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

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

doi:10.1016/j.cell.2013.10.014

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

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

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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 Rtt101^Mms1 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 Rtt101^Mms1 ligase impairs nucleosome assembly and promotes Asf1-H3 interactions. Similar phenotypes occur in human cells in which the ortholog of Rtt101^Mms1, Cul4A^DDB1, 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 language	English (US)
Pages (from-to)	817
Number of pages	1
Journal	Cell
Volume	155
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2013.10.014
State	Published - Nov 7 2013

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2013.10.014

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title = "XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly",

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.",

author = "Junhong Han and Hui Zhang and Honglian Zhang and Zhiquan Wang and Hui Zhou and Zhiguo Zhang",

note = "Funding Information: We thank Drs. Burgess, Lou, Katzmann, van Deursen, Ekker,and Wu and Mr. Dahlin for critical reading of this manuscript. We thank Dr. Kamura for plasmids and Dr. Verreault for a yeast histone purification protocol. This work is supported by NIH grants (GM72719 and GM81838). ",

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doi = "10.1016/j.cell.2013.10.014",

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T1 - XA Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly

AU - Han, Junhong

AU - Zhang, Hui

AU - Zhang, Honglian

AU - Wang, Zhiquan

AU - Zhou, Hui

AU - Zhang, Zhiguo

N1 - Funding Information: We thank Drs. Burgess, Lou, Katzmann, van Deursen, Ekker,and Wu and Mr. Dahlin for critical reading of this manuscript. We thank Dr. Kamura for plasmids and Dr. Verreault for a yeast histone purification protocol. This work is supported by NIH grants (GM72719 and GM81838).

PY - 2013/11/7

Y1 - 2013/11/7

N2 - 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.

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

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