Structure-function analysis of SUV39H1 reveals a dominant role in heterochromatin organization, chromosome segregation, and mitotic progression

Molecular and Cellular Biology

Volumn 20, Issue 10, 2000, Pages 3728-3841

  Melcher, Martin ^a   Schmid, Manfred ^a   Aagaard, Louise ^a   Selenko, Philipp ^a,b   Laible, GÖTZ ^a,c   Jenuwein, Thomas ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c AgRescarch   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMOSOME SEGREGATION; DROSOPHILA; HETEROCHROMATIN; HUMAN; HUMAN CELL; INTERPHASE; METAPHASE; MITOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SCHIZOSACCHAROMYCES POMBE; STRUCTURE ACTIVITY RELATION;

CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME ABERRATIONS; CHROMOSOME SEGREGATION; CHROMOSOMES, HUMAN, PAIR 1; DROSOPHILA PROTEINS; HETEROCHROMATIN; HISTONES; HUMANS; METHYLTRANSFERASES; MITOSIS; PHOSPHOPROTEINS; PROTEIN BINDING; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 0034056777     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.10.3728-3741.2000     Document Type: Article

References (51)

1. Aagaard, L., G. Laible, P. Selenko, M. Schmid, R. Dorn, G. Schotta, S. Kuhfittig, A. Wolf, A. Lebersorger, P. B. Singh, G. Reuter, and T. Jenuwein. 1999. Functional mammalian homologues of the Drosophila PEV modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18:1923-1938.
2. Aagaard, L., M. Schmid, P. Warburton, and T. Jenuwein. 2000. Mitotic phosphorylation of SUV39H1, a novel component of active centromeres, coincides with transient accumulation at mammalian centromeres. J. Cell Sci. 113:817-829.
3. Aasland, R., and A. F. Stewart. 1995. The chromo shadow domain, a second chromodomain in heterochromatin-binding protein 1, HP1. Nucleic Acids Res. 23:3168-3173.
4. Allshire, R. C., E. R. Nimmo, K. Ekwall, J. P. Javerzat, and G. Granston. 1995. Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev. 9:218-233.
5. Baksa, K., H. Morawietz, V. Dombradi, M. Axton, H. Taubert, G. Szabo, I. Török, A. Udvardy, H. Gyuorkovics, B. Szöör, D. Glover, G. Reuter, and J. Gausz. 1993. Mutations in the protein phosphatase 1 gene at 87B can differentially affect suppression of position effect variegation and mitosis in Drosophila melanogaster. Genetics 135:117-125.
6. Ball, L. J., N. V. Murzina, R. W. Broadhurst, A. R. C. Raine, S. J. Archer, F. J. Stott, A. G., Murzin, P. B. Singh, P. J. Domaille, and E. D. Laue. 1997. Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J. 16:2473-2481.
7. Cardoso, C., S. Timsit, L. Villard, M. Khrestchatisky, M. Fontes, and L. Colleaux. 1998. Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum. Mol. Genet. 7:679-684.
8. Cléard, F., M. Delattre, and P. Spierer. 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.
9. Corda, Y., V. Schranke, M. P. Longhese, T. Smokvina, V. Paciotti, V. Brevet, E. Gilson, and V. Géli. 1999. Interaction between Set1p and checkpoint protein Mec3p in DNA repair and telomere functions. Nat. Genet. 21:204-208.
10. Cui, X., I. De Vito, R. Slany, A. Miyamoto, R. Firestein, and M. L. Cleary. 1998. Association of SET domain and myotubularin-related proteins modulates growth control. Nat. Genet. 18:331-337.
11. De Rubertis, F., D. Kadosh, S. Henchoz, S. Pauli, G. Reuter, G. Struhl, and P. Spierer. 1996. The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast. Nature 384:589-591.
12. Eissenberg, J. C., G. D. Morris, G. Reuter, and T. Hartnett. 1992. The heterochromatin-associated protein HP-1 is an essential protein in Drosophlia with dosage-dependent effects on position-effect variegation. Genetics 131:345-352.
13. + disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J. Cell Sci. 109:2637-2648.
14. Fanti, L., G. Giovinazzo, M. Berlocco, and S. Pimpinelli. 1998. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2:527-538.
15. Firestein, R., X. Cui, P. Huie, and M. L. Cleary. SET domain-dependent regulation of transcriptional silencing and growth control by SUV39H1, a mammalian ortholog of Drosophila Su(var)3-9. Mol. Cell. Biol., in press.
16. Grewal, S. I., M. J. Bonaduce, and A. J. Klar. 1999. Histone deacetylase homologs regulate epigenetic inheritance of transcriptional silencing and chromosome segregation in fission yeast. Genetics 150:563-576.
17. Grunstein, M. 1998. Yeast heterochromatin: regulation of its assembly and inheritance by histones. Cell 93:325-328.
18. Hecht, A., T. Laroche, S. Strahl-Bolsinger, S. M. Gasser, and M. Grunstein. 1995. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80:583-592.
19. Hecht, A., S. Strahl-Bolsinger, and M. Grunstein. 1996. Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature 383:92-95.
20. Hendzel, M. J., Y. Wei, M. A. Mancini, A. van Hooser, T. Ranalli, B. R. Brinkley, D. P. Bazett-Jones, and C. D. Allis. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360.
21. Henikoff, S. 1996. Position-effect-variegation in Drosophila: recent progress, p. 319-334. In V. E. A. Russo, R. A. Martienssen, and A. D. Riggs (ed.), Epigenetic mechanisms of gene regulation. CSHL Press, New York, N.Y.
22. Huang, N., E. vom Baur, J.-M. Garnier, T. Lerouge, J.-L. Vonesch, Y. Lutz, P. Chambon, and R. Losson. 1998. Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators. EMBO J. 17:3398-3412.
23. Ivanova, A. V., M. J. Bonaduce, S. V. Ivanov, and A. J. S. Klar. 1998. The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nat. Genet. 19:192-195.
24. James, T. C., and S. C. R. Elgin. 1986. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila and its gene. Mol. Cell. Biol. 6:3862-3872.
25. Jenuwein, T., G. Laible, R. Dorn, and G. Reuter. 1998. SET-domain proteins modulate chromatin domains in eu-and heterochromatin. Cell. Mol. Life Sci. 54:80-93.
26. Karpen, G., and R. C. Allshire. 1997. The case for epigenetic effects on centromere identity and function. Trends Genet. 13:489-196.
27. Koonin, E. V., S. Zhou, and J. C. Lucchesi. 1995. The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. Nucleic Acids Res. 23:4229-4232.
28. Lorentz, A., K. Ostermann, O. Fleck, and H. Schmidt. 1994. Switching gene swi6, involved in repression of silent mating-type loci in fission yeast, encodes a homologue of chromatin-associated proteins from Drosophila and mammals. Gene 143:139-143.
29. Martin-Zanca, D., R. Oskam, G. Mitra, T. Copeland, and M. Barbacid. 1989. Molecular and biochemical characterisation of the human trk protooncogene. Mol. Cell. Biol. 9:24-33.
30. Messmer, S., A. Franke, and R. Paro. 1992. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 6:1241-1254.
31. Minc, E., Y. Allory, H. J. Worman, J.-C. Courvalin, and B. Buendia. 1999. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108:220-234.
32. Murzina, N., A. Verrault, E. Laue, and B. Stillman. 1999. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell 4:529-540.
33. Nielsen, A. L., J. A. Ortiz, J. You, M. Oulad-Abdelghani, R. Khechumian, A. Gansmuller, P. Chambon, and R. Losson. 1999. Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J. 18:6385-6395.
34. Paro, R., and D. S. Hogness. 1991. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc. Natl. Acad. Sci. USA 88:263-267.
35. Paro, R., and P. J. Harte. 1996. The role of Polycomb group and trithorax group complexes in the maintenance of determined cell states, p. 507-528. In V. E. A. Russo, R. A. Martienssen, and A. D. Riggs (ed.), Epigenetic mechanisms of gene regulation. CSHL Press, New York, N.Y.
36. Pirrotta, V. 1996. Stable chromatin states regulating homeotic genes in Drosophila, p. 489-505. In V. E. A. Russo, R. A. Martienssen, and A. D. Riggs (ed.), Epigenetic mechanisms of gene regulation. CSHL Press, New York, N.Y.
37. Platero, J. S., T. Harnett, and J. C. Eissenberg. 1995. Functional analysis of the chromo domain of HP-1. EMBO J. 14:3977-3986.
38. Renauld, H., O. Aparicio, P. Zierath, L. Billington, S. Chhablani, and D. Gottschling. 1993. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev. 7:1133-1145.
39. Reuter, G., M. Giarre, J. Farah, J. Gausz, A. Spierer, and P. Spierer. 1990. Dependence of position-effect variegation in Drosophila on dose of a gene encoding an unusual zinc-finger protein. Nature 344:219-223.
40. Reuter, G., and P. Spierer. 1992. Position-effect variegation and chromatin proteins. Bioessays 14:605-612.
41. Rosenblatt-Rosen, O., T. Rozovskaia, D. Burakov, Y. Sedkov, S. Tillib, J. Blechman, T. Nakamura, C. M. Croce, A. Mazo, and E. Canaani. 1998. The C-terminal SET domains of ALL-1 and TRITHORAX interact with the INI1 and SNR1 proteins, components of the SWI/SNF complex. Proc. Natl. Acad. Sci. USA 95:4152-4157.
42. Ryan, R. F., D. C. Schultz, K. Ayyanathan, P. B. Singh, J. R. Friedman, W. J. Fredericks, and F. J. Rauscher III. 1999. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Krüppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19:4366-4378.
43. Saunders, W. S., C. C. Chue, M. Goebl, C. Craig, R. F. Clark, J. A. Powers, J. C. Eissenberg, S. C. R. Elgin, N. F. Rothfield, and W. C. Earnshaw. 1993. Molecular cloning of a human homologue of Drosophila heterochromatin protein HP1 using anti-centromere autoantibodies with anti-chromo specificity. J. Cell Sci. 104:573-582.
44. Schultz, J., R. R. Copley, T. Doerks, C. P. Ponting, and P. Bork. 2000. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28:231-234.
45. Stone, E. M., and L. Pillus. 1996. Activation of a MAP kinase cascade leads to Sir3p hyperphosphorylation and strengthens transcriptional silencing. J. Cell Biol. 135:571-583.
46. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403:41-45.
47. Tschiersch, B., A. Hofmann, V. Krauss, R. Dorn, G. Korge, and G. Reuter. 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.
48. Turner, B. M. 1998. Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell. Mol. Life Sci. 54:21-31.
49. Wallrath, L. L. 1998. Unfolding the mysteries of heterochromatin. Curr. Opin. Genet. Dev. 8:147-153.
50. Wei, Y., Y. Lanlan, J. Bowen, M. A. Gorovsty, and C. D. Allis. 1999. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97:99-109.
51. Wreggett, K. A., F. Hill, P. S. James, G. W. Hutchings, and P. B. Singh. 1994. A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet. 66:99-103.