Structural basis of H2A.Z recognition by SRCAP chromatin-remodeling subunit YL1

被引:70
作者
Liang, Xiaoping [1 ,2 ]
Shan, Shan [1 ]
Pan, Lu [1 ,2 ]
Zhao, Jicheng [1 ]
Ranjan, Anand [3 ]
Wang, Feng [4 ]
Zhang, Zhuqiang [1 ]
Huang, Yingzi [1 ]
Feng, Hanqiao [4 ]
Wei, Debbie [4 ]
Huang, Li [1 ,2 ]
Liu, Xuehui [1 ]
Zhong, Qiang [1 ]
Lou, Jizhong [1 ]
Li, Guohong [1 ]
Wu, Carl [3 ,4 ]
Zhou, Zheng [1 ,2 ]
机构
[1] Chinese Acad Sci, Inst Biophys, Natl Lab Biomacromol, Beijing 100080, Peoples R China
[2] Univ Chinese Acad Sci, Beijing, Peoples R China
[3] Howard Hughes Med Inst, Janelia Res Campus, Ashburn, VA USA
[4] NCI, Lab Biochem & Mol Biol, Ctr Canc Res, Bethesda, MD 20892 USA
关键词
NUCLEOSOME CORE PARTICLE; HISTONE CHAPERONE; CRYSTAL-STRUCTURE; REMOVES H2A.Z; BAH DOMAIN; COMPLEX; SWR1; EXCHANGE; ANP32E; REPLACEMENT;
D O I
10.1038/nsmb.3190
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Histone variant H2A.Z, a universal mark of dynamic nucleosomes flanking gene promoters and enhancers, is incorporated into chromatin by SRCAP (SWR1), an ATP-dependent, multicomponent chromatin-remodeling complex. The YL1 (Swc2) subunit of SRCAP (SWR1) plays an essential role in H2A.Z recognition, but how it achieves this has been unclear. Here, we report the crystal structure of the H2A.Z-binding domain of Drosophila melanogaster YL1 (dYL1-Z) in complex with an H2A.Z-H2B dimer at 1.9-angstrom resolution. The dYL1-Z domain adopts a new whip-like structure that wraps over H2A.Z-H2B, and preferential recognition is largely conferred by three residues in loop 2, the hyperacidic patch and the extended alpha C helix of H2A.Z. Importantly, this domain is essential for deposition of budding yeast H2A.Z in vivo and SRCAP (SWR1)-catalyzed histone H2A.Z replacement in vitro. Our studies distinguish YL1-Z from known H2A.Z chaperones and suggest a hierarchical mechanism based on increasing binding affinity facilitating H2A.Z transfer from SRCAP (SWR1) to the nucleosome.
引用
收藏
页码:317 / 323
页数:7
相关论文
共 27 条
[1]   Structural Basis of Silencing: Sir3 BAH Domain in Complex with a Nucleosome at 3.0 Å Resolution [J].
Armache, Karim-Jean ;
Garlick, Joseph D. ;
Canzio, Daniele ;
Narlikar, Geeta J. ;
Kingston, Robert E. .
SCIENCE, 2011, 334 (6058) :977-982
[2]   The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA [J].
Barbera, AJ ;
Chodaparambil, JV ;
Kelley-Clarke, B ;
Joukov, V ;
Walter, JC ;
Luger, K ;
Kaye, KM .
SCIENCE, 2006, 311 (5762) :856-861
[3]   Histone chaperone Anp32e removes H2A.Z from DNA double-strand breaks and promotes nucleosome reorganization and DNA repair [J].
Gursoy-Yuzugullu, Ozge ;
Ayrapetov, Marina K. ;
Price, Brendan D. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (24) :7507-7512
[4]   Histone Variants and Epigenetics [J].
Henikoff, Steven ;
Smith, M. Mitchell .
COLD SPRING HARBOR PERSPECTIVES IN BIOLOGY, 2015, 7 (01)
[5]   Structural basis of histone H2A-H2B recognition by the essential chaperone FACT [J].
Hondele, Maria ;
Stuwe, Tobias ;
Hassler, Markus ;
Halbach, Felix ;
Bowman, Andrew ;
Zhang, Elisa T. ;
Nijmeijer, Bianca ;
Kotthoff, Christiane ;
Rybin, Vladimir ;
Amlacher, Stefan ;
Hurt, Ed ;
Ladurner, Andreas G. .
NATURE, 2013, 499 (7456) :111-+
[6]   The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer [J].
Hong, Jingjun ;
Feng, Hanqiao ;
Wang, Feng ;
Ranjan, Anand ;
Chen, Jianhong ;
Jiang, Jiansheng ;
Ghirlando, Rodolfo ;
Xiao, T. Sam ;
Wu, Carl ;
Bai, Yawen .
MOLECULAR CELL, 2014, 53 (03) :498-505
[7]   A Conserved Mechanism for Centromeric Nucleosome Recognition by Centromere Protein CENP-C [J].
Kato, Hidenori ;
Jiang, Jiansheng ;
Zhou, Bing-Rui ;
Rozendaal, Marieke ;
Feng, Hanqiao ;
Ghirlando, Rodolfo ;
Xiao, T. Sam ;
Straight, Aaron F. ;
Bai, Yawen .
SCIENCE, 2013, 340 (6136) :1110-1113
[8]   Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR [J].
Kato, Hidenori ;
van Ingen, Hugo ;
Zhou, Bing-Rui ;
Feng, Hanqiao ;
Bustin, Michael ;
Kay, Lewis E. ;
Bai, Yawen .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2011, 108 (30) :12283-12288
[9]   FACT Disrupts Nucleosome Structure by Binding H2A-H2B with Conserved Peptide Motifs [J].
Kemble, David J. ;
McCullough, Laura L. ;
Whitby, Frank G. ;
Formosa, Tim ;
Hill, Christopher P. .
MOLECULAR CELL, 2015, 60 (02) :294-306
[10]   A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin [J].
Kobor, MS ;
Venkatasubrahmanyam, S ;
Meneghini, MD ;
Gin, JW ;
Jennings, JL ;
Link, AJ ;
Madhani, HD ;
Rine, J .
PLOS BIOLOGY, 2004, 2 (05) :587-599