Histone- and DNA sequence-dependent stability of nucleosomes studied by single-pair FRET

Cytometry Part A

Volumn 83, Issue 9, 2013, Pages 839-846

  Tóth, Katalin ^a   Böhm, Vera ^a   Sellmann, Carolin ^a   Danner, Maria ^a   Hanne, Janina ^a   Berg, Marina ^a   Barz, Ina ^a   Gansen, Alexander ^a   Langowski, Jörg ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Chromatin structure; Resonance energy transfer; Salt destabilization; Single molecule spectroscopy

Indexed keywords

FLUORESCENT DYE; HISTONE; RIBOSOME DNA; RNA 5S;

ANIMAL; ARTICLE; CHEMISTRY; CHROMATIN; CHROMATIN STRUCTURE; DNA SEQUENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; METHODOLOGY; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NUCLEOSOME; NUCLEOTIDE SEQUENCE; RESONANCE ENERGY TRANSFER; SALT DESTABILIZATION; SINGLE MOLECULE SPECTROSCOPY; XENOPUS LAEVIS; YEAST;

CHROMATIN STRUCTURE; RESONANCE ENERGY TRANSFER; SALT DESTABILIZATION; SINGLE MOLECULE SPECTROSCOPY;

ANIMALS; BASE SEQUENCE; CHROMATIN; DNA, RIBOSOMAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HISTONES; MAMMARY TUMOR VIRUS, MOUSE; MICE; NUCLEOSOMES; RNA, RIBOSOMAL, 5S; SEQUENCE ANALYSIS, DNA; XENOPUS LAEVIS; YEASTS;

EID: 84883055423     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.22320     Document Type: Article

References (35)

1. Olins AL, Olins DE. Spheroid chromatin units (v bodies). Science 1974;183:330-332.
2. Woodcock CLF. Ultrastructure of inactive chromatin. J Cell Biol 1973;59:368a.
3. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 1997;389:251-260.
4. Tan S, Davey CA. Nucleosome structural studies. Curr Opin Struct Biol 2011;21:128-136.
5. Gurunathan K, Levitus M. Single-molecule fluorescence studies of nucleosome dynamics. Curr Pharm Biotechnol 2009;10:559-568.
6. White CL, Suto RK, Luger K. Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J 2001;20:5207-5218.
7. Tsunaka Y, Kajimura N, Tate S, Morikawa K. Alteration of the nucleosomal DNA path in the crystal structure of a human nucleosome core particle. Nucleic Acids Res 2005;33:3424-3434.
8. Clapier CR, Chakravarthy S, Petosa C, Fernandez-Tornero C, Luger K, Muller CW. Structure of the Drosophila nucleosome core particle highlights evolutionary constraints on the H2A-H2B histone dimer. Proteins 2008;71:1-7.
9. Bertin A, Mangenot S, Renouard M, Durand D, Livolant F. Structure and phase diagram of nucleosome core particles aggregated by multivalent cations. Biophys J 2007;93:3652-3663.
10. Bertin A, Leforestier A, Durand D, Livolant F. Role of histone tails in the conformation and interactions of nucleosome core particles. Biochemistry 2004;43:4773-4780.
11. Hayes JJ, Hansen JC. Nucleosomes and the chromatin fiber. Curr Opin Genet Dev 2001;11:124-129.
12. Hammermann M, Toth K, Rodemer C, Waldeck W, May RP, Langowski J. Salt-dependent compaction of di- and trinucleosomes studied by small-angle neutron scattering. Biophys J 2000;79:584-594.
13. Förster T. Energiewanderung und Fluoreszenz. Naturwissenschaften 1946;6:166-175.
14. Provencher SW. A Fourier method for the analysis of exponential decay curves. Biophys J 1976;16:27-41.
15. Ha T, Enderle T, Ogletree DF, Chemla DS, Selvin PR, Weiss S. Probing the interaction between two single molecules: Fluorescence resonance energy transfer between a single donor and a single acceptor. Proc Natl Acad Sci USA 1996;93:6264-6268.
16. Deniz AA, Dahan M, Grunwell JR, Ha T, Faulhaber AE, Chemla DS, Weiss S, Schultz PG. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: Observation of Forster distance dependence and subpopulations. Proc Natl Acad Sci USA 1999;96:3670-3675.
17. Eggeling C, Fries JR, Brand L, Gunther R, Seidel CA. Monitoring conformational dynamics of a single molecule by selective fluorescence spectroscopy. Proc Natl Acad Sci USA 1998;95:1556-1561.
18. Buning R, van Noort J. Single-pair FRET experiments on nucleosome conformational dynamics. Biochimie 2010;92:1729-1740.
19. Toth K, Brun N, Langowski J. Trajectory of nucleosomal linker DNA studied by fluorescence resonance energy transfer. Biochemistry 2001;40:6921-6928.
20. Tóth K, Brun N, Langowski J. Chromatin compaction at the mononucleosome level. Biochemistry 2006;45:1591-1598.
21. Bussiek M, Toth K, Schwarz N, Langowski J. Trinucleosome compaction studied by fluorescence energy transfer and scanning force microscopy. Biochemistry 2006;45:10838-10846.
22. Li G, Levitus M, Bustamante C, Widom J. Rapid spontaneous accessibility of nucleosomal DNA. Nat Struct Mol Biol 2005;12:46-53.
23. Poirier MG, Bussiek M, Langowski J, Widom J. Spontaneous access to DNA target sites in folded chromatin fibers. J Mol Biol 2008;379:772-786.
24. Gansen A, Toth K, Schwarz N, Langowski J. Structural variability of nucleosomes detected by single-pair Forster resonance energy transfer: Histone acetylation, sequence variation, and salt effects. J Phys Chem B 2009;113:2604-2613.
25. Lowary PT, Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 1998;276:19-42.
26. Gansen A, Valeri A, Hauger F, Felekyan S, Kalinin S, Toth K, Langowski J, Seidel CA. Nucleosome disassembly intermediates characterized by single-molecule FRET. Proc Natl Acad Sci USA 2009;106:15308-15313.
27. Bohm V, Hieb AR, Andrews AJ, Gansen A, Rocker A, Toth K, Luger K, Langowski J. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res 2011;39:3093-3102.
28. Pineiro M, Puerta C, Palacian E. Yeast nucleosomal particles: Structural and transcriptional properties. Biochemistry 1991;30:5805-5810.
29. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 2002;319:1097-1113.
30. Park YJ, Dyer PN, Tremethick DJ, Luger K. A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J Biol Chem 2004;279:24274-24282.
31. Gansen A, Hieb AR, Böhm V, Tóth K, Langowski J. Closing the gap between single molecule and bulk FRET analysis of nucleosomes. PLoS ONE 2013;8:e57018.
32. Clegg RM. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol 1992;211:353-388.
33. Bonisch C, Schneider K, Punzeler S, Wiedemann SM, Bielmeier C, Bocola M, Eberl HC, Kuegel W, Neumann J, Kremmer E, et al. H2A.Z.2.2 is an alternatively spliced histone H2A.Z variant that causes severe nucleosome destabilization. Nucleic Acids Res 2012;40:5951-5964.
34. Kelbauskas L, Sun J, Woodbury N, Lohr D. Nucleosomal stability and dynamics vary significantly when viewed by internal versus terminal labels. Biochemistry 2008;47:9627-9635.
35. Koopmans WJ, Buning R, Schmidt T, van Noort J. spFRET using alternating excitation and FCS reveals progressive DNA unwrapping in nucleosomes. Biophys J 2009;97:195-204.