Probing SWI/SNF remodeling of the nucleosome by unzipping single DNA molecules

Nature Structural and Molecular Biology

Volumn 13, Issue 6, 2006, Pages 549-554

  Shundrovsky, Alla ^a   Smith, Corey L ^b   Lis, John T ^c   Peterson, Craig L ^b   Wang, Michelle D ^a  

^a Cornell University   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; HISTONE; PROTEIN SWI;

ACCURACY; ARTICLE; CATALYSIS; DNA BINDING; DNA HISTONE INTERACTION; GENETIC CODE; GENETICS; MOLECULAR INTERACTION; NUCLEOSOME; PRIORITY JOURNAL;

CHROMOSOMAL PROTEINS, NON-HISTONE; DNA; MOLECULAR PROBES; NUCLEOSOMES; TRANSCRIPTION FACTORS;

EID: 33744900357     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1102     Document Type: Article

References (39)

1. Davey, C.A., Sargent, D.F., Luger, K., Maeder, A.W. & Richmond, T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319, 1097-1113 (2002).
2. Kingston, R.E. & Narlikar, G.J. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev. 13, 2339-2352 (1999).
3. Kornberg, R.D. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285-294 (1999).
4. Vignali, M., Hassan, A.H., Neely, K.E. & Workman, J.L. ATP-dependent chromatin-remodeling complexes. Mol. Cell. Biol. 20, 1899-1910 (2000).
5. Smith, C.L. & Peterson, C.L. ATP-dependent chromatin remodeling. Curr. Top. Dev. Biol. 65, 115-148 (2005).
6. Becker, P.B. & Horz, W. ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71, 247-273 (2002).
7. Winston, F. & Carlson, M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 8, 387-391 (1992).
8. Sudarsanam, P. & Winston, F. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16, 345-351 (2000).
9. Bazett-Jones, D.P., Cote, J., Landel, C.C., Peterson, C.L. & Workman, J.L. The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA-histone contacts within these domains. Mol. Cell. Biol. 19, 1470-1478 (1999).
10. Schnitzler, G.R. et al. Direct imaging of human SWI/SNF-remodeled mono- and polynucleosomes by atomic force microscopy employing carbon nanotube tips. Mol. Cell. Biol. 21, 8504-8511 (2001).
11. Aoyagi, S. et al. Nucleosome remodeling by the human SWI/SNF complex requires transient global disruption of histone-DNA interactions. Mol. Cell. Biol. 22, 3653-3662 (2002).
12. Narlikar, G.J., Phelan, M.L. & Kingston, R.E. Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity. Mol. Cell 8, 1219-1230 (2001).
13. Kassabov, S.R., Zhang, B., Persinger, J. & Bartholomew, B. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol. Cell 11, 391-403 (2003).
14. Fan, H.Y., He, X., Kingston, R.E. & Narlikar, G.J. Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11, 1311-1322 (2003).
15. Cote, J., Peterson, C.L. & Workman, J.L. Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. Proc. Natl. Acad. Sci. USA 95, 4947-4952 (1998).
16. Schnitzler, G., Sif, S. & Kingston, R.E. Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94, 17-27 (1998).
17. Lorch, Y., Cairns, B.R., Zhang, M. & Kornberg, R.D. Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94, 29-34 (1998).
18. Jaskelioff, M., Gavin, I.M., Peterson, C.L. & Logie, C. SWI-SNF-mediated nucleosome remodeling: role of histone octamer mobility in the persistence of the remodeled state. Mol. Cell. Biol. 20, 3058-3068 (2000).
19. Flaus, A. & Owen-Hughes, T. Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol. Cell. Biol. 23, 7767-7779 (2003).
20. 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. 13, 339-346 (2006).
21. Whitehouse, I. et al. Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400, 784-787 (1999).
22. Koch, S.J., Shundrovsky, A., Jantzen, B.C. & Wang, M.D. Probing protein-DNA interactions by unzipping a single DNA double helix. Biophys. J. 83, 1098-1105 (2002).
23. Koch, S.J. & Wang, M.D. Dynamic force spectroscopy of protein-DNA interactions by unzipping DNA. Phys. Rev. Lett. 91, 028103 (2003).
24. Jiang, J. et al. Detection of high-affinity and sliding clamp modes for MSH2-MSH6 by single-molecule unzipping force analysis. Mol. Cell 20, 771-781 (2005).
25. 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).
26. Thastrom, A., Bingham, L.M. & Widom, J. Nucleosomal locations of dominant DNA sequence motifs for histone-DNA interactions and nucleosome positioning. J. Mol. Biol. 338, 695-709 (2004).
27. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. & Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997).
28. Brower-Toland, B.D. et al. Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA 99, 1960-1965 (2002).
29. Brower-Toland, B. & Wang, M.D. Use of optical trapping techniques to study single-nucleosome dynamics. Methods Enzymol. 376, 62-72 (2004).
30. Brower-Toland, B. et al. Specific contributions of histone tails and their acetylation to the mechanical stability of nucleosomes. J. Mol. Biol. 346, 135-146 (2005).
31. Meersseman, G., Pennings, S. & Bradbury, E.M. Mobile nucleosomes - a general behavior. EMBO J. 11, 2951-2959 (1992).
32. Cote, J., Quinn, J., Workman, J.L. & Peterson, C.L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265, 53-60 (1994).
33. Bruno, M. et al. Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities. Mol. Cell 12, 1599-1606 (2003).
34. Vicent, G.P. et al. DNA instructed displacement of histones H2A and H2B at an inducible promoter. Mol. Cell 16, 439-452 (2004).
35. Schafer, D.A., Gelles, J., Sheetz, M.P. & Landick, R. Transcription by single molecules of RNA polymerase observed by light microscopy. Nature 352, 444-448 (1991).
36. Lee, K.-M. & Narlikar, G. Assembly of nucleosomal templates by salt dialysis. in Current Protocols in Molecular Biology Vol. 3 (eds. Ausubel, F.A. et al.) 21.6.3 (Wiley, New York, 2001).
37. Smith, C.L., Horowitz-Scherer, R., Flanagan, J.F., Woodcock, C.L. & Peterson, C.L. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat. Struct. Biol. 10, 141-145 (2003).
38. Bockelmann, U., Essevaz-Roulet, B. & Heslot, F. DNA strand separation studied by single molecule force measurements. Phys. Rev. E 58, 2386-2394 (1998).
39. Orear, J. Notes on statistics for physicists. (Laboratory for Nuclear Studies report CLNS 82/511, Cornell University, New York, 1982).