Functional consequences of histone modifications

Current Opinion in Genetics and Development

Volumn 13, Issue 2, 2003, Pages 154-160

  Iizuka, Masayoshi ^a   Smith, M Mitchell ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; HISTONE; HISTONE DEACETYLASE; RNA;

ACETYLATION; DNA METHYLATION; DNA REPAIR; GENE EXPRESSION REGULATION; GENE SILENCING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW;

ACETYLATION; ACETYLTRANSFERASES; ANIMALS; HISTONES; HUMANS; METHYLATION; METHYLTRANSFERASES; PHOSPHORYLATION; PHOSPHOTRANSFERASES; RNA; SCHIZOSACCHAROMYCES;

EID: 0037382605     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(03)00020-0     Document Type: Review

References (63)

1. Santisteban M.S., Kalashnikova T., Smith M.M. Histone H2A.Z regulates transcription and is partially redundant with nucleosome remodeling complexes. Cell. 103:2000;411-422.
2. Smith M.M. Centromeres and variant histones: what, where, when and why? Curr. Opin. Cell Biol. 14:2002;279-285.
3. Ahmad K., Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell. 9:2002;1191-1200.
4. Berger S.L. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12:2002;142-148.
5. Kouzarides T. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:2002;198-209.
6. Dhalluin C., Carlson J.E., Zeng L., He C., Aggarwal A.K., Zhou M.M. Structure and ligand of a histone acetyltransferase bromodomain. Nature. 399:1999;491-496.
7. Jacobs S.A., Khorasanizadeh S. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science. 295:2002;2080-2083.
8. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 403:2000;41-45.
9. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 389:1997;349-352.
10. Suka N., Luo K., Grunstein M. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat. Genet. 32:2002;378-383.
11. Kimura A., Umehara T., Horikoshi M. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32:2002;370-377.
12. Howe L., Auston D., Grant P., John S., Cook R.G., Workman J.L., Pillus L. Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 15:2001;3144-3154.
13. Loyola A., LeRoy G., Wang Y.H., Reinberg D. Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. Genes Dev. 15:2001;2837-2851.
14. Georges S.A., Kraus W.L., Luger K., Nyborg J.K., Laybourn P.J. p300-mediated tax transactivation from recombinant chromatin: histone tail deletion mimics coactivator function. Mol. Cell Biol. 22:2002;127-137.
15. An W., Palhan V.B., Karymov M.A., Leuba S.H., Roeder R.G. Selective requirements for histone H3 and H4 N termini in p300-dependent transcriptional activation from chromatin. Mol. Cell. 9:2002;811-821.
16. Levenstein M.E., Kadonaga J.T. Biochemical analysis of chromatin containing recombinant Drosophila core histones. J. Biol. Chem. 277:2002;8749-8754.
17. Terrell A.R., Wongwisansri S., Pilon J.L., Laybourn P.J. Reconstitution of nucleosome positioning, remodeling, histone acetylation, and transcriptional activation on the PHO5 promoter. J. Biol. Chem. 277:2002;31038-31047.
18. Agalioti T., Chen G., Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell. 111:2002;381-392 In this outstanding paper, the authors directly address the specificity of H3 and H4 lysine acetylations and the recruitment of specific coactivators. Nucleosomal templates for the IFN-β gene are reconstituted using recombinant wild-type and mutated histones, as well as histones modified in vitro, to test the role of specific acetylation sites in gene activation. The results demonstrate a specific decoding of distinct H3 and H4 modifications by particular transcription complexes.
19. Hassan A.H., Prochasson P., Neely K.E., Galasinski S.C., Chandy M., Carrozza M.J., Workman J.L. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell. 111:2002;369-379 The results of the experiments reported in this paper demonstrate that the sustained recruitment of transcription factors to modified chromatin (i.e. its epigenetic memory state) depends on the recognition of histone acetylation by specific bromodomain components. However, the specificity relies on the protein context of the bromodomain motif.
20. Bird A.W., Yu D.Y., Pray-Grant M.G., Qiu Q., Harmon K.E., Megee P.C., Grant P.A., Smith M.M., Christman M.F. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature. 419:2002;411-415 This paper reports a three-pronged approach to understand the maintenance of genome stability. Using H4 acetylation site mutations, high-copy suppressor screens, and targeted mutations of the ESA1 gene, the authors identify a role for the NuA4 HAT complex in both NHEJ and replication coupled DSB repair. The results of ChIP experiments show that Arp4, a subunit of NuA4, is specifically recruited to the site of a DSB in vivo. Furthermore, in vitro purified NuA4 preferentially acetylates histones on reconstituted nucleosome arrays containing linear double-strand ends, as compared to circular arrays without ends.
21. Choy J.S., Kron S.J. NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol. Cell Biol. 22:2002;8215-8225 This paper reports the results of experiments on the YNG2 gene, which encodes a nonessential subunit of the NuA4 HAT complex. Genetic experiments show that loss of function of YNG2 results in defects in replication-coupled DNA damage repair.
22. Qin S., Parthun M.R. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell Biol. 22:2002;8353-8365 In this work, a comprehensive set of mutations in the acetylation sites of H3 were examined for defects in DNA-damage repair. An H3 K14,23R double point mutant impaired HR-mediated DSB repair on its own, whereas the triple K9,18,27R point mutant was synergistically defective when combined with a hat1 deletion.
23. Megee P.C., Morgan B.A., Smith M.M. Histone H4 and the maintenance of genome integrity. Genes Dev. 9:1995;1716-1727.
24. Dou Y., Gorovsky M.A. Regulation of transcription by H1 phosphorylation in Tetrahymena is position independent and requires clustered sites. Proc. Natl. Acad Sci. USA. 99:2002;6142-6146.
25. Dou Y., Bowen J., Liu Y., Gorovsky M.A. Phosphorylation and an ATP-dependent process increase the dynamic exchange of H1 in chromatin. J. Cell Biol. 158:2002;1161-1170 In this paper, the authors test the prediction that phosphorylation of a 'charge patch' of H1 regulates its dissociation from chromatin in vivo. The dissociation rates of GFP-tagged H1 constructs, with a variety mutations in the charge patch, were measured by FRAP. The results argue that phosphorylation of the H1 charge patch increases its rate of dissociation from chromatin in vivo.
26. Dou Y., Gorovsky M.A. Phosphorylation of linker histone H1 regulates gene expression in vivo by creating a charge patch. Mol. Cell. 6:2000;225-231.
27. Ren Q., Gorovsky M.A. Histone H2A.Z acetylation modulates an essential charge patch. Mol. Cell. 7:2001;1329-1335.
28. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12:2002;162-169.
29. Madigan J.P., Chotkowski H.L., Glaser R.L. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res. 30:2002;3698-3705.
30. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:1999;905-916.
31. Downs J.A., Lowndes N.F., Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature. 408:2000;1001-1004.
32. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio M.J.et al. Genomic instability in mice lacking histone H2AX. Science. 296:2002;922-927 This paper reports the construction and characterization of mouse knockout strains for the H2AX gene. The mice, and derived cell lines, are examined for viability and growth, meiotic function, genomic stability, DNA damage checkpoint response, NHEJ and HR repair function, and formation of DNA-repair foci. The results argue that phosphorylation of H2AX plays an important role in maintaining genome integrity, likely by recruiting repair functions to DSB sites.
33. ••], this work supports a model in which phosphorylation of H2AX is important in the efficient response to IR-induced damage and generation of DNA-repair foci.
34. Kobayashi J., Tauchi H., Sakamoto S., Nakamura A., Morishima K., Matsuura S., Kobayashi T., Tamai K., Tanimoto K., Komatsu K. NBS1 localizes to γ-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12:2002;1846-1851 This paper provides biochemical evidence that Nbs1, a subunit of the Rad50/Mre11/Nbs1 repair complex, physically interacts with H2AX in a phosphorylation-dependent manner. The interacting region of Nbs1 maps to an N-terminal FHA/BRCT domain. These results support a role for γ-H2AX in recruiting repair complexes to sites of damage.
35. Lachner M., Jenuwein T. The many faces of histone lysine methylation. Curr. Opin. Cell Biol. 14:2002;286-298.
36. Briggs S.D., Bryk M., Strahl B.D., Cheung W.L., Davie J.K., Dent S.Y., Winston F., Allis C.D. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:2001;3286-3295.
37. Bryk M., Briggs S.D., Strahl B.D., Curcio M.J., Allis C.D., Winston F. Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr. Biol. 12:2002;165-170.
38. Santos-Rosa H., Schneider R., Bannister A.J., Sherriff J., Bernstein B.E., Emre N.C., Schreiber S.L., Mellor J., Kouzarides T. Active genes are tri-methylated at K4 of histone H3. Nature. 419:2002;407-411.
39. Nishioka K., Chuikov S., Sarma K., Erdjument-Bromage H., Allis C.D., Tempst P., Reinberg D. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev. 16:2002;479-489.
40. Zegerman P., Canas B., Pappin D., Kouzarides T. Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J. Biol. Chem. 277:2002;11621-11624.
41. ••] leads to similar conclusions.
42. ••]. The functional consequences of H3 K79 mutations and Dot1 mutations on silencing and Sir protein binding are reported.
43. Lacoste N., Utley R.T., Hunter J.M., Poirier G.G., Cote J. Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J. Biol. Chem. 277:2002;30421-30424.
44. Park J.H., Cosgrove M.S., Youngman E., Wolberger C., Boeke J.D. A core nucleosome surface crucial for transcriptional silencing. Nat. Genet. 32:2002;273-279 This paper reports the results of an unbiased screen for mutations in H3 and H4 affecting the silencing of reporter genes inserted into the rDNA locus. The mutations mapped to a region located within the H3 and H4 histone-fold motifs comprising residues located on the nucleosome disk surface and an adjacent DNA-interacting surface. Interestingly, the side chains are around H3 K79, a target for methylation by Dot1. The finding that spatially adjacent amino acid residues affected all three forms of silencing indicates that specific interactions are important for each form of silencing.
45. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 406:2000;593-599.
46. •]) presents the first demonstration that the histone code on one tail can control that of another on a different histone tail. The work shows that the ubiquitin-conjugating enzyme Rad6 mediates methylation of H3 K4 through ubiquitination of H2B at K123 in budding yeast. H3 K4 methylation is abolished in the H2B K123R mutant, whereas H3 K4R retains H2B K123 ubiquitination, suggesting a unidirectional regulatory pathway. An H2B K123R mutation perturbs silencing at the telomere, providing functional links between Rad6-mediated H2B K123 ubiquitination, Set1-mediated H3 K4 methylation, and transcriptional silencing.
47. •].
48. Ng H.H., Xu R.M., Zhang Y., Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 277:2002;34655-34657.
49. Briggs S.D., Xiao T., Sun Z.W., Caldwell J.A., Shabanowitz J., Hunt D.F., Allis C.D., Strahl B.D. Gene silencing: trans-histone regulatory pathway in chromatin. Nature. 418:2002;498.
50. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 16:2002;6-21.
51. Tamaru H., Selker E.U. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature. 414:2001;277-283.
52. Jackson J.P., Lindroth A.M., Cao X., Jacobsen S.E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 416:2002;556-560.
53. Goll M.G., Bestor T.H. Histone modification and replacement in chromatin activation. Genes Dev. 16:2002;1739-1742.
54. Fuks F., Hurd P.J., Wolf D., Nan X., Bird A.P., Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278:2003;4035-4040.
55. Nan X., Campoy F.J., Bird A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell. 88:1997;471-481.
56. Tachibana M., Sugimoto K., Nozaki M., Ueda J., Ohta T., Ohki M., Fukuda M., Takeda N., Niida H., Kato H., Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:2002;1779-1791.
57. Grewal S.I., Elgin S.C. Heterochromatin: new possibilities for the inheritance of structure. Curr. Opin. Genet. Dev. 12:2002;178-187.
58. Volpe T.A., Kidner C., Hall I.M., Teng G., Grewal S.I., Martienssen R.A. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 297:2002;1833-1837.
59. Hall I.M., Shankaranarayana G.D., Noma K., Ayoub N., Cohen A., Grewal S.I. Establishment and maintenance of a heterochromatin domain. Science. 297:2002;2232-2237 The authors of this paper report an outstanding genetic study to unravel the pathways for the initiation and spread of heterochromatin in the mating type region of fission yeast. Swi6/HP1 is required for the spread and maintenance of heterochromatin. The centromere homologous repeat (cenH) at the mating-type region is sufficient for nucleation of heterochromatin at an ectopic, otherwise euchromatic site. Silencing at the mat2/3 region is intact in the mutants of RNAi machinery, whereas upon erasing the epigenetic imprint, silencing at the mat2/3 region is strikingly lost in the ago1Δ, dcrΔ, and rdpΔ strains, suggesting that RNAi machinery is dispensable for maintenance of heterochromatin but required for initiation of heterochromatin.
60. Mochizuki K., Fine N.A., Fujisawa T., Gorovsky M.A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell. 110:2002;689-699.
61. Taverna S.D., Coyne R.S., Allis C.D. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell. 110:2002;701-711.
62. Heard E., Rougeulle C., Arnaud D., Avner P., Allis C.D., Spector D.L. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell. 107:2001;727-738.
63. Sleutels F., Zwart R., Barlow D.P. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature. 415:2002;810-813.