Chromatin fiber folding: Requirement for the histone H4 N-terminal tail

Journal of Molecular Biology

Volumn 327, Issue 1, 2003, Pages 85-96

  Dorigo, Benedetta ^a   Schalch, Thomas ^a   Bystricky, Kerstin ^a,b   Richmond, Timothy J ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Chromatin fiber; Higher order structure; Histone tails; Nucleosome array; Sedimentation

Indexed keywords

AMINO ACID; DNA; HISTONE H4; MAGNESIUM CHLORIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN; NUCLEOSOME; PRIORITY JOURNAL; ULTRACENTRIFUGATION;

EID: 0037436410     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00025-1     Document Type: Article

References (71)

1. Finch J.T., Klug A. Solenoidal model for superstructure in chromatin. Proc. Natl Acad. Sci. USA. 73:1976;1897-1901.
2. Widom J. Toward a unified model of chromatin folding. Annu. Rev. Biophys. Biophys. Chem. 18:1989;365-395.
3. Woodcock C.L., Grigoryev S.A., Horowitz R.A., Whitaker N. A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. Proc. Natl Acad. Sci. USA. 90:1993;9021-9025.
4. Beard D.A., Schlick T. Computational modeling predicts the structure and dynamics of chromatin fiber. Structure (Camb). 9:2001;105-114.
5. Wu J., Grunstein M. 25 years after the nucleosome model: chromatin modifications. Trends Biochem. Sci. 25:2000;619-623.
6. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 389:1997;251-260.
7. Davey C.A., Sargent D.F., Luger K., Mäder A.W., Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319:2002;1097-1113.
8. Bradbury E.M. Reversible histone modifications and the chromosome cell cycle. Bioessays. 14:1992;9-16.
9. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 389:1997;349-352.
10. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 403:2000;41-45.
11. Rice J.C., Allis C.D. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13:2001;263-273.
12. Marmorstein R. Protein modules that manipulate histone tails for chromatin regulation. Nature Rev. Mol. Cell Biol. 2:2001;422-432.
13. Turner B.M. Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell. Mol. Life Sci. 54:1998;21-31.
14. Brown C.E., Lechner T., Howe L., Workman J.L. The many HATs of transcription coactivators. Trends Biochem. Sci. 25:2000;15-19.
15. Imhof A., Becker P.B. Modifications of the histone N-terminal domains. Evidence for an "epigenetic code"? Mol. Biotechnol. 17:2001;1-13.
16. Jenuwein T., Allis C.D. Translating the histone code. Science. 293:2001;1074-1080.
17. Wells D., Brown D. Histone and histone gene compilation and alignment update. Nucl. Acids Res. 19:1991;2173-2188.
18. Kayne P.S., Kim U.J., Han M., Mullen J.R., Yoshizaki F., Grunstein M. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell. 55:1988;27-39.
19. Ling X., Harkness T.A., Schultz M.C., Fisher-Adams G., Grunstein M. Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev. 10:1996;686-699.
20. Park E.C., Szostak J.W. Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locus HML. Mol. Cell. Biol. 10:1990;4932-4934.
21. Megee P.C., Morgan B.A., Mittman B.A., Smith M.M. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science. 247:1990;841-845.
22. Durrin L.K., Mann R.K., Kayne P.S., Grunstein M. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell. 65:1991;1023-1031.
23. Johnson L.M., Fisher-Adams G., Grunstein M. Identification of a non-basic domain in the histone H4 N-terminus required for repression of the yeast silent mating loci. EMBO J. 11:1992;2201-2209.
24. Wan J.S., Mann R.K., Grunstein M. Yeast histone H3 and H4 N termini function through different GAL1 regulatory elements to repress and activate transcription. Proc. Natl Acad. Sci. USA. 92:1995;5664-5668.
25. Hecht A., Laroche T., Strahl-Bolsinger S., Gasser S.M., Grunstein M. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell. 80:1995;583-592.
26. Edmondson D.G., Zhang W., Watson A., Xu W., Bone J.R., Yu Y., et al. In vivo functions of histone acetylation/deacetylation in Tup1p repression and Gcn5p activation. Cold Spring Harb. Symp. Quant. Biol. 63:1998;459-468.
27. Lachner M., O'Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 410:2001;116-120.
28. Schuster T., Han M., Grunstein M. Yeast histone H2A and H2B amino termini have interchangeable functions. Cell. 45:1986;445-451.
29. Allfrey V.G., Faulkner R., Mirsky A.E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl Acad. Sci. USA. 51:1964;786-794.
30. Wolffe A.P., Hayes J.J. Chromatin disruption and modification. Nucl. Acids Res. 27:1999;711-720.
31. Hassan A.H., Neely K.E., Vignali M., Reese J.C., Workman J.L. Promoter targeting of chromatin-modifying complexes. Front. Biosci. 6:2001;D1054-D1064.
32. Krajewski W.A., Ausio J. Modulation of the higher-order folding of chromatin by deletion of histone H3 and H4 terminal domains. Biochem. J. 316:1996;395-400.
33. Luger K., Rechsteiner T.J., Richmond T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304:1999;3-19.
34. Lowary P.T., Widom J., New D.N.A. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:1998;19-42.
35. Flaus A., Luger K., Tan S., Richmond T.J. Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals. Proc. Natl Acad. Sci. USA. 93:1996;1370-1375.
36. Widom J. A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells. Proc. Natl Acad. Sci. USA. 89:1992;1095-1099.
37. Hansen J.C., Ausio J., Stanik V.H., van Holde K.E. Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry. 28:1989;9129-9136.
38. Hansen J.C., Lohr D. Assembly and structural properties of subsaturated chromatin arrays. J. Biol. Chem. 268:1993;5840-5848.
39. Noll M., Kornberg R.D. Action of micrococcal nuclease on chromatin and the location of histone H1. J Mol Biol. 109:1977;393-404.
40. van Holde K.E., Weischet W.O. Boundary analysis of sedimentation velocity experiments with monodisperse and polydisperse solutes. Biopolymers. 17:1978;1387-1403.
41. Schwarz P.M., Hansen J.C. Formation and stability of higher order chromatin structures. Contributions of the histone octamer. J. Biol. Chem. 269:1994;16284-16289.
42. Collins K.D. Charge density-dependent strength of hydration and biological structure. Biophys. J. 72:1997;65-76.
43. Demeler B., Behlke J., Ristau O. Molecular parameters from sedimentation velocity experiments: whole boundary fitting using approximate and numerical solutions of Lamm equation. Methods Enzymol. 321:2000;38-66.
44. Aalan J., Harborne N., Rau D.C., Gould H. Participation of core histone "tails" in the stabilization of the chromatin solenoid. J. Cell Biol. 93:1982;285-297.
45. Schwarz P.M., Felthauser A., Fletcher T.M., Hansen J.C. Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. Biochemistry. 35:1996;4009-4015.
46. Luger K., Rechsteiner T.J., Flaus A.J., Waye M.M., Richmond T.J. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272:1997;301-311.
47. Buttinelli M., Di Mauro E., Negri R. Multiple nucleosome positioning with unique rotational setting for the Saccharomyces cerevisiae 5 S rRNA gene in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 90:1993;9315-9319.
48. Dong F., Hansen J.C., van Holde K.E. DNA and protein determinants of nucleosome positioning on sea urchin 5 S rRNA gene sequences in vitro. Proc. Natl Acad. Sci. USA. 87:1990;5724-5728.
49. Simpson R.T., Thoma F., Brubaker J.M. Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: a model system for study of higher order structure. Cell. 42:1985;799-808.
50. Hansen J.C. Conformational dynamics of the chromatin fiber in solutions: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31:2002;361-392.
51. Tse C., Hansen J.C. Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 N-termini in chromatin fiber compaction. Biochemistry. 36:1997;11381-11388.
52. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 83:1979;403-427.
53. Clark D.J., Kimura T. Electrostatic mechanism of chromatin folding. J. Mol. Biol. 211:1990;883-896.
54. Davey C.A., Richmond T.J. DNA-dependent divalent cation binding in the nucleosome core particle. Proc. Natl Acad. Sci. USA. 99:2002;11169-11174.
55. Olvera de la Cruz M., Belloni L., Delsanti M., Dalbiez J.P., Spalla O., Drifford M. Precipitation of highly charged polyelectrolyte solutions in the presence of multivalent salts. J. Chem. Phys. 103:1995;5781-5791.
56. de Frutos M., Raspaud E., Leforestier A., Livolant F. Aggregation of nucleosomes by divalent cations. Biophys. J. 81:2001;1127-1132.
57. Huang L., Zhang W., Roth S.Y. Amino termini of histones H3 and H4 are required for a1-alpha2 repression in yeast. Mol. Cell. Biol. 17:1997;6555-6562.
58. Winston F., Allis C.D. The bromodomain: a chromatin-targeting module? Nature Struct. Biol. 6:1999;601-604.
59. Jones D.O., Cowell I.G., Singh P.B. Mammalian chromodomain proteins: their role in genome organisation and expression. Bioessays. 22:2000;124-137.
60. Herrera J.E., Schiltz R.L., Bustin M. The accessibility of histone H3 tails in chromatin modulates their acetylation by P300/CBP-associated factor. J. Biol. Chem. 275:2000;12994-12999.
61. Nishioka K.R.J., Sarma K., Erdjument-Bromage H., Werner J., Wang Y., Chuikov S., et al. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell. 9:2002;1201-1213.
62. Mizzen C.A., Allis C.D. Transcription. New insights into an old modification. Science. 289:2000;2290-2291.
63. Sobel R.E., Cook R.G., Perry C.A., Annunziato A.T., Allis C.D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl Acad. Sci. USA. 92:1995;1237-1241.
64. Richmond T.J., Searles M.A., Simpson R.T. Crystals of a nucleosome core particle containing defined sequence DNA. J. Mol. Biol. 199:1988;161-170.
65. Luger K., Rechsteiner T.J., Richmond T.J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119:1999;1-16.
66. Hansen J.C., Kreider J.I., Demeler B., Fletcher T.M. Analytical ultracentrifugation and agarose gel electrophoresis as tools for studying chromatin folding in solution. Methods. 12:1997;62-72.
67. Cohen G., Eisenberg H. Deoxyribonucleate solutions: sedimentation in a density gradient, partial specific volumes, density and refractive index increments, and preferential interactions. Biopolymers. 6:1968;1077-1100.
68. Stein A. DNA folding by histones: the kinetics of chromatin core particle reassembly and the interaction of nucleosomes with histones. J. Mol. Biol. 130:1979;103-134.
69. Bowen T.J., Rowe A.J. An Introduction to Ultracentrifugation. 1970;Wiley-Interscience, New York.
70. Perry M., Thomsen G.H., Roeder R.G. Genomic organization and nucleotide sequence of two distinct histone gene clusters from Xenopus laevis. Identification of novel conserved upstream sequence elements. J. Mol. Biol. 185:1985;479-499.
71. Böhm L., Crane-Robinson C. Proteases as structural probes for chromatin: the domain structure of histones. Biosci. Rep. 4:1984;365-386.