rtt101Mms1 E3 ubiquitin ligase preferentially binds and ubiquitylates new histone H3 acetylated at lysine 56. Inactivation of Rtt101 or mutating H3 lysine residues ubiquitylated by the Rtt101Mms1 ligase impairs nucleosome assembly and promotes Asf1-H3 interactions. Similar phenotypes occur in human cells in which the ortholog of Rtt101Mms1, Cul4ADDB1, is depleted. These results indicate that the transfer of H3-H4 from the Asf1-H3-H4 complex to other histone chaperones is regulated by a conserved E3 ligase and provide evidence for crosstalk between histone acetylation and ubiquitylation in nucleosome assembly.

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