Dynamics of nucleosomes revealed by time-lapse atomic force microscopy

Biochemistry

Volumn 48, Issue 33, 2009, Pages 7842-7848

  Shlyakhtenko, Luda S ^a   Lushnikov, Alexander Y ^a   Lyubchenko, Yuri L ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; BASE PAIRS; CHROMATIN REMODELING; MOLECULAR MECHANISM; NUCLEOSOMES; SINGLE-MOLECULE; UNWRAPPING PROCESS;

ATOMS; DNA; DYNAMICS; GENES; NUCLEIC ACIDS; PROTEINS;

ATOMIC FORCE MICROSCOPY;

ADENOSINE TRIPHOSPHATE; HISTONE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHROMATIN; HYDROLYSIS; MOLECULE; NUCLEOSOME; PRIORITY JOURNAL;

DNA, SUPERHELICAL; HISTONES; HUMANS; MICROSCOPY, ATOMIC FORCE; MODELS, GENETIC; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PARTICLE SIZE; TEMPLATES, GENETIC; TIME FACTORS;

EID: 69049097259     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900977t     Document Type: Article

References (47)

1. Luger, K., and Hansen, J. C. (2005) Nucleosome and chromatin fiber dynamics. Curr. Opin. Struct. Biol. 15, 188-196.
2. Thoma, F. (2005) Repair of UV lesions in nucleosomes: Intrinsic properties and remodeling. DNA Repair 4, 855-869.
3. Saha, A., Wittmeyer, J., and Cairns, B. R. (2006) Chromatin remodelling: The industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7, 437-447.
4. Cairns, B. R. (2007) Chromatin remodeling: Insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 14, 989-996.
5. Ahmad, K., and Henikoff, S. (2002) Epigenetic consequences of nucleosome dynamics. Cell 111, 281-284.
6. Anderson, J. D., Thastrom, A., and Widom, J. (2002) Spontaneous access of proteins to buried nucleosomalDNAtarget sites occurs via a mechanism that is distinct from nucleosome translocation. Mol. Cell. Biol. 22, 7147-7157.
7. Li, G., and Widom, J. (2004) Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 11, 763-769.
8. Li, G., Levitus, M., Bustamante, C., and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12, 46-53.
9. Bucceri, A., Kapitza, K., and Thoma, F. (2006) Rapid accessibility of nucleosomalDNAin yeast on a second time scale.EMBOJ. 25, 3123-3132.
10. Tims, H. S., and Widom, J. (2007) Stopped-flow fluorescence resonance energy transfer for analysis of nucleosome dynamics. Methods 41, 296-303.
11. Koopmans, W. J., Brehm, A., Logie, C., Schmidt, T., and van Noort, J. (2007) Single-pair FRET microscopy reveals mononucleosome dynamics. J. Fluoresc. 17, 785-795.
12. Leuba, S. H., Yang, G., Robert, C., Samori, B., van Holde, K., Zlatanova, J., and Bustamante, C. (1994) Three-dimensional structure of extended chromatin fibers as revealed by tapping-mode scanning force microscopy. Proc. Natl. Acad. Sci. U.S.A. 91, 11621-11625.
13. Leuba, S. H., Bustamante, C., Zlatanova, J., and van Holde, K. (1998) Contributions of linker histones and histone H3 to chromatin structure: Scanning force microscopy studies on trypsinized fibers. Biophys. J. 74, 2823-2829.
14. Yodh, J. G., Lyubchenko, Y. L., Shlyakhtenko, L. S., Woodbury, N., and Lohr, D. (1999) Evidence for nonrandom behavior in 208-12 subsaturated nucleosomal array populations analyzed by AFM. Biochemistry 38, 15756-15763.
15. Yodh, J. G., Woodbury, N., Shlyakhtenko, L. S., Lyubchenko, Y. L., and Lohr, D. (2002) Mapping nucleosome locations on the 208-12 by AFM provides clear evidence for cooperativity in array occupation. Biochemistry 41, 3565-3574.
16. Nikova, D. N., Pope, L. H., Bennink, M. L., van Leijenhorst-Groener, K. A., van der Werf, K., and Greve, J. (2004) Unexpected binding motifs for subnucleosomal particles revealed by atomic force microscopy. Biophys. J. 87, 4135-4145.
17. Guthold, M., Bezanilla, M., Erie, D. A., Jenkins, B., Hansma, H. G., and Bustamante, C. (1994) Following the assembly of RNA polymerase-DNA complexes in aqueous solutions with the scanning force microscope. Proc. Natl. Acad. Sci. U.S.A. 91, 12927-12931.
18. Hansma, H. G., Bezanilla, M., Zenhausern, F., Adrian, M., and Sinsheimer, R. L. (1993) Atomic force microscopy ofDNAin aqueous solutions. Nucleic Acids Res. 21, 505-512.
19. Bustamante, C., Rivetti, C., and Keller, D. J. (1997) Scanning force microscopy under aqueous solutions. Curr. Opin. Struct. Biol. 7, 709-716.
20. Lyubchenko, Y. L., and Shlyakhtenko, L. S. (1997) Visualization of supercoiled DNA with atomic force microscopy in situ. Proc. Natl. Acad. Sci. U.S.A. 94, 496-501.
21. Mikheikin, A. L., Lushnikov, A. Y., and Lyubchenko, Y. L. (2006) Effect of DNA supercoiling on the geometry of holliday junctions. Biochemistry 45, 12998-13006.
22. Lushnikov, A. Y., Bogdanov, A., and Lyubchenko, Y. L. (2003)DNA recombination: Holliday junctions, dynamics and branch migration. J. Biol. Chem. 278, 43130-43134.
23. Lyubchenko, Y. L. (2004) DNA structure and dynamics: An atomic force microscopy study. Cell Biochem. Biophys. 41, 75-98.
24. Ando, T., Uchihashi, T., Kodera, N., Yamamoto, D., Taniguchi, M., Miyagi, A., and Yamashita, H. (2007) High-speed atomic force microscopy for observing dynamic biomolecular processes. J. Mol. Recognit. 20, 448-458.
25. Crampton, N., Roes, S., Dryden, D. T., Rao, D. N., Edwardson, J. M., and Henderson, R. M. (2007) DNA looping and translocation provide an optimal cleavage mechanism for the type III restriction enzymes. EMBO J. 26, 3815-3825.
26. Luger, K., Rechsteiner, T. J., and Richmond, T. J. (1999) Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304, 3-19.
27. Dyer, P. N., Edayathumangalam, R. S., White, C. L., Bao, Y., Chakravarthy, S., Muthurajan, U. M., and Luger, K. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44.
28. Lowary, P. T., and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42.
29. Shlyakhtenko, L. S., Gall, A. A., Filonov, A., Cerovac, Z., Lushnikov, A., and Lyubchenko,Y. L. (2003) Silatrane-based surface chemistry for immobilization of DNA, protein-DNA complexes and other biological materials. Ultramicroscopy 97, 279-287.
30. Lushnikov, A. Y., Potaman, V. N., Oussatcheva, E. A., Sinden, R. R., and Lyubchenko, Y. L. (2006) DNA strand arrangement within the SfiI-DNA complex: Atomic force microscopy analysis. Biochemistry 45, 152-158.
31. Lyubchenko, Y. L., and Shlyakhtenko, L. S. (2009)AFMfor analysis of structure and dynamics of DNA and protein-DNA complexes. Methods 47, 206-213.
32. Lyubchenko, Y. L., Shlyakhtenko, L. S., and Gall, A. A. (2009) Atomic force microscopy imaging and probing of DNA, proteins, and protein DNA complexes: Silatrane surface chemistry. Methods Mol. Biol. 543, 337-351.
33. Shlyakhtenko, L. S., Gilmore, J., Portillo, A., Tamulaitis, G., Siksnys, V., and Lyubchenko, Y. L. (2007) Direct visualization of the EcoRII-DNA triple synaptic complex by atomic force microscopy. Biochemistry 46, 11128-11136.
34. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260.
35. Feng, J., and Chun-Cheng, Z. (2007) Thermodynamics of nucleosomal core particles. Biochemistry 46, 2594-2598.
36. Pavlicek, J. W., Oussatcheva, E. A., Sinden, R. R., Potaman, V. N., Sankey, O. F., and Lyubchenko, Y. L. (2004) Supercoiling-induced DNA bending. Biochemistry 43, 10664-10668.
37. Furrer, P., Bednar, J., Dubochet, J., Hamiche, A., and Prunell, A. (1995) DNA at the entry-exit of the nucleosome observed by cryoelectron microscopy. J. Struct. Biol. 114, 177-183.
38. Chakravarthy, S., Park,Y. J., Chodaparambil, J., Edayathumangalam, R. S., and Luger, K. (2005) Structure and dynamic properties of nucleosome core particles. FEBS Lett. 579, 895-898.
39. Park, Y. J., Chodaparambil, J. V., Bao, Y., McBryant, S. J., and Luger, K. (2005) Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J. Biol. Chem. 280, 1817-1825.
40. Luger, K. (2006) Dynamic nucleosomes. Chromosome Res. 14, 5-16.
41. van Holde, K., and Zlatanova, J. (2006) Scanning chromatin: A new paradigm? J. Biol. Chem. 281, 12197-12200.
42. Sharma, S., and Dokholyan, N. V. (2008) DNA sequence mediates nucleosome structure and stability. Biophys. J. 94, 1-3.
43. Kimura, H. (2005) Histone dynamics in living cells revealed by photobleaching. DNA Repair 4, 939-950.
44. Kelbauskas, L., Chan, N., Bash, R., Yodh, J., Woodbury, N., and Lohr, D. (2007) Sequence-dependent nucleosome structure and stability variations detected by Forster resonance energy transfer. Biochemistry 46, 2239-2248.
45. Kelbauskas, L., Chan,N., Bash, R.,DeBartolo, P., Sun, J., Woodbury, N., and Lohr,D. (2008) Sequence-dependent variations associated with H2A/H2B depletion of nucleosomes. Biophys. J. 94, 147-158.
46. Tomschik, M., van Holde, K., and Zlatanova, J. (2009) Nucleosome dynamics as studied by single-pair fluorescence resonance energy transfer: A reevaluation. J. Fluoresc. 19, 53-62.
47. Tomschik, M., Zheng, H., van Holde, K., Zlatanova, J., and Leuba, S. H. (2005) Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. U.S.A. 102, 3278-3283.