The trithorax group proteins Kismet and ASH1 promote H3K36 dimethylation to counteract Polycomb group repression in Drosophila

Development (Cambridge)

Volumn 140, Issue 20, 2013, Pages 4182-4192

  Dorighi, Kristel M ^a   Tamkun, John W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chromatin; Histone methylation; Polycomb group; Transcription; Trithorax group

Indexed keywords

HISTONE H3; HISTONE H3K36; HISTONE METHYLTRANSFERASE; LYSINE; NUCLEAR PROTEIN; POLYCOMB GROUP PROTEIN; TRITHORAX GROUP HISTONE METHYLTRANSFERASE; TRITHORAX GROUP PROTEIN KISMET; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DROSOPHILA; DROSOPHILA STRAIN; HISTONE METHYLATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SALIVARY GLAND; TRANSCRIPTION ELONGATION;

CHROMATIN; HISTONE METHYLATION; POLYCOMB GROUP; TRANSCRIPTION; TRITHORAX GROUP;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; DNA HELICASES; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HOMEODOMAIN PROTEINS; METHYLATION; NUCLEIC ACID SYNTHESIS INHIBITORS; POLYCOMB-GROUP PROTEINS; SALIVARY GLANDS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84884931891     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.095786     Document Type: Article

References (71)

1. An, S., Yeo, K. J., Jeon, Y. H. and Song, J. J. (2011). Crystal structure of the human histone methyltransferase ASH1L catalytic domain and its implications for the regulatory mechanism. J. Biol. Chem. 286, 8369-8374.
2. Ardehali, M. B., Mei, A., Zobeck, K. L., Caron, M., Lis, J. T. and Kusch, T. (2011). Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. EMBO J. 30, 2817-2828.
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. Bartkowiak, B., Mackellar, A. L. and Greenleaf, A. L. (2011). Updating the CTD story: from tail to epic. Genet. Res. Int. 2011, 623718.
5. 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.
6. Bell, O., Wirbelauer, C., Hild, M., Scharf, A. N., Schwaiger, M., MacAlpine, D. M., Zilbermann, F., van Leeuwen, F., Bell, S. P., Imhof, A. et al. (2007). Localized H3K36 methylation states define histone H4K16 acetylation during transcriptional elongation in Drosophila. EMBO J. 26, 4974-4984.
7. Bensaude, O. (2011). Inhibiting eukaryotic transcription: which compound to choose? How to evaluate its activity? Transcription 2, 103-108.
8. Bouazoune, K. and Kingston, R. E. (2012). Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc. Natl. Acad. Sci. USA 109, 19238-19243.
9. Buratowski, S. (2009). Progression through the RNA polymerase II CTD cycle. Mol. Cell 36, 541-546.
10. 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.
11. 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.
12. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S. and Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043.
13. Chodosh, L. A., Fire, A., Samuels, M. and Sharp, P. A. (1989). 5,6-Dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription elongation by RNA polymerase II in vitro. J. Biol. Chem. 264, 2250-2257.
14. 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.
15. Corona, D. F., Siriaco, G., Armstrong, J. A., Snarskaya, N., McClymont, S. A., Scott, M. P. and Tamkun, J. W. (2007). ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol. 5, e232.
16. 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.
17. 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.
18. Egyházi, E., Ossoinak, A., Pigon, A., Holmgren, C., Lee, J. M. and Greenleaf, A. L. (1996). Phosphorylation dependence of the initiation of productive transcription of Balbiani ring 2 genes in living cells. Chromosoma 104, 422-433.
19. 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.
20. Fasulo, B., Deuring, R., Murawska, M., Gause, M., Dorighi, K. M., Schaaf, C. A., Dorsett, D., Brehm, A. and Tamkun, J. W. (2012). The Drosophila MI-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet. 8, e1002878.
21. Fisher, C. L. and Fisher, A. G. (2011). Chromatin states in pluripotent, differentiated, and reprogrammed cells. Curr. Opin. Genet. Dev. 21, 140-146.
22. Gaydos, L. J., Rechtsteiner, A., Egelhofer, T. A., Carroll, C. R. and Strome, S. (2012). Antagonism between MES-4 and Polycomb repressive complex 2 promotes appropriate gene expression in C. elegans germ cells. Cell Reports 2, 1169-1177.
23. Giardina, C. and Lis, J. T. (1993). Polymerase processivity and termination on Drosophila heat shock genes. J. Biol. Chem. 268, 23806-23811.
24. Gregory, G. D., Vakoc, C. R., Rozovskaia, T., Zheng, X., Patel, S., Nakamura, T., Canaani, E. and Blobel, G. A. (2007). Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Mol. Cell. Biol. 27, 8466-8479.
25. Grimaud, C., Nègre, N. and Cavalli, G. (2006). From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res. 14, 363-375.
26. Hallson, G., Hollebakken, R. E., Li, T., Syrzycka, M., Kim, I., Cotsworth, S., Fitzpatrick, K. A., Sinclair, D. A. and Honda, B. M. (2012). dSet1 is the main H3K4 di-and tri-methyltransferase throughout Drosophila development. Genetics 190, 91-100.
27. Henikoff, S., McKittrick, E. and Ahmad, K. (2004). Epigenetics, histone H3 variants, and the inheritance of chromatin states. Cold Spring Harb. Symp. Quant. Biol. 69, 235-244.
28. Janssen, N., Bergman, J. E., Swertz, M. A., Tranebjaerg, L., Lodahl, M., Schoots, J., Hofstra, R. M., van Ravenswaaij-Arts, C. M. and Hoefsloot, L. H. (2012). Mutation update on the CHD7 gene involved in CHARGE syndrome. Hum. Mutat. 33, 1149-1160.
29. Jongmans, M. C., Admiraal, R. J., van der Donk, K. P., Vissers, L. E., Baas, A. F., Kapusta, L., van Hagen, J. M., Donnai, D., de Ravel, T. J., Veltman, J. A. et al. (2006). CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J. Med. Genet. 43, 306-314.
30. 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.
31. 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.
32. Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., Minoda, A., Riddle, N. C., Ernst, J., Sabo, P. J., Larschan, E., Gorchakov, A. A., Gu, T. et al. (2011). Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471, 480-485.
33. Kimura, H., Hayashi-Takanaka, Y., Goto, Y., Takizawa, N. and Nozaki, N. (2008). The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct. Funct. 33, 61-73.
34. Klymenko, T. and Müller, J. (2004). The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep. 5, 373-377.
35. Kuzmichev, A., Nishioka, K., Erdjument-Bromage, H., Tempst, P. and Reinberg, D. (2002). Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16, 2893-2905.
36. Lanzuolo, C. and Orlando, V. (2012). Memories from the polycomb group proteins. Annu. Rev. Genet. 46, 561-589.
37. Levine, S. S., King, I. F. and Kingston, R. E. (2004). Division of labor in polycomb group repression. Trends Biochem. Sci. 29, 478-485.
38. Mancebo, H. S., Lee, G., Flygare, J., Tomassini, J., Luu, P., Zhu, Y., Peng, J., Blau, C., Hazuda, D., Price, D. et al. (1997). P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11, 2633-2644.
39. Margueron, R. and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.
40. 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.
41. Mills, A. A. (2010). Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat. Rev. Cancer 10, 669-682.
42. Mito, Y., Henikoff, J. G. and Henikoff, S. (2007). Histone replacement marks the boundaries of cis-regulatory domains. Science 315, 1408-1411.
43. Mohrmann, L. and Verrijzer, C. P. (2005). Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681, 59-73.
44. 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.
45. Ni, Z., Saunders, A., Fuda, N. J., Yao, J., Suarez, J. R., Webb, W. W. and Lis, J. T. (2008). P-TEFb is critical for the maturation of RNA polymerase II into productive elongation in vivo. Mol. Cell. Biol. 28, 1161-1170.
46. 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.
47. Papp, B. and Müller, J. (2006). Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 20, 2041-2054.
48. Petruk, S., Sedkov, Y., Smith, S., Tillib, S., Kraevski, V., Nakamura, T., Canaani, E., Croce, C. M. and Mazo, A. (2001). Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294, 1331-1334.
49. Rank, G., Prestel, M. and Paro, R. (2002). Transcription through intergenic chromosomal memory elements of the Drosophila bithorax complex correlates with an epigenetic switch. Mol. Cell. Biol. 22, 8026-8034.
50. Reisman, D., Glaros, S. and Thompson, E. A. (2009). The SWI/SNF complex and cancer. Oncogene 28, 1653-1668.
51. Richly, H., Aloia, L. and Di Croce, L. (2011). Roles of the Polycomb group proteins in stem cells and cancer. Cell Death Dis. 2, e204.
52. Schmitges, F. W., Prusty, A. B., Faty, M., Stützer, A., Lingaraju, G. M., Aiwazian, J., Sack, R., Hess, D., Li, L., Zhou, S. et al. (2011). Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42, 330-341.
53. Schmitt, S., Prestel, M. and Paro, R. (2005). Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev. 19, 697-708.
54. Schuettengruber, B. and Cavalli, G. (2013). Polycomb domain formation depends on short and long distance regulatory cues. PLoS ONE 8, e56531.
55. Schuettengruber, B., Martinez, A. M., Iovino, N. and Cavalli, G. (2011). Trithorax group proteins: switching genes on and keeping them active. Nat. Rev. Mol. Cell Biol. 12, 799-814.
56. Schwartz, Y. B., Kahn, T. G., Stenberg, P., Ohno, K., Bourgon, R. and Pirrotta, V. (2010). Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 6, e1000805.
57. Smith, E. R., Lee, M. G., Winter, B., Droz, N. M., Eissenberg, J. C., Shiekhattar, R. and Shilatifard, A. (2008). Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol. Cell. Biol. 28, 1041-1046.
58. Srinivasan, S., Armstrong, J. A., Deuring, R., Dahlsveen, I. K., McNeill, H. and Tamkun, J. W. (2005). The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132, 1623-1635.
59. Srinivasan, S., Dorighi, K. M. and Tamkun, J. W. (2008). Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet. 4, e1000217.
60. Stabell, M., Larsson, J., Aalen, R. B. and Lambertsson, A. (2007). Drosophila dSet2 functions in H3-K36 methylation and is required for development. Biochem. Biophys. Res. Commun. 359, 784-789.
61. Steffen, P. A., Fonseca, J. P., Gänger, C., Dworschak, E., Kockmann, T., Beisel, C. and Ringrose, L. (2013). Quantitative in vivo analysis of chromatin binding of Polycomb and Trithorax group proteins reveals retention of ASH1 on mitotic chromatin. Nucleic Acids Res. 41, 5235-5250.
62. Tanaka, Y., Katagiri, Z., Kawahashi, K., Kioussis, D. and Kitajima, S. (2007). Trithorax-group protein ASH1 methylates histone H3 lysine 36. Gene 397, 161-168.
63. 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.
64. Tie, F., Banerjee, R., Stratton, C. A., Prasad-Sinha, J., Stepanik, V., Zlobin, A., Diaz, M. O., Scacheri, P. C. and Harte, P. J. (2009). CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136, 3131-3141.
65. Tripoulas, N. A., Hersperger, E., La Jeunesse, D. and Shearn, A. (1994). Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs1 (ash1). Genetics 137, 1027-1038.
66. Tripoulas, N., LaJeunesse, D., Gildea, J. and Shearn, A. (1996). The Drosophila ash1 gene product, which is localized at specific sites on polytene chromosomes, contains a SET domain and a PHD finger. Genetics 143, 913-928.
67. 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.
68. Wada, T., Takagi, T., Yamaguchi, Y., Watanabe, D. and Handa, H. (1998). Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J. 17, 7395-7403.
69. Yoh, S. M., Cho, H., Pickle, L., Evans, R. M. and Jones, K. A. (2007). The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev. 21, 160-174.
70. Yuan, W., Xu, M., Huang, C., Liu, N., Chen, S. and Zhu, B. (2011). H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J. Biol. Chem. 286, 7983-7989.
71. Zhang, D. W., Rodríguez-Molina, J. B., Tietjen, J. R., Nemec, C. M. and Ansari, A. Z. (2012). Emerging views on the CTD code. Genet. Res. Int. 2012, 347214.