Structure of the histone chaperone CIA/ASF1-double bromodomain complex linking histone modifications and site-specific histone eviction.
Nucleosomes around the promoter region are disassembled for transcription in response to various signals, such as acetylation and methylation of histones. Although the interactions between histone-acetylation-recognizing bromodomains and factors involved in nucleosome disassembly have been reported, no structural basis connecting histone modifications and nucleosome disassembly has been obtained. Here, we determined at 3.3 A resolution the crystal structure of histone chaperone cell cycle gene 1 (CCG1) interacting factor A/antisilencing function 1 (CIA/ASF1) in complex with the double bromodomain in the CCG1/TAF1/TAF(II)250 subunit of transcription factor IID. Structural, biochemical, and biological studies suggested that interaction between double bromodomain and CIA/ASF1 is required for their colocalization, histone eviction, and pol II entry at active promoter regions. Furthermore, the present crystal structure has characteristics that can connect histone acetylation and CIA/ASF1-mediated histone eviction. These findings suggest that the molecular complex between CIA/ASF1 and the double bromodomain plays a key role in site-specific histone eviction at active promoter regions. The model we propose here is the initial structure-based model of the biological signaling from histone modifications to structural change of the nucleosome (hi-MOST model).
Akai
Yusuke
Y
Biomedicinal Information Research Center, National Institute of Advanced Industrial Science and Technology, 2-4-7 Aomi, Koto-ku, Tokyo 135-0064, Japan.
Adachi
Naruhiko
N
Hayashi
Yohei
Y
Eitoku
Masamitsu
M
Sano
Norihiko
N
Natsume
Ryo
R
Kudo
Norio
N
Tanokura
Masaru
M
Senda
Toshiya
T
Horikoshi
Masami
M
D018797:Cell Cycle Proteins / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism; D018360:Crystallography, X-Ray; D006657:Histones / Q000737:chemistry* / Q000378:metabolism; D006801:Humans; D008958:Models, Molecular; D018832:Molecular Chaperones; D009154:Mutation; D011401:Promoter Regions, Genetic; D011485:Protein Binding; D020836:Protein Structure, Quaternary; D017434:Protein Structure, Tertiary
C491641:ASF1A protein, human; D018797:Cell Cycle Proteins; D006657:Histones; D018832:Molecular Chaperones
Science. 2000 May 26;288(5470):1422-5
10827952
Nature. 2009 May 7;459(7243):113-7
19270680
EMBO J. 2000 Nov 15;19(22):6141-9
11080160
Mol Cell. 2006 May 5;22(3):415-22
16678113
Genes Dev. 2000 Apr 15;14(8):951-62
10783167
Nature. 1999 Jun 3;399(6735):491-6
10365964
Curr Biol. 2001 Apr 3;11(7):463-73
11412995
Nat Struct Mol Biol. 2007 Nov;14(11):997-1007
17984962
Mol Cell. 2009 May 14;34(4):405-15
19481521
Mol Cell. 2003 Feb;11(2):353-63
12620224
Mol Cell Biol. 2007 Aug;27(15):5327-35
17526728
Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9334-9
12093919
Curr Opin Struct Biol. 2008 Jun;18(3):282-9
18534842
Mol Cell. 2004 Jun 4;14(5):657-66
15175160
Nat Struct Mol Biol. 2006 Oct;13(10):921-9
16980972
Cell. 2007 Feb 23;128(4):707-19
17320508
Cell. 2007 Feb 23;128(4):693-705
17320507
Nature. 1999 Dec 2;402(6761):555-60
10591219
Cell. 2004 Jan 9;116(1):51-61
14718166
Nat Struct Mol Biol. 2007 Nov;14(11):989-96
17984961
Curr Protoc Mol Biol. 2005 Feb;Chapter 21:Unit 21.3
18265358
J Biol Chem. 2003 Sep 12;278(37):35660-7
12842904
Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489-93
8248135
Nat Struct Mol Biol. 2008 Jul;15(7):738-45
18568037
Mol Cell. 2007 Aug 3;27(3):393-405
17679090
Proc Natl Acad Sci U S A. 2008 Jul 1;105(26):9000-5
18577595
Bioessays. 2000 Sep;22(9):836-45
10944586
Genes Dev. 2001 May 1;15(9):1061-6
11331602
Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12347-52
16895980
Cell Mol Life Sci. 2008 Feb;65(3):414-44
17955179
Mol Cell. 2001 Jan;7(1):13-20
11172707
Nature. 2000 Jan 6;403(6765):41-5
10638745
Mol Cell. 2003 Feb;11(2):365-76
12620225
Genes Cells. 2000 Mar;5(3):221-33
10759893
J Biol Chem. 2004 Aug 13;279(33):35113-20
15192097
Cell. 2007 Feb 23;128(4):721-33
17320509
Mol Cell. 2004 Feb 27;13(4):573-85
14992726
Nature. 1997 Sep 18;389(6648):251-60
9305837
Proc Natl Acad Sci U S A. 2006 May 23;103(21):8060-5
16690741
Cell. 2006 Nov 3;127(3):495-508
17081973
Nature. 2007 Mar 15;446(7133):338-41
17293877
Yeast. 1997 Sep 15;13(11):1029-42
9290207
Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148-52
1946434
Science. 1974 May 24;184(4139):868-71
4825889