Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant

Development (Cambridge)

Volumn 141, Issue 3, 2014, Pages 526-537

  Denissov, Sergei ^a   Hofemeister, Helmut ^b   Marks, Hendrik ^a   Kranz, Andrea ^b   Ciotta, Giovanni ^b   Singh, Sukhdeep ^b   Anastassiadis, Konstantinos ^b   Stunnenberg, Hendrik G ^a   Stewart, A Francis ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Bivalent promoters; Epigenetics; Epigenome; Histone methylation; Kmt2; Polycomb group; Trithorax group

Indexed keywords

CXXC1 ENZYME; H3K4 METHYLTRANSFERASE; MESSENGER RNA; METHYLTRANSFERASE; MLL1 ENZYME; MLL2 ENZYME; POLYCOMB GROUP PROTEIN; RETINOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME SUBUNIT; GENE EXPRESSION; HISTONE METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION;

BIVALENT PROMOTERS; EPIGENETICS; EPIGENOME; HISTONE METHYLATION; KMT2; POLYCOMB GROUP; TRITHORAX GROUP;

ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CHROMOSOMES, ARTIFICIAL, BACTERIAL; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HOMEODOMAIN PROTEINS; LYSINE; METHYLATION; MICE; MODELS, BIOLOGICAL; MYELOID-LYMPHOID LEUKEMIA PROTEIN; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSGENES; TRETINOIN;

EID: 84892683106     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.102681     Document Type: Article

References (82)

1. Akkers, R. C., van Heeringen, S. J., Jacobi, U. G., Janssen-Megens, E. M., Françoijs, K.-J., Stunnenberg, H. G. and Veenstra, G. J. C. (2009). A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev. Cell 17, 425-434.
2. Albert, M. and Helin, K. (2010). Histone methyltransferases in cancer. Semin. Cell Dev. Biol. 21, 209-220.
3. Allis, C. D., Berger, S. L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R. et al. (2007). New nomenclature for chromatin-modifying enzymes. Cell 131, 633-636.
4. Andreu-Vieyra, C. V., Chen, R., Agno, J. E., Glaser, S., Anastassiadis, K., Stewart, A. F. and Matzuk, M. M. (2010). MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 8, doi: 10.1371/journal.pbio.1000453.
5. 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.
6. Austenaa, L., Barozzi, I., Chronowska, A., Termanini, A., Ostuni, R., Prosperini, E., Stewart, A. F., Testa, G. and Natoli, G. (2012). The histone methyltransferase Wbp7 controls macrophage function through GPI glycolipid anchor synthesis. Immunity 36, 572-585.
7. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538.
8. Bannister, A. J. and Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell. Res. 21, 381-395.
9. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006a). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
10. Bernstein, E., Duncan, E. M., Masui, O., Gil, J., Heard, E. and Allis, C. D. (2006b). Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26, 2560-2569.
11. Blackledge, N. P. and Klose, R. (2011). CpG island chromatin: a platform for gene regulation. Epigenetics 6, 147-152.
12. Blackledge, N. P., Zhou, J. C., Tolstorukov, M. Y., Farcas, A. M., Park, P. J. and Klose, R. J. (2010). CpG islands recruit a histone H3 lysine 36 demethylase. Mol. Cell 38, 179-190.
13. Brock, H. W. and Fisher, C. L. (2005). Maintenance of gene expression patterns. Dev. Dyn. 232, 633-655.
14. Butler, J. S., Koutelou, E., Schibler, A. C. and Dent, S. Y. R. (2012). Histonemodifying enzymes: regulators of developmental decisions and drivers of human disease. Epigenomics 4, 163-177.
15. 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 Polycombgroup silencing. Science 298, 1039-1043.
16. Champagne, K. S. and Kutateladze, T. G. (2009). Structural insight into histone recognition by the ING PHD fingers. Curr. Drug Targets 10, 432-441.
17. Clouaire, T., Webb, S., Skene, P., Illingworth, R., Kerr, A., Andrews, R., Lee, J. H., Skalnik, D. and Bird, A. (2012). Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev. 26, 1714-1728.
18. Eberl, H. C., Spruijt, C. G., Kelstrup, C. D., Vermeulen, M. and Mann, M. (2013). A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol. Cell 49, 368-378.
19. Ernst, P., Fisher, J. K., Avery, W., Wade, S., Foy, D. and Korsmeyer, S. J. (2004). Definitive hematopoiesis requires the mixed-lineage leukemia gene. Dev. Cell 6, 437-443.
20. Fischle, W., Wang, Y., Jacobs, S. A., Kim, Y., Allis, C. D. and Khorasanizadeh, S. (2003). Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17, 1870-1881.
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. FitzGerald, K. T. and Diaz, M. O. (1999). MLL2: A new mammalian member of the trx/MLL family of genes. Genomics 59, 187-192.
23. Fu, J., Teucher, M., Anastassiadis, K., Skarnes, W. and Stewart, A. F. (2010). A recombineering pipeline to make conditional targeting constructs. Methods Enzymol. 477, 125-144.
24. Glaser, S., Schaft, J., Lubitz, S., Vintersten, K., van der Hoeven, F., Tufteland, K. R., Aasland, R., Anastassiadis, K., Ang, S.-L. and Stewart, A. F. (2006). Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133, 1423-1432.
25. Glaser, S., Lubitz, S., Loveland, K. L., Ohbo, K., Robb, L., Schwenk, F., Seibler, J., Roellig, D., Kranz, A., Anastassiadis, K. et al. (2009). The histone 3 lysine 4 methyltransferase, Mll2, is only required briefly in development and spermatogenesis. Epigenetics Chromatin 2, 5.
26. Goldberg, A. D., Allis, C. D. and Bernstein, E. (2007). Epigenetics: a landscape takes shape. Cell 128, 635-638.
27. Guenther, M. G., Jenner, R. G., Chevalier, B., Nakamura, T., Croce, C. M., Canaani, E. and Young, R. A. (2005). Global and Hox-specific roles for the MLL1 methyltransferase. Proc. Natl. Acad. Sci. USA 102, 8603-8608.
28. Guo, C., Chang, C.-C., Wortham, M., Chen, L. H., Kernagis, D. N., Qin, X., Cho, Y.-W., Chi, J.-T., Grant, G. A., McLendon, R. E. et al. (2012). Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways. Proc. Natl. Acad. Sci. USA 109, 17603-17608.
29. Hansen, K. H., Bracken, A. P., Pasini, D., Dietrich, N., Gehani, S. S., Monrad, A., Rappsilber, J., Lerdrup, M. and Helin, K. (2008). A model for transmission of the H3K27me3 epigenetic mark. Nat. Cell Biol. 10, 1291-1300.
30. Herz, H.-M., Nakanishi, S. and Shilatifard, A. (2009). The curious case of bivalent marks. Dev. Cell 17, 301-303.
31. Hofemeister, H., Ciotta, G., Fu, J., Seibert, P. M., Schulz, A., Maresca, M., Sarov, M., Anastassiadis, K. and Stewart, A. F. (2011). Recombineering, transfection, Western, IP and ChIP methods for protein tagging via gene targeting or BAC transgenesis. Methods 53, 437-452.
32. Hsieh, J. J. D., Ernst, P., Erdjument-Bromage, H., Tempst, P. and Korsmeyer, S. J. (2003a). Proteolytic cleavage of MLL generates a complex of N-and C-terminal fragments that confers protein stability and subnuclear localization. Mol. Cell. Biol. 23, 186-194.
33. Hsieh, J. J.-D., Cheng, E. H.-Y. and Korsmeyer, S. J. (2003b). Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression. Cell 115, 293-303.
34. Huang, Y., Fang, J., Bedford, M. T., Zhang, Y. and Xu, R. M. (2006). Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312, 748-751.
35. Hubner, N. C., Bird, A. W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A. and Mann, M. (2010). Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739-754.
36. Huntsman, D. G., Chin, S. F., Muleris, M., Batley, S. J., Collins, V. P., Wiedemann, L. M., Aparicio, S. and Caldas, C. (1999). MLL2, the second human homolog of the Drosophila trithorax gene, maps to 19q13.1 and is amplified in solid tumor cell lines. Oncogene 18, 7975-7984.
37. Jaenisch, R. and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245-254.
38. Klymenko, T. and Müller, J. (2004). The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep. 5, 373-377.
39. Ku, M., Koche, R. P., Rheinbay, E., Mendenhall, E. M., Endoh, M., Mikkelsen, T. S., Presser, A., Nusbaum, C., Xie, X., Chi, A. S. et al. (2008). Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242.
40. 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.
41. Ladopoulos, V., Hofemeister, H., Hoogenkamp, M., Riggs, A. D., Stewart, A. F. and Bonifer, C. (2013). The histone methyltransferase KMT2B is required for RNA polymerase II association and protection from DNA methylation at the MagohB CpG island promoter. Mol. Cell. Biol. 33, 1383-1393.
42. Lee, J. H., Voo, K. S. and Skalnik, D. G. (2001). Identification and characterization of the DNA binding domain of CpG-binding protein. J. Biol. Chem. 276, 44669-44676.
43. Li, G., Margueron, R., Ku, M., Chambon, P., Bernstein, B. E. and Reinberg, D. (2010). Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24, 368-380.
44. Lubitz, S., Glaser, S., Schaft, J., Stewart, A. F. and Anastassiadis, K. (2007). Increased apoptosis and skewed differentiation in mouse embryonic stem cells lacking the histone methyltransferase Mll2. Mol. Biol. Cell 18, 2356-2366.
45. Magnúsdóttir, E., Gillich, A., Grabole, N. and Surani, M. A. (2012). Combinatorial control of cell fate and reprogramming in the mammalian germline. Curr. Opin. Genet. Dev. 22, 466-474.
46. Margueron, R., Justin, N., Ohno, K., Sharpe, M. L., Son, J., Drury, W. J., 3rd, Voigt, P., Martin, S. R., Taylor, W. R., De Marco, V. et al. (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461, 762-767.
47. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A. F., Smith, A. et al. (2012). The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
48. Mendenhall, E. M., Koche, R. P., Truong, T., Zhou, V. W., Issac, B., Chi, A. S., Ku, M. and Bernstein, B. E. (2010). GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet. 6, e1001244.
49. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.-K., Koche, R. P. et al. (2007). Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
50. 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.
51. Milne, T. A., Kim, J., Wang, G. G., Stadler, S. C., Basrur, V., Whitcomb, S. J., Wang, Z., Ruthenburg, A. J., Elenitoba-Johnson, K. S. J., Roeder, R. G. et al. (2010). Multiple interactions recruit MLL1 and MLL1 fusion proteins to the HOXA9 locus in leukemogenesis. Mol. Cell 38, 853-863.
52. 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.
53. Nowak, D. E., Tian, B. and Brasier, A. R. (2005). Two-step cross-linking method for identification of NF-kappaB gene network by chromatin immunoprecipitation. Biotechniques 39, 715-725.
54. Ooi, S. K. T., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument-Bromage, H., Tempst, P., Lin, S.-P., Allis, C. D. et al. (2007). DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717.
55. Reik, W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432.
56. Ringrose, L. and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38, 413-443.
57. 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.
58. Ruthenburg, A. J., Allis, C. D. and Wysocka, J. (2007). Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25, 15-30.
59. Scacheri, P. C., Davis, S., Odom, D. T., Crawford, G. E., Perkins, S., Halawi, M. J., Agarwal, S. K., Marx, S. J., Spiegel, A. M., Meltzer, P. S. et al. (2006). Genomewide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2, e51.
60. 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.
61. Seibler, J., Zevnik, B., Küter-Luks, B., Andreas, S., Kern, H., Hennek, T., Rode, A., Heimann, C., Faust, N., Kauselmann, G. et al. (2003). Rapid generation of inducible mouse mutants. Nucleic Acids Res. 31, e12.
62. Shi, X., Kachirskaia, I., Walter, K. L., Kuo, J.-H. A., Lake, A., Davrazou, F., Chan, S. M., Martin, D. G. E., Fingerman, I. M., Briggs, S. D. et al. (2007). Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J. Biol. Chem. 282, 2450-2455.
63. 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.
64. Sims, R. J., 3rd, Millhouse, S., Chen, C.-F., Lewis, B. A., Erdjument-Bromage, H., Tempst, P., Manley, J. L. and Reinberg, D. (2007). Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 28, 665-676.
65. Suganuma, T. and Workman, J. L. (2011). Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 80, 473-499.
66. Testa, G., Zhang, Y., Vintersten, K., Benes, V., Pijnappel, W. W. M. P., Chambers, I., Smith, A. J. H., Smith, A. G. and Stewart, A. F. (2003). Engineering the mouse genome with bacterial artificial chromosomes to create multipurpose alleles. Nat. Biotechnol. 21, 443-447.
67. Thomson, J. P., Skene, P. J., Selfridge, J., Clouaire, T., Guy, J., Webb, S., Kerr, A. R. W., Deaton, A., Andrews, R., James, K. D. et al. (2010). CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464, 1082-1086.
68. van den Berg, D. L. C., Zhang, W., Yates, A., Engelen, E., Takacs, K., Bezstarosti, K., Demmers, J., Chambers, I. and Poot, R. A. (2008). Estrogen-related receptor beta interacts with Oct4 to positively regulate Nanog gene expression. Mol. Cell. Biol. 28, 5986-5995.
69. Vastenhouw, N. L. and Schier, A. F. (2012). Bivalent histone modifications in early embryogenesis. Curr. Opin. Cell Biol. 24, 374-386.
70. Vastenhouw, N. L., Zhang, Y., Woods, I. G., Imam, F., Regev, A., Liu, X. S., Rinn, J. and Schier, A. F. (2010). Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464, 922-926.
71. Vermeulen, M., Mulder, K. W., Denissov, S., Pijnappel, W. W. M. P., van Schaik, F. M. A., Varier, R. A., Baltissen, M. P. A., Stunnenberg, H. G., Mann, M. and Timmers, H. T. M. (2007). Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58-69.
72. Vermeulen, M., Eberl, H. C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K. K., Olsen, J. V., Hyman, A. A., Stunnenberg, H. G. et al. (2010). Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142, 967-980.
73. Voigt, P., LeRoy, G., Drury, W. J., 3rd, Zee, B. M., Son, J., Beck, D. B., Young, N. L., Garcia, B. A. and Reinberg, D. (2012). Asymmetrically modified nucleosomes. Cell 151, 181-193.
74. Voigt, P., Tee, W. W. and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev. 27, 1318-1338.
75. Wan, M., Liang, J., Xiong, Y., Shi, F., Zhang, Y., Lu, W., He, Q., Yang, D., Chen, R., Liu, D. et al. (2013). The trithorax group protein Ash2l is essential for pluripotency and maintaining open chromatin in embryonic stem cells. J. Biol. Chem. 288, 5039-5048.
76. Wang, P., Lin, C., Smith, E. R., Guo, H., Sanderson, B. W., Wu, M., Gogol, M., Alexander, T., Seidel, C., Wiedemann, L. M. et al. (2009). Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol. 29, 6074-6085.
77. Wray, J., Kalkan, T. and Smith, A. G. (2010). The ground state of pluripotency. Biochem. Soc. Trans. 38, 1027-1032.
78. Wysocka, J., Swigut, T., Xiao, H., Milne, T. A., Kwon, S. Y., Landry, J., Kauer, M., Tackett, A. J., Chait, B. T., Badenhorst, P. et al. (2006). A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442, 86-90.
79. Xu, H., Handoko, L., Wei, X., Ye, C., Sheng, J., Wei, C. L., Lin, F. and Sung, W. K. (2010). A signal-noise model for significance analysis of ChIP-seq with negative control. Bioinformatics 26, 1199-1204.
80. Yagi, H., Deguchi, K., Aono, A., Tani, Y., Kishimoto, T. and Komori, T. (1998). Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Blood 92, 108-117.
81. 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.
82. Zegerman, P., Canas, B., Pappin, D. and Kouzarides, T. (2002). Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J. Biol. Chem. 277, 11621-11624.