Protein-Protein Förster Resonance Energy Transfer Analysis of Nucleosome Core Particles Containing H2A and H2A.Z

Journal of Molecular Biology

Volumn 371, Issue 4, 2007, Pages 971-988

  Hoch, Duane A ^a   Stratton, Jessica J ^a   Gloss, Lisa M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

chromatin; fluorescence; FRET; histone variants; thermodynamics

Indexed keywords

DIMER; HISTONE;

ANISOTROPY; ARTICLE; CRYSTAL STRUCTURE; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; KINETICS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN FOLDING; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

EID: 34547128660     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.05.075     Document Type: Article

References (79)

1. Workman J.L., and Kingston R.E. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67 (1998) 545-579
2. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 116 (2004) 259-272
3. Luger K. Dynamic nucleosomes. Chromosome Res. 14 (2006) 5-16
4. Wolffe A.P. Chromatin remodeling: why it is important in cancer. Oncogene 20 (2001) 2988-2990
5. Huang C., Sloan E.A., and Boerkoel C.F. Chromatin remodeling and human disease. Curr. Opin. Genet. Dev. 13 (2003) 246-252
6. Yasui W., Oue N., Ono S., Mitani Y., Ito R., and Nakayama H. Histone acetylation and gastrointestinal carcinogenesis. Ann. NY Acad. Sci. 983 (2003) 220-231
7. Arents G., and Moudrianakis E.N. The histone fold: A ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl Acad. Sci. USA 92 (1995) 11170-11174
8. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 (1997) 251-260
9. Davey C.A., Sargent D.F., Luger K., Maeder A.W., and Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319 (2002) 1097-1113
10. Suto R.K., Clarkson M.J., Tremethick D.J., and Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A. Z. Nature Struct. Biol. 7 (2000) 1121-1124
11. Oohara I., and Wada A. Spectroscopic studies on histone-DNA interactions. I. The interaction of Histone (H2A,H2B) dimer with DNA: DNA sequence dependence. J. Mol. Biol. 196 (1987) 389-397
12. Smith S., and Stillman B. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 10 (1991) 971-980
13. Akey C.W., and Luger K. Histone chaperones and nucleosome assembly. Curr. Opin. Struct. Biol. 13 (2003) 6-14
14. Oohara I., and Wada A. Spectroscopic studies on histone-DNA interactions. II. Three transitions in nucleosomes resolved by salt-titration. J. Mol. Biol. 196 (1987) 399-411
15. Park Y.J., Dyer P.N., Tremethick D.J., and Luger K. A new FRET approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J. Biol. Chem. 13 (2004) 24274-24282
16. Polach K.J., and Widom J. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258 (1996) 800-812
17. Polach K.J., and Widom J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254 (1995) 130-149
18. Li G., and Widom J. Nucleosomes facilitate their own invasion. Nature Struct. Mol. Biol. 11 (2004) 763-769
19. Li G., Levitus M., Bustamante C., and Widom J. Rapid spontaneous accessibility of nucleosomal DNA. Nature Struct. Mol. Biol. 12 (2005) 46-53
20. Tomschik M., Zheng H., van Holde K., Zlatanova J., and Leuba S.H. Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 102 (2005) 3278-3283
21. Ausio J., Abbott D.W., Wang X., and Moore S.C. Histone variants and histone modifications: a structural perspective. Biochem. Cell Biol. 79 (2001) 693-708
22. Ausio J., and Abbott D.W. The many tales of a tail: carboxyl-terminal tail heterogeneity specializes histone H2A variants for defined chromatin function. Biochemistry 41 (2002) 5945-5949
23. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., and Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12 (2002) 162-169
24. Henikoff S., and Ahmad K. Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21 (2005) 133-153
25. Kamakaka R.T., and Biggins S. Histone variants: deviants?. Genes Dev. 19 (2005) 295-310
26. Meneghini M.D., Wu M., and Madhani H.D. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112 (2003) 725-736
27. Rangasamy D., Berven L., Ridgway P., and Tremethick D.J. Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. EMBO J. 22 (2003) 1599-1607
28. Fan J.Y., Rangasamy D., Luger K., and Tremethick D.J. H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol. Cell 16 (2004) 655-661
29. Guillemette B., Bataille A.R., Gevry N., Adam M., Blanchette M., Robert F., and Gaudreau L. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 3 (2005) e384
30. Raisner R.M., Hartley P.D., Meneghini M.D., Bao M.Z., Liu C.L., Schreiber S.L., et al. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123 (2005) 233-248
31. Zhang H., Roberts D.N., and Cairns B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123 (2005) 219-231
32. Dryhurst D., Thambirajah A.A., and Ausio J. New twists on H2A.Z: a histone variant with a controversial structural and functional past. Biochem. Cell Biol. 82 (2004) 490-497
33. Raisner R.M., and Madhani H.D. Patterning chromatin: form and function for H2A.Z variant nucleosomes. Curr. Opin. Genet. Dev. 16 (2006) 119-124
34. Abbott D.W., Ivanova V.S., Wang X., Bonner W.M., and Ausio J. Characterization of the stability and folding of H2A.Z chromatin particles: implications for transcriptional activation. J. Biol. Chem. 276 (2001) 41945-41949
35. Thambirajah A.A., Dryhurst D., Ishibashi T., Li A., Maffey A.H., and Ausio J. H2A.Z stabilizes chromatin in a way that is dependent on core histone acetylation. J. Biol. Chem. 281 (2006) 20036-20044
36. Flaus A., Rencurel C., Ferreira H., Wiechens N., and Owen-Hughes T. Sin mutations alter inherent nucleosome mobility. EMBO J. 23 (2004) 343-353
37. Lowary P.T., and Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276 (1998) 19-42
38. Thastrom A., Lowary P.T., Widlund H.R., Cao H., Kubista M., and Widom J. Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 288 (1999) 213-229
39. Kelbauskas L., Chan N., Bash R., Yodh J., Woodbury N., and Lohr D. Sequence-dependent nucleosome structure and stability variations detected by Forster resonance energy transfer. Biochemistry 46 (2007) 2239-2248
40. Lovullo D., Daniel D., Yodh J., Lohr D., and Woodbury N.W. A fluorescence resonance energy transfer-based probe to monitor nucleosome structure. Anal. Biochem. 341 (2005) 165-172
41. Dalbey R.E., Weiel J., and Yount R.G. Forster energy transfer measurements of thiol 1 to thiol 2 distances in myosin subfragment 1. Biochemistry 22 (1983) 4696-4706
42. Lakowicz J.R. Principles of Fluorescence Spectroscopy. Second edit., (1999), Plenum Press, New York
43. Banks D.D., and Gloss L.M. Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry 42 (2003) 6827-6839
44. Wang A., and Bolen D.W. A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36 (1997) 9101-9108
45. Bolen D.W. Protein stabilization by naturally occurring osmolytes. Methods Mol. Biol. 168 (2001) 17-36
46. Henkels C.H., Kurz J.C., Fierke C.A., and Oas T.G. Linked folding and anion binding of the Bacillus subtilis ribonuclease P protein. Biochemistry 40 (2001) 2777-2789
47. Luger K., Rechsteiner T.J., Flaus A.J., Waye M.M., and Richmond T.J. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272 (1997) 301-311
48. Luger K., Rechsteiner T.J., and Richmond T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304 (1999) 3-19
49. Steer B.A., and Merrill A.R. The colicin E1 insertion-competent state: detection of structural changes using fluorescence resonance energy transfer. Biochemistry 33 (1994) 1108-1115
50. Spudich G., and Marqusee S. A change in the apparent m value reveals a populated intermediate under equilibrium conditions in Escherichia coli ribonuclease HI. Biochemistry 39 (2000) 11677-11683
51. Hobart S.A., Meinhold D.W., Osuna R., and Colon W. From two-state to three-state: the effect of the P61A mutation on the dynamics and stability of the Factor for Inversion Stimulation in an altered equilibrium denaturation mechanism. Biochemistry 41 (2002) 13744-13754
52. Record Jr. M.T., Zhang W., and Anderson C.F. Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: a practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects and osmotic effects of salts. Advan. Protein Chem. 51 (1998) 282-355
53. van Holde K. In: Rich A. (Ed). Chromatin. Springer Series in Molecular Biology (1989), Springer-Verlag, New York
54. Randolph J.B., and Waggoner A.S. Stability, specificity and fluorescence brightness of multiply-labeled fluorescent DNA probes. Nucl. Acids Res. 25 (1997) 2923-2929
55. Aragay A.M., Diaz P., and Daban J.-R. Association of nucleosome core particle DNA with different histone oligomers: transfer of histones between DNA-(H2A,H2B) and DNA-(H3,H4) complexes. J. Mol. Biol. 204 (1988) 141-154
56. Thastrom A., Gottesfeld J.M., Luger K., and Widom J. Histone-DNA binding free energy cannot be measured in dilution-driven dissociation experiments. Biochemistry 43 (2004) 736-741
57. Dorigo B., Schalch T., Kulangara A., Duda S., Schroeder R.R., and Richmond T.J. Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306 (2004) 1571-1573
58. Schalch T., Duda S., Sargent D.F., and Richmond T.J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436 (2005) 138-141
59. 2 tetramer. Proc. Natl Acad. Sci. USA 88 (1991) 10596-10600
60. Thiriet C., and Hayes J.J. Histone dynamics during transcription: exchange of H2A/H2B dimers and H3/H4 tetramers during pol II elongation. Results Probl. Cell Differ. 41 (2006) 77-90
61. Thastrom A., Lowary P.T., and Widom J. Measurement of histone-DNA interaction free energy in nucleosomes. Methods 33 (2004) 33-44
62. Gottesfeld J.M., and Luger K. Energetics and affinity of the histone octamer for defined DNA sequences. Biochemistry 40 (2001) 10927-10933
63. Mazurkiewicz J., Kepert J.F., and Rippe K. On the mechanism of nucleosome assembly by histone chaperone NAP1. J. Biol. Chem. 281 (2006) 16462-16472
64. Read C.M., Baldwin J.P., and Crane-Robinson C. Structure of subnucleosomal particles. Tetrameric (H3/H4)2 146 base pair DNA and hexameric (H3/H4)2(H2A/H2B)1 146 base pair DNA complexes. Biochemistry 24 (1985) 4435-4450
65. Arents G., Burlingame R.W., Wang B.C., Love W.E., and Moudrianakis E.N. The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl Acad. Sci. USA 88 (1991) 10148-10152
66. Luger K. Structure and dynamic behavior of nucleosomes. Curr. Opin. Genet. Dev. 13 (2003) 127-135
67. Gloss L.M., and Placek B.J. The effect of salts on the stability of the H2A-H2B histone dimer. Biochemistry 41 (2002) 14951-14959
68. Placek B.J., Harrison L.N., Villers B.M., and Gloss L.M. The H2A.Z/H2B dimer is unstable compared to the dimer containing the major H2A isoform. Protein Sci. 14 (2005) 514-522
69. Nelson D.A., and Alonso W.R. Extraction of histones H2A, H3 and H4 from yeast nuclei. Measurement of the extent of yeast histone acetylation following one-dimensional gel electrophoresis. Biochim. Biophys. Acta 741 (1983) 269-271
70. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
71. Dyer P.N., Edayathumangalam R.S., White C.L., Bao Y., Chakravarthy S., Muthurajan U.M., and Luger K. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375 (2004) 23-44
72. 2 histone tetramer of the core nucleosome. Protein Sci. 13 (2004) 1304-1316
73. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131 (1986) 266-280
74. Santoro M.M., and Bolen D.W. A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range. Biochemistry 31 (1992) 4901-4907
75. Myers J.K., Pace C.N., and Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessble surface areas of protein folding. Protein Sci. 4 (1995) 2138-2148
76. Zitzewitz J.A., Bilsel O., Luo J., Jones B.E., and Matthews C.R. Probing the folding mechanism of a leucine zipper peptide by stopped-flow circular dichroism spectroscopy. Biochemistry 34 (1995) 12812-12819
77. Bilsel O., Zitzewitz J.A., Bowers K.E., and Matthews C.R. Folding mechanism of the alpha-subunit of tryptophan synthase, an alpha/beta barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 38 (1999) 1018-1029
78. Beechem J.M. Global analysis of biochemical and biophysical data. Methods Enzymol. 210 (1992) 37-54
79. Richmond T.J., and Davey C.A. The structure of DNA in the nucleosome core. Nature 423 (2003) 145-150