Interaction between the Drosophila heterochromatin proteins SUUR and HP1

Journal of Cell Science

Volumn 121, Issue 10, 2008, Pages 1693-1703

  Pindyurin, Alexey V ^a   Boldyreva, Lidiya V ^a   Shloma, Victor V ^a   Kolesnikova, Tatiana D ^a,b   Pokholkova, Galina V ^a   Andreyeva, Evgeniya N ^a   Kozhevnikova, Elena N ^a,c   Ivanoschuk, Igor G ^a   Zarutskaya, Ekaterina A ^a   Demakov, Sergey A ^a   Gorchakov, Andrey A ^a,d   Belyaeva, Elena S ^a   Zhimulev, Igor F ^a,b  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Drosophila melanogaster; Heterochromatin; HP1; Polytene chromosomes; SUUR

Indexed keywords

DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE METHYLTRANSFERASE; NUCLEAR PROTEIN; SUPPRESSOR OF UNDER REPLICATION PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; GENE OVEREXPRESSION; HETEROCHROMATIN; IN VIVO STUDY; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HETEROCHROMATIN; TWO-HYBRID SYSTEM TECHNIQUES;

DROSOPHILA MELANOGASTER;

EID: 46249111785     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.018655     Document Type: Article

References (69)

1. Badugu, R., Shareef, M. M. and Kellum, R. (2003). Novel Drosophila heterochromatin protein 1 (HP1)/origin recognition complex-associated protein (HOAP) repeat motif in HP1/HOAP interactions and chromocenter associations. J. Biol. Chem. 278, 34491-34498.
2. Badugu, R., Yoo, Y., Singh, P. B. and Kellum, R. (2005). Mutations in the heterochromatin protein 1 (HP1) hinge domain affect HP1 protein interactions and chromosomal distribution. Chromosoma 113, 370-384.
3. Becker, D. M. and Lundblad, V. (2002). Introduction of DNA into yeast cells. In Current Protocols in Molecular Biology (ed. F. M. Ausubel), Unit 13.7. New York: John Wiley.
4. Belyaeva, E. S., Zhimulev, I. F., Volkova, E. I., Alekseyenko, A. A., Moshkin, Y. M. and Koryakov, D. E. (1998). Su(UR)ES: a gene suppressing DNA underreplication in intercalary and pericentric heterochromatin of Drosophila melanogaster polytene chromosomes. Proc. Natl. Acad. Sci. USA 95, 7532-7537.
5. Belyaeva, E. S., Boldyreva, L. V., Volkova, E. L, Nanayev, R. A., Alekseyenko, A. A. and Zhimulev, I. F. (2003). Effect of the Suppressor of Underreplication (SuUR) gene on position-effect variegation silencing in Drosophila melanogaster. Genetics 165, 1209-1220.
6. Belyaeva, E. S., Demakov, S. A., Pokholkova, G. V., Alekseyenko, A. A., Kolesnikova, T. D. and Zhimulev, I. F. (2006). DNA underreplication in intercalary heterochromatin regions in polytene chromosomes of Drosophila melanogaster correlates with the formation of partial chromosomal aberrations and ectopic pairing. Chromosoma 115, 355-366.
7. Belyakin, S. N., Christophides, G. K., Alekseyenko, A. A., Kriventseva, E. V., Belyaeva, E. S., Nanayev, R. A., Makunin, I. V., Kafatos, F. C. and Zhimulev, I. F. (2005). Genomic analysis of Drosophila chromosome underreplication reveals a link between replication control and transcriptional territories. Proc. Natl. Acad. Sci. USA 102, 8269-8274.
8. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
9. Brock, H. W. and Fisher, C. L. (2005). Maintenance of gene expression patterns. Dev. Dyn. 232, 633-655.
10. 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.
11. Craig, J. M. (2005). Heterochromatin-many flavours, common themes. BioEssays 27, 17-28.
12. Cryderman, D. E., Grade, S. K., Li, Y., Fanti, L., Pimpinelli, S. and Wallrath, L. L. (2005). Role of Drosophila HP1 in euchromatic gene expression. Dev. Dyn. 232, 767-774.
13. 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.
14. Delattre, M., Spierer, A., Tonks, 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.
15. Delattre, M., Spierer, A., Jaquet, Y. and Spierer, P. (2004). Increased expression of Drosophila Su(var)3-7 triggers Su(var)3-9-dependent heterochromatin formation. J. Cell Sci. 117, 6239-6247.
16. Dillon, N. and Festenstein, R. (2002). Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. Trends Genet. 18, 252-258.
17. Donaldson, A. D. (2005). Shaping time: chromatin structure and the DNA replication programme. Trends Genet. 21, 444-449.
18. 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.
19. Eissenberg, J. C. and Hartnett, T. (1993). A heat shock-activated cDNA rescues the recessive lethality of mutations in the heterochromatin-associated protein HP1 of Drosophila melanogaster. Mol. Gen. Genet. 240, 333-338.
20. Eissenberg, J. C., Morris, G. D., Reuter, G. and Hartnett, T. (1992). The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics 131, 345-352.
21. Fanti, L., Berloco, M., Piacentini, L. and Pimpinelli, S. (2003). Chromosomal distribution of heterochromatin protein 1 (HP1) in Drosophila: a cytological map of euchromatic HP1 binding sites. Genetica 117, 135-147.
22. Finley, R. L., Jr, Thomas, B. J., Zipursky, S. L. and Brent, R. (1996). Isolation of Drosophila cyclin D, a protein expressed in the morphogenetic furrow before entry into S phase. Proc. Natl. Acad. Sci. USA 93, 3011-3015.
23. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E. et al. (2003). A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736.
24. Glaser, R. L. and Spradling, A. C. (1994). Unusual properties of genomic DNA molecules spanning the euchromatic-heterochromatic junction of a Drosophila minichromosome. Nucleic Acids Res. 22, 5068-5075.
25. Golemis, E. A., Serebriiskii, L, Finley, Jr, R. L., Kolonin, M. G., Gyuris, J. and Brent, R. (2002). Interaction trap/two-hybrid system to identify interacting proteins. In Current Protocols in Molecular Biology (ed. F. M. Ausubel), Unit 20.1. New York: John Wiley.
26. Greil, R, de Wit, E., Bussemaker, H. J. and van Steensel, B. (2007). BP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila. EMBO J. 26, 741-751.
27. Hediger, F. and Gasser, S. M. (2006). Heterochromatin protein 1, don't judge the book by its cover! Curr. Opin. Genet. Dev. 16, 143-150.
28. Hiragami, K. and Festenstein, R. (2005). Heterochromatin protein 1, a pervasive controlling influence. Cell. Mol. Life Sci. 62, 2711-2726.
29. Huang, D. W., Fanti, L., Pak, D. T., Botchan, M. R., Pimpinelli, S. and Kellum, R. (1998). Distinct cytoplasmic and nuclear fractions of Drosophila heterochromatin protein 1, their phosphorylation levels and associations with origin recognition complex proteins. J. Cell Biol. 142, 307-318.
30. James, T. C. and Elgin, S. C. (1986). Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol. Cell. Biol. 6, 3862-3872.
31. 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.
32. Jimenez, G., Verrijzer, C. P. and Ish-Horowicz, D. (1999). A conserved motif in goosecoid mediates groucho-dependent repression in Drosophila embryos. Mol. Cell. Biol. 19, 2080-2087.
33. Kadonaga, J. T. (1990). Assembly and disassembly of the Drosophila RNA polymerase II complex during transcription, J. Biol. Chem. 265, 2624-2631.
34. Klymenko, T., Papp, B., Fischle, W., Köcher, T., Schelder, M., Fritsch, C., Wild, B., Wilm, M. and Muller, J. (2006). A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 20, 1110-1122.
35. Koike, N., Maita, H., Taira, T., Ariga, H. and Iguchi-Ariga, S. M. (2000). Identification of heterochromatin protein 1 (HP1) as a phosphorylation target by Pim-1 kinase and the effect of phosphorylation on the transcriptional repression function of HP1(1). FEBS Lett. 467, 17-21.
36. Kolesnikova, T. D., Makunin, I. V., Volkova, E. I., Pirrotta, V., Belyaeva, E. S. and Zhimulev, I. F. (2005). Functional dissection of the Suppressor of UnderReplication protein of Drosophila melanogaster: identification of domains influencing chromosome binding and DNA replication. Genetica 124, 187-200.
37. Kuhfittig, S., Szabad, J., Schotta, G., Hoffmann, J., Máthé, E. and Reuter, G. (2001). pitkin(D), a novel gain-of-function enhancer of position-effect variegation, affects chromatin regulation during oogenesis and early embryogenesis in Drosophila. Genetics 157, 1227-1244.
38. Maison, C. and Almouzni, G. (2004). HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5, 296-304.
39. Makunin, I. V., Volkova, E. I., Belyaeva, E. S., Nabirochkina, E. N., Pirrotta, V. and Zhimulev, I. F. (2002). The Drosophila suppressor of underreplication protein binds to late-replicating regions of polytene chromosomes. Genetics 160, 1023-1034.
40. Moshkin, Y. M., Alekseyenko, A. A., Semeshin, V. R, Spierer, A., Spierer, P., Makarevich, G. F., Belyaeva, E. S. and Zhimulev, I. F. (2001). The bithorax complex of Drosophila melanogaster: Underreplication and morphology in polytene chromosomes. Proc. Natl. Acad. Sci. USA 98, 570-574.
41. 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.
42. Nielsen, A. L., Ortiz, J. A., You, J., Oulad-Abdelghani, M., Khechumian, R., Gansmuller, A., Chambon, P. and Losson, R. (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.
43. Pak, D. T., Pflumm, M., Chesnokov, I., Huang, D. W., Kellum, R., Marr, J., Romanowski, P. and Botchan, M. R. (1997). Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91, 311-323.
44. Pindyurin, A. V., Moorman, C., de Wit, E., Belyakin, S. N., Belyaeva, E. S., Christophides, G. K., Kafatos, F. C., van Steensel, B. and Zhimulev, I. F. (2007). SUUR joins separate subsets of PcG, HP1 and B-type lamin targets in Drosophila. J. Cell Sci. 120, 2344-2351.
45. Poux, S., McCabe, D. and Pirrotta, V. (2001). Recruitment of components of Polycomb Group chromatin complexes in Drosophila. Development 128, 75-85.
46. Ringrose, L. and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38, 413-443.
47. Ryan, R. F., Schultz, D. C., Ayyanathan, K., Singh, P. B., Friedman, J. R., Fredericks, W. J. and Rauscher, E. J., 3rd (1999). KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19, 4366-4378.
48. Saurin, A. J., Shao, Z., Erdjument-Bromage, H., Tempst, P. and Kingston, R. E. (2001). A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412, 655-660.
49. 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 historic H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21, 1121-1131.
50. Schotta, G., Ebert, A. and Reuter, G. (2003). SU(VAR)3-9 is a conserved key function in heterochromatic gene silencing. Genetica 117, 149-158.
51. Schübeler, D., Scalzo, D., Kooperberg, C., van Steensel, B., Debrow, J. and Groudine, M. (2002). Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat. Genet. 32, 438-442.
52. Schwartz, Y. B. and Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9-22.
53. Serebriiskii, I., Khazak, V. and Golemis, E. A. (1999). A two-hybrid dual bait system to discriminate specificity of protein interactions. J. Biol. Chem. 274, 17080-17087.
54. Seum, C., Spierer, A., Delattre, M., Pauli, D. and Spierer, P. (2000). A GAL4-HP1 fusion protein targeted near heterochromatin promotes gene silencing. Chromosoma 109, 453-459.
55. Shaffer, C. D., Stephens, G. E., Thompson, B. A., Funches, L., Bernat, J. A., Craig, C. A. and Elgin, S. C. (2002). Heterochromatin protein 2 (HP2), a partner of HP1 in Drosophila heterochromatin. Proc. Natl. Acad. Sci. USA 99, 14332-14337.
56. Shao, Z., Raible, F., Mollaaghababa, R., Guyon, J. R., Wu, C. T., Bender, W. and Kingston, R. E. (1999). Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98, 37-46.
57. Smothers, J. F. and Henikoff, S. (2000). The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr. Biol. 10, 27-30.
58. Smothers, J. F. and Henikoff, S. (2001). The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins. Mol. Cell. Biol. 21, 2555-2569.
59. Stanyon, C. A., Liu, G., Mangiola, B. A., Patel, N., Giot, L., Kuang, B., Zhang, H., Zhong, J. and Finley, R. L., Jr (2004). A Drosophila protein-interaction map centered on cell-cycle regulators. Genome Biol. 5, R96.
60. Tchurikov, N. A., Kretova, O. V., Chernov, B. K., Golova, Y. B., Zhimulev, I. F. and Zykov, I. A. (2004). SuUR protein binds to the boundary regions separating forum domains in Drosophila melanogaster. J. Biol. Chem. 279, 11705-11710.
61. Tie, F., Prasad-Sinha, J., Birve, A., Rasmuson-Lestander, A. and Harte, P. J. (2003). A 1-megadalton ESC/E(Z) complex from Drosophila that contains polycomblike and RPD3. Mol. Cell. Biol. 23, 3352-3362.
62. Vermaak, D., Henikoff, S. and Malik, H. S. (2005). Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila. PLoS Genet. 1, 96-108.
63. Verschure, P. J., van der Kraan, I., de Leeuw, W., van der Vlag, J., Carpenter, A. E., Belmont, A. S. and van Driel, R. (2005). In vivo HP1 targeting causes large-scale chromatin condensation and enhanced histone lysine methylation. Mol. Cell. Biol. 25, 4552-4564.
64. Volpe, A. M., Horowitz, H., Grafer, C. M., Jackson, S. M. and Berg, C. A. (2001). Drosophila rhino encodes a female-specific chromo-domain protein that affects chromosome structure and egg polarity. Genetics 159, 1117-1134.
65. Zhao, T., Heyduk, T. and Eissenberg, J. C. (2001). Phosphorylation site mutations in heterochromatin protein 1 (HP1) reduce or eliminate silencing activity. J. Biol. Chem. 276, 9512-9518.
66. Zhimulev, I. F. and Belyaeva, E. S. (2003). Intercalary heterochromatin and genetic silencing. BioEssays 25, 1040-1051.
67. Zhimulev, I. F., Semeshin, V. F., Kulichkov, V. A. and Belyaeva, E. S. (1982). Intercalary heterochromatin in Drosophila. 1. Localization and general characteristics. Chromosoma 87, 197-228.
68. Zhimulev, I. F., Belyaeva, E. S., Makunin, I. V., Pirrotta, V., Volkova, E. I., Alekseyenko, A. A., Andreyeva, E. N., Makarevich, G. F., Boldyreva, L. V., Nanayev, R. A. et al. (2003a). Influence of the SuUR gene on intercalary heterochromatin in Drosophila melanogaster polytene chromosomes. Chromosoma 111, 377-398.
69. Zhimulev, I. E., Belyaeva, E. S., Semeshin, V. F., Shloma, V. V., Makunin, I. V. and Volkova, E. I. (2003b). Overexpression of the SuUR gene induces reversible modifications at pericentric, telomeric and intercalary heterochromatin of Drosophila melanogaster polytene chromosomes. J Cell Sci. 116, 169-176.