Distortion of histone octamer core promotes nucleosome mobilization by a chromatin remodeler

Science

Volumn 355, Issue 6322, 2017, Pages

  Sinha, Kalyan K ^a   Gross, John D ^a   Narlikar, Geeta J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE H3; HISTONE H4; ISOLEUCINE; LEUCINE; VALINE; 2-FLUORO-ADP; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CHROMATIN; DNA; DNA BINDING PROTEIN; NONHISTONE PROTEIN; NUCLEOSOME; RSC COMPLEX, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

CHROMOSOME; DNA; ENZYME; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE; PROTEIN; SPECTROSCOPY;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DISSOCIATION RATE CONSTANT; DNA FLANKING REGION; DNA HISTONE INTERACTION; DROSOPHILA; HETERONUCLEAR MULTIPLE QUANTUM COHERENCE; HUMAN; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; XENOPUS; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; CHROMATIN; DROSOPHILA MELANOGASTER; HYDROLYSIS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN MULTIMERIZATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; HISTONES; HYDROLYSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEOSOMES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; XENOPUS;

EID: 85010645289     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aaa3761     Document Type: Article

References (68)

1. L. Ho, G. R. Crabtree, Chromatin remodelling during development. Nature 463, 474-484 (2010). doi: 10.1038/nature08911; pmid: 20110991
2. C. R. Clapier, B. R. Cairns, The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304 (2009). doi: 10.1146/annurev.biochem.77.062706.153223; pmid: 19355820
3. G. J. Narlikar, R. Sundaramoorthy, T. Owen-Hughes, Mechanisms and functions of ATP-dependent chromatinremodeling enzymes. Cell 154, 490-503 (2013). doi: 10.1016/j.cell.2013.07.011; pmid: 23911317
4. K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, T. J. Richmond, Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 (1997). doi: 10.1038/38444; pmid: 9305837
5. A. Saha, J. Wittmeyer, B. R. Cairns, Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes Dev. 16, 2120-2134 (2002). doi: 10.1101/gad.995002; pmid: 12183366
6. G. Lia et al., Direct observation of DNA distortion by the RSC complex. Mol. Cell 21, 417-425 (2006). doi: 10.1016/j.molcel.2005.12.013; pmid: 16455496
7. I. Whitehouse, C. Stockdale, A. Flaus, M. D. Szczelkun, T. Owen-Hughes, Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell. Biol. 23, 1935-1945 (2003). doi: 10.1128/MCB.23.6.1935-1945.2003; pmid: 12612068
8. Y. Zhang et al., DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol. Cell 24, 559-568 (2006). doi: 10.1016/j.molcel.2006.10.025; pmid: 17188033
9. S. Deindl et al., ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 152, 442-452 (2013). doi: 10.1016/j.cell.2012.12.040; pmid: 23374341
10. H. Y. Fan, X. He, R. E. Kingston, G. J. Narlikar, Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11, 1311-1322 (2003). doi: 10.1016/S1097-2765(03)00192-8; pmid: 12769854
11. G. J. Narlikar, H. Y. Fan, R. E. Kingston, Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475-487 (2002). doi: 10.1016/S0092-8674(02) 00654-2; pmid: 11909519
12. G. Schnitzler, S. Sif, R. E. Kingston, Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94, 17-27 (1998). doi: 10.1016/S0092-8674(00)81217-9; pmid: 9674423
13. Y. Lorch, B. R. Cairns, M. Zhang, R. D. Kornberg, Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94, 29-34 (1998). doi: 10.1016/S0092-8674 (00)81218-0; pmid: 9674424
14. J. Côté, C. L. Peterson, J. L. Workman, Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. Proc. Natl. Acad. Sci. U.S.A. 95, 4947-4952 (1998). doi: 10.1073/pnas.95.9.4947; pmid: 9560208
15. C. Y. Zhou, S. L. Johnson, N. I. Gamarra, G. J. Narlikar, Mechanisms of ATP-Dependent Chromatin Remodeling Motors. Annu. Rev. Biophys. 45, 153-181 (2016). doi: 10.1146/annurev-biophys-051013-022819; pmid: 27391925
16. M. Alilat, A. Sivolob, B. Révet, A. Prunell, Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer- DNA particle. J. Mol. Biol. 291, 815-841 (1999). doi: 10.1006/jmbi.1999.2988; pmid: 10452891
17. R. Rosenzweig, L. E. Kay, Bringing dynamic molecular machines into focus by methyl-TROSY NMR. Annu. Rev. Biochem. 83, 291-315 (2014). doi: 10.1146/annurev-biochem- 060713-035829; pmid: 24905784
18. R. Sprangers, A. Gribun, P. M. Hwang, W. A. Houry, L. E. Kay, Quantitative NMR spectroscopy of supramolecular complexes: Dynamic side pores in ClpP are important for product release. Proc. Natl. Acad. Sci. U.S.A. 102, 16678-16683 (2005). doi: 10.1073/pnas.0507370102; pmid: 16263929
19. R. Sprangers, L. E. Kay, Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445, 618-622 (2007). doi: 10.1038/nature05512; pmid: 17237764
20. H. Kato et al., Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc. Natl. Acad. Sci. U.S.A. 108, 12283-12288 (2011). doi: 10.1073/pnas.1105848108; pmid: 21730181
21. L. R. Racki et al., The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462, 1016-1021 (2009). doi: 10.1038/nature08621; pmid: 20033039
22. C. R. Clapier, G. Längst, D. F. Corona, P. B. Becker, K. P. Nightingale, Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21, 875-883 (2001). doi: 10.1128/MCB.21.3.875-883.2001; pmid: 11154274
23. A. Hamiche, J. G. Kang, C. Dennis, H. Xiao, C. Wu, Histone tails modulate nucleosome mobility and regulate ATPdependent nucleosome sliding by NURF. Proc. Natl. Acad. Sci. U.S.A. 98, 14316-14321 (2001). doi: 10.1073/pnas.251421398; pmid: 11724935
24. C. R. Clapier, K. P. Nightingale, P. B. Becker, A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 30, 649-655 (2002). doi: 10.1093/nar/30.3.649; pmid: 11809876
25. W. Dang, M. N. Kagalwala, B. Bartholomew, Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol. Cell. Biol. 26, 7388-7396 (2006). doi: 10.1128/MCB.01159-06; pmid: 17015471
26. L. R. Racki et al., The histone H4 tail regulates the conformation of the ATP-binding pocket in the SNF2h chromatin remodeling enzyme. J. Mol. Biol. 426, 2034-2044 (2014). doi: 10.1016/j.jmb.2014.02.021; pmid: 24607692
27. V. Tugarinov, P. M. Hwang, J. E. Ollerenshaw, L. E. Kay, Crosscorrelated relaxation enhanced 1H[bond]13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J. Am. Chem. Soc. 125, 10420-10428 (2003). doi: 10.1021/ja030153x; pmid: 12926967
28. A. Mittermaier, L. E. Kay, New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228 (2006). doi: 10.1126/science.1124964; pmid: 16614210
29. D. J. Hamel, F. W. Dahlquist, The contact interface of a 120 kD CheA-CheW complex by methyl TROSY interaction spectroscopy. J. Am. Chem. Soc. 127, 9676-9677 (2005). doi: 10.1021/ja052517m; pmid: 15998058
30. M. Schlosshauer, D. Baker, Realistic protein-protein association rates from a simple diffusional model neglecting long-range interactions, free energy barriers, and landscape ruggedness. Protein Sci. 13, 1660-1669 (2004). doi: 10.1110/ps.03517304; pmid: 15133165
31. W. Dang, B. Bartholomew, Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 27, 8306-8317 (2007). doi: 10.1128/MCB.01351-07; pmid: 17908792
32. M. Zofall, J. Persinger, S. R. Kassabov, B. Bartholomew, Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 13, 339-346 (2006). doi: 10.1038/nsmb1071; pmid: 16518397
33. M. N. Kagalwala, B. J. Glaus, W. Dang, M. Zofall, B. Bartholomew, Topography of the ISW2-nucleosome complex: Insights into nucleosome spacing and chromatin remodeling. EMBO J. 23, 2092-2104 (2004). doi: 10.1038/sj.emboj.7600220; pmid: 15131696
34. www.bmrb.wisc.edu.
35. W. Kruger et al., Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. Genes Dev. 9, 2770-2779 (1995). doi: 10.1101/gad.9.22.2770; pmid: 7590252
36. U. M. Muthurajan et al., Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions. EMBO J. 23, 260-271 (2004). doi: 10.1038/sj.emboj.7600046; pmid: 14739929
37. A. Flaus, C. Rencurel, H. Ferreira, N. Wiechens, T. Owen-Hughes, Sin mutations alter inherent nucleosome mobility. EMBO J. 23, 343-353 (2004). doi: 10.1038/sj.emboj.7600047; pmid: 14726954
38. P. J. Horn, K. A. Crowley, L. M. Carruthers, J. C. Hansen, C. L. Peterson, The SIN domain of the histone octamer is essential for intramolecular folding of nucleosomal arrays. Nat. Struct. Biol. 9, 167-171 (2002). pmid: 11836537
39. T. Tsukiyama, C. Wu, Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83, 1011-1020 (1995). doi: 10.1016/0092-8674(95)90216-3; pmid: 8521501
40. T. Ito, M. Bulger, M. J. Pazin, R. Kobayashi, J. T. Kadonaga, ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145-155 (1997). doi: 10.1016/S0092-8674(00)80321-9; pmid: 9230310
41. J. D. Aalfs, G. J. Narlikar, R. E. Kingston, Functional differences between the human ATP-dependent nucleosome remodeling proteins BRG1 and SNF2H. J. Biol. Chem. 276, 34270-34278 (2001). doi: 10.1074/jbc.M104163200; pmid: 11435432
42. D. F. V. Corona et al., ISWI is an ATP-dependent nucleosome remodeling factor. Mol. Cell 3, 239-245 (1999). doi: 10.1016/S1097-2765(00)80314-7; pmid: 10078206
43. C. Horigome et al., SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol. Cell 55, 626-639 (2014). doi: 10.1016/j.molcel.2014.06.027; pmid: 25066231
44. X. Shen, G. Mizuguchi, A. Hamiche, C. Wu, A chromatin remodelling complex involved in transcription and DNA processing. Nature 406, 541-544 (2000). doi: 10.1038/35020123; pmid: 10952318
45. M. Udugama, A. Sabri, B. Bartholomew, The INO80 ATPdependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 31, 662-673 (2011). doi: 10.1128/MCB.01035-10; pmid: 21135121
46. A. Tosi et al., Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 154, 1207-1219 (2013). doi: 10.1016/j.cell.2013.08.016; pmid: 24034245
47. M. Bruno et al., Histone H2A/H2B dimer exchange by ATPdependent chromatin remodeling activities. Mol. Cell 12, 1599-1606 (2003). doi: 10.1016/S1097-2765(03)00499-4; pmid: 14690611
48. B. T. Harada et al., Stepwise nucleosome translocation by RSC remodeling complexes. eLife 5, e10051 (2016). doi: 10.7554/eLife.10051; pmid: 26895087
49. V. K. Gangaraju, P. Prasad, A. Srour, M. N. Kagalwala, B. Bartholomew, Conformational changes associated with template commitment in ATP-dependent chromatin remodeling by ISW2. Mol. Cell 35, 58-69 (2009). doi: 10.1016/j.molcel.2009.05.013; pmid: 19595716
50. J. D. Leonard, G. J. Narlikar, A nucleotide-driven switch regulates flanking DNA length sensing by a dimeric chromatin remodeler. Mol. Cell 57, 850-859 (2015). doi: 10.1016/j.molcel.2015.01.008; pmid: 25684208
51. C. R. Clapier et al., Regulation of DNA Translocation Efficiency within the Chromatin Remodeler RSC/Sth1 Potentiates Nucleosome Sliding and Ejection. Mol. Cell 62, 453-461 (2016). doi: 10.1016/j.molcel.2016.03.032; pmid: 27153540
52. J. R. Guyon, G. J. Narlikar, E. K. Sullivan, R. E. Kingston, Stability of a human SWI-SNF remodeled nucleosomal array. Mol. Cell. Biol. 21, 1132-1144 (2001). doi: 10.1128/MCB.21.4.1132-1144.2001; pmid: 11158300
53. A. N. Imbalzano, G. R. Schnitzler, R. E. Kingston, Nucleosome disruption by human SWI/SNF is maintained in the absence of continued ATP hydrolysis. J. Biol. Chem. 271, 20726-20733 (1996). doi: 10.1074/jbc.271.34.20726; pmid: 8702824
54. L. A. Boyer, X. Shao, R. H. Ebright, C. L. Peterson, Roles of the histone H2A-H2B dimers and the (H3-H4)(2) tetramer in nucleosome remodeling by the SWI-SNF complex. J. Biol. Chem. 275, 11545-11552 (2000). doi: 10.1074/jbc.275.16.11545; pmid: 10766768
55. D. P. Bazett-Jones, J. Côté, C. C. Landel, C. L. Peterson, J. L. Workman, The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNAhistone contacts within these domains. Mol. Cell. Biol. 19, 1470-1478 (1999). doi: 10.1128/MCB.19.2.1470; pmid: 9891080
56. A. J. Andrews, K. Luger, Nucleosome structure(s) and stability: Variations on a theme. Annu. Rev. Biophys. 40, 99-117 (2011). doi: 10.1146/annurev-biophys-042910-155329; pmid: 21332355
57. C. P. Prior, C. R. Cantor, E. M. Johnson, V. C. Littau, V. G. Allfrey, Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin. Cell 34, 1033-1042 (1983). doi: 10.1016/0092-8674(83)90561-5; pmid: 6313204
58. J. Fei et al., The prenucleosome, a stable conformational isomer of the nucleosome. Genes Dev. 29, 2563-2575 (2015). pmid: 26680301
59. M. S. Cosgrove, J. D. Boeke, C. Wolberger, Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11, 1037-1043 (2004). doi: 10.1038/nsmb851; pmid: 15523479
60. K. S. Zaret, J. S. Carroll, Pioneer transcription factors: Establishing competence for gene expression. Genes Dev. 25, 2227-2241 (2011). doi: 10.1101/gad.176826.111; pmid: 22056668
61. P. N. Dyer et al., Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44 (2004). doi: 10.1016/S0076-6879(03)75002-2; pmid: 14870657
62. V. Tugarinov, V. Kanelis, L. E. Kay, Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat. Protoc. 1, 749-754 (2006). doi: 10.1038/nprot.2006.101; pmid: 17406304
63. F. Delaglio et al., NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995). doi: 10.1007/BF00197809; pmid: 8520220
64. T. D. Goddard, D. G. Kneller, University of California San Francisco, "SPARKY 3" (1996).
65. J. G. Yang, T. S. Madrid, E. Sevastopoulos, G. J. Narlikar, The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 13, 1078-1083 (2006). doi: 10.1038/nsmb1170; pmid: 17099699
66. J. E. Lindsley, Use of a real-time, coupled assay to measure the ATPase activity of DNA topoisomerase II. Methods Mol. Biol. 95, 57-64 (2001). pmid: 11089219
67. C. A. Davey, D. F. Sargent, K. Luger, A. W. Maeder, T. J. Richmond, Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J. Mol. Biol. 319, 1097-1113 (2002). doi: 10.1016/S0022- 2836(02)00386-8; pmid: 12079350
68. L. Cavallo, J. Kleinjung, F. Fraternali, POPS: A fast algorithm for solvent accessible surface areas at atomic and residue level. Nucleic Acids Res. 31, 3364-3366 (2003). doi: 10.1093/nar/gkg601; pmid: 12824328