A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin

Genes and Development

Volumn 18, Issue 11, 2004, Pages 1251-1262

  Schotta, Gunnar ^a   Lachner, Monika ^a   Sarma, Kavitha ^b   Ebert, Anja ^c   Sengupta, Roopsha ^a   Reuter, Gunter ^c   Reinberg, Danny ^b   Jenuwein, Thomas ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Combinatorial histone methyl marks; Heterochromatin; Histone code; Histone H4 Lys 20; Mono , di , trimethylation; Suv4 20h HMTases

Indexed keywords

COMPLEMENTARY DNA; GLUTATHIONE TRANSFERASE; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HYBRID PROTEIN; RNA;

ARTICLE; CHROMATIN; DNA TEMPLATE; DROSOPHILA; ENZYME ASSAY; ESCHERICHIA COLI; EVOLUTION; GENE SILENCING; HETEROCHROMATIN; METHYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN PURIFICATION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; FIBROBLASTS; GENE SILENCING; GENES, SUPPRESSOR; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; MAMMALS; METHYLATION; METHYLTRANSFERASES; MICE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; MAMMALIA;

EID: 2642542643     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.300704     Document Type: Article

References (60)

1. Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C., and Kouzarides T. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
2. Beisel, C., Imhof, A., Greene, J., Kremmer, E., and Sauer, F. 2002. Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature 419: 857-862.
3. Bernard, P. and Allshire, R. 2002. Centromeres become unstuck without heterochromatin. Trends Cell. Biol. 12: 419-424.
4. Birchler, J.A., Bhadra, M.P., and Bhadra, U. 2000. Making noise about silence: Repression of repeated genes in animals. Curr. Opin. Genet. Dev. 10: 211-216.
5. Brummelkamp, T.R., Bernards, R., and Agami, R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
6. Cleard, F., Delattre, M., and Spierer, P. 1997. SU(VAR)3-7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation. EMBO J. 16: 5280-5288.
7. Czermin, B., Melfi, R., McCabe, D., Seitz, V., Imhof, A., and Pirrotta, V. 2002. Drosophila Enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal polycomb sites. Cell 111: 185-196.
8. DeLange, R.J., Hooper, J.A., and Smith, E.L. 1973. Histone H3.3: Sequence studies on the cyanogen bromide peptides; complete amino acid sequence of calf thymus histone 3. J. Biol. Chem. 248: 3261-3274.
9. Eissenberg, J.C., James, T.C., Foster-Hartnett, D.M., Hartnett, T., Ngan, V.K.W., and Elgin, S.C. 1990. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. 87: 9923-9927.
10. Fang, J., Feng, Q., Ketel, C.S., Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., Simon, J.A., and Zhang, Y. 2002. Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12: 1086-1099.
11. Fischle, W., Wang, Y., and Allis, C.D. 2003. Extending the histone code: Modification cassettes and switches. Nature 425: 475-479.
12. Hall, I.M., Shankaranarayana, G.D., Noma, K., Ayoub, N., Cohen, A., and Grewal, S.I. 2002. Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237.
13. Jenuwein, T. 2002. Molecular biology: An RNA-guided pathway for the epigenome. Science 297: 2215-2218.
14. Jenuwein, T. and Allis, C.D. 2001. Translating the histone code. Science 293: 1074-1080.
15. Karpen, G.H. and Allshire, R.C. 1997. The case for epigenetic effects on centromere identity and function. Trends Genet. 13: 489-496.
16. Kohlmaier, A., Savarese, F., Lachner, M., Martens, J., Jenuwein, T., and Wutz, A. 2004. Kinetics of histone methylation triggered by Xist reveals an epigenetic memory independent of silencing. PLOS (in press).
17. Kouzarides, T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12: 198-209.
18. Kurdistani, S.K. and Grunstein M 2003. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell. Biol. 4: 276-284.
19. Kuzmichev, A., Nishioka, K., Erdiument-Bromage, H., Tempst, P., and Reinberg, D. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes & Dev. 16: 2893-2905.
20. Lachner, M. and Jenuwein, T. 2002. The many faces of histone lysine methylation. Curr. Opin. Cell. Biol. 14: 286-298.
21. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
22. Lachner, M., O'Sullivan, R.J., and Jenuwein, T. 2003. An epigenetic road map for histone lysine methylation. J. Cell. Sci. 116: 2117-2124.
23. Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251-260.
24. Milne, T.A., Briggs, S.D., Brock, H.W., Martin, M.E., Gibbs, D., Allis, C.D., and Hess, J.L. 2002. MLL Targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10: 1107-1117.
25. Müller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E., and Simon, J.A. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
26. Nishioka, K., Rice, J.C., Sarma, K., Erdjument-Bromage, H., Werner, J., Wang, Y., Chuikov, S., Valenzuela, P., Tempst, P., Steward, R., et al. 2002a. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and Is associated with silent chromatin. Mol. Cell 9: 1201-1213.
27. Nishioka, K., Chuikov, S., Sarma, K., Erdjument-Bromage, H., Allis, C.D., Tempst, P., and Reinberg, D. 2002b. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes & Dev. 16: 479-489.
28. Notredame, C., Higgins, D.G., and Heringa, J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217.
29. Okamoto, I., Otte, A.P., Allis, C.D., Reinberg, D., and Heard, E. 2004. Epigenetic dynamics of imprinted x inactivation during early mouse development. Science 303: 644-649.
30. Paik, W.K. and Kim, S. 1971. Protein methylation. Science 174: 114-119.
31. Pal-Bhadra, M., Leibovitch, B.A., Gandhi, S.G., Rao, M., Bhadra, U., Birchler, J.A., and Elgin, S.C. 2004. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669-672.
32. Peters, A.H., Kubicek, S., Mechtler, K., O'Sullivan, R.J., Derijck, A.A., Perez-Burgos, L., Kohlmaier, A., Opravil, S., Tachibana, M., Shinkai, Y., et al. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12: 1577-1589.
33. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B., and Zhang, Y. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135.
34. Rayasam, G.V., Wendling, O., Angrand, P.O., Mark, M., Niederreither, K., Song, L., Lerouge, T., Hager, G.L., Chambon, P., and Losson, R. 2003. NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 22: 3153-3163.
35. 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., et al. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599.
36. Reuter, G. and Spierer, P. 1992. Position effect variegation and chromatin proteins. Bioessays 14: 605-612.
37. Rice, J.C., Nishioka, K., Sarma, K., Steward, R., Reinberg, D., and Allis, C.D. 2002. Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes & Dev. 16: 2225-2230.
38. Rice, J.C., Briggs, S.D., Ueberheide, B., Barber, C.M., Shabanowitz, J., Hunt, D.F., Shinkai, Y., and Allis, C.D. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12: 1591-1598.
39. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J., and Kouzarides, T. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411
40. Sarg, B., Koutzamani, E., Helliger, W., Rundquist, I., and Lindner, H.H. 2002. Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J. Biol Chem. 277: 39195-39201.
41. Schotta, G., Ebert, A., Krauss, V., Fischer, A., Hoffmann, J., Rea, S., Jenuwein, T., Dorn, R., and Reuter, G. 2002. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21: 1121-1131.
42. Schotta, G., Ebert, A., Dorn, R., and Reuter, G. 2003. Position-effect variegation and the genetic dissection of chromatin regulation in Drosophila. Semin. Cell. Dev. Biol. 14: 67-75.
43. Schramke, V. and Allshire, R. 2003. Hairpin RNAs and retrotransposon LTRs effect RNAi and chromatin-based gene silencing. Science 301: 1069-1074.
44. Silva, J., Mak, W., Zvetkova, I., Appanah, R., Nesterova, T.B., Webster, Z., Peters, A.H., Jenuwein, T., Otte, A.P., and Brockdorff, N. 2003. Establishment of histone H3 methylation on the inactive X chromosome requires transient recruitment of eed-enx1 polycomb group complexes. Dev. Cell. 4: 481-495.
45. Sims, R.J., Nishioka, K., and Reinberg, D. 2003. Histone lysine methylation: A signature for chromatin function. Trends Genet. 19: 629-639.
46. Sinclair, D.A.R., Mottus, R.C., and Grigliatti, T.A. 1983. Genes which suppress position effect variegation in Drosophila melanogaster are clustered. Mol. Gen. Genet. 191: 326-333.
47. Strahl, B.D. and Allis, C.D. 2000. The language of covalent histone modifications. Nature 403: 41-45.
48. Tachibana, M., Sugimoto, K., Fukushima, T., and Shinkai, Y. 2001. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 276: 25309-25317.
49. Tagami, H., Ray-Gallet, D., Almouzni, G., and Nakatani, Y. 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61.
50. Tamaru, H., Zhang, X., McMillen, D., Singh, P.B., Nakayama, J., Grewal, S.I., Allis, C.D., Cheng, X., and Selker, E.U. 2003. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat. Genet. 34: 75-79.
51. Tschiersch, B., Hofmann, A., Krauss, V., Dom, R., Korge, G., and Reuter, G. 1994. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 13: 3822-3831.
52. Turner, B.M. 2000. Histone acetylation and an epigenetic code. Bioessays 22: 836-845.
53. van Holde, K.E. 1988. Chromatin. Springer, New York.
54. Vaquero, A., Loyola, A., and Reinberg, D. 2003 The constantly changing face of chromatin. Sci. Aging Knowl. Environ. 14: RE4.http://sageke.sciencemag.org/cgi/content/full/sageke; 2003/14/re4.
55. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I., and Moazed, D. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
56. Vermaak, D., Ahmad, K., and Henikoff, S. 2003. Maintenance of chromatin states: An open-and-shut case. Curr. Opin. Cell. Biol. 15: 266-274.
57. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., and Martienssen, R.A. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837
58. Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Borchers, C., Tempst, P., and Zhang, Y. 2001. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol. Cell 8: 1207-1217.
59. Xiao, B., Wilson, J.R., and Gamblin, S.J. 2003. SET domains and histone methylation. Curr. Opin. Struct. Biol. 13: 699-705.
60. Yang, L., Xia, L., Wu, D.Y., Wang, H., Chansky, H.A., Schubach, W.H., Hickstein, D.D., and Zhang, Y. 2002. Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor. Oncogene 21: 148-152.