Increased expression of Drosophila Su(var)3-7 triggers Su(var)3-9-dependent heterochromatin formation

Journal of Cell Science

Volumn 117, Issue 25, 2004, Pages 6239-6247

  Delattre, Marion ^a   Spierer, Anne ^a   Jaquet, Yannis ^a   Spierer, Pierre ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Drosophila; Heterochromatin; Position effect variegation; Su(var)3 7

Indexed keywords

DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE; HISTONE H3K9; HISTONE METHYLTRANSFERASE; NUCLEAR PROTEIN; PROTEIN METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUTOSOME; CHROMATIN STRUCTURE; CHROMOSOME BANDING PATTERN; CHROMOSOME CONDENSATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; HETEROCHROMATIN; IN VIVO STUDY; LETHALITY; MALE; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; SEX DIFFERENCE; SURVIVAL; X CHROMOSOME;

ANIMALS; CHROMATIN; CHROMOSOME BANDING; CHROMOSOMES; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; HETEROCHROMATIN; HISTONES; HOMOZYGOTE; MALE; METHYLATION; OXAZINES; REPRESSOR PROTEINS; X CHROMOSOME;

ANIMALIA; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 12344254250     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01549     Document Type: Article

References (36)

1. Aagaard, L., Laible, G., Selenko, P., Schmid, M., Dorn, R., Schotta, G., Kuhfittig, S., Wolf, A., Lebersorger, A., Singh, P. B. et al. (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. Akhtar, A. (2003). Dosage compensation: an intertwined world of RNA and chromatin remodelling. Curr. Opin. Genet. Dev. 13, 161-169.
3. Ayyanathan, K., Lechner, M. S., Bell, P., Maul, G. G., Schultz, D. C., Yamada, Y., Tanaka, K., Torigoe, K. and Rauscher, F. J., III (2003). Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 17, 1855-1869.
4. 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.
5. Cléard, F. and Spierer, P. (2001). Position-effect variegation in Drosophila: the modifier Su(var)3-7 is a modular DNA-binding protein. EMBO Rep. 2, 1095-1100.
6. Cléard, F., Matsarskaia, M. and Spierer, P. (1995). The modifier of position-effect variegation Suvar(3)7 of Drosophila: there are two alternative transcripts and seven scattered zinc fingers, each preceded by a tryptophan box. Nucleic Acids Res. 23, 796-802.
7. Cléard, 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.
8. 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, 915-919.
9. Delattre, M., Spierer, A., Tonka, C. H. and Spierer, P. (2000). The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1. J. Cell Sci. 113, 4253-4261.
10. Eissenberg, J. C. and Elgin, S. C. (2000). The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev. 10, 204-210.
11. Eissenberg, J. C., James, T. C., Foster-Hartnett, D. M., Hartnett, T., Ngan, V. 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. USA 87, 9923-9927.
12. Eskeland, R., Czermin, B., Boeke, J., Bonaldi, T., Regula, J. T. and Imhof, A. (2004). The N-terminus of Drosophila SU(VAR)3-9 mediates dimerization and regulates its methyltransferase activity. Biochemistry 43, 3740-3749.
13. Greil, F., van der Kraan, I., Delrow, J., Smothers, J. F., de Wit, E., Bussemaker, H. J., van Driel, R., Henikoff, S. and van Steensel, B. (2003). Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev. 17, 2825-2838.
14. Henikoff, S. (2000). Heterochromatin function in complex genomes. Biochim. Biophys. Acta 1470, 1-8.
15. Jacobs, S. A., Taverna, S. D., Zhang, Y., Briggs, S. D., Li, J., Eissenberg, J. C., Allis, C. D. and Khorasanizadeh, S. (2001 . Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J. 20, 5232-5241.
16. James, T. C., Eissenberg, J. C., Craig, C., Dietrich, V., Hobson, A. and Elgin, S. C. (1989). Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur. J. Cell Biol. 50, 170-180.
17. Jaquet, Y., Delattre, M., Spierer, A. and Spierer, P. (2002). Functional dissection of the Drosophila modifier of variegation Su(var)3-7. Development 129, 3975-3982.
18. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. and Jenuwein, T. (2001). Methylation of historic H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120.
19. Li, Y., Kirschmann, D. A. and Wallrath, L. L. (2002). Does heterochromatin protein 1 always follow code? Proc. Natl. Acad. Sci. USA 99, 16462-16469.
20. Li, Y., Danzer, J. R., Alvarez, P., Belmont, A. S. and Wallrath, L. L. (2003). Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130, 1817-1824.
21. Nielsen, S. J., Schneider, R., Bauer, U. M., Bannister, A. J., Morrison, A., O'Carroll, D., Firestein, R., Cleary, M., Jenuwein, T., Herrera, R. E. et al. (2001). Rb targets histone H3 methylation and HP1 to promoters. Nature 412, 561-565.
22. 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 1132-1136.
23. Platero, J. S., Hartnett, T. and Eissenberg, J. C. (1995). Functional analysis of the chromo domain of HP1. EMBO J. 14, 3977-3986.
24. 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.
25. Reuter, G. and Spierer, P. (1992). Position effect variegation and chromatin proteins. Bioessays 14, 605-612.
26. Reuter, G., Giarre, M., Farah, J., Gausz, J., Spierer, A. and Spierer, P. (1990). Dependence of position-effect variegation in Drosophila on dose of a gene encoding an unusual zinc-finger protein. Nature 344, 219-223.
27. Richards, E. J. and Elgin, S. C. (2002). Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108, 489-500.
28. 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.
29. 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.
30. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. and Rauscher, F. J., III (2002). SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919-932.
31. Seum, C., Pauli, D., Delattre, M., Jaquet, Y., Spierer, A. and Spierer, P. (2002). Isolation of Su(var)3-7 mutations by homologous recombination in Drosophila melanogaster, Genetics 161, 1125-1136.
32. Tachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., Fukuda, M., Takeda, N., Niida, H., Kato, H. et al. (2002). G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779-1791.
33. Tschiersch, B., Hofmann, A., Krauss, V., Dorn, 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.
34. Turner, B. M., Birley, A. J. and Lavender, J. (1992). Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69, 375-384.
35. Wallrath, L. L. (1998). Unfolding the mysteries of heterochromatin. Curr. Opin. Genet. Dev. 8, 147-153.
36. Weiler, K. S. and Wakimoto, B. T. (1995). Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 29, 577-605.