The PBAP remodeling complex is required for histone H3.3 replacement at chromatin boundaries and for boundary functions

Development (Cambridge)

Volumn 139, Issue 24, 2012, Pages 4582-4590

  Nakayama, Takahiro ^a   Shimojima, Tsukasa ^a,b   Hirose, Susumu ^a  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Chromatin boundary; Drosophila; FACT; Histone H3.3; PBAP complex; Trithorax group

Indexed keywords

CHAPERONE; DNA BINDING PROTEIN; GAGA FACTOR; HISTONE H3; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CHROMATIN STRUCTURE; COMPLEX FORMATION; DROSOPHILA; ENHANCER REGION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CELL CYCLE PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; HISTONES; INSULATOR ELEMENTS; MULTIPROTEIN COMPLEXES; PROTEIN TRANSPORT; TELOMERE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84870028442     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.083246     Document Type: Article

References (37)

1. Ahmad, K. and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200.
2. Becker, P. B. and Hörz, W. (2002). ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71, 247-273.
3. Bell, A. C., West, A. G. and Felsenfeld, G. (2001). Insulators and boundaries: versatile regulatory elements in the eukaryotic genome. Science 291, 447-450.
4. Belotserkovskaya, R., Oh, S., Bondarenko, V. A., Orphanides, G., Studitsky, V. M. and Reinberg, D. (2003). FACT facilitates transcription-dependent nucleosome alteration. Science 301, 1090-1093.
5. Belozerov, V. E., Majumder, P., Shen, P. and Cai, H. N. (2003). A novel boundary element may facilitate independent gene regulation in the Antennapedia complex of Drosophila. EMBO J. 22, 3113-3121.
6. Bernués, J., Piñeyro, D. and Kosoy, A. (2007). General, negative feedback mechanism for regulation of Trithorax-like gene expression in vivo: new roles for GAGA factor in flies. Nucleic Acids Res. 35, 7150-7159.
7. Bonnefoy, E., Orsi, G. A., Couble, P. and Loppin, B. (2007). The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet. 3, 1991-2006.
8. Busturia, A., Lloyd, A., Bejarano, F., Zavortink, M., Xin, H. and Sakonju, S. (2001). The MCP silencer of the Drosophila Abd-B gene requires both Pleiohomeotic and GAGA factor for the maintenance of repression. Development 128, 2163-2173.
9. Carrera, I., Zavadil, J. and Treisman, J. E. (2008). Two subunits specific to the PBAP chromatin remodeling complex have distinct and redundant functions during drosophila development. Mol. Cell. Biol. 28, 5238-5250.
10. Clapier, C. R. and Cairns, B. R. (2009). The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304.
11. Collins, R. T. and Treisman, J. E. (2000). Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes Dev. 14, 3140-3152.
12. Drané, P., Ouararhni, K., Depaux, A., Shuaib, M. and Hamiche, A. (2010). The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24, 1253-1265.
13. Farkas, G., Gausz, J., Galloni, M., Reuter, G., Gyurkovics, H. and Karch, F. (1994). The Trithorax-like gene encodes the Drosophila GAGA factor. Nature 371, 806-808.
14. Goldberg, A. D., Banaszynski, L. A., Noh, K.-M., Lewis, P. W., Elsaesser, S. J., Stadler, S. J., Dewell, S., Law, M., Guo, X., Li, X. et al. (2010). Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691.
15. Henikoff, S. and Ahmad, K. (2005). Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21, 133-153.
16. Jack, R. S. and Eggert, H. (1990). Restriction enzymes have limited access to DNA sequences in Drosophila chromosomes. EMBO J. 9, 2603-2609.
17. Jenuwein, T. and Allis, C. D. (2001). Translating the histone code. Science 293, 1074-1080.
18. Jin, C. and Felsenfeld, G. (2007). Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 21, 1519-1529.
19. Kamakaka, R. T. and Biggins, S. (2005). Histone variants: deviants? Genes Dev. 19, 295-316.
20. Konev, A. Y., Tribus, M., Park, S. Y., Podhraski, V., Lim, C. Y., Emelyanov, A. V., Vershilova, E., Pirrotta, V., Kadonaga, J. T., Lusser, A. et al. (2007). CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317, 1087-1090.
21. Loppin, B., Bonnefoy, E., Anselme, C., Laurençon, A., Karr, T. L. and Couble, P. (2005). The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437, 1386-1390.
22. Lorch, Y., Zhang, M. and Kornberg, R. D. (1999). Histone octamer transfer by a chromatin-remodeling complex. Cell 96, 389-392.
23. Maeda, R. K. and Karch, F. (2007). Making connections: boundaries and insulators in Drosophila. Curr. Opin. Genet. Dev. 17, 394-399.
24. McKittrick, E., Gafken, P. R., Ahmad, K. and Henikoff, S. (2004). Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101, 1525-1530.
25. Mihaly, J., Hogga, I., Gausz, J., Gyurkovics, H. and Karch, F. (1997). In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. Development 124, 1809-1820.
26. Mito, Y., Henikoff, J. G. and Henikoff, S. (2007). Histone replacement marks the boundaries of cis-regulatory domains. Science 315, 1408-1411.
27. 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.
28. Moon, H., Filippova, G., Loukinov, D., Pugacheva, E., Chen, Q., Smith, S. T., Munhall, A., Grewe, B., Bartkuhn, M., Arnold, R. et al. (2005). CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 6, 165-170.
29. Moshkin, Y. M., Mohrmann, L., van Ijcken, W. F. and Verrijzer, C. P. (2007). Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol. Cell. Biol. 27, 651-661.
30. Nakayama, T., Nishioka, K., Dong, Y. X., Shimojima, T. and Hirose, S. (2007). Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading. Genes Dev. 21, 552-561.
31. O'Donnell, K. H., Chen, C. T. and Wensink, P. C. (1994). Insulating DNA directs ubiquitous transcription of the Drosophila melanogaster alpha 1-tubulin gene. Mol. Cell. Biol. 14, 6398-6408.
32. Ray-Gallet, D., Woolfe, A., Vassias, I., Pellentz, C., Lacoste, N., Puri, A., Schultz, D. C., Pchelintsev, N. A., Adams, P. D., Jansen, L. E. T. et al. (2011). Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol. Cell 44, 928-941.
33. Sarma, K. and Reinberg, D. (2005). Histone variants meet their match. Nat. Rev. Mol. Cell Biol. 6, 139-149.
34. Shimojima, T., Okada, M., Nakayama, T., Ueda, H., Okawa, K., Iwamatsu, A., Handa, H. and Hirose, S. (2003). Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor. Genes Dev. 17, 1605-1616.
35. Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y. (2004). Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51-61.
36. Workman, J. L. (2006). Nucleosome displacement in transcription. Genes Dev. 20, 2009-2017.
37. Xiao, H., Sandaltzopoulos, R., Wang, H. M., Hamiche, A., Ranallo, R., Lee, K. M., Fu, D. and Wu, C. (2001). Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol. Cell 8, 531-543.