Insulator protein Su(Hw) recruits SAGA and Brahma complexes and constitutes part of Origin Recognition Complex-binding sites in the Drosophila genome

Nucleic Acids Research

Volumn 41, Issue 11, 2013, Pages 5717-5730

  Vorobyeva, Nadezhda E ^a   Mazina, Marina U ^a   Golovnin, Anton K ^a,b   Kopytova, Daria V ^a   Gurskiy, Dmitriy Y ^a   Nabirochkina, Elena N ^a   Georgieva, Sofia G ^a,c   Georgiev, Pavel G ^a   Krasnov, Aleksey N ^a,b  

^a INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^b UNIVERSITY OF OSLO   (Norway)

^c ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BRM PROTEIN; DNA BINDING PROTEIN; HISTONE ACETYLTRANSFERASE; INSULATOR PROTEIN HW; INSULATOR PROTEIN SU; ORIGIN RECOGNITION COMPLEX; PROTEIN SWI; TRANSCRIPTION FACTOR SAGA; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; BINDING SITE; CELL CYCLE S PHASE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DROSOPHILA; GC RICH SEQUENCE; INSECT GENOME; NONHUMAN; NUCLEOSOME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE;

EID: 84878880603     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt297     Document Type: Article

References (63)

1. Gerasimova, T.I., Gdula, D.A., Gerasimov, D.V., Simonova, O. and Corces, V.G. (1995) A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of positioneffect variegation. Cell, 82, 587-597.
2. Georgiev, P. and Kozycina, M. (1996) Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations. Genetics, 142, 425-436.
3. Pai, C.Y., Lei, E.P., Ghosh, D. and Corces, V.G. (2004) The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell, 16, 737-748.
4. Kurshakova, M., Maksimenko, O., Golovnin, A., Pulina, M., Georgieva, S., Georgiev, P. and Krasnov, A. (2007) Evolutionarily conserved E(y)2/Sus1 protein is essential for the barrier activity of Su(Hw)-dependent insulators in Drosophila. Mol. Cell, 27, 332-338.
5. Kurshakova, M.M., Krasnov, A.N., Kopytova, D.V., Shidlovskii, Y.V., Nikolenko, J.V., Nabirochkina, E.N., Spehner, D., Schultz, P., Tora, L. and Georgieva, S.G. (2007) SAGA and a novel Drosophila export complex anchor efficient transcription and mRNA export to NPC. EMBO J., 26, 4956-4965.
6. Gurskiy, D., Orlova, A., Vorobyeva, N., Nabirochkina, E., Krasnov, A., Shidlovskii, Y., Georgieva, S. and Kopytova, D. (2012) The DUBm subunit Sgf11 is required for mRNA export and interacts with Cbp80 in Drosophila. Nucleic Acids Res., 40, 10689-10700.
7. Zhao, Y., Lang, G., Ito, S., Bonnet, J., Metzger, E., Sawatsubashi, S., Suzuki, E., Le Guezennec, X., Stunnenberg, H.G., Krasnov, A. et al. (2008) A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol. Cell, 29, 92-101.
8. Koutelou, E., Hirsch, C.L. and Dent, S.Y. (2010) Multiple faces of the SAGA complex. Curr. Opin. Cell Biol., 22, 374-382.
9. Muratoglu, S., Georgieva, S., Papai, G., Scheer, E., Enunlu, I., Komonyi, O., Cserpan, I., Lebedeva, L., Nabirochkina, E., Udvardy, A. et al. (2003) Two different Drosophila ADA2 homologues are present in distinct GCN5 histone acetyltransferase-containing complexes. Mol. Cell. Biol., 23, 306-321.
10. Kusch, T., Guelman, S., Abmayr, S.M. and Workman, J.L. (2003) Two Drosophila Ada2 homologues function in different multiprotein complexes. Mol. Cell. Biol., 23, 3305-3319.
11. Baker, S.P. and Grant, P.A. (2007) The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene, 26, 5329-5340.
12. Brown, C.E., Howe, L., Sousa, K., Alley, S.C., Carrozza, M.J., Tan, S. and Workman, J.L. (2001) Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science, 292, 2333-2337.
13. Li, B., Carey, M. and Workman, J.L. (2007) The role of chromatin during transcription. Cell, 128, 707-719.
14. Chatterjee, N., Sinha, D., Lemma-Dechassa, M., Tan, S., Shogren-Knaak, M.A. and Bartholomew, B. (2011) Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms. Nucleic Acids Res., 39, 8378-8391.
15. Mohrmann, L., Langenberg, K., Krijgsveld, J., Kal, A.J., Heck, A.J. and Verrijzer, C.P. (2004) Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol. Cell. Biol., 24, 3077-3088.
16. Chalkley, G.E., Moshkin, Y.M., Langenberg, K., Bezstarosti, K., Blastyak, A., Gyurkovics, H., Demmers, J.A. and Verrijzer, C.P. (2008) The transcriptional coactivator SAYP is a trithorax group signature subunit of the PBAP chromatin remodeling complex. Mol. Cell. Biol., 28, 2920-2929.
17. Vorobyeva, N.E., Soshnikova, N.V., Nikolenko, J.V., Kuzmina, J.L., Nabirochkina, E.N., Georgieva, S.G. and Shidlovskii, Y.V. (2009) Transcription coactivator SAYP combines chromatin remodeler Brahma and transcription initiation factor TFIID into a single supercomplex. Proc. Natl Acad. Sci. USA, 106, 11049-11054.
18. Vorobyeva, N.E., Nikolenko, J.V., Nabirochkina, E.N., Krasnov, A.N., Shidlovskii, Y.V. and Georgieva, S.G. (2012) SAYP and Brahma are important for 'repressive' and 'transient' Pol II pausing. Nucleic Acids Res., 40, 7319-7331.
19. Mechali, M. (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol., 11, 728-738.
20. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N. and Oda, M. (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem., 79, 89-130.
21. MacAlpine, H.K., Gordan, R., Powell, S.K., Hartemink, A.J. and MacAlpine, D.M. (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res., 20, 201-211.
22. Eaton, M.L., Prinz, J.A., MacAlpine, H.K., Tretyakov, G., Kharchenko, P.V. and MacAlpine, D.M. (2011) Chromatin signatures of the Drosophila replication program. Genome Res., 21, 164-174.
23. Kim, J.C., Nordman, J., Xie, F., Kashevsky, H., Eng, T., Li, S., Macalpine, D.M. and Orr-Weaver, T.L. (2011) Integrative analysis of gene amplification in Drosophila follicle cells: parameters of origin activation and repression. Genes Dev., 25, 1384-1398.
24. Deal, R.B., Henikoff, J.G. and Henikoff, S. (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science, 328, 1161-1164.
25. Euskirchen, G.M., Auerbach, R.K., Davidov, E., Gianoulis, T.A., Zhong, G., Rozowsky, J., Bhardwaj, N., Gerstein, M.B. and Snyder, M. (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet., 7, e1002008.
26. Atanasiu, C., Deng, Z., Wiedmer, A., Norseen, J. and Lieberman, P.M. (2006) ORC binding to TRF2 stimulates OriP replication. EMBO Rep., 7, 716-721.
27. Beall, E.L., Manak, J.R., Zhou, S., Bell, M., Lipsick, J.S. and Botchan, M.R. (2002) Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature, 420, 833-837.
28. Dhar, S.K., Yoshida, K., Machida, Y., Khaira, P., Chaudhuri, B., Wohlschlegel, J.A., Leffak, M., Yates, J. and Dutta, A. (2001) Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell, 106, 287-296.
29. Dominguez-Sola, D., Ying, C.Y., Grandori, C., Ruggiero, L., Chen, B., Li, M., Galloway, D.A., Gu, W., Gautier, J. and Dalla-Favera, R. (2007) Non-transcriptional control of DNA replication by c-Myc. Nature, 448, 445-451.
30. Hubner, K. and Phi-van, L. (2012) In vivo binding of Orc2 to a region of the chicken lysozyme GAS41 origin containing multiple Sp1-binding sites. DNA Cell Biol., 31, 180-186.
31. Minami, H., Takahashi, J., Suto, A., Saitoh, Y. and Tsutsumi, K. (2006) Binding of AlF-C, an Orc1-binding transcriptional regulator, enhances replicator activity of the rat aldolase B origin. Mol. Cell. Biol., 26, 8770-8780.
32. 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.
33. Schepers, A., Ritzi, M., Bousset, K., Kremmer, E., Yates, J.L., Harwood, J., Diffley, J.F
34. Shen, Z., Sathyan, K.M., Geng, Y., Zheng, R., Chakraborty, A., Freeman, B., Wang, F., Prasanth, K.V. and Prasanth, S.G. (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol. Cell, 40, 99-111.
35. Sibani, S., Price, G.B. and Zannis-Hadjopoulos, M. (2005) Ku80 binds to human replication origins prior to the assembly of the ORC complex. Biochemistry, 44, 7885-7896.
36. Thomae, A.W., Pich, D., Brocher, J., Spindler, M.P., Berens, C., Hock, R., Hammerschmidt, W. and Schepers, A. (2008) Interaction between HMGA1a and the origin recognition complex creates site-specific replication origins. Proc. Natl Acad. Sci. USA, 105, 1692-1697.
37. Clemens, J.C., Worby, C.A., Simonson-Leff, N., Muda, M., Maehama, T., Hemmings, B.A. and Dixon, J.E. (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl Acad. Sci. USA, 97, 6499-6503.
38. Golovnin, A., Melnikova, L., Volkov, I., Kostuchenko, M., Galkin, A.V. and Georgiev, P. (2008) 'Insulator bodies' are aggregates of proteins but not of insulators. EMBO Rep., 9, 440-445.
39. Chesnokov, I.N., Chesnokova, O.N. and Botchan, M. (2003) A cytokinetic function of Drosophila ORC6 protein resides in a domain distinct from its replication activity. Proc. Natl Acad. Sci. USA, 100, 9150-9155.
40. Georgieva, S., Nabirochkina, E., Dilworth, F.J., Eickhoff, H., Becker, P., Tora, L., Georgiev, P. and Soldatov, A. (2001) The novel transcription factor e(y)2 interacts with TAF(II)40 and potentiates transcription activation on chromatin templates. Mol. Cell. Biol., 21, 5223-5231.
41. Chen, Y., Negre, N., Li, Q., Mieczkowska, J.O., Slattery, M., Liu, T., Zhang, Y., Kim, T.K., He, H.H., Zieba, J. et al. (2012) Systematic evaluation of factors influencing ChIP-seq fidelity. Nat. Methods, 9, 609-614.
42. Huang, S., Li, X., Yusufzai, T.M., Qiu, Y. and Felsenfeld, G. (2007) USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol. Cell. Biol., 27, 7991-8002.
43. Baxley, R.M., Soshnev, A.A., Koryakov, D.E., Zhimulev, I.F. and Geyer, P.K. (2011) The role of the suppressor of hairy-wing insulator protein in Drosophila oogenesis. Dev. Biol., 356, 398-410.
44. Soshnev, A.A., He, B., Baxley, R.M., Jiang, N., Hart, C.M., Tan, K. and Geyer, P.K. (2012) Genome-wide studies of the multi-zinc finger Drosophila suppressor of hairy-wing protein in the ovary. Nucleic Acids Res., 40, 5415-5431.
45. Celniker, S.E., Dillon, L.A., Gerstein, M.B., Gunsalus, K.C., Henikoff, S., Karpen, G.H., Kellis, M., Lai, E.C., Lieb, J.D., MacAlpine, D.M. et al. (2009) Unlocking the secrets of the genome. Nature, 459, 927-930.
46. Mitra, D., Parnell, E.J., Landon, J.W., Yu, Y. and Stillman, D.J. (2006) SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol. Cell. Biol., 26, 4095-4110.
47. Hassan, A.H., Neely, K.E., Vignali, M., Reese, J.C. and Workman, J.L. (2001) Promoter targeting of chromatin-modifying complexes. Front. Biosci., 6, D1054-D1064.
48. Negre, N., Brown, C.D., Shah, P.K., Kheradpour, P., Morrison, C.A., Henikoff, J.G., Feng, X., Ahmad, K., Russell, S., White, R.A. et al. (2010) A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet., 6, e1000814.
49. Golovnin, A., Mazur, A., Kopantseva, M., Kurshakova, M., Gulak, P.V., Gilmore, B., Whitfield, W.G., Geyer, P., Pirrotta, V. and Georgiev, P. (2007) Integrity of the Mod(mdg4)-67.2 BTB domain is critical to insulator function in Drosophila melanogaster. Mol. Cell. Biol., 27, 963-974.
50. Smith, S.T., Wickramasinghe, P., Olson, A., Loukinov, D., Lin, L., Deng, J., Xiong, Y., Rux, J., Sachidanandam, R., Sun, H. et al. (2009) Genome wide ChIP-chip analyses reveal important roles for CTCF in Drosophila genome organization. Dev. Biol., 328, 518-528.
51. MacAlpine, D.M., Rodriguez, H.K. and Bell, S.P. (2004) Coordination of replication and transcription along a Drosophila chromosome. Genes Dev., 18, 3094-3105.
52. Balasov, M., Huijbregts, R.P. and Chesnokov, I. (2007) Role of the Orc6 protein in origin recognition complex-dependent DNA binding and replication in Drosophila melanogaster. Mol. Cell. Biol., 27, 3143-3153.
53. Cayrou, C., Coulombe, P., Vigneron, A., Stanojcic, S., Ganier, O., Peiffer, I., Rivals, E., Puy, A., Laurent-Chabalier, S., Desprat, R. et al. (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res., 21, 1438-1449.
54. Cayrou, C., Coulombe, P., Puy, A., Rialle, S., Kaplan, N., Segal, E. and Mechali, M. (2012) New insights into replication origin characteristics in metazoans. Cell Cycle, 11, 658-667.
55. Cayrou, C., Gregoire, D., Coulombe, P., Danis, E. and Mechali, M. (2012) Genome-scale identification of active DNA replication origins. Methods, 57, 158-164.
56. Edwards, M.C., Tutter, A.V., Cvetic, C., Gilbert, C.H., Prokhorova, T.A. and Walter, J.C. (2002) MCM2-7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J. Biol. Chem., 277, 33049-33057.
57. Mimura, S., Masuda, T., Matsui, T. and Takisawa, H. (2000) Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells, 5, 439-452.
58. Takisawa, H., Mimura, S. and Kubota, Y. (2000) Eukaryotic DNA replication: from pre-replication complex to initiation complex. Curr. Opin. Cell Biol., 12, 690-696.
59. Filion, G.J., van Bemmel, J.G., Braunschweig, U., Talhout, W., Kind, J., Ward, L.D., Brugman, W., de Castro, I.J., Kerkhoven, R.M., Bussemaker, H.J. et al. (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell, 143, 212-224.
60. Geyer, P.K. and Corces, V.G. (1987) Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev., 1, 996-1004.
61. Cockerill, P.N. (2011) Structure and function of active chromatin and DNase I hypersensitive sites. FEBS J., 278, 2182-2210.
62. Gross, D.S. and Garrard, W.T. (1988) Nuclease hypersensitive sites in chromatin. Annu. Rev. Biochem., 57, 159-197.
63. Bosco, G., Du, W. and Orr-Weaver, T.L. (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nature Cell Biol., 3, 289-295.