The N-Terminus of Drosophila SU(VAR)3-9 Mediates Dimerization and Regulates Its Methyltransferase Activity

Biochemistry

Volumn 43, Issue 12, 2004, Pages 3740-3749

  Eskeland, Ragnhild ^a   Czermin, Birgit ^a   Boeke, Jörn ^a   Bonaldi, Tiziana ^a   Regula, Jörg T ^a   Imhof, Axel ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CONCENTRATION (PROCESS); DIMERS; MOLECULAR WEIGHT; PURIFICATION;

CENTROMERIC HETEROCHROMATIN; LINEAR DEPENDENCE;

ENZYMES;

DROSOPHILA SU(VAR)3-9 PROTEIN; HISTONE METHYLTRANSFERASE SU(VAR)3-9; LYSINE; METHYLTRANSFERASE; PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CENTROMERE; CHROMATIN STRUCTURE; DIMERIZATION; DROSOPHILA; ENZYME ACTIVITY; ENZYME REGULATION; ESCHERICHIA COLI; EUKARYOTE; GEL FILTRATION CHROMATOGRAPHY; GENE DELETION; HETEROCHROMATIN; IN VITRO STUDY; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; DIMERIZATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; ISOENZYMES; KINETICS; LYSINE; METHYLATION; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; SEQUENCE DELETION;

ESCHERICHIA COLI; EUKARYOTA;

EID: 1642369447     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035964s     Document Type: Article

References (58)

1. Choo, K. H. (1997) Centromere DNA dynamics: latent centromeres and neocentromere formation. Am. J. Hum. Genet. 61, 1225-33.
2. Karpen, G. H., and Allshire, R. C. (1997) The case for epigenetic effects on centromere identity and function. Trends Genet. 13, 489-96.
3. Earnshaw, W. C., and Cooke, C. A. (1989) Proteins of the inner and outer centromere of mitotic chromosomes. Genome 31, 541-52.
4. Sugata, N., Li, S., Earnshaw, W. C., Yen, T. J., Yoda, K., Masumoto, H., Munekata, E., Warburton, P. E., and Todokoro, K. (2000) Human CENP-H multimers colocalize with CENP-A and CENP-C at active centromere-kinetochore complexes. Hum. Mol. Genet. 9, 2919-26.
5. Weimer, R., Haaf, T., Kruger, J., Poot, M., and Schmid, M. (1992) Characterization of centromere arrangements and test for random distribution in G0, G1, S, G2, G1, and early S′ phase in human lymphocytes. Hum. Genet. 88, 673-82.
6. Zalensky, A. O., Allen, M. J., Kobayashi, A., Zalenskaya, I. A., Balhorn, R., and Bradbury, E. M. (1995) Well-defined genome architecture in the human sperm nucleus. Chromosoma 103, 577-90.
7. Warburton, P. E., Dolled, M., Mahmood, R., Alonso, A., Li, S., Naritomi, K., Tohma, T., Nagai, T., Hasegawa, T., Ohashi, H., Govaerts, L. C., Eussen, B. H., Van Hemel, J. O., Lozzio, C., Schwartz, S., Dowhanick-Morrissette, J. J., Spinner, N. B., Rivera, H., Crolla, J. A., Yu, C., and Warburton, D. (2000) Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am. J. Hum. Genet. 66, 1794-806.
8. Depinet, T. W., Zackowski, J. L., Earnshaw, W. C., Kaffe, S., Sekhon, G. S., Stallard, R., Sullivan, B. A., Vance, G. H., Van Dyke, D. L., Willard, H. F., Zinn, A. B., and Schwartz, S. (1997) Characterization of neo-centromeres in marker chromosomes lacking detectable alpha-satellite DNA. Hum. Mol. Genet. 6, 1195-204.
9. Richards, E. J., and Elgin, S. C. (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108, 489-500.
10. Reuter, G., and Spierer, P. (1992) Position effect variegation and chromatin proteins. Bioessays 14, 605-12.
11. Henikoff, S. (1992) Position effect and related phenomena. Curr. Opin. Genet. Dev. 2, 907-12.
12. Choo, K. H. (2000) Centromerization. Trends Cell Biol. 10, 18-28.
13. Pidoux, A. L., and Allshire, R. C. (2000) Centromeres: getting a grip of chromosomes. Curr. Opin. Cell Biol. 12, 308-19.
14. 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, 1121-31.
15. 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., and Jenuwein, T. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-9.
16. 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.
17. Ivanova, A. V., Bonaduce, M. J., Ivanov, S. V., and Klar, A. J. (1998) The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nat. Genet. 19, 192-5.
18. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil, S., Doyle, M., Sibilia, M., and Jenuwein, T. (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-37.
19. Firestein, R., Cui, X., Huie, P., and Cleary, M. L. (2000) Set domain-dependent regulation of transcriptional silencing and growth control by SUV39H1, a mammalian ortholog of Drosophila Su(var)3-9. Mol. Cell Biol. 20, 4900-9.
20. Snowden, A. W., Gregory, P. D., Case, C. C., and Pabo, C. O. (2002) Gene-Specific Targeting of H3K9 Methylation Is Sufficient for Initiating Repression In Vivo. Curr. Biol. 12, 2159-66.
21. Min, J., Zhang, X., Cheng, X., Grewal, S. I., and Xu, R. M. (2002) Structure of the SET domain histone lysine methyltransferase Clr4. Nat. Struct. Biol. 9, 828-32.
22. Zhang, X., Tamaru, H., Khan, S. I., Horton, J. R., Keefe, L. J., Selker, E. U., and Cheng, X. (2002) Structure of the Neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase. Cell 111, 117-27.
23. Trievel, R. C., Beach, B. M., Dirk, L. M., Houtz, R. L., and Hurley, J. H. (2002) Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell 111, 91-103.
24. Wilson, J. R., Jing, C., Walker, P. A., Martin, S. R., Howell, S. A., Blackburn, G. M., Gamblin, S. J., and Xiao, B. (2002) Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell 111, 105-15.
25. Xiao, B., Jing, C., Wilson, J. R., Walker, P. A., Vasisht, N., Kelly, G., Howell, S., Taylor, I. A., Blackburn, G. M., and Gamblin, S. J. (2003) Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature 421, 652-6.
26. Manzur, K. L., Farooq, A., Zeng, L., Plotnikova, O., Koch, A. W., Sachchidanand, and Zhou, M. M. (2003) A dimeric viral SET domain methyltransferase specific to Lys27 of historic H3. Nat. Struct. Biol. 10, 187-96.
27. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S., and Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-43.
28. Muller, 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.
29. Kuzmichev, A., Nishioka, K., Erdjument-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, 2893-905.
30. 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, 185-96.
31. 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, 1086-99.
32. Nishioka, K., Rice, J. C., Sarma, K., Erdjument-Bromage, H., Werner, J., Wang, Y., Chuikov, S., Valenzuela, P., Tempst, P., Steward, R., Lis, J. T., Allis, C. D., and Reinberg, D. (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201-13.
33. Melcher, M., Schmid, M., Aagaard, L., Selenko, P., Laible, G., and Jenuwein, T. (2000) Structure-function analysis of SUV39H1 reveals a dominant role in heterochromatin organization, chromosome segregation, and mitotic progression. Mol. Cell Biol. 20, 3728-41.
34. Yamamoto, K., and Sonoda, M. (2003) Self-interaction of heterochromatin protein 1 is required for direct binding to histone methyltransferase, SUV39H1. Biochem. Biophys. Res. Commun. 301, 287-92.
35. Melnick, A., and Licht, J. D. (1999) Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 93, 3167-215.
36. Kentsis, A., Gordon, R. E., and Borden, K. L. (2002) Control of biochemical reactions through supramolecular RING domain self-assembly. Proc. Natl. Acad. Sci. U.S.A. 99, 15404-9.
37. Henikoff, S. (1996) Dosage-dependent modification of position-effect variegation in Drosophila. Bioessays 18, 401-9.
38. Zhao, T., and Eissenberg, J. C. (1999) Phosphorylation of heterochromatin protein 1 by casein kinase II is required for efficient heterochromatin binding in Drosophila. J. Biol. Chem. 274, 15095-100.
39. Luger, K., Mader, 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. 251-60.
40. Brackertz, M., Boeke, J., Zhang, R., and Renkawitz, R. (2002) Two highly related p66 proteins comprise a new family of potent transcriptional repressors interacting with MBD2 and MBD3. J. Biol. Chem. 277, 40958-66.
41. Ogawa, H., Ishiguro, K., Gaubatz, S., Livingston, D. M., and Nakatani, Y. (2002) A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 296, 1132-6.
42. 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, 25309-17.
43. Czermin, B., Schotta, G., Hulsmann, B. B., Brehm, A., Becker, P. B., Reuter, G., and Imhof, A. (2001) Physical and functional association of SU(VAR)3-9 and HDAC1 in Drosophila. EMBO Rep. 2, 915-9.
44. 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, 407-11.
45. Tamaru, H., Zhang, X., McMillen, D., Singh, P. B., Nakayama, J. I., 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, 75-9.
46. Bheemanaik, S., Chandrashekaran, S., Nagaraja, V., and Rao, D. N. (2003) Kinetic and catalytic properties of dimeric KpnI DNA methyltransferase. J. Biol. Chem. 278, 7863-74.
47. Schymkowitz, J. W., Rousseau, F., Wilkinson, H. R., Friedler, A., and Itzhaki, L. S. (2001) Observation of signal transduction in three-dimensional domain swapping. Nat. Struct. Biol. 8, 888-92.
48. Hoffman, D. R., Marion, D. W., Cornatzer, W. E., and Duerre, J. A. (1980) S-Adenosylmethionine and S-adenosylhomocystein metabolism in isolated rat liver. Effects of L-methionine, L-homocystein, and adenosine. J. Biol. Chem. 255, 10822-7.
49. Larsson, J., and Rasmuson-Lestander, A. (1994) Molecular cloning of the S-adenosylmethionine synthetase gene in Drosophila melanogaster. FEBS Lett. 342, 329-33.
50. Zhang, X., Yang, Z., Khan, S. I., Horton, J. R., Tamaru, H., Selker, E. U., and Cheng, X. (2003) Structural basis for the product specificity of histone lysine methyltransferases. Mol. Cell 12, 177-85.
51. Baumbusch, L. O., Thorstensen, T., Krauss, V., Fischer, A., Naumann, K., Assalkhou, R., Schulz, I., Reuter, G., and Aalen, R. B. (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 29, 4319-33.
52. Ng, H. H., Robert, F., Young, R. A., and Struhl, K. (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709-19.
53. Aagaard, L., Schmid, M., Warburton, P., and Jenuwein, T. (2000) Mitotic phosphorylation of SUV39H1, a novel component of active centromeres, coincides with transient accumulation at mammalian centromeres. J. Cell Sci. 113, 817-29.
54. Wang, H., An, W., Cao, R., Xia, L., Erdjument-Bromage, H., Chatton, B., Tempst, P., Roeder, R. G., and Zhang, Y. (2003) mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Mol. Cell 12, 475-87.
55. Tang, J., Frankel, A., Cook, R. J., Kim, S., Paik, W. K., Williams, K. R., Clarke, S., and Herschman, H. R. (2000) PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J. Biol. Chem. 275, 7723-30.
56. Tang, J., Gary, J. D., Clarke, S., and Herschman, H. R. (1998) PRMT 3, a type I protein arginine N-methyltransferase that differs from PRMT1 in its oligomerization, subcellular localization, substrate specificity, and regulation. J. Biol. Chem. 273, 16935-45.
57. Newcomer, M. E. (2002) Protein folding and three-dimensional domain swapping: a strained relationship? Curr. Opin. Struct. Biol. 12, 48-53.
58. McGee, A. W., Dakoji, S. R., Olsen, O., Bredt, D. S., Lim, W. A., and Prehoda, K. E. (2001) Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol. Cell 8, 1291-301.