Modulation of chromatin boundary activities by nucleosome-remodeling activities in Drosophila melanogaster

Molecular and Cellular Biology

Volumn 30, Issue 4, 2010, Pages 1067-1076

  Li, Mo ^a   Belozerov, Vladimir E ^a   Cai, Haini N ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; HOX PROTEIN; PROTEIN DMI 2; PROTEIN EBX; PROTEIN ISWI; PROTEIN NURD; PROTEIN NURF301; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENHANCER REGION; EVOLUTION; GENE CONTROL; GENE DISRUPTION; GENOME; INSULATOR ELEMENT; MUTATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL;

ACETYLATION; ADENOSINE TRIPHOSPHATASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUTATION; NUCLEOSOMES; PROTEIN BINDING; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER;

EID: 75749100236     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00183-09     Document Type: Article

References (78)

1. Adkins, N. L., T. A. Hagerman, and P. Georgel. 2006. GAGA protein: a multi-faceted transcription factor. Biochem. Cell. Biol. 84:559-567.
2. Adryan, B., G. Woerfel, I. Birch-Machin, S. Gao, M. Quick, L. Meadows, S. Russell, and R. White. 2007. Genomic mapping of Suppressor of Hairy-wing binding sites in Drosophila. Genome Biol. 8:R167.
3. Ameres, S. L., L. Drueppel, K. Pfleiderer, A. Schmidt, W. Hillen, and C. Berens. 2005. Inducible DNA-loop formation blocks transcriptional activation by an SV40 enhancer. EMBO J. 24:358-367.
4. Avramova, Z., and A. Tikhonov. 1999. Are scs and scs' 'neutral' chromatin domain boundaries of the locus? Trends Genet. 15:138-139.
5. Babu, P., K. S. Selvakumar, and S. Bhosekar. 1987. Studies on transvection at the bithorax complex in Drosophila melanogaster. Mol. Gen. Genet. 210:557-563.
6. Badenhorst, P., M. Voas, I. Rebay, and C. Wu. 2002. Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev. 16:3186-3198.
7. Badenhorst, P., H. Xiao, L. Cherbas, S. Y. Kwon, M. Voas, I. Rebay, P. Cherbas, and C. Wu. 2005. The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev. 19:2540-2545.
8. Barges, S., J. Mihaly, M. Galloni, K. Hagstrom, M. Muller, G. Shanower, P. Schedl, H. Gyurkovics, and F. Karch. 2000. The Fab-8 boundary defines the distal limit of the bithorax complex iab-7 domain and insulates iab-7 from initiation elements and a PRE in the adjacent iab-8 domain. Development 127:779-790.
9. Bartkuhn, M., T. Straub, M. Herold, M. Herrmann, C. Rathke, H. Saumweber, G. D. Gilfillan, P. B. Becker, and R. Renkawitz. 2009. Active promoters and insulators are marked by the centrosomal protein 190. EMBO J. 28:877-888.
10. Bell, A. C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485.
11. Bell, A. C., A. G. West, and G. Felsenfeld. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387-396.
12. Belozerov, V. E., P. Majumder, P. Shen, and H. N. Cai. 2003. A novel boundary element may facilitate independent gene regulation in the Antennapedia Complex of Drosophila. EMBO J. 22:3113-3121.
13. Bi, X., and J. R. Broach. 1999. UASrpg can function as a heterochromatin boundary element in yeast. Genes Dev. 13:1089-1101.
14. Brehm, A., G. Langst, J. Kehle, C. R. Clapier, A. Imhof, A. Eberharter, J. Muller, and P. B. Becker. 2000. dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J. 19:4332-4341.
15. Bushey, A. M., E. R. Dorman, and V. G. Corces. 2008. Chromatin insulators: regulatory mechanisms and epigenetic inheritance. Mol. Cell 32:1-9.
16. Bushey, A. M., E. Ramos, and V. G. Corces. 2009. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev. 23:1338-1350.
17. Cai, H. N. 2006. Function and mechanism of chromatin boundaries. In J. Ma (ed.), Gene expression and regulation. Higher Education Press, Beijing, China.
18. Cai, H. N., and M. Levine. 1997. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J. 16:1732-1741.
19. Cai, H. N., and P. Shen. 2001. Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science 291:493-495.
20. Celniker, S. E., and R. A. Drewell. 2007. Chromatin looping mediates boundary element promoter interactions. Bioessays 29:7-10.
21. Clemens, J. C., C. A. Worby, N. Simonson-Leff, M. Muda, T. Maehama, B. A. Hemmings, and J. E. Dixon. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. U. S. A. 97:6499-6503.
22. Corona, D. F., G. Langst, C. R. Clapier, E. J. Bonte, S. Ferrari, J. W. Tamkun, and P. B. Becker. 1999. ISWI is an ATP-dependent nucleosome remodeling factor. Mol. Cell 3:239-245.
23. Deuring, R., L. Fanti, J. A. Armstrong, M. Sarte, O. Papoulas, M. Prestel, G. Daubresse, M. Verardo, S. L. Moseley, M. Berloco, T. Tsukiyama, C. Wu, S. Pimpinelli, and J. W. Tamkun. 2000. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol. Cell 5:355-365.
24. Dunn, K. L., H. Zhao, and J. R. Davie. 2003. The insulator binding protein CTCF associates with the nuclear matrix. Exp. Cell Res. 288:218-223.
25. Elfring, L. K., R. Deuring, C. M. McCallum, C. L. Peterson, and J. W. Tamkun. 1994. Identification and characterization of Drosophila relatives of the yeast transcriptional activator SNF2/SWI2. Mol. Cell. Biol. 14:2225-2234.
26. Farkas, G., B. A. Leibovitch, and S. C. Elgin. 2000. Chromatin organization and transcriptional control of gene expression in Drosophila. Gene 253:117-136.
27. Ferreira, R., A. Eberharter, T. Bonaldi, M. Chioda, A. Imhof, and P. B. Becker. 2007. Site-specific acetylation of ISWI by GCN5. BMC Mol. Biol. 8:73.
28. Fu, Y., M. Sinha, C. L. Peterson, and Z. Weng. 2008. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet. 4:e1000138.
29. Galloni, M., H. Gyurkovics, P. Schedl, and F. Karch. 1993. The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J. 12:1087-1097.
30. Gaszner, M., and G. Felsenfeld. 2006. Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 7:703-713.
31. Gaszner, M., J. Vazquez, and P. Schedl. 1999. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancerpromoter interaction. Genes Dev. 13:2098-2107.
32. Gerasimova, T. I., K. Byrd, and V. G. Corces. 2000. A chromatin insulator determines the nuclear localization of DNA. Mol. Cell 6:1025-1035.
33. Geyer, P. K., and I. Clark. 2002. Protecting against promiscuity: the regulatory role of insulators. Cell. Mol. Life Sci. 59:2112-2127.
34. Geyer, P. K., and V. G. Corces. 1992. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 6:1865-1873.
35. Gruzdeva, N., O. Kyrchanova, A. Parshikov, A. Kullyev, and P. Georgiev. 2005. The Mcp element from the bithorax complex contains an insulator that is capable of pairwise interactions and can facilitate enhancer-promoter communication. Mol. Cell. Biol. 25:3682-3689.
36. Gyurkovics, H., J. Gausz, J. Kummer, and F. Karch. 1990. A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. EMBO J. 9:2579-2585.
37. Hamiche, A., R. Sandaltzopoulos, D. A. Gdula, and C. Wu. 1999. ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97:833-842.
38. Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancerblocking activity at the H19/Igf2 locus. Nature 405:486-489.
39. Hogga, I., and F. Karch. 2002. Transcription through the iab-7 cis-regulatory domain of the bithorax complex interferes with maintenance of Polycombmediated silencing. Development 129:4915-4922.
40. Holohan, E. E., C. Kwong, B. Adryan, M. Bartkuhn, M. Herold, R. Renkawitz, S. Russell, and R. White. 2007. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet. 3:e112.
41. Johnson, C. A., A. L. Barlow, and B. M. Turner. 1998. Molecular cloning of Drosophila melanogaster cDNAs that encode a novel histone deacetylase dHDAC3. Gene 221:127-134.
42. Kehle, J., D. Beuchle, S. Treuheit, B. Christen, J. A. Kennison, M. Bienz, and J. Muller. 1998. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282:1897-1900.
43. Kellum, R., and P. Schedl. 1991. A position-effect assay for boundaries of higher order chromosomal domains. Cell 64:941-950.
44. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
45. Kunert, N., and A. Brehm. 2008. Mass production of Drosophila embryos and chromatographic purification of native protein complexes. Methods Mol. Biol. 420:359-371.
46. Kunert, N., and A. Brehm. 2009. Novel Mi-2 related ATP-dependent chromatin remodelers. Epigenetics 4:209-211.
47. Kunert, N., E. Wagner, M. Murawska, H. Klinker, E. Kremmer, and A. Brehm. 2009. dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J. 28:533-544.
48. Kyrchanova, O., S. Toshchakov, A. Parshikov, and P. Georgiev. 2007. Study of the functional interaction between Mcp insulators from the Drosophila bithorax complex: effects of insulator pairing on enhancer-promoter communication. Mol. Cell. Biol. 27:3035-3043.
49. Lanctot, C., T. Cheutin, M. Cremer, G. Cavalli, and T. Cremer. 2007. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8:104-115.
50. Langst, G., E. J. Bonte, D. F. Corona, and P. B. Becker. 1999. Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97:843-852.
51. Leighton, P. A., R. S. Ingram, J. Eggenschwiler, A. Efstratiadis, and S. M. Tilghman. 1995. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 375:34-39.
52. Li, M., V. E. Belozerov, and H. N. Cai. 2008. Analysis of chromatin boundary activity in Drosophila cells. BMC Mol. Biol. 9:109.
53. Lin, Q., Q. Chen, L. Lin, S. Smith, and J. Zhou. 2007. Promoter targeting sequence mediates enhancer interference in the Drosophila embryo. Proc. Natl. Acad. Sci. U. S. A. 104:3237-3242.
54. Lutz, M., L. J. Burke, G. Barreto, F. Goeman, H. Greb, R. Arnold, H. Schultheiss, A. Brehm, T. Kouzarides, V. Lobanenkov, and R. Renkawitz. 2000. Transcriptional repression by the insulator protein CTCF involves histone deacetylases. Nucleic Acids Res. 28:1707-1713.
55. Mahmoudi, T., K. R. Katsani, and C. P. Verrijzer. 2002. GAGA can mediate enhancer function in trans by linking two separate DNA molecules. EMBO J. 21:1775-1781.
56. Maier, V. K., M. Chioda, and P. B. Becker. 2008. ATP-dependent chromatosome remodeling. Biol. Chem. 389:345-352.
57. Martens, J. A., and F. Winston. 2003. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13:136-142.
58. Melnikova, L., F. Juge, N. Gruzdeva, A. Mazur, G. Cavalli, and P. Georgiev. 2004. Interaction between the GAGA factor and Mod(mdg4) proteins promotes insulator bypass in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 101:14806-14811.
59. Mishra, R. K., J. Mihaly, S. Barges, A. Spierer, F. Karch, K. Hagstrom, S. E. Schweinsberg, and P. Schedl. 2001. The iab-7 polycomb response element maps to a nucleosome-free region of chromatin and requires both GAGA and Pleiohomeotic for Silencing. Mol. Cell. Biol. 21:1311-1318.
60. Mlynarova, L., A. Loonen, E. Mietkiewska, R. C. Jansen, and J. P. Nap. 2002. Assembly of two transgenes in an artificial chromatin domain gives highly coordinated expression in tobacco. Genetics 160:727-740.
61. Moon, H., G. Filippova, D. Loukinov, E. Pugacheva, Q. Chen, S. T. Smith, A. Munhall, B. Grewe, M. Bartkuhn, R. Arnold, L. J. Burke, R. Renkawitz- Pohl, R. Ohlsson, J. Zhou, R. Renkawitz, and V. Lobanenkov. 2005. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 6:165-170.
62. Ohtsuki, S., and M. Levine. 1998. GAGA mediates the enhancer blocking activity of the eve promoter in the Drosophila embryo. Genes Dev. 12:3325-3330.
63. Okada, M., and S. Hirose. 1998. Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro. Mol. Cell. Biol. 18:2455-2461.
64. Petesch, S. J., and J. T. Lis. 2008. Rapid, transcription- independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134:74-84.
65. Schweinsberg, S., K. Hagstrom, D. Gohl, P. Schedl, R. P. Kumar, R. Mishra, and F. Karch. 2004. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 168:1371-1384.
66. Spana, C., D. A. Harrison, and V. G. Corces. 1988. The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 2:1414-1423.
67. Tautz, D., and C. Pfeifle. 1989. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81-85.
68. Tong, J. K., C. A. Hassig, G. R. Schnitzler, R. E. Kingston, and S. L. Schreiber. 1998. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395:917-921.
69. Tsukiyama, T., P. B. Becker, and C. Wu. 1994. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367:525-532.
70. Tsukiyama, T., C. Daniel, J. Tamkun, and C. Wu. 1995. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83:1021-1026.
71. Varga-Weisz, P. D., T. A. Blank, and P. B. Becker. 1995. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system. EMBO J. 14:2209-2216.
72. West, A. G., S. Huang, M. Gaszner, M. D. Litt, and G. Felsenfeld. 2004. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16:453-463.
73. Xiao, H., R. Sandaltzopoulos, H. M. Wang, A. Hamiche, R. Ranallo, K. M. Lee, D. Fu, and C. Wu. 2001. Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol. Cell 8:531-543.
74. Xue, Y., J. Wong, G. T. Moreno, M. K. Young, J. Cote, and W. Wang. 1998. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 2:851-861.
75. Yasui, D., M. Miyano, S. Cai, P. Varga-Weisz, and T. Kohwi-Shigematsu. 2002. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419:641-645.
76. Zhang, Y., G. LeRoy, H. P. Seelig, W. S. Lane, and D. Reinberg. 1998. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95:279-289.
77. Zhao, K., C. M. Hart, and U. K. Laemmli. 1995. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81:879-889.
78. Zhou, J., H. Ashe, C. Burks, and M. Levine. 1999. Characterization of the transvection mediating region of the abdominal-B locus in Drosophila. Development 126:3057-3065.