The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes

Nature

Volumn 462, Issue 7276, 2009, Pages 1016-1021

  Racki, Lisa R ^a   Yang, Janet G ^a   Naber, Nariman ^a   Partensky, Peretz D ^a   Acevedo, Ashley ^a   Purcell, Thomas J ^a   Cooke, Roger ^a   Cheng, Yifan ^a,b   Narlikar, Geeta J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SNF;

CHROMOSOME; DNA; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ENGINEERING; NERVOUS SYSTEM;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA FLANKING REGION; ELECTRON MICROSCOPY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DIMERIZATION; GENE SILENCING; HISTONES; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEOSOMES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 72949099482     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08621     Document Type: Article

References (47)

1. Corona, D. F. et al. ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol. 5, e232 (2007).
2. Fyodorov, D. V., Blower, M. D., Karpen, G. H. & Kadonaga, J. T. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev. 18, 170-183 (2004).
3. Ito, T., Bulger, M., Pazin, M. J., Kobayashi, R. & Kadonaga, J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145-155 (1997).
4. Varga-Weisz, P. D. et al. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598-602 (1997).
5. Deuring, R. et al. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol. Cell 5, 355-365 (2000).
6. Poot, R. A. et al. HuCHRAC, a human ISWI chromatin remodelling complex contains hACF1 and two novel histone-fold proteins. EMBO J. 19, 3377-3387 (2000).
7. Bochar, D. A. et al. A family of chromatin remodeling factors related to Williams syndrome transcription factor. Proc. Natl Acad. Sci. USA 97, 1038-1043 (2000).
8. 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. Nature Struct. Mol. Biol. 13, 1078-1083 (2006).
9. 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. 23, 2092-2104 (2004).
10. Sun, F. L., Cuaycong, M. H. & Elgin, S. C. Long-range nucleosome ordering is associated with gene silencing in Drosophila melanogaster pericentric heterochromatin. Mol. Cell. Biol. 21, 2867-2879 (2001).
11. Corona, D. F. et al. ISWI is an ATP-dependent nucleosome remodeling factor. Mol. Cell 3, 239-245 (1999).
12. Aalfs, J. D., Narlikar, G. J. & Kingston, R. E. Functional differences between the human ATP-dependent nucleosome remodeling proteins BRG1 and SNF2H. J. Biol. Chem. 276, 34270-34278 (2001).
13. Eberharter, A. et al. Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J. 20, 3781-3788 (2001).
14. Längst, G., Bonte, E. J., Corona, D. F. & Becker, P. B. Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97, 843-852 (1999).
15. Ito, T. et al. ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev. 13, 1529-1539 (1999).
16. Dürr, H., Flaus, A., Owen-Hughes, T. & Hopfner, K. P. Snf2 family ATPases and DExx box helicases: differences and unifying concepts from high-resolution crystal structures. Nucleic Acids Res. 34, 4160-4167 (2006).
17. Dang, W. & Bartholomew, B. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 27, 8306-8317 (2007).
18. Grüne, T. et al. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 12, 449-460 (2003).
19. Clapier, C. R., Langst, G., Corona, D. F., Becker, P. B. & Nightingale, K. P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21, 875-883 (2001).
20. Clapier, C. R., Nightingale, K. P. & Becker, P. B. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 30, 649-655 (2002).
21. Hamiche, A., Kang, J. G., Dennis, C., Xiao, H. & Wu, C. Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc. Natl Acad. Sci. USA 98, 14316-14321 (2001).
22. Fazzio, T. G., Gelbart, M. E. & Tsukiyama, T. Two distinct mechanisms of chromatin interaction by the Isw2 chromatin remodeling complex in vivo. Mol. Cell. Biol. 25, 9165-9174 (2005).
23. Ferreira, H., Flaus, A. & Owen-Hughes, T. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J. Mol. Biol. 374, 563-579 (2007).
24. Dang, W., Kagalwala, M. N. & Bartholomew, B. Regulation of ISW2 by concerted action of the histone H4 tail and extranucleosomal DNA. Mol. Cell. Biol. 26, 7388-7396 (2006).
25. Shogren-Knaak, M. et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844-847 (2006). (Pubitemid 43228847)
26. Rice, S. et al. A structural change in the kinesin motor protein that drives motility. Nature 402, 778-784 (1999).
27. Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42 (1998).
28. Naber, N., Purcell, T. J., Pate, E. & Cooke, R. Dynamics of the nucleotide pocket of myosin measured by spin-labeled nucleotides. Biophys. J. 92, 172-184 (2007).
29. Rice, S. et al. Thermodynamic properties of the kinesin neck-region docking to the catalytic core. Biophys. J. 84, 1844-1854 (2003).
30. Schwanbeck, R., Xiao, H. & Wu, C. Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J. Biol. Chem. 279, 39933-39941 (2004).
31. Lohman, T. M., Thorn, K. & Vale, R. D. Staying on track: common features of DNA helicases and microtubule motors. Cell 93, 9-12 (1998).
32. Chin, J., Langst, G., Becker, P. B. & Widom, J. Fluorescence anisotropy assays for analysis of ISWI-DNA and ISWI-nucleosome interactions. Methods Enzymol. 376, 3-16 (2003).
33. Dürr, 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 121, 363-373 (2005).
34. Thomä, N. H. et al. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nature Struct. Mol. Biol. 12, 350-356 (2005).
35. Radermacher, M. et al. Cryo-electron microscopy and three-dimensional reconstruction of the calcium release channel/ryanodine receptor from skeletal muscle. J. Cell Biol. 127, 411-423 (1994).
36. Stockdale, C., Flaus, A., Ferreira, H. & Owen-Hughes, T. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 281, 16279-16288 (2006).
37. Zofall, M., Persinger, J., Kassabov, S. R. & Bartholomew, B. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nature Struct. Mol. Biol. 13, 339-346 (2006).
38. Whitehouse, I., Stockdale, C., Flaus, A., Szczelkun, M. D. & Owen-Hughes, T. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell. Biol. 23, 1935-1945 (2003).
39. Cairns, B. R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nature Struct. Mol. Biol. 14, 989-996 (2007).
40. Strohner, R. et al. A 'loop recapture' mechanism for ACF-dependent nucleosome remodeling. Nature Struct. Mol. Biol. 12, 683-690 (2005).
41. Längst, G. & Becker, P. B. Nucleosome remodeling: one mechanism, many phenomena? Biochim. Biophys. Acta 1677, 58-63 (2004).
42. Racki, L. R. & Narlikar, G. J. ATP-dependent chromatin remodeling enzymes: two heads are not better, just different. Curr. Opin. Genet. Dev. 18, 137-144 (2008).
43. Enemark, E. J. & Joshua-Tor, L. On helicases and other motor proteins. Curr. Opin. Struct. Biol. 18, 243-257 (2008).
44. Blosser, T. R., Yang, J. G., Stone, M. D., Narlikar, G. J. & Zhuang, X. Dynamics of nucleosome remodelling by individual ACF complexes. Nature doi:10.1038/ nature08627 (in the press).
45. Fyodorov, D. V. & Kadonaga, J. T. Dynamics of ATP-dependent chromatin assembly by ACF. Nature 418, 896-900 (2002).
46. 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 35, 58-69 (2009).
47. He, X., Fan, H. Y., Narlikar, G. J. & Kingston, R. E. Human ACF1 alters the remodeling strategy of SNF2h. J. Biol. Chem. 281, 28636-28647 (2006).