Diversity of operation in ATP-dependent chromatin remodelers

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1809, Issue 9, 2011, Pages 476-487

  Hota, Swetansu K ^a   Bartholomew, Blaine ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP dependent chromatin remodeling; DNA helicase; ISWI; Nucleosome disassembly; Nucleosome spacing; SWI SNF

Indexed keywords

CARRIER PROTEIN; DIMER; HISTONE; MONOMER;

ABERRANT CRYPT FOCUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HISTONE INTERACTION; DNA TEMPLATE; HUMAN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DNA-BINDING PROTEINS; HISTONES; NUCLEOSOMES; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 80052651122     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.05.007     Document Type: Review

References (73)

1. Ho L., Crabtree G.R. Chromatin remodelling during development. Nature 2010, 463:474-484.
2. Thoma N.H., Czyzewski B.K., Alexeev A.A., Mazin A.V., Kowalczykowski S.C., Pavletich N.P. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 2005, 12:350-356.
3. Durr H., Korner C., Muller M., Hickmann V., Hopfner K.P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005, 121:363-373.
4. Hauk G., McKnight J.N., Nodelman I.M., Bowman G.D. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol. Cell 2010, 39:711-723.
5. Dang W., Bartholomew B. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 2007, 27:8306-8317.
6. Dang W., Kagalwala M.N., Bartholomew B. Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol. Cell. Biol. 2006, 26:7388-7396.
7. Kagalwala M.N., Glaus B.J., Dang W., Zofall M., Bartholomew B. Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 2004, 23:2092-2104.
8. Grune T., Brzeski J., Eberharter A., Clapier C.R., Corona D.F., Becker P.B., Muller C.W. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 2003, 12:449-460.
9. Dechassa M.L., Zhang B., Horowitz-Scherer R., Persinger J., Woodcock C.L., Peterson C.L., Bartholomew B. Architecture of the SWI/SNF-nucleosome complex. Mol. Cell. Biol. 2008.
10. Kassabov S.R., Zhang B., Persinger J., Bartholomew B. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol. Cell 2003, 11:391-403.
11. Gangaraju V.K., Prasad P., Srour A., Kagalwala M.N., Bartholomew B. Conformational changes associated with template commitment in ATP-dependent chromatin remodeling by ISW2. Mol. Cell 2009, 35:58-69.
12. Zofall M., Persinger J., Bartholomew B. Functional role of extranucleosomal DNA and the entry site of the nucleosome in chromatin remodeling by ISW2. Mol. Cell. Biol. 2004, 24:10047-10057.
13. Zofall M., Persinger J., Kassabov S.R., Bartholomew B. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 2006, 13:339-346.
14. Lorch Y., Davis B., Kornberg R.D. Chromatin remodeling by DNA bending, not twisting. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1329-1332.
15. Saha A., Wittmeyer J., Cairns B.R. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 2005, 12:747-755.
16. Dang W., Kagalwala M.N., Bartholomew B. The Dpb4 subunit of ISW2 is anchored to extranucleosomal DNA. J. Biol. Chem. 2007, 282:19418-19425.
17. Ebralidse K.K., Grachev S.A., Mirzabekov A.D. A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA. Nature 1988, 331:365-367.
18. Luger K., Mader 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.
19. Clapier C.R., Langst G., Corona D.F., Becker P.B., Nightingale K.P. Critical role for the histone H4N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 2001, 21:875-883.
20. Strohner R., Nemeth A., Jansa P., Hofmann-Rohrer U., Santoro R., Langst G., Grummt I. NoRC-a novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J. 2001, 20:4892-4900.
21. Alenghat T., Yu J., Lazar M.A. The N-CoR complex enables chromatin remodeler SNF2H to enhance repression by thyroid hormone receptor. EMBO J. 2006, 25:3966-3974.
22. Clapier C.R., Nightingale K.P., Becker P.B. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 2002, 30:649-655.
23. Corona D.F., Clapier C.R., Becker P.B., Tamkun J.W. Modulation of ISWI function by site-specific histone acetylation. EMBO Rep. 2002, 3:242-247.
24. Udugama M., Sabri A., Bartholomew B. The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 2010.
25. Li H., Ilin S., Wang W., Duncan E.M., Wysocka J., Allis C.D., Patel D.J. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 2006, 442:91-95.
26. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., Wu C., Allis C.D. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
27. Syed S.H., Boulard M., Shukla M.S., Gautier T., Travers A., Bednar J., Faivre-Moskalenko C., Dimitrov S., Angelov D. The incorporation of the novel histone variant H2AL2 confers unusual structural and functional properties of the nucleosome. Nucleic Acids Res. 2009, 37:4684-4695.
28. Doyen C.M., Montel F., Gautier T., Menoni H., Claudet C., Delacour-Larose M., Angelov D., Hamiche A., Bednar J., Faivre-Moskalenko C., Bouvet P., Dimitrov S. Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome. EMBO J. 2006, 25:4234-4244.
29. Shukla M.S., Syed S.H., Goutte-Gattat D., Richard J.L., Montel F., Hamiche A., Travers A., Faivre-Moskalenko C., Bednar J., Hayes J.J., Angelov D., Dimitrov S. The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. Nucleic Acids Res. 2010.
30. Lemieux K., Larochelle M., Gaudreau L. Variant histone H2A.Z, but not the HMG proteins Nhp6a/b, is essential for the recruitment of Swi/Snf, Mediator, and SAGA to the yeast GAL1 UAS(G). Biochem. Biophys. Res. Commun. 2008, 369:1103-1107.
31. Xu F., Zhang K., Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005, 121:375-385.
32. Neumann H., Hancock S.M., Buning R., Routh A., Chapman L., Somers J., Owen-Hughes T., van Noort J., Rhodes D., Chin J.W. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3K56 acetylation. Mol. Cell 2009, 36:153-163.
33. Tsukiyama T., Palmer J., Landel C.C., Shiloach J., Wu C. Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 1999, 13:686-697.
34. Whitehouse I., Rando O.J., Delrow J., Tsukiyama T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 2007, 450:1031-1035.
35. Whitehouse I., Tsukiyama T. Antagonistic forces that position nucleosomes in vivo. Nat. Struct. Mol. Biol. 2006, 13:633-640.
36. Gangaraju V.K., Bartholomew B. Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol. Cell. Biol. 2007, 27:3217-3225.
37. Stockdale C., Flaus A., Ferreira H., Owen-Hughes T. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 2006, 281:16279-16288.
38. Dechassa M.L., Sabri A., Pondugula S., Kassabov S.R., Chatterjee N., Kladde M.P., Bartholomew B. SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. Mol. Cell 2010, 38:590-602.
39. Yang J.G., Madrid T.S., Sevastopoulos E., Narlikar G.J. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 2006, 13:1078-1083.
40. Racki L.R., Narlikar G.J. ATP-dependent chromatin remodeling enzymes: two heads are not better, just different. Curr. Opin. Genet. Dev. 2008, 18:137-144.
41. Racki L.R., Yang J.G., Naber N., Partensky P.D., Acevedo A., Purcell T.J., Cooke R., Cheng Y., Narlikar G.J. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 2009, 462:1016-1021.
42. Fitzgerald D.J., DeLuca C., Berger I., Gaillard H., Sigrist R., Schimmele K., Richmond T.J. Reaction cycle of the yeast Isw2 chromatin remodeling complex. EMBO J. 2004, 23:3836-3843.
43. He X., Fan H.Y., Narlikar G.J., Kingston R.E. Human ACF1 alters the remodeling strategy of SNF2h. J. Biol. Chem. 2006, 281:28636-28647.
44. He X., Fan H.Y., Garlick J.D., Kingston R.E. Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemistry 2008, 47:7025-7033.
45. Kassabov S.R., Bartholomew B. Site-directed histone-DNA contact mapping for analysis of nucleosome dynamics. Methods Enzymol. 2004, 375:193-210.
46. Kassabov S.R., Henry N.M., Zofall M., Tsukiyama T., Bartholomew B. High-resolution mapping of changes in histone-DNA contacts of nucleosomes remodeled by ISW2. Mol. Cell. Biol. 2002, 22:7524-7534.
47. Blosser T.R., Yang J.G., Stone M.D., Narlikar G.J., Zhuang X. Dynamics of nucleosome remodelling by individual ACF complexes. Nature 2009, 462:1022-1027.
48. Yang J.G., Narlikar G.J. FRET-based methods to study ATP-dependent changes in chromatin structure. Methods 2007, 41:291-295.
49. Bouazoune K., Miranda T.B., Jones P.A., Kingston R.E. Analysis of individual remodeled nucleosomes reveals decreased histone-DNA contacts created by hSWI/SNF. Nucleic Acids Res. 2009, 37:5279-5294.
50. Strick T.R., Croquette V., Bensimon D. Single-molecule analysis of DNA uncoiling by a type II topoisomerase. Nature 2000, 404:901-904.
51. Strick T.R., Croquette V., Bensimon D. Homologous pairing in stretched supercoiled DNA. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:10579-10583.
52. Lia G., Praly E., Ferreira H., Stockdale C., Tse-Dinh Y.C., Dunlap D., Croquette V., Bensimon D., Owen-Hughes T. Direct observation of DNA distortion by the RSC complex. Mol. Cell 2006, 21:417-425.
53. Lia G., Indrieri M., Owen-Hughes T., Finzi L., Podesta A., Milani P., Dunlap D. ATP-dependent looping of DNA by ISWI. J. Biophotonics 2008, 1:280-286.
54. Zhang Y., Smith C.L., Saha A., Grill S.W., Mihardja S., Smith S.B., Cairns B.R., Peterson C.L., Bustamante C. DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol. Cell 2006, 24:559-568.
55. Cairns B.R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 2007, 14:989-996.
56. Jain S.S., Tullius T.D. Footprinting protein-DNA complexes using the hydroxyl radical. Nat. Protoc. 2008, 3:1092-1100.
57. Schwanbeck R., Xiao H., Wu C. Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J. Biol. Chem. 2004, 279:39933-39941.
58. Rippe K., Schrader A., Riede P., Strohner R., Lehmann E., Langst G. DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15635-15640.
59. Erdel F., Schubert T., Marth C., Langst G., Rippe K. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19873-19878.
60. Gelbart M.E., Bachman N., Delrow J., Boeke J.D., Tsukiyama T. Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes Dev. 2005, 19:942-954.
61. Fyodorov D.V., Kadonaga J.T. Dynamics of ATP-dependent chromatin assembly by ACF. Nature 2002, 418:897-900.
62. Flaus A., Owen-Hughes T. Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol. Cell. Biol. 2003, 23:7767-7779.
63. Bruno M., Flaus A., Stockdale C., Rencurel C., Ferreira H., Owen-Hughes T. Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities. Mol. Cell 2003, 12:1599-1606.
64. Asturias F.J., Ezeokonkwo C., Kornberg R.D., Lorch Y. Electron microscopic analysis of the RSC chromatin remodeling complex. Methods Enzymol. 2004, 376:48-62.
65. Chaban Y., Ezeokonkwo C., Chung W.H., Zhang F., Kornberg R.D., Maier-Davis B., Lorch Y., Asturias F.J. Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat. Struct. Mol. Biol. 2008, 15:1272-1277.
66. Leschziner A.E., Saha A., Wittmeyer J., Zhang Y., Bustamante C., Cairns B.R., Nogales E. Conformational flexibility in the chromatin remodeler RSC observed by electron microscopy and the orthogonal tilt reconstruction method. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:4913-4918.
67. Engeholm M., de Jager M., Flaus A., Brenk R., van Noort J., Owen-Hughes T. Nucleosomes can invade DNA territories occupied by their neighbors. Nat. Struct. Mol. Biol. 2009, 16:151-158.
68. Boeger H., Griesenbeck J., Kornberg R.D. Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 2008, 133:716-726.
69. Boeger H., Griesenbeck J., Strattan J.S., Kornberg R.D. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell 2004, 14:667-673.
70. Boeger H., Griesenbeck J., Strattan J.S., Kornberg R.D. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 2003, 11:1587-1598.
71. Korber P., Luckenbach T., Blaschke D., Horz W. Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter. Mol. Cell. Biol. 2004, 24:10965-10974.
72. Studitsky V.M., Walter W., Kireeva M., Kashlev M., Felsenfeld G. Chromatin remodeling by RNA polymerases. Trends Biochem. Sci. 2004, 29:127-135.
73. Kireeva M.L., Walter W., Tchernajenko V., Bondarenko V., Kashlev M., Studitsky V.M. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol. Cell 2002, 9:541-552.