The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer

Jingjun Hong; Hanqiao Feng; Feng Wang; Anand Ranjan; Jianhong Chen; Jiansheng Jiang; Rodolfo Ghirlando; T. Sam Xiao; Carl Wu; Yawen Bai

doi:10.1016/j.molcel.2014.01.010

The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer

Jingjun Hong
, Hanqiao Feng
, Feng Wang
, Anand Ranjan
, Jianhong Chen
, Jiansheng Jiang
, Rodolfo Ghirlando
, T. Sam Xiao
, Carl Wu
, Yawen Bai

Research output: Contribution to journal › Article › peer-review

Abstract

Histone variant H2A.Z-containing nucleosomes exist at most eukaryotic promoters and play important roles in gene transcription and genome stability. The multisubunit nucleosome-remodeling enzyme complex SWR1, conserved from yeast to mammals, catalyzes the ATP-dependent replacement of histone H2A in canonical nucleosomes with H2A.Z. How SWR1 catalyzes the replacement reaction is largely unknown. Here, we determined the crystal structure of the N-terminal region (599-627) of the catalytic subunit Swr1, termed Swr1-Z domain, in complex with the H2A.Z-H2B dimer at 1.78Å resolution. The Swr1-Z domain forms a 3₁₀ helix and an irregular chain. A conserved LxxLF motif in the Swr1-Z 3₁₀ helix specifically recognizes the αC helix of H2A.Z. Our results show that the Swr1-Z domain can deliver the H2A.Z-H2B dimer to the DNA-(H3-H4)₂ tetrasome to form the nucleosome by a histone chaperone mechanism.

Original language	English (US)
Pages (from-to)	498-505
Number of pages	8
Journal	Molecular cell
Volume	53
Issue number	3
DOIs	https://doi.org/10.1016/j.molcel.2014.01.010
State	Published - Feb 6 2014
Externally published	Yes

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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10.1016/j.molcel.2014.01.010

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@article{7ecedc1282e0424e8d2c994e081aa9d8,

title = "The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer",

abstract = "Histone variant H2A.Z-containing nucleosomes exist at most eukaryotic promoters and play important roles in gene transcription and genome stability. The multisubunit nucleosome-remodeling enzyme complex SWR1, conserved from yeast to mammals, catalyzes the ATP-dependent replacement of histone H2A in canonical nucleosomes with H2A.Z. How SWR1 catalyzes the replacement reaction is largely unknown. Here, we determined the crystal structure of the N-terminal region (599-627) of the catalytic subunit Swr1, termed Swr1-Z domain, in complex with the H2A.Z-H2B dimer at 1.78{\AA} resolution. The Swr1-Z domain forms a 310 helix and an irregular chain. A conserved LxxLF motif in the Swr1-Z 310 helix specifically recognizes the αC helix of H2A.Z. Our results show that the Swr1-Z domain can deliver the H2A.Z-H2B dimer to the DNA-(H3-H4)2 tetrasome to form the nucleosome by a histone chaperone mechanism.",

author = "Jingjun Hong and Hanqiao Feng and Feng Wang and Anand Ranjan and Jianhong Chen and Jiansheng Jiang and Rodolfo Ghirlando and Xiao, \{T. Sam\} and Carl Wu and Yawen Bai",

note = "Funding Information: We thank the staff at the Advanced Photon Source (beamline 23-ID) for technical support, S. Li for protein purification, D. Wei for purification of SWR1, Dr. B. Zhou for assistance in ITC data collection and analysis, and Dr. J. Barrowman for editing the manuscript. This research was supported by the Intramural Research Programs of the National Cancer Institute (J.H., H.F., F.W., A.R., J.C., C.W., and Y.B.), the National Institute of Allergy and Infectious Diseases (J.J. and T.S.X.), and the National Institute of Diabetes and Digestive and Kidney Diseases (R.G.), National Institutes of Health, the Janelia Farm Research Campus of Howard Hughes Medical Institute (C.W.) as well as National Cancer Institute grant Y1-CO-1020, National Institute of General Medical Sciences grant Y1-GM-1104, and U.S. Department of Energy grant DE-AC02-06CH11357 (Advanced Photon Source). ",

year = "2014",

month = feb,

day = "6",

doi = "10.1016/j.molcel.2014.01.010",

language = "English (US)",

volume = "53",

pages = "498--505",

journal = "Molecular cell",

issn = "1097-2765",

publisher = "Cell Press",

number = "3",

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T1 - The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer

AU - Hong, Jingjun

AU - Feng, Hanqiao

AU - Wang, Feng

AU - Ranjan, Anand

AU - Chen, Jianhong

AU - Jiang, Jiansheng

AU - Ghirlando, Rodolfo

AU - Xiao, T. Sam

AU - Wu, Carl

AU - Bai, Yawen

N1 - Funding Information: We thank the staff at the Advanced Photon Source (beamline 23-ID) for technical support, S. Li for protein purification, D. Wei for purification of SWR1, Dr. B. Zhou for assistance in ITC data collection and analysis, and Dr. J. Barrowman for editing the manuscript. This research was supported by the Intramural Research Programs of the National Cancer Institute (J.H., H.F., F.W., A.R., J.C., C.W., and Y.B.), the National Institute of Allergy and Infectious Diseases (J.J. and T.S.X.), and the National Institute of Diabetes and Digestive and Kidney Diseases (R.G.), National Institutes of Health, the Janelia Farm Research Campus of Howard Hughes Medical Institute (C.W.) as well as National Cancer Institute grant Y1-CO-1020, National Institute of General Medical Sciences grant Y1-GM-1104, and U.S. Department of Energy grant DE-AC02-06CH11357 (Advanced Photon Source).

PY - 2014/2/6

Y1 - 2014/2/6

N2 - Histone variant H2A.Z-containing nucleosomes exist at most eukaryotic promoters and play important roles in gene transcription and genome stability. The multisubunit nucleosome-remodeling enzyme complex SWR1, conserved from yeast to mammals, catalyzes the ATP-dependent replacement of histone H2A in canonical nucleosomes with H2A.Z. How SWR1 catalyzes the replacement reaction is largely unknown. Here, we determined the crystal structure of the N-terminal region (599-627) of the catalytic subunit Swr1, termed Swr1-Z domain, in complex with the H2A.Z-H2B dimer at 1.78Å resolution. The Swr1-Z domain forms a 310 helix and an irregular chain. A conserved LxxLF motif in the Swr1-Z 310 helix specifically recognizes the αC helix of H2A.Z. Our results show that the Swr1-Z domain can deliver the H2A.Z-H2B dimer to the DNA-(H3-H4)2 tetrasome to form the nucleosome by a histone chaperone mechanism.

AB - Histone variant H2A.Z-containing nucleosomes exist at most eukaryotic promoters and play important roles in gene transcription and genome stability. The multisubunit nucleosome-remodeling enzyme complex SWR1, conserved from yeast to mammals, catalyzes the ATP-dependent replacement of histone H2A in canonical nucleosomes with H2A.Z. How SWR1 catalyzes the replacement reaction is largely unknown. Here, we determined the crystal structure of the N-terminal region (599-627) of the catalytic subunit Swr1, termed Swr1-Z domain, in complex with the H2A.Z-H2B dimer at 1.78Å resolution. The Swr1-Z domain forms a 310 helix and an irregular chain. A conserved LxxLF motif in the Swr1-Z 310 helix specifically recognizes the αC helix of H2A.Z. Our results show that the Swr1-Z domain can deliver the H2A.Z-H2B dimer to the DNA-(H3-H4)2 tetrasome to form the nucleosome by a histone chaperone mechanism.

UR - https://www.scopus.com/pages/publications/84893460190

UR - https://www.scopus.com/pages/publications/84893460190#tab=citedBy

U2 - 10.1016/j.molcel.2014.01.010

DO - 10.1016/j.molcel.2014.01.010

M3 - Article

C2 - 24507717

AN - SCOPUS:84893460190

SN - 1097-2765

VL - 53

SP - 498

EP - 505

JO - Molecular cell

JF - Molecular cell

IS - 3

ER -

The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer

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