XNucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement

Cell

Volumn 154, Issue 6, 2013, Pages 1232-

  Ranjan, Anand ^a   Mizuguchi, Gaku ^b   Fitzgerald, Peter C ^a   Wei, Debbie ^a   Wang, Feng ^a   Huang, Yingzi ^a   Luk, Ed ^c   Woodcock, Christopher L ^d   Wu, Carl ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DEOXYRIBONUCLEASE I; FLUORESCENT DYE; GENERAL TRANSCRIPTION FACTOR; HISTONE ACETYLTRANSFERASE; HISTONE H2AZ; MULTIPROTEIN COMPLEX; NAKED DNA; RESTRICTION ENDONUCLEASE; SWR1 PROTEIN; TATA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING; DROSOPHILA; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; GENE MAPPING; GENETIC ASSOCIATION; HISTONE ACETYLATION; HISTONE MODIFICATION; INTERACTIONS WITH DNA; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE; SCANNING TRANSMISSION ELECTRON MICROSCOPY;

EUKARYOTA;

EID: 84884214357     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.08.005     Document Type: Article

References (77)

1. I. Albert, T.N. Mavrich, L.P. Tomsho, J. Qi, S.J. Zanton, S.C. Schuster, and B.F. Pugh Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome Nature 446 2007 572 576
2. S.G. Alkhatib, and J.W. Landry The nucleosome remodeling factor FEBS Lett. 585 2011 3197 3207
3. M. Altaf, A. Auger, J. Monnet-Saksouk, J. Brodeur, S. Piquet, M. Cramet, N. Bouchard, N. Lacoste, R.T. Utley, L. Gaudreau, and J. Côté NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex J. Biol. Chem. 285 2010 15966 15977
4. M.L. Angus-Hill, A. Schlichter, D. Roberts, H. Erdjument-Bromage, P. Tempst, and B.R. Cairns A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control Mol. Cell 7 2001 741 751
5. G. Arents, R.W. Burlingame, B.C. Wang, W.E. Love, and E.N. Moudrianakis The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix Proc. Natl. Acad. Sci. USA 88 1991 10148 10152
6. G. Badis, E.T. Chan, H. van Bakel, L. Pena-Castillo, D. Tillo, K. Tsui, C.D. Carlson, A.J. Gossett, M.J. Hasinoff, and C.L. Warren A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters Mol. Cell 32 2008 878 887
7. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
8. B.E. Bernstein, C.L. Liu, E.L. Humphrey, E.O. Perlstein, and S.L. Schreiber Global nucleosome occupancy in yeast Genome Biol. 5 2004 R62
9. C.E. Brown, L. Howe, K. Sousa, S.C. Alley, M.J. Carrozza, S. Tan, and J.L. Workman Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit Science 292 2001 2333 2337
10. Y. Cai, J. Jin, L. Florens, S.K. Swanson, T. Kusch, B. Li, J.L. Workman, M.P. Washburn, R.C. Conaway, and J.W. Conaway The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes J. Biol. Chem. 280 2005 13665 13670
11. B.R. Cairns, A. Schlichter, H. Erdjument-Bromage, P. Tempst, R.D. Kornberg, and F. Winston Two functionally distinct forms of the RSC nucleosome-remodeling complex, containing essential AT hook, BAH, and bromodomains Mol. Cell 4 1999 715 723
12. H.A. Cole, B.H. Howard, and D.J. Clark The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere Proc. Natl. Acad. Sci. USA 108 2011 12687 12692
13. G. Da, J. Lenkart, K. Zhao, R. Shiekhattar, B.R. Cairns, and R. Marmorstein Structure and function of the SWIRM domain, a conserved protein module found in chromatin regulatory complexes Proc. Natl. Acad. Sci. USA 103 2006 2057 2062
14. N. Dhillon, M. Oki, S.J. Szyjka, O.M. Aparicio, and R.T. Kamakaka H2A.Z functions to regulate progression through the cell cycle Mol. Cell. Biol. 26 2006 489 501
15. M. Durant, and B.F. Pugh NuA4-directed chromatin transactions throughout the Saccharomyces cerevisiae genome Mol. Cell. Biol. 27 2007 5327 5335
16. J.Y. Fan, F. Gordon, K. Luger, J.C. Hansen, and D.J. Tremethick The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states Nat. Struct. Biol. 9 2002 172 176
17. X. Fan, Z. Moqtaderi, Y. Jin, Y. Zhang, X.S. Liu, and K. Struhl Nucleosome depletion at yeast terminators is not intrinsic and can occur by a transcriptional mechanism linked to 3′-end formation Proc. Natl. Acad. Sci. USA 107 2010 17945 17950
18. C.L. Gallant-Behm, M.R. Ramsey, C.L. Bensard, I. Nojek, J. Tran, M. Liu, L.W. Ellisen, and J.M. Espinosa ΔNp63α represses anti-proliferative genes via H2A.Z deposition Genes Dev. 26 2012 2325 2336
19. A.C. Gavin, P. Aloy, P. Grandi, R. Krause, M. Boesche, M. Marzioch, C. Rau, L.J. Jensen, S. Bastuck, and B. Dümpelfeld Proteome survey reveals modularity of the yeast cell machinery Nature 440 2006 631 636
20. J.E. Halley, T. Kaplan, A.Y. Wang, M.S. Kobor, and J. Rine Roles for H2A.Z and its acetylation in GAL1 transcription and gene induction, but not GAL1-transcriptional memory PLoS Biol. 8 2010 e1000401
21. P.D. Hartley, and H.D. Madhani Mechanisms that specify promoter nucleosome location and identity Cell 137 2009 445 458
22. F.C. Holstege, E.G. Jennings, J.J. Wyrick, T.I. Lee, C.J. Hengartner, M.R. Green, T.R. Golub, E.S. Lander, and R.A. Young Dissecting the regulatory circuitry of a eukaryotic genome Cell 95 1998 717 728
23. I. Horikawa, H. Tanaka, Y. Yuasa, M. Suzuki, and M. Oshimura Molecular cloning of a novel human cDNA on chromosome 1q21 and its mouse homolog encoding a nuclear protein with DNA-binding ability Biochem. Biophys. Res. Commun. 208 1995 999 1007
24. C. Jiang, and B.F. Pugh A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome Genome Biol. 10 2009 R109
25. C. Jin, and G. Felsenfeld Nucleosome stability mediated by histone variants H3.3 and H2A.Z Genes Dev. 21 2007 1519 1529
26. M. Kalocsay, N.J. Hiller, and S. Jentsch Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break Mol. Cell 33 2009 335 343
27. M.C. Keogh, T.A. Mennella, C. Sawa, S. Berthelet, N.J. Krogan, A. Wolek, V. Podolny, L.R. Carpenter, J.F. Greenblatt, K. Baetz, and S. Buratowski The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4 Genes Dev. 20 2006 660 665
28. M.S. Kobor, S. Venkatasubrahmanyam, M.D. Meneghini, J.W. Gin, J.L. Jennings, A.J. Link, H.D. Madhani, and J. Rine A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin PLoS Biol. 2 2004 E131
29. N.J. Krogan, M.C. Keogh, N. Datta, C. Sawa, O.W. Ryan, H. Ding, R.A. Haw, J. Pootoolal, A. Tong, and V. Canadien A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1 Mol. Cell 12 2003 1565 1576
30. N.J. Krogan, K. Baetz, M.C. Keogh, N. Datta, C. Sawa, T.C. Kwok, N.J. Thompson, M.G. Davey, J. Pootoolal, and T.R. Hughes 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 101 2004 13513 13518
31. T. Kusch, L. Florens, W.H. Macdonald, S.K. Swanson, R.L. Glaser, J.R. Yates 3rd, S.M. Abmayr, M.P. Washburn, and J.L. Workman Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions Science 306 2004 2084 2087
32. S.Y. Kwon, H. Xiao, C. Wu, and P. Badenhorst Alternative splicing of NURF301 generates distinct NURF chromatin remodeling complexes with altered modified histone binding specificities PLoS Genet. 5 2009 e1000574
33. A.G. Ladurner, C. Inouye, R. Jain, and R. Tjian Bromodomains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries Mol. Cell 11 2003 365 376
34. J.W. Landry, S. Banerjee, B. Taylor, P.D. Aplan, A. Singer, and C. Wu Chromatin remodeling complex NURF regulates thymocyte maturation Genes Dev. 25 2011 275 286
35. B. Li, M. Gogol, M. Carey, D. Lee, C. Seidel, and J.L. Workman Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin Science 316 2007 1050 1054
36. P.T. Lowary, and J. Widom New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning J. Mol. Biol. 276 1998 19 42
37. K. Luger, A.W. Mäder, R.K. Richmond, D.F. Sargent, and T.J. Richmond Crystal structure of the nucleosome core particle at 2.8 A resolution Nature 389 1997 251 260
38. E. Luk, A. Ranjan, P.C. Fitzgerald, G. Mizuguchi, Y. Huang, D. Wei, and C. Wu Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome Cell 143 2010 725 736
39. O. Matangkasombut, and S. Buratowski Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation Mol. Cell 11 2003 353 363
40. T.N. Mavrich, I.P. Ioshikhes, B.J. Venters, C. Jiang, L.P. Tomsho, J. Qi, S.C. Schuster, I. Albert, and B.F. Pugh A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome Genome Res. 18 2008 1073 1083
41. T.N. Mavrich, C. Jiang, I.P. Ioshikhes, X. Li, B.J. Venters, S.J. Zanton, L.P. Tomsho, J. Qi, R.L. Glaser, and S.C. Schuster Nucleosome organization in the Drosophila genome Nature 453 2008 358 362
42. M.D. Meneghini, M. Wu, and H.D. Madhani Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin Cell 112 2003 725 736
43. C.B. Millar, and M. Grunstein Genome-wide patterns of histone modifications in yeast Nat. Rev. Mol. Cell Biol. 7 2006 657 666
44. G. Mizuguchi, X. Shen, J. Landry, W.H. Wu, S. Sen, and C. Wu ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex Science 303 2004 343 348
45. M. Morillo-Huesca, M. Clemente-Ruiz, E. Andújar, and F. Prado The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z PLoS ONE 5 2010 e12143
46. H. Neil, C. Malabat, Y. d'Aubenton-Carafa, Z. Xu, L.M. Steinmetz, and A. Jacquier Widespread bidirectional promoters are the major source of cryptic transcripts in yeast Nature 457 2009 1038 1042
47. S. Neph, J. Vierstra, A.B. Stergachis, A.P. Reynolds, E. Haugen, B. Vernot, R.E. Thurman, S. John, R. Sandstrom, and A.K. Johnson An expansive human regulatory lexicon encoded in transcription factor footprints Nature 489 2012 83 90
48. M. Ptashne Epigenetics: core misconcept Proc. Natl. Acad. Sci. USA 110 2013 7101 7103
49. M. Radman-Livaja, and O.J. Rando Nucleosome positioning: how is it established, and why does it matter? Dev. Biol. 339 2010 258 266
50. R.M. Raisner, P.D. Hartley, M.D. Meneghini, M.Z. Bao, C.L. Liu, S.L. Schreiber, O.J. Rando, and H.D. Madhani Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin Cell 123 2005 233 248
51. O.J. Rando Combinatorial complexity in chromatin structure and function: revisiting the histone code Curr. Opin. Genet. Dev. 22 2012 148 155
52. D. Rangasamy, I. Greaves, and D.J. Tremethick RNA interference demonstrates a novel role for H2A.Z in chromosome segregation Nat. Struct. Mol. Biol. 11 2004 650 655
53. A.J. Ruthenburg, H. Li, T.A. Milne, S. Dewell, R.K. McGinty, M. Yuen, B. Ueberheide, Y. Dou, T.W. Muir, D.J. Patel, and C.D. Allis Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions Cell 145 2011 692 706
54. M.S. Santisteban, T. Kalashnikova, and M.M. Smith Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes Cell 103 2000 411 422
55. D.E. Schones, K. Cui, S. Cuddapah, T.Y. Roh, A. Barski, Z. Wang, G. Wei, and K. Zhao Dynamic regulation of nucleosome positioning in the human genome Cell 132 2008 887 898
56. R.K. Suto, M.J. Clarkson, D.J. Tremethick, and K. Luger Crystal structure of a nucleosome core particle containing the variant histone H2A.Z Nat. Struct. Biol. 7 2000 1121 1124
57. R.E. Thurman, E. Rynes, R. Humbert, J. Vierstra, M.T. Maurano, E. Haugen, N.C. Sheffield, A.B. Stergachis, H. Wang, and B. Vernot The accessible chromatin landscape of the human genome Nature 489 2012 75 82
58. I. Tirosh, and N. Barkai Two strategies for gene regulation by promoter nucleosomes Genome Res. 18 2008 1084 1091
59. B.J. Venters, and B.F. Pugh A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome Genome Res. 19 2009 360 371
60. V.M. Weake, and J.L. Workman SAGA function in tissue-specific gene expression Trends Cell Biol. 22 2012 177 184
61. A. Weiner, A. Hughes, M. Yassour, O.J. Rando, and N. Friedman High-resolution nucleosome mapping reveals transcription-dependent promoter packaging Genome Res. 20 2010 90 100
62. C. Wu The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I Nature 286 1980 854 860
63. C. Wu Two protein-binding sites in chromatin implicated in the activation of heat-shock genes Nature 309 1984 229 234
64. W.H. Wu, S. Alami, E. Luk, C.H. Wu, S. Sen, G. Mizuguchi, D. Wei, and C. Wu Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange Nat. Struct. Mol. Biol. 12 2005 1064 1071
65. W.H. Wu, C.H. Wu, A. Ladurner, G. Mizuguchi, D. Wei, H. Xiao, E. Luk, A. Ranjan, and C. Wu N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex J. Biol. Chem. 284 2009 6200 6207
66. J. Wysocka, T. Swigut, H. Xiao, T.A. Milne, S.Y. Kwon, J. Landry, M. Kauer, A.J. Tackett, B.T. Chait, and P. Badenhorst A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling Nature 442 2006 86 90
67. Y. Xi, J. Yao, R. Chen, W. Li, and X. He Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation Genome Res. 21 2011 718 724
68. H. Xiao, R. Sandaltzopoulos, H.M. Wang, A. Hamiche, R. Ranallo, K.M. Lee, D. Fu, and C. Wu Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions Mol. Cell 8 2001 531 543
69. Z. Xu, W. Wei, J. Gagneur, F. Perocchi, S. Clauder-Münster, J. Camblong, E. Guffanti, F. Stutz, W. Huber, and L.M. Steinmetz Bidirectional promoters generate pervasive transcription in yeast Nature 457 2009 1033 1037
70. G.C. Yuan, Y.J. Liu, M.F. Dion, M.D. Slack, L.F. Wu, S.J. Altschuler, and O.J. Rando Genome-scale identification of nucleosome positions in S. cerevisiae Science 309 2005 626 630
71. H. Zhang, D.N. Roberts, and B.R. Cairns Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss Cell 123 2005 219 231
72. S.K. Kurdistani, and M. Grunstein In vivo protein-protein and protein-DNA crosslinking for genomewide binding microarray Methods 31 2003 90 95
73. K. Luger, T.J. Rechsteiner, and T.J. Richmond Expression and purification of recombinant histones and nucleosome reconstitution Methods Mol. Biol. 119 1999 1 16
74. G. Mizuguchi, W.H. Wu, S. Alami, and E. Luk Biochemical assay for histone H2A.Z replacement by the yeast SWR1 chromatin remodeling complex Methods Enzymol. 512 2012 275 291
75. A.J. Saldanha Java Treeview - extensible visualization of microarray data Bioinformatics 20 2004 3246 3248
76. J.C. Vary Jr., T.G. Fazzio, and T. Tsukiyama Assembly of yeast chromatin using ISWI complexes Methods Enzymol. 375 2004 88 102
77. Y. Zhang, Z. Moqtaderi, B.P. Rattner, G. Euskirchen, M. Snyder, J.T. Kadonaga, X.S. Liu, and K. Struhl Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo Nat. Struct. Mol. Biol. 16 2009 847 852