The Drosophila trithorax group protein kismet facilitates an early step in transcriptional elongation by RNA polymerase II

Development

Volumn 132, Issue 7, 2005, Pages 1623-1635

  Srinivasan, Shrividhya ^a   Armstrong, Jennifer A ^a,c   Deuring, Renate ^a   Dahlsveen, Ina K ^b,d   McNeill, Helen ^b   Tamkun, John W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c The Claremont Colleges   (United States)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

BRM complex; Chromatin; Kismet; Polycomb; RNA polymerase II; Transcription; Trithorax

Indexed keywords

ELONGATION FACTOR; NUCLEAR PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; LARVAL STAGE; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SALIVARY GLAND; TISSUE DISTRIBUTION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; DROSOPHILA; DROSOPHILA PROTEINS; HOMEODOMAIN PROTEINS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EID: 17744371151     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01713     Document Type: Article

References (93)

1. Aasland, R., Gibson, T. J. and Stewart, A. F. (1995). The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20, 56-59.
2. Ahn, S. H., Kim, M. and Buratowski, S. (2004). Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell 13, 67-76.
3. Armstrong, J. A., Papoulas, O., Daubresse, G., Sperling, A. S., Lis, J. T., Scott, M. P. and Tamkun, J. W. (2002). The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J. 21, 5245-5254.
4. Beisel, C., Imhof, A., Greene, J., Kremmer, E. and Sauer, F. (2002). Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature 419, 857-862.
5. Berger, S. L. (2002). Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12, 142-148.
6. Brehm, A., Langst, G., Kehle, J., Clapier, C. R., Imhof, A., Eberharter, A., Müller, J. and Becker, P. B. (2000). dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J. 19, 4332-4341.
7. Brehm, A., Tufteland, K. R., Aasland, R. and Becker, P. B. (2004). The many colours of chromodomains. BioEssays 26, 133-140.
8. Breiling, A., Turner, B. M., Bianchi, M. E. and Orlando, V. (2001). General transcription factors bind promoters repressed by Polycomb group proteins. Nature 412, 651-655.
9. Breiling, A., O'Neill, L. P., D'Eliseo, D., Turner, B. M. and Orlando, V. (2004). Epigenome changes in active and inactive Polycomb-group-controlled regions. EMBO Rep. 5, 976-982.
10. Brizuela, B. J., Elfring, L., Ballard, J., Tamkun, J. W. and Kennison, J. A. (1994). Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics 137, 803-813.
11. Brown, S. A., Imbalzano, A. N. and Kingston, R. E. (1996). Activator-dependent regulation of transcriptional pausing on nucleosomal templates. Genes Dev. 10, 1479-1490.
12. Buratowski, S. (2000). Snapshots of RNA polymerase II transcription initiation. Curr. Opin. Cell Biol. 12, 320-325.
13. Byrd, K. N. and Shearn, A. (2003). ASH1, a Drosophila trithorax group protein, is required for methylation of lysine 4 residues on histone H3. Proc. Natl. Acad. Sci. USA 100 11535-11540.
14. Cao, R. and Zhang, Y. (2004). The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14, 155-164.
15. Cho, E. J., Kobor, M. S., Kim, M., Greenblatt, J. and Buratowski, S. (2001). Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15, 3319-3329.
16. Collins, R. T., Furukawa, T., Tanese, N. and Treisman, J. E. (1999). Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. EMBO J. 18, 7029-7040.
17. Corey, L. L., Weirich, C. S., Benjamin, I. J. and Kingston, R. E. (2003). Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev. 17, 1392-1401.
18. Corona, D. F. and Tamkun, J. W. (2004). Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim. Biophys. Acta 1677, 113-119.
19. Corona, D. F., Armstrong, J. A. and Tamkun, J. W. (2004). Genetic and cytological analysis of Drosophila chromatin-remodeling factors. Methods Enzymol. 377, 70-85.
20. Crosby, M. A., Miller, C., Alon, T., Watson, K. L., Verrijzer, C. P., Goldman-Levi, R. and Zak, N. B. (1999). The trithorax group gene moira encodes a Brahma-associated putative chromatin-remodeling factor in Drosophila melanogaster. Mol. Cell. Biol. 19, 1159-1170.
21. Daubresse, G., Deuring, R., Moore, L., Papoulas, O., Zakrajsek, I., Waldrip, W. R., Scott, M. P., Kennison, J. A. and Tamkun, J. W. (1999). The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development 126, 1175-1187.
22. Dellino, G. I., Schwartz, Y. B., Farkas, G., McCabe, D., Elgin, S. C. and Pirrotta, V. (2004). Polycomb silencing blocks transcription initiation. Mol. Cell 13, 887-893.
23. Elfring, L. K., Daniel, C., Papoulas, O., Deuring, R., Sarte, M., Moseley, S., Beek, S. J., Waldrip, W. R., Daubresse, G., DePace, A. et al. (1998). Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2 /SNF2. Genetics 148, 251-265.
24. Flaus, A. and Owen-Hughes, T. (2004). Mechanisms for ATP-dependent chromatin remodelling: farewell to the tuna-can octamer? Curr. Opin. Genet. Dev. 14, 165-173.
25. Francis, N. J. and Kingston, R. E. (2001). Mechanisms of transcriptional memory. Nat. Rev. Mol. Cell Biol. 2, 409-421.
26. Francis, N. J., Saurin, A. J., Shao, Z. and Kingston, R. E. (2001). Reconstitution of a functional core Polycomb repressive complex. Mol. Cell 8, 545-556.
27. Gellon, G. and McGinnis, W. (1998). Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20, 116-125.
28. Go, M. J. and Artavanis-Tsakonas, S. (1998). A genetic screen for novel components of the Notch signaling pathway during Drosophila bristle development. Genetics 150, 211-220.
29. Gould, A. (1997). Functions of mammalian Polycomb group and trithorax group related genes. Curr. Opin. Genet. Dev. 7, 488-494.
30. Harlow, E. and Lane, D. (1988). Antibodies: A Labratory Manual. Cold Spring Harbor: Cold Spring Harbor Publications.
31. 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.
32. Hirose, Y. and Manley, J. L. (2000). RNA polymerase II and the integration of nuclear events. Genes Dev. 14, 1415-1429.
33. Hughes, C. M., Rozenblatt-Rosen, O., Milne, T. A., Copeland, T. D., Levine, S. S., Lee, J. C., Hayes, D. N., Shanmugam, K. S., Bhattacharjee, A., Biondi, C. A. et al. (2004). Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13, 587-597.
34. Kaplan, C. D., Morris, J. R., Wu, C. and Winston, F. (2000). Spt5 and Spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev. 14, 2623-2634.
35. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J. A., Bienz, M. and Müller, J. (1998). dMi-2, a hunchback-interacfing protein that functions in Polycomb repression. Science 282, 1897-1900.
36. Kelley, D. E., Stokes, D. G. and Perry, R. P. (1999). CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin. Chromosoma 108, 10-25.
37. Kennison, J. A. (1995). The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29, 289-303.
38. Kennison, J. A. and Tamkun, J. W. (1988). Dosage-dependent modifiers of Polycomb and Antennapedia mutations in Drosophila. Proc. Natl. Acad. Sci. USA 85, 8136-8140.
39. Klymenko, T. and Müller, J. (2004). The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep. 5, 373-377.
40. Komarnitsky, P., Cho, E. J. and Buratowski, S. (2000). Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460.
41. Krogan, N. J., Kim, M., Tong, A., Golshani, A., Cagney, G., Canadien, V., Richards, D. P., Beattie, B. K., Emili, A., Boone, C. et al. (2003). Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23, 4207-4218.
42. Levine, S. S., King, I. F. and Kingston, R. E. (2004). Division of labor in Polycomb group repression. Trends Biochem. Sci. 29, 478-485.
43. Levine, S. S., Weiss, A., Erdjument-Bromage, H., Shao, Z., Tempst, P. and Kingston, R. E. (2002). The core of the Polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol. Cell. Biol. 22, 6070-6078.
44. McGrail, M. and Hays, T. S. (1997). The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409-2419.
45. Miller, T., Krogan, N. J., Dover, J., Erdjument-Bromage, H., Tempst, P., Johnston, M., Greenblatt, J. F. and Shilatifard, A. (2001). COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 98, 12902-12907.
46. Milne, T. A., Briggs, S. D., Brock, H. W., Martin, M. E., Gibbs, D., Allis, C. D. and Hess, J. L. (2002). MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10 1107-1117.
47. 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.
48. Nagy, P. L., Griesenbeck, J., Kornberg, R. D. and Cleary, M. L. (2002). A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc. Natl. Acad. Sci. USA 99, 90-94.
49. Nakamura, T., Mori, T., Tada, S., Krajewski, W., Rozovskaia, T., Wassell, R., Dubois, G., Mazo, A., Croce, C. M. and Canaani, E. (2002). ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10, 1119-1128.
50. Narlikar, G. J., Fan, H. Y. and Kingston, R. E. (2002). Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475-487.
51. Neish, A. S., Anderson, S. F., Schlegel, B. P., Wei, W. and Parvin, J. D. (1998). Factors associated with the mammalian RNA polymerase II holoenzyme. Nucleic Acids Res. 26, 847-853.
52. Ng, H. H., Robert, F., Young, R. A. and Struhl, K. (2003). Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709-719.
53. Ni, Z., Schwartz, B. E., Werner, J., Suarez, J. R. and Lis, J. T. (2004). Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell 13 55-65.
54. O'Brien, T., Hardin, S., Greenleaf, A. and Lis, J. T. (1994). Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature 370, 75-77.
55. Papoulas, O., Beek, S. J., Moseley, S. L., McCallum, C. M., Sarte, M., Shearn, A. and Tamkun, J. W. (1998). The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development 125, 3955-3966.
56. Papoulas, O., Daubresse, G., Armstrong, J. A., Jin, J., Scott, M. P. and Tamkun, J. W. (2001). The HMG-domain protein BAP111 is important for the function of the BRM chromatin-remodeling complex in vivo. Proc. Natl. Acad. Sci. USA 98, 5728-5733.
57. Peterson, C. L. and Logie, C. (2000). Recruitment of chromatin remodeling machines. J. Cell Biochem. 78, 179-185.
58. Pokholok, D. K., Hannett, N. M. and Young, R. A. (2002). Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9, 799-809.
59. Prelich, G. (2002). RNA polymerase II carboxy-terminal domain kinases: emerging clues to their function. Eukaryot. Cell 1, 153-162.
60. Proudfoot, N. J., Furger, A. and Dye, M. J. (2002). Integrating mRNA processing with transcription. Cell 108, 501-512.
61. Ringrose, L. and Paro, R. (2004). Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annu. Rev. Genet. 38, 413-443.
62. Roch, F., Serras, F., Cifuentes, F. J., Corominas, M., Alsina, B., Amoros, M., Lopez-Varea, A., Hernandez, R., Guerra, D., Cavicchi, S. et al. (1998). Screening of larval/pupal P-element induced lethals on the second chromosome in Drosophila melanogaster clonal analysis and morphology of imaginal discs. Mol. Gen. Genet. 257, 103-112.
63. Roguev, A., Schaft, D., Shevchenko, A., Pijnappel, W. W., Wilm, M., Aasland, R. and Stewart, A. F. (2001). The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 20, 7137-7148.
64. Ruhf, M. L., Braun, A., Papoulas, O., Tamkun, J. W., Randsholt, N. and Meister, M. (2001). The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes. Development 128, 1429-1441.
65. Santos-Rosa, H., Schneider, R., Bannister, A. J., Sherriff, J., Bernstein, B. E., Emre, N. C., Schreiber, S. L., Mellor, J. and Kouzarides, T. (2002). Active genes are tri-methylated at K4 of histone H3. Nature 419, 407-411.
66. Saunders, A., Werner, J., Andrulis, E. D., Nakayama, T., Hirose, S., Reinberg, D. and Lis, J. T. (2003). Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301, 1094-1096.
67. 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.
68. Schumacher, A. and Magnuson, T. (1997). Murine Polycomb- and trithorax-group genes regulate homeotic pathways and beyond. Trends Genet. 13, 167-170.
69. Schuster, E. F. and Stoger, R. (2002). CHD5 defines a new subfamily of chromodomain-SWI2/SNF2-like helicases. Mamm. Genome 13, 117-119.
70. 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.
71. Simic, R., Lindstrom, D. L., Tran, H. G., Roinick, K. L., Costa, P. J., Johnson, A. D., Hartzog, G. A. and Arndt, K. M. (2003). Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 22, 1846-1856.
72. Simon, J. (1995). Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol. 7, 376-385.
73. Simon, J. A. and Tamkun, J. W. (2002). Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12, 210-218.
74. Sims, R. J., 3rd, Belotserkovskaya, R. and Reinberg, D. (2004). Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18, 2437-2468.
75. Skantar, A. M. and Greenleaf, A. L. (1995). Identifying a transcription factor interaction site on RNA polymerase II. Gene Expr. 5, 49-69.
76. Smith, S. T., Petruk, S., Sedkov, Y., Cho, E., Tillib, S., Canaani, E. and Mazo, A. (2004). Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex. Nat. Cell Biol. 6, 162-7.
77. Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty, T., Mozden, N., Misra, S. and Rubin, G. M. (1999). The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153, 135-177.
78. Stokes, D. G., Tartof, K. D. and Perry, R. P. (1996). CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. Proc. Natl. Acad. Sci. USA 93, 7137-7142.
79. Strutt, H., Cavalli, G. and Paro, R. (1997). Co-localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression. EMBO J. 16, 3621-3632.
80. Svejstrup, J. Q. (2004). The RNA polymerase II transcription cycle: cycling through chromatin. Biochim. Biophys. Acta 1677, 64-73.
81. Svejstrup, J. Q., Li, Y., Fellows, J., Gnatt, A., Bjorklund, S. and Kornberg, R. D. (1997). Evidence for a mediator cycle at the initiation of transcription. Proc. Natl. Acad. Sci. USA 94, 6075-6078.
82. Tamkun, J. W., Deuring, R., Scott, M. P., Kissinger, M., Pattatucci, A. M., Kaufman, T. C. and Kennison, J. A. (1992). brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561-572.
83. Therrien, M., Morrison, D. K., Wong, A. M. and Rubin, G. M. (2000). A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 156 1231-1242.
84. Tsukiyama, T., Daniel, C., Tamkun, J. and Wu, C. (1995). ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83, 1021-1026.
85. Verheyen, E. M., Purcell, K. J., Fortini, M. E. and Artavanis-Tsakonas, S. (1996). Analysis of dominant enhancers and suppressors of activated Notch in Drosophila. Genetics 144, 1127-1141.
86. Wang, L., Brown, J. L., Cao, R., Zhang, Y., Kassis, J. A. and Jones, R. S. (2004). Hierarchical recruitment of Polycomb group silencing complexes. Mol. Cell 14, 637-646.
87. Weeks, J. R., Hardin, S. E., Shen, J., Lee, J. M. and Greenleaf, A. L. (1993). Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing. Genes Dev. 7, 2329-2344.
88. Wilson, C. J., Chao, D. M., Imbalzano, A. N., Schnitzler, G. R., Kingston, R. E. and Young, R. A. (1996). RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell 84, 235-244.
89. Xiao, T., Hall, H., Kizer, K. O., Shibata, Y., Hall, M. C., Borchers, C. H. and Strahl, B. D. (2003). Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17, 654-663.
90. Yokoyama, A., Wang, Z., Wysocka, J., Sanyal, M., Aufiero, D. J., Kitabayashi, I., Herr, W. and Cleary, M. L. (2004). Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24 5639-5649.
91. Zeng, L. and Zhou, M. M. (2002). Bromodomain: an acetyl-lysine binding domain. FEBS Lett. 513, 124-128.
92. Zhang, Y., LeRoy, G., Seelig, H. P., Lane, W. S. and Reinberg, D. (1998). The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95, 279-289.
93. Zink, B. and Paro, R. (1989). In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature 337, 468-471.