Regulation of histone H2A and H2B ubiquitylation

Briefings in Functional Genomics and Proteomics

Volumn 5, Issue 3, 2006, Pages 179-189

  Osley, Mary Ann ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Bbiquitin conjugation; Histones H2A and H2B; Transcription activation and silencing

Indexed keywords

HISTONE H2A; HISTONE H2B; UBIQUITIN; HISTONE; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN CONJUGATING ENZYME;

CELL FUNCTION; CHROMATIN; GENETIC TRANSCRIPTION; NONHUMAN; PROTEIN BINDING; PROTEIN METHYLATION; REGULATORY MECHANISM; REVIEW; UBIQUITINATION; ANIMAL; BIOLOGICAL MODEL; GENETICS; HUMAN; METABOLISM; METHYLATION;

ANIMALS; HISTONES; HUMANS; METHYLATION; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

EID: 33947509939     PISSN: 14739550     EISSN: 14774062     Source Type: Journal    
DOI: 10.1093/bfgp/ell022     Document Type: Review

References (104)

1. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001;70:503-33.
2. Pickart CM, Eddins MJ. Ubiquitin: Structures, functions, mechanisms. Biochim Biophys Acta 2004;1695:55-72.
3. Daniel JA, Torok MS, Sun ZW, et al. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 2004;279:1867-71.
4. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2001;2:195-201.
5. Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003;19:141-72.
6. Osley MA, Fleming AB, Kao C. Histone ubiquitylation and the regulation of transcription. In. In: Laurent B (ed). Chromatin Dynamics in Cellular Function. Edition Heidelberg, Springer-Verlag 2005.
7. Ballal NR, Kang YJ, Olson MO, Busch H. Changes in nucleolar proteins and their phosphorylation patterns during liver regeneration. J Biol Chem 1975;250:5921-5.
8. Goldknopf IL, Taylor CW, Baum RM, et al. Isolation and characterization of protein A24, a "histone-like" non-histone chromosomal protein. J Biol Chem 1975;250: 7182-7.
9. Thorne AW, Sautiere P, Briand G, Crane-Robinson C. The structure of ubiquitinated histone H2B. Embo J 1987;6: 1005-10.
10. Robzyk K, Recht J, Osley MA. Rad6-dependent ubiquitination of histone H2B in yeast. Science 2000;287:501-4.
11. Luger K, Mader AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997;389:251-60.
12. Jentsch S, McGrath JP, Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature 1987;329:131-4.
13. Zhu B, Zheng Y, Pham AD, et al. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol Cell 2005;20:601-11.
14. Sung P, Prakash S, Prakash L. The RAD6 protein of Saccharomyces cerevisiae polyubiquitinates histones, and its acidic domain mediates this activity. Genes Dev 1988;2: 1476-85.
15. Prakash L. The structure and function of RAD6 and RAD18 DNA repair genes of Saccharomyces cerevisiae. Genome 1989;31:597-600.
16. Koken MH, Smit EM, Jaspers-Dekker I, et al. Localization of two human homologs, HHR6A and HHR6B, of the yeast DNA repair gene RAD6 to chromosomes Xq24-q25 and 5q23-q31. Genomics 1992;12:447-53.
17. Koken M, Reynolds P, Bootsma D, et al. Dhr6, a Drosophila homolog of the yeast DNA-repair gene RAD6. Proc Natl Acad Sci USA 1991;88:3832-6.
18. Koken MH, Reynolds P, Jaspers-Dekker I, et al. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc Natl Acad Sci USA 1991; 88:8865-9.
19. Reynolds P, Koken MH, Hoeijmakers JH, et al. The rhp6+ gene of Schizosaccharomyces pombe: A structural and functional homolog of the RAD6 gene from the distantly related yeast Saccharomyces cerevisiae. Embo J 1990;9:1423-30.
20. Sung P, Prakash S, Prakash L. Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions. Proc Natl Acad Sci USA 1990;87:2695-9.
21. Morrison A, Miller EJ, Prakash L. Domain structure and functional analysis of the carboxyl-terminal polyacidic sequence of the RAD6 protein of Saccharomyces cerevisiae. Mol Cell Biol 1988;8:1179-85.
22. Dor Y, Raboy B, Kulka RG. Role of the conserved carboxy-terminal alpha-helix of Rad6p in ubiquitination and DNA repair. Mol Microbiol 1996;21:1197-206.
23. Raboy B, Kulka RG. Role of the C-terminus of Saccharomyces cerevisiae ubiquitin-conjugating enzyme (Rad6) in substrate and ubiquitin-protein-ligase (E3-R) interactions. Eur J Biochem 1994;221:247-51.
24. Worthylake DK, Prakash S, Prakash L, Hill CP. Crystal structure of the Saccharomyces cerevisiae ubiquitin-conjugating enzyme Rad6 at 2.6 A resolution. J Biol Chem 1998;273:6271-6.
25. Sarcevic B, Mawson A, Baker RT, Sutherland RL. Regulation of the ubiquitin-conjugating enzyme hHR6A by CDK-mediated phosphorylation. Embo J 2002; 21:2009-18.
26. Wood A, Schneider J, Dover J, et al. The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell 2005;20:589-99.
27. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol Gen Genet 1981;184:471-8.
28. Broomfield S, Hryciw T, Xiao W. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat Res 2001;486:167-84.
29. Xiao W, Chow BL, Broomfield S, Hanna M. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways. Genetics 2000;155:1633-41.
30. Hoege C, Pfander B, Moldovan GL, et al. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002;419:135-41.
31. Sung P, Berleth E, Pickart C, et al. Yeast RAD6 encoded ubiquitin conjugating enzyme mediates protein degradation dependent on the N-end-recognizing E3 enzyme. Embo J 1991;10:2187-93.
32. Watkins JF, Sung P, Prakash S, Prakash L. The extremely conserved amino terminus of RAD6 ubiquitin-conjugating enzyme is essential for amino-end rule-dependent protein degradation. Genes Dev 1993;7:250-61.
33. Ulrich HD, Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. Embo J 2000;19:3388-97.
34. Xie Y, Varshavsky A. The E2-E3 interaction in the N-end rule pathway: the RING-H2 finger of E3 is required for the synthesis of multiubiquitin chain. Embo J 1999;18:6832-44.
35. Wood A, Krogan NJ, Dover J, et al. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell 2003;11:267-74.
36. Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, et al. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 2003;11:261-6.
37. Joazeiro CA, Weissman AM. RING finger proteins: Mediators of ubiquitin ligase activity. Cell 2000;102:549-52.
38. Bray S, Musisi H, Bienz M. Bre1 is required for Notch signaling and histone modification. Dev Cell 2005;8:279-86.
39. Davie JR, Murphy LC. Level of ubiquitinated histone H2B in chromatin is coupled to ongoing transcription. Biochemistry 1990;29:4752-7.
40. Kao CF, Hillyer C, Tsukuda T, et al. Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev 2004;18:184-95.
41. Cismowski MJ, Laff GM, Solomon MJ, Reed SI. KIN28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity. Mol Cell Biol 1995;15:2983-92.
42. Xiao T, Kao CF, Krogan NJ, et al. Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol Cell Biol 2005;25:637-51.
43. Shi X, Finkelstein A, Wolf AJ, et al. Paf1p, an RNA polymerase II-associated factor in Saccharomyces cerevisiae, may have both positive and negative roles in transcription. Mol Cell Biol 1996;16:669-76.
44. Ng HH, Dole S, Struhl K. The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J Biol Chem 2003;278: 33625-8.
45. Keogh MC, Podolny V, Buratowski S. Bur1 kinase is required for efficient transcription elongation by RNA polymerase II. Mol Cell Biol 2003;23:7005-18.
46. Wood A, Schneider J, Dover J, et al. The Paf1 complex is essential for histone monoubiquitination by the Rad6/Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J Biol Chem 2003;37:34739-42.
47. Laribee RN, Krogan NJ, Xiao T, et al. BUR kinase selectively regulates H3 K4 trimethylation and H2B ubiquitylation through recruitment of the PAF elongation complex. Curr Biol 2005;15:1487-93.
48. Henry KW, Wyce A, Lo WS, et al. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 2003;17:2648-63.
49. Turner SD, Ricci AR, Petropoulos H, et al. The E2 ubiquitin conjugase Rad6 is required for the ArgR/Mcm1 repression of ARG1 transcription. Mol Cell Biol 2002;22: 4011-9.
50. Carvin CD, Kladde MP. Effectors of lysine 4 methylation of histone H3 in Saccharomyces cerevisiae are negative regulators of PHO5 and GAL1-10. J Biol Chem 2004;279: 33057-62.
51. Goldknopf IL, Sudhakar S, Rosenbaum F, Busch H. Timing of ubiquitin synthesis and conjugation into protein A24 during the HeLa cell cycle. Biochem Biophys Res Commun 1980;95:1253-60.
52. Bradbury EM. Reversible histone modifications and the chromosome cell cycle. Bioessays 1992;14:9-16.
53. Mueller RD, Yasuda H, Hatch CL, et al. Identification of ubiquitinated histones 2A and 2B in Physarum polycephalum. Disappearance of these proteins at metaphase and reappearance at anaphase. J Biol Chem 1985;260:5147-53.
54. Dong L, Xu CW. Carbohydrates induce mono-ubiquitination of H2B in yeast. J Biol Chem 2004;279: 1577-80.
55. Amerik AY, Li SJ, Hochstrasser M. Analysis of the deubiquitinating enzymes of the yeast Saccharomyces cerevisiae. Biol Chem 2000;381:981-92.
56. Hochstrasser M. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 1995;7:215-23.
57. Wilkinson KD. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. Faseb J 1997;11: 1245-56.
58. Emre NC, Ingvarsdottir K, Wyce A, et al. Maintenance of low histone ubiquitylation by ubp10 correlates with telomere-proximal sir2 association and gene silencing. Mol Cell 2005;17:585-94.
59. Gardner RG, Nelson ZW, Gottschling DE. Ubp10/Dot4p regulates the persistence of ubiquitinated histone H2B: Distinct roles in telomeric silencing and general chromatin. Mol Cell Biol 2005;25:6123-39.
60. van Leeuwen F, Gottschling DE. Genome-wide histone modifications: gaining specificity by preventing promiscuity. Curr Opin Cell Biol 2002;14:756-62.
61. van der Knaap JA, Kumar BR, Moshkin YM, et al. GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Mol Cell 2005;17:695-707.
62. Sun ZW, Allis CD. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 2002;418:104-8.
63. Ng HH, Xu RM, Zhang Y, Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dotl-mediated methylation of histone H3 lysine 79. J Biol Chem 2002;277:34655-7.
64. Briggs SD, Xiao T, Sun ZW, et al. Gene silencing: Transhistone regulatory pathway in chromatin. Nature 2002;418: 498.
65. Dover J, Schneider J, Tawiah-Boateng MA, et al. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 2002; 277:28368-71.
66. Strahl BD, Ohba R, Cook RG, Allis CD. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci USA 1999;96:14967-72.
67. Santos-Rosa H, Schneider R, Bannister AJ, et al. Active genes are tri-methylated at K4 of histone H3. Nature 2002; 419:407-11.
68. Ng HH, Ciccone DN, Morshead KB, et al. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: A potential mechanism for position-effect variegation. Proc Natl Acad Sci USA 2003;100:1820-5.
69. Noma K, Grewal SI. Histone H3 lysine 4 methylation is mediated by Set1 and promotes maintenance of active chromatin states in fission yeast. Proc Natl Acad Sci USA 2002;99(Suppl 4)16438-45.
70. Briggs SD, Bryk M, Strahl BD, et al. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 2001;15:3286-95.
71. Bryk M, Briggs SD, Strahl BD, et al. Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 2002;12:165-70.
72. Ng HH, Robert F, Young RA, Struhl K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 2003;11:709-19.
73. Gerber M, Shilatifard A. Transcriptional elongation by RNA polymerase II and histone methylation. J Biol Chem 2003;278:26303-6.
74. Krogan NJ, Dover J, Wood A, et al. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation. Mol Cell 2003;11:721-9.
75. Henry KW, Berger SL. Trans-tail histone modifications: Wedge or bridge?. Nat Struct Biol 2002;9:565-6.
76. Ezhkova E, Tansey WP. Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol Cell 2004;13:435-42.
77. Miller T, Krogan NJ, Dover J, et al. COMPASS: A complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci USA 2001;98:12902-7.
78. van Leeuwen F, Gafken PR, Gottschling DE. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002;109:745-56.
79. Shahbazian MD, Zhang K, Grunstein M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol Cell 2005;19:271-7.
80. Fingerman IM, Wu CL, Wilson BD, Briggs SD. Global loss of Set1-mediated H3 Lys4 trimethylation is associated with silencing defects in Saccharomyces cerevisiae. J Biol Chem 2005; 280:28761-5.
81. Schlichter A, Cairns BR. Histone trimethylation by Set1 is coordinated by the RRM, autoinhibitory, and catalytic domains. Embo J 2005;24:1222-31.
82. Schneider J, Wood A, Lee JS, et al. Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 2005;19:849-56.
83. Bohm L, Crane-Robinson C, Sautiere P. Proteolytic digestion studies of chromatin core-histone structure. Identification of a limit peptide of histone H2A. Eur J Biochem 1980;106:525-30.
84. Swerdlow PS, Schuster T, Finley D. A conserved sequence in histone H2A which is a ubiquitination site in higher eucaryotes is not required for growth in Saccharomyces cerevisiae. Mol Cell Biol 1990;10:4905-11.
85. Baarends WM, Hoogerbrugge JW, Roest HP, et al. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 1999;207:322-33.
86. Baarends WM, Wassenaar E, van der Laan R, et al. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 2005;25:1041-53.
87. Smith KP, Byron M, Clemson CM, Lawrence JB. Ubiquitinated proteins including uH2A on the human and mouse inactive X chromosome: Enrichment in gene rich bands. Chromosoma 2004;113:324-35.
88. de Napoles M, Mermoud JE, Wakao R, et al. Polycomb group proteins Ring1A/ B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 2004;7:663-76.
89. Hanson RD, Hess JL, Yu BD, et al. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci USA 1999; 96:14372-7.
90. Dejardin J, Cavalli G. Epigenetic inheritance of chromatin states mediated by Polycomb and trithorax group proteins in Drosophila. Prog Mol Subcell Biol 2005;38:31-63.
91. Wang H, Wang L, Erdjument-Bromage H, et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004;431:873-8.
92. Cao R, Tsukada Y, Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 2005;20:845-54.
93. Fang J, Chen T, Chadwick B, et al. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem 2004; 279:52812-5.
94. Zhang Y, Cao R, Wang L, Jones RS. Mechanism of Polycomb group gene silencing. Cold Spring Harb Symp Quant Biol 2004;69:309-17.
95. Wang L, Brown JL, Cao R, et al. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 2004;14: 637-46.
96. Muller J, Hart CM, Francis NJ, et al. Histone methyl-transferase activity of a Drosophila Polycomb group repressor complex. Cell 2002;111:197-208.
97. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002;298:1039-43.
98. Cohen HR, Royce-Tolland ME, Worringer KA, Panning B. Chromatinmodifications on the inactive X chromosome. Prog Mol Subcell Biol 2005;38:91-122.
99. Cai SY, Babbitt RW, Marchesi VT. A mutant deubiquitinating enzyme (Ubp-M) associates with mitotic chromosomes and blocks cell division. Proc Natl Acad Sci USA 1999;96:2828-33.
100. Chadwick BP, Willard HF. Chromatin of the Barr body: Histone and non-histone proteins associated with or excluded from the inactive X chromosome. Hum Mol Genet 2003;12:2167-78.
101. Francis NJ, Kingston RE, Woodcock CL. Chromatin compaction by a polycomb group protein complex. Science 2004;306:1574-7.
102. Hernandez-Munoz I, Lund AH, van der Stoop P, et al. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci USA 2005;102:7635-40.
103. Jason LJ, Finn RM, Lindsey G, Ausio J. Histone H2A ubiquitination does not preclude histone H1 binding, but it facilitates its association with the nucleosome. J Biol Chem 2005;280:4975-82.
104. Dellino GI, Schwartz YB, Farkas G, et al. Polycomb silencing blocks transcription initiation. Mol Cell 2004;13: 887-93.