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

Molecular Cell

Volumn 53, Issue 3, 2014, Pages 498-505

  Hong, Jingjun ^a   Feng, Hanqiao ^a   Wang, Feng ^a   Ranjan, Anand ^a   Chen, Jianhong ^a   Jiang, Jiansheng ^b   Ghirlando, Rodolfo ^c   Xiao, T Sam ^b   Wu, Carl ^a,d   Bai, Yawen ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DIMER; HISTONE H2AZ; HISTONE H2B; SWR1 PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVE SITE; IN VITRO STUDY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOSOME; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; CATALYTIC SUBUNIT SWR1; CRYSTAL STRUCTURE; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; NUCLEAR MAGNETIC RESONANCE; PROMOTER REGION; PROTEIN MOTIF;

EUKARYOTA; MAMMALIA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HISTONES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; X-RAY DIFFRACTION;

EID: 84893460190     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.01.010     Document Type: Article

References (39)

1. Ausió J. Histone variants-the structure behind the function. Brief. Funct. Genomics Proteomics 2006, 5:228-243.
2. Cairns B.R. The logic of chromatin architecture and remodelling at promoters. Nature 2009, 461:193-198.
3. Carr A.M., Dorrington S.M., Hindley J., Phear G.A., Aves S.J., Nurse P. Analysis of a histone H2A variant from fission yeast: evidence for a role in chromosome stability. Mol. Gen. Genet. 1994, 245:628-635.
4. Eberharter A., Becker P.B. ATP-dependent nucleosome remodelling: factors and functions. J.Cell Sci. 2004, 117:3707-3711.
5. Elsässer S.J., Huang H., Lewis P.W., Chin J.W., Allis C.D., Patel D.J. DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 2012, 491:560-565.
6. Fischle W., Wang Y., Allis C.D. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 2003, 15:172-183.
7. Gévry N., Chan H.M., Laflamme L., Livingston D.M., Gaudreau L. p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev. 2007, 21:1869-1881.
8. Hondele M., Stuwe T., Hassler M., Halbach F., Bowman A., Zhang E.T., Nijmeijer B., Kotthoff C., Rybin V., Amlacher S., et al. Structural basis of histone H2A-H2B recognition by the essential chaperone FACT. Nature 2013, 499:111-114.
9. Hu H., Liu Y., Wang M., Fang J., Huang H., Yang N., Li Y., Wang J., Yao X., Shi Y., et al. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 2011, 25:901-906.
10. Hua S., Kallen C.B., Dhar R., Baquero M.T., Mason C.E., Russell B.A., Shah P.K., Liu J., Khramtsov A., Tretiakova M.S., et al. Genomic analysis of estrogen cascade reveals histone variant H2A.Z associated with breast cancer progression. Mol. Syst. Biol. 2008, 4:188.
11. Jackson J.D., Gorovsky M.A. Histone H2A.Z has a conserved function that is distinct from that of the major H2A sequence variants. Nucleic Acids Res. 2000, 28:3811-3816.
12. Jiang C., Pugh B.F. Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet. 2009, 10:161-172.
13. Kobor M.S., Venkatasubrahmanyam S., Meneghini M.D., Gin J.W., Jennings J.L., Link A.J., Madhani H.D., Rine J. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2004, 2:E131.
14. Kornberg R.D. Chromatin structure: a repeating unit of histones and DNA. Science 1974, 184:868-871.
15. Kornberg R.D., Thomas J.O. Chromatin structure; oligomers of the histones. Science 1974, 184:865-868.
16. Krogan N.J., Keogh M.C., Datta N., Sawa C., Ryan O.W., Ding H., Haw R.A., Pootoolal J., Tong A., Canadien V., et al. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 2003, 12:1565-1576.
17. Krogan N.J., Baetz K., Keogh M.C., Datta N., Sawa C., Kwok T.C., Thompson N.J., Davey M.G., Pootoolal J., Hughes T.R., et al. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc. Natl. Acad. Sci. USA 2004, 101:13513-13518.
18. Liu C.P., Xiong C., Wang M., Yu Z., Yang N., Chen P., Zhang Z., Li G., Xu R.M. Structure of the variant histone H3.3-H4 heterodimer in complex with its chaperone DAXX. Nat. Struct. Mol. Biol. 2012, 19:1287-1292.
19. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251-260.
20. Luk E., Vu N.D., Patteson K., Mizuguchi G., Wu W.H., Ranjan A., Backus J., Sen S., Lewis M., Bai Y., Wu C. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 2007, 25:357-368.
21. Luk E., Ranjan A., Fitzgerald P.C., Mizuguchi G., Huang Y., Wei D., Wu C. Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 2010, 143:725-736.
22. Meneghini M.D., Wu M., Madhani H.D. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 2003, 112:725-736.
23. Mizuguchi G., Shen X., Landry J., Wu W.H., Sen S., Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 2004, 303:343-348.
24. Morrison A.J., Shen X. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 2009, 10:373-384.
25. Rando O.J., Chang H.Y. Genome-wide views of chromatin structure. Annu. Rev. Biochem. 2009, 78:245-271.
26. Rangasamy D. Histone variant H2A.Z can serve as a new target for breast cancer therapy. Curr. Med. Chem. 2010, 17:3155-3161.
27. Ranjan A., Mizuguchi G., FitzGerald P.C., Wei D., Wang F., Huang Y., Luk E., Woodcock C.L., Wu C. Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 2013, 154:1232-1245.
28. Ruhl D.D., Jin J., Cai Y., Swanson S., Florens L., Washburn M.P., Conaway R.C., Conaway J.W., Chrivia J.C. Purification of a human SRCAP complex that remodels chromatin by incorporating the histone variant H2A.Z into nucleosomes. Biochemistry 2006, 45:5671-5677.
29. Santisteban M.S., Kalashnikova T., Smith M.M. Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes. Cell 2000, 103:411-422.
30. Svotelis A., Gévry N., Grondin G., Gaudreau L. H2A.Z overexpression promotes cellular proliferation of breast cancer cells. Cell Cycle 2010, 9:364-370.
31. Venters B.J., Pugh B.F. A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res. 2009, 19:360-371.
32. Watanabe S., Radman-Livaja M., Rando O.J., Peterson C.L. A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 2013, 340:195-199.
33. Weiner A., Hughes A., Yassour M., Rando O.J., Friedman N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res. 2010, 20:90-100.
34. Wollmann P., Cui S., Viswanathan R., Berninghausen O., Wells M.N., Moldt M., Witte G., Butryn A., Wendler P., Beckmann R., et al. Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 2011, 475:403-407.
35. Wu W.H., Alami S., Luk E., Wu C.H., Sen S., Mizuguchi G., Wei D., Wu C. Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 2005, 12:1064-1071.
36. Wu W.H., Wu C.H., Ladurner A., Mizuguchi G., Wei D., Xiao H., Luk E., Ranjan A., Wu C. N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J.Biol. Chem. 2009, 284:6200-6207.
37. Zhou Z., Feng H., Hansen D.F., Kato H., Luk E., Freedberg D.I., Kay L.E., Wu C., Bai Y. NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat. Struct. Mol. Biol. 2008, 15:868-869.
38. Zhou Z., Feng H., Zhou B.R., Ghirlando R., Hu K., Zwolak A., Miller Jenkins L.M., Xiao H., Tjandra N., Wu C., Bai Y. Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 2011, 472:234-237.
39. Zofall M., Fischer T., Zhang K., Zhou M., Cui B., Veenstra T.D., Grewal S.I. Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature 2009, 461:419-422.