The histone deacetylase Rpd3 regulates the heterochromatin structure of Drosophila telomeres

Journal of Cell Science

Volumn 124, Issue 12, 2011, Pages 2041-2048

  Burgio, Giosalba ^a,b   Cipressa, Francesca ^c   Ingrassia, Antonia Maria Rita ^a,b   Cenci, Giovanni ^c   Corona, Davide F V ^a,b  

^a Istituto Telethon Dulbecco   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Heterochromatin; Histone acetylation; Histone H3K9 trimethylation; HP2; Rpd3; Telomere

Indexed keywords

HISTONE DEACETYLASE 1; HISTONE DEACETYLASE RPD 3; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME ABERRATION; CHROMOSOME STRUCTURE; DROSOPHILA; ENZYME ACTIVITY; EPIGENETICS; HETEROCHROMATIN; HISTONE ACETYLATION; HISTONE METHYLATION; MALE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TELOMERE;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPIGENOMICS; HETEROCHROMATIN; HISTONE DEACETYLASE 1; MALE; POLYTENE CHROMOSOME; TELOMERE;

DROSOPHILA MELANOGASTER; EUKARYOTA; MAMMALIA;

EID: 79958167832     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.078261     Document Type: Article

References (37)

1. Ahringer, J. (2000). NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16, 351-356.
2. Altaf, M., Utley, R. T., Lacoste, N., Tan, S., Briggs, S. D. and Cote, J. (2007). Interplay of chromatin modifiers on a short basic patch of histone H4 tail defines the boundary of telomeric heterochromatin. Mol. Cell 28, 1002-1014.
3. Andreyeva, E. N., Belyaeva, E. S., Semeshin, V. F., Pokholkova, G. V. and Zhimulev, I. F. (2005). Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. J. Cell Sci. 118, 5465-5477.
4. Blasco, M. A. (2007). The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8, 299-309.
5. Burgio, G., La Rocca, G., Sala, A., Arancio, W., Di Gesu, D., Collesano, M., Sperling, A. S., Armstrong, J. A., van Heeringen, S. J., Logie, C. et al. (2008). Genetic identification of a network of factors that functionally interact with the nucleosome remodeling ATPase ISWI. PLoS Genet. 4, e1000089.
6. Cenci, G., Siriaco, G., Raffa, G. D., Kellum, R. and Gatti, M. (2003). The Drosophila HOAP protein is required for telomere capping. Nat. Cell Biol. 5, 82-84.
7. Cenci, G., Ciapponi, L. and Gatti, M. (2005). The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 114, 135-145.
8. Ciapponi, L. and Cenci, G. (2008). Telomere capping and cellular checkpoints: clues from fruit flies. Cytogenet. Genome Res. 122, 365-373.
9. Corona, D. F., Siriaco, G., Armstrong, J. A., Snarskaya, N., McClymont, S. A., Scott, M. P. and Tamkun, J. W. (2007). ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol. 5, e232.
10. De Lange, T. (2005). Telomere-related genome instability in cancer. Cold Spring Harb. Symp. Quant. Biol. 70, 197-204.
11. De Rubertis, F., Kadosh, D., Henchoz, S., Pauli, D., Reuter, G., Struhl, K. and Spierer, P. (1996). The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast. Nature 384, 589-591.
12. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
13. Ebert, A., Schotta, G., Lein, S., Kubicek, S., Krauss, V., Jenuwein, T. and Reuter, G. (2004). Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev. 18, 2973-2983.
14. Ebert, A., Lein, S., Schotta, G. and Reuter, G. (2006). Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res. 14, 377-392.
15. Fanti, L., Giovinazzo, G., Berloco, M. and Pimpinelli, S. (1998). The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2, 527-538.
16. Ferreira, M. G., Miller, K. M. and Cooper, J. P. (2004). Indecent exposure: when telomeres become uncapped. Mol. Cell 13, 7-18.
17. Gelbart, M. E., Larschan, E., Peng, S., Park, P. J. and Kuroda, M. I. (2009). Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat. Struct. Mol. Biol. 16, 825-832.
18. Hazelett, D. J., Bourouis, M., Walldorf, U. and Treisman, J. E. (1998). decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125, 3741-3751.
19. Johansen, K. M., Johansen, J., Jin, Y., Walker, D. L., Wang, D. and Wang, Y. (1999). Chromatin structure and nuclear remodeling. Crit. Rev. Eukaryot. Gene Expr. 9, 267-277.
20. Kadosh, D. and Struhl, K. (1998). Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol. Cell. Biol. 18, 5121-5127.
21. Larschan, E., Alekseyenko, A. A., Gortchakov, A. A., Peng, S., Li, B., Yang, P., Workman, J. L., Park, P. J. and Kuroda, M. I. (2007). MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol. Cell 28, 121-133.
22. Mason, J. M., Frydrychova, R. C. and Biessmann, H. (2008). Drosophila telomeres: an exception providing new insights. BioEssays 30, 25-37.
23. Nugent, C. I. and Lundblad, V. (1998). The telomerase reverse transcriptase: components and regulation. Genes Dev. 12, 1073-1085.
24. Palm, W. and de Lange, T. (2008). How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334.
25. Perrini, B., Piacentini, L., Fanti, L., Altieri, F., Chichiarelli, S., Berloco, M., Turano, C., Ferraro, A. and Pimpinelli, S. (2004). HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol. Cell 15, 467-476.
26. Pile, L. A. and Wassarman, D. A. (2000). Chromosomal localization links the SIN3-RPD3 complex to the regulation of chromatin condensation, histone acetylation and gene expression. EMBO J. 19, 6131-6140.
27. Raffa, G. D., Cenci, G., Siriaco, G., Goldberg, M. L. and Gatti, M. (2005). The putative Drosophila transcription factor woc is required to prevent telomeric fusions. Mol. Cell 20, 821-831.
28. Rashkova, S., Karam, S. E., Kellum, R. and Pardue, M. L. (2002). Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends. J. Cell Biol. 159, 397-402.
29. Rundlett, S. E., Carmen, A. A., Kobayashi, R., Bavykin, S., Turner, B. M. and Grunstein, M. (1996). HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. USA 93, 14503-14508.
30. Schoeftner, S. and Blasco, M. A. (2009). A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J. 28, 2323-2336.
31. Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G., Reinberg, D. and Jenuwein, T. (2004). A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251-1262.
32. Shaffer, C. D., Cenci, G., Thompson, B., Stephens, G. E., Slawson, E. E., Adu-Wusu, K., Gatti, M. and Elgin, S. C. (2006). The large isoform of Drosophila melanogaster heterochromatin protein 2 plays a critical role in gene silencing and chromosome structure. Genetics 174, 1189-1204.
33. Shareef, M. M., King, C., Damaj, M., Badagu, R., Huang, D. W. and Kellum, R. (2001). Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol. Biol. Cell 12, 1671-1685.
34. Shpiz, S., Kwon, D., Uneva, A., Kim, M., Klenov, M., Rozovsky, Y., Georgiev, P., Savitsky, M. and Kalmykova, A. (2007). Characterization of Drosophila telomeric retroelement TAHRE: transcription, transpositions, and RNAi-based regulation of expression. Mol. Biol. Evol. 24, 2535-2545.
35. Siriaco, G. M., Cenci, G., Haoudi, A., Champion, L. E., Zhou, C., Gatti, M. and Mason, J. M. (2002). Telomere elongation (Tel), a new mutation in Drosophila melanogaster that produces long telomeres. Genetics 160, 235-245.
36. Steitz, M. C., Wickenheisser, J. K. and Siegfried, E. (1998). Overexpression of zeste white 3 blocks wingless signaling in the Drosophila embryonic midgut. Dev. Biol. 197, 218-233.
37. Stephens, G. E., Craig, C. A., Li, Y., Wallrath, L. L. and Elgin, S. C. (2004). Immunofluorescent staining of polytene chromosomes: exploiting genetic tools. Methods Enzymol. 376, 372-393.