Human histone H3K79 methyltransferase DOT1L methyltransferase binds actively transcribing RNA polymerase II to regulate gene expression

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39698-39709

  Kim, Seung Kyoon ^a   Jung, Inkyung ^a   Lee, Hosuk ^a   Kang, Keunsoo ^a   Kim, Mirang ^b   Jeong, Kwiwan ^a   Kwon, Chang Seob ^a   Han, Yong Mahn ^a   Kim, Yong Sung ^b   Kim, Dongsup ^a   Lee, Daeyoup ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; FUNCTIONAL INTERACTION; GENOME-WIDE PROFILING; HISTONE H3; METHYLTRANSFERASES; PLURIPOTENCY; RNA POLYMERASE II; TARGET GENES; TRANSCRIPTIONAL ACTIVATIONS;

ALKYLATION; AMINO ACIDS; GENES; METHYLATION; PHOSPHORYLATION; PROTEINS; RNA;

TRANSCRIPTION;

HISTONE H3; HISTONE METHYLTRANSFERASE; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN DOT1L; RNA POLYMERASE II; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYONAL CARCINOMA; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENOME ANALYSIS; HISTONE METHYLATION; HUMAN; HUMAN CELL; NANOG GENE; NUCLEOTIDE SEQUENCE; OCT4 GENE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE;

GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HEK293 CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; METHYLATION; METHYLTRANSFERASES; PROTEIN BINDING; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EID: 84869221559     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384057     Document Type: Article

References (59)

1. Kornberg, R. D. (1974) Chromatin structure. A repeating unit of histones and DNA. Science 184, 868-871
2. Kornberg, R. D., and Lorch, Y. (1999) Twenty-five years of the nucleosome, review fundamental particle of the eukaryote chromosome. Cell 98, 285-294 (Pubitemid 29380564)
3. Shilatifard, A. (2006) Chromatin modifications by methylation and ubiquitination. Implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243-269
4. Lachner, M., O'Sullivan, R. J., and Jenuwein, T. (2003) An epigenetic road map for histone lysine methylation. J. Cell Sci. 116, 2117-2124 (Pubitemid 36722358)
5. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 (Pubitemid 27406632)
6. Lacoste, N., Utley, R. T., Hunter, J. M., Poirier, G. G., and Côte, J. (2002) Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J. Biol. Chem. 277, 30421-30424 (Pubitemid 34970731)
7. Ng, H. H., Feng, Q., Wang, H., Erdjument-Bromage, H., Tempst, P., Zhang, Y., and Struhl, K. (2002) Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 16, 1518-1527 (Pubitemid 34686333)
8. van Leeuwen, F., Gafken, P. R., and Gottschling, D. E. (2002) Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745-756 (Pubitemid 34727348)
9. Wysocki, R., Javaheri, A., Allard, S., Sha, F., Côté, J., and Kron, S. J. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell Biol. 25, 8430-8443 (Pubitemid 41369165)
10. Giannattasio, M., Lazzaro, F., Plevani, P., and Muzi-Falconi, M. (2005) The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 280, 9879-9886 (Pubitemid 40395835)
11. Ng, H. H., Ciccone, D. N., Morshead, K. B., Oettinger, M. A., and Struhl, K. (2003) Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells. A potential mechanism for position-effect variegation. Proc. Natl. Acad. Sci. U.S.A. 100, 1820-1825 (Pubitemid 36254532)
12. San-Segundo, P. A., and Roeder, G. S. (2000) Role for the silencing protein Dot1 in meiotic checkpoint control. Mol. Biol. Cell 11, 3601-3615
13. Schulze, J. M., Jackson, J., Nakanishi, S., Gardner, J. M., Hentrich, T., Haug, J., Johnston, M., Jaspersen, S. L., Kobor, M. S., and Shilatifard, A. (2009) Linking cell cycle to histone modifications. SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol. Cell 35, 626-641
14. Schübeler, D., MacAlpine, D. M., Scalzo, D., Wirbelauer, C., Kooperberg, C., van Leeuwen, F., Gottschling, D. E., O'Neill, L. P., Turner, B. M., Delrow, J., Bell, S. P., and Groudine, M. (2004) The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18, 1263-1271 (Pubitemid 38720594)
15. Zhang, W., Hayashizaki, Y., and Kone, B. C. (2004) Structure and regulation of the mDot1 gene, a mouse histone H3 methyltransferase. Biochem. J. 377, 641-651 (Pubitemid 38221835)
16. Feng, Q., Wang, H., Ng, H. H., Erdjument-Bromage, H., Tempst, P., Struhl, K., and Zhang, Y. (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12, 1052-1058 (Pubitemid 34703339)
17. Shanower, G. A., Muller, M., Blanton, J. L., Honti, V., Gyurkovics, H., and Schedl, P. (2005) Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 169, 173-184 (Pubitemid 40239162)
18. Mueller, D., Bach, C., Zeisig, D., Garcia-Cuellar, M. P., Monroe, S., Sreekumar, A., Zhou, R., Nesvizhskii, A., Chinnaiyan, A., and Hess, J. L. (2007) A role for the MLL fusion partner ENL in transcriptional elongation and chromatin modification. Blood 110, 4445-4454 (Pubitemid 351377811)
19. Mohan, M., Herz, H. M., Takahashi, Y. H., Lin, C., Lai, K. C., Zhang, Y., Washburn, M. P., Florens, L., and Shilatifard, A. (2010) Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev. 24, 574-589
20. Bitoun, E., Oliver, P. L., and Davies, K. E. (2007) The mixed-lineage leukemia fusion partner AF4 stimulates RNA polymerase II transcriptional elongation and mediates coordinated chromatin remodeling. Hum. Mol. Genet. 16, 92-106 (Pubitemid 46152547)
21. Jones, B., Su, H., Bhat, A., Lei, H., Bajko, J., Hevi, S., Baltus, G. A., Kadam, S., Zhai, H., and Valdez, R. (2008) The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet. 4, e1000190
22. Barry, E. R., Krueger, W., Jakuba, C. M., Veilleux, E., Ambrosi, D. J., Nelson, C. E., and Rasmussen, T. P. (2009) ES cell cycle progression and differentiation require the action of the histone methyltransferase Dot1L. Stem Cells 27, 1538-1547
23. Okada, Y., Feng, Q., Lin, Y., Jiang, Q., Li, Y., Coffield, V. M., Su, L., Xu, G., and Zhang, Y. (2005) hDOT1L links histone methylation to leukemogenesis. Cell 121, 167-178 (Pubitemid 40546386)
24. Dover, J., Schneider, J., Tawiah-Boateng, M. A., Wood, A., Dean, K., Johnston, M., and Shilatifard, A. (2002) Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J. Biol. Chem. 277, 28368-28371 (Pubitemid 41079257)
25. Sun, Z. W., and Allis, C. D. (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108
26. Lee, J. S., Shukla, A., Schneider, J., Swanson, S. K., Washburn, M. P., Florens, L., Bhaumik, S. R., and Shilatifard, A. (2007) Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131, 1084-1096 (Pubitemid 350235018)
27. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., and Reinberg, D. (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125, 703-717 (Pubitemid 43732350)
28. Weake, V. M., and Workman, J. L. (2008) Histone ubiquitination. Triggering gene activity. Mol. Cell 29, 653-663 (Pubitemid 351400924)
29. Kim, J., Guermah, M., McGinty, R. K., Lee, J. S., Tang, Z., Milne, T. A., Shilatifard, A., Muir, T. W., and Roeder, R. G. (2009) RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137, 459-471
30. McGinty, R. K., Kim, J., Chatterjee, C., Roeder, R. G., and Muir, T. W. (2008) Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453, 812-816 (Pubitemid 351793779)
31. Oh, S., Jeong, K., Kim, H., Kwon, C. S., and Lee, D. (2010) A lysine rich region in Dot1p is crucial for direct interaction with H2B ubiquitylation and high level methylation of H3K79. Biochem. Biophys. Res. Commun. 399, 512-517
32. Jung, I., Kim, S. K., Kim, M., Han, Y. M., Kim, Y. S., Kim, D., and Lee, D. (2012) H2B monoubiquitylation is a 5′-enriched active transcription mark and correlates with exon-intron structure in human cells. Genome Res. 22, 1026-1035
33. Steger, D. J., Lefterova, M. I., Ying, L., Stonestrom, A. J., Schupp, M., Zhuo, D., Vakoc, A. L., Kim, J. E., Chen, J., and Lazar, M. A. (2008) DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell Biol. 28, 2825-2839 (Pubitemid 351542379)
34. Kouskouti, A., and Talianidis, I. (2005) Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBOJ. 24, 347-357 (Pubitemid 40216139)
35. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (Pubitemid 46802390)
36. Damjanov, I. (1993) Pathogenesis of testicular germ cell tumours. Eur. Urol. 23, 2-5
37. Teshima, T., Chatani, M., Hata, K., and Inoue, T. (1988) High-dose rate intracavitary therapy for carcinoma of the uterine cervix. II. Risk factors for rectal complication. Int. J. Radiat. Oncol. Biol. Phys. 14, 281-286 (Pubitemid 18042189)
38. Damjanov, I., Horvat, B., and Gibas, Z. (1993) Retinoic acid-induced differentiation of the developmentally pluripotent human germ cell tumor-derived cell line, NCCIT. Lab. Invest. 68, 220-232 (Pubitemid 23084295)
39. Spencer, V. A., Sun, J. M., Li, L., and Davie, J. R. (2003) Chromatin immunoprecipitation. A tool for studying histone acetylation and transcription factor binding. Methods 31, 67-75 (Pubitemid 36945172)
40. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25
41. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009) TopHat. Discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111
42. Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., and Pachter, L. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515
43. Suganuma, T., Kawabata, M., Ohshima, T., and Ikeda, M. A. (2002) Growth suppression of human carcinoma cells by reintroduction of the p300 coactivator. Proc. Natl. Acad. Sci. U.S.A. 99, 13073-13078
44. Li, B., Howe, L., Anderson, S., Yates, J. R., 3rd, and Workman, J. L. (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278, 8897-8903 (Pubitemid 36800365)
45. de la Mata, M., and Kornblihtt, A. R. (2006)RNApolymerase II C-terminal domain mediates regulation of alternative splicing by SRp20. Nat. Struct. Mol. Biol. 13, 973-980
46. Li, J., Moazed, D., and Gygi, S. P. (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J. Biol. Chem. 277, 49383-49388 (Pubitemid 36014370)
47. Ho, C. K., and Shuman, S. (1999) Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3, 405-411 (Pubitemid 29290681)
48. Kizer, K. O., Phatnani, H. P., Shibata, Y., Hall, H., Greenleaf, A. L., and Strahl, B. D. (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell Biol. 25, 3305-3316 (Pubitemid 40464330)
49. Min, J., Feng, Q., Li, Z., Zhang, Y., and Xu, R. M. (2003) Structure of the catalytic domain of human DOT1L, a non-SET domain nucleosomal histone methyltransferase. Cell 112, 711-723 (Pubitemid 36331782)
50. Hiromi, N. (2009) Evolutionary conservation levels of subunits of histone-modifying protein complexes in fungi. Comp. Funct. Genomics 2009, 8
51. Zhang, K., Sridhar, V. V., Zhu, J., Kapoor, A., and Zhu, J. K. (2007) Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One 2, e1210
52. Shahbazian, M. D., Zhang, K., and Grunstein, M. (2005) Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell 19, 271-277 (Pubitemid 41019673)
53. 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 (Pubitemid 39362887)
54. 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 (Pubitemid 34008196)
55. Zhou, K., Kuo, W. H., Fillingham, J., and Greenblatt, J. F. (2009) Control of transcriptional elongation and cotranscriptional histone modification by the yeast BUR kinase substrate Spt5. Proc. Natl. Acad. Sci. U.S.A. 106, 6956-6961
56. Qiu, H., Hu, C., and Hinnebusch, A. G. (2009) Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 33, 752-762
57. 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
58. Phatnani, H. P., Jones, J. C., and Greenleaf, A. L. (2004) Expanding the functional repertoire of CTD kinase I and RNA polymerase II. Novel phosphoCTD-associating proteins in the yeast proteome. Biochemistry 43, 15702-15719 (Pubitemid 39665070)
59. Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., and Liu, X. S. (2008) Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137