Enhancer-associated H3K4 monomethylation by trithorax-related, the drosophila homolog of mammalian MLL3/MLL4

Genes and Development

Volumn 26, Issue 23, 2012, Pages 2604-2620

  Herz, Hans Martin ^a   Mohan, Man ^a   Garruss, Alexander S ^a   Liang, Kaiwei ^a   Takahashi, Yoh hei ^a   Mickey, Kristen ^a   Voets, Olaf ^a   Verrijzer, C Peter ^b   Shilatifard, Ali ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

COMPASS like complexes; Enhancers; H3K4 monomethylation; Trithorax like

Indexed keywords

DROSOPHILA PROTEIN; HISTONE DEMETHYLASE; HISTONE H3; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; PROTEIN TRITHORAX RELATED; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DROSOPHILA; ENHANCER REGION; GENETIC ANALYSIS; HISTONE METHYLATION; HISTONE MODIFICATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN SUBUNIT; RNA INTERFERENCE;

ANIMALS; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; GENOME-WIDE ASSOCIATION STUDY; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; METHYLATION;

MAMMALIA;

EID: 84870490787     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.201327.112     Document Type: Article

References (77)

1. Akhtar-Zaidi B, Cowper-Sal-lari R, Corradin O, Saiakhova A, Bartels CF, Balasubramanian D, Myeroff L, Lutterbaugh J, Jarrar A, Kalady MF, et al. 2012. Epigenomic enhancer profiling defines a signature of colon cancer. Science 336: 736-739.
2. Ardehali MB, Mei A, Zobeck KL, Caron M, Lis JT, Kusch T. 2011. Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. EMBO J 30: 2817-2828.
3. Ashktorab H, Schaffer AA, Daremipouran M, Smoot DT, Lee E, Brim H. 2010. Distinct genetic alterations in colorectal cancer. PLoS ONE 5: e8879. doi: 10.1371/journal.pone.0008879.
4. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
5. Beisel C, Paro R. 2011. Silencing chromatin: Comparing modes and mechanisms. Nat Rev Genet 12: 123-135.
6. Bonn S, Zinzen RP, Girardot C, Gustafson EH, Perez-Gonzalez A, Delhomme N, Ghavi-Helm Y, Wilczynski B, Riddell A, Furlong EE. 2012. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat Genet 44: 148-156.
7. Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15: 3286-3295.
8. Bulger M, Groudine M. 2011. Functional and mechanistic diversity of distal transcription enhancers. Cell 144: 327-339.
9. Chauhan C, Zraly CB, Parilla M, Diaz MO, Dingwall AK. 2012. Histone recognition and nuclear receptor co-activator functions of Drosophila Cara Mitad, a homolog of the N-terminal portion of mammalian MLL2 and MLL3. Development 139: 1997-2008.
10. Chen S, Ma J, Wu F, Xiong LJ, Ma H, Xu W, Lv R, Li X, Villen J, Gygi SP, et al. 2012. The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 26: 1364-1375.
11. Cheung AC, Cramer P. 2012. A movie of RNA polymerase II transcription. Cell 149: 1431-1437.
12. Cho YW, Hong T, Hong S, Guo H, Yu H, Kim D, Guszczynski T, Dressler GR, Copeland TD, Kalkum M, et al. 2007. PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282: 20395-20406.
13. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
14. Dorsett D, Eissenberg JC, Misulovin Z, Martens A, Redding B, McKim K. 2005. Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. Development 132: 4743-4753.
15. Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, Allis CD, Roeder RG. 2006. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 13: 713-719.
16. Eissenberg JC, Shilatifard A. 2010. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339: 240-249.
17. Goo YH, Sohn YC, Kim DH, Kim SW, Kang MJ, Jung DJ, Kwak E, Barlev NA, Berger SL, Chow VT, et al. 2003. Activating signal cointegrator 2 belongs to a novel steady-state complex that contains a subset of trithorax group proteins. Mol Cell Biol 23: 140-149.
18. Hallson G, Hollebakken RE, Li T, Syrzycka M, Kim I, Cotsworth S, Fitzpatrick KA, Sinclair DA, Honda BM. 2012. DSet1 is the main H3K4 di- and tri-methyltransferase throughout Drosophila development. Genetics 190: 91-100.
19. Hanson RD, Hess JL, Yu BD, Ernst P, van Lohuizen M, Berns A, van der Lugt NM, Shashikant CS, Ruddle FH, Seto M, et al. 1999. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci 96: 14372-14377.
20. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318.
21. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
22. Herz HM, Madden LD, Chen Z, Bolduc C, Buff E, Gupta R, Davuluri R, Shilatifard A, Hariharan IK, Bergmann A. 2010. The H3K27me3 demethylase dUTX is a suppressor of Notchand Rb-dependent tumors in Drosophila. Mol Cell Biol 30: 2485-2497.
23. Herz HM, Mohan M, Garrett AS, Miller C, Casto D, Zhang Y, Seidel C, Haug JS, Florens L, Washburn MP, et al. 2012. Polycomb repressive complex 2-dependent and -independent functions of Jarid2 in transcriptional regulation in Drosophila. Mol Cell Biol 32: 1683-1693.
24. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, et al. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 13: 587-597.
25. Issaeva I, Zonis Y, Rozovskaia T, Orlovsky K, Croce CM, Nakamura T, Mazo A, Eisenbach L, Canaani E. 2007. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol Cell Biol 27: 1889-1903.
26. Jack J, Dorsett D, Delotto Y, Liu S. 1991. Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer. Development 113: 735-747.
27. Jin Q, Yu LR, Wang L, Zhang Z, Kasper LH, Lee JE, Wang C, Brindle PK, Dent SY, Ge K. 2011. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J 30: 249-262.
28. Johnston DM, Sedkov Y, Petruk S, Riley KM, Fujioka M, Jaynes JB, Mazo A. 2011. Ecdysone- and NO-mediated gene regulation by competing EcR/Usp and E75A nuclear receptors during Drosophila development. Mol Cell 44: 51-61.
29. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, et al. 2011. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480-485.
30. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activityregulated enhancers. Nature 465: 182-187.
31. Klymenko T, Muller J. 2004. The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep 5: 373-377.
32. Krogan NJ, Dover J, Khorrami S, Greenblatt JF, Schneider J, Johnston M, Shilatifard A. 2002. COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 277: 10753-10755.
33. Lee JH, Skalnik DG. 2008. Wdr82 is a C-terminal domainbinding protein that recruits the Setd1A histone H3-Lys4 methyltransferase complex to transcription start sites of transcribed human genes. Mol Cell Biol 28: 609-618.
34. Lee S, Lee DK, Dou Y, Lee J, Lee B, Kwak E, Kong YY, Lee SK, Roeder RG, Lee JW. 2006. Coactivator as a target gene specificity determinant for histone H3 lysine 4 methyltransferases. Proc Natl Acad Sci 103: 15392-15397.
35. Lee JH, Tate CM, You JS, Skalnik DG. 2007. Identification and characterization of the human Set1B histone H3-Lys4 methyltransferase complex. J Biol Chem 282: 13419-13428.
36. Lee MG, Villa R, Trojer P, Norman J, Yan KP, Reinberg D, Di Croce L, Shiekhattar R. 2007. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318: 447-450.
37. Levine M. 2010. Transcriptional enhancers in animal development and evolution. Curr Biol 20: R754-R763. doi: 10.1016/j.cub.2010.06.070.
38. Mar BG, Bullinger L, Basu E, Schlis K, Silverman LB, Dohner K, Armstrong SA. 2012. Sequencing histone-modifying enzymes identifies UTX mutations in acute lymphoblastic leukemia. Leukemia 26: 1881-1883.
39. Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, Greenblatt JF, Shilatifard A. 2001. COMPASS: A complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci 98: 12902-12907.
40. Mo R, Rao SM, Zhu YJ. 2006. Identification of the MLL2 complex as a coactivator for estrogen receptor a. J Biol Chem 281: 15714-15720.
41. Mohan M, Herz HM, Smith ER, Zhang Y, Jackson J, Washburn MP, Florens L, Eissenberg JC, Shilatifard A. 2011. The COMPASS family of H3K4 methylases in Drosophila. Mol Cell Biol 31: 4310-4318.
42. Mohan M, Herz HM, Shilatifard A. 2012. SnapShot: Histone lysine methylase complexes. Cell 149: 498-498e1. doi: 10.1016/j.cell.2012.03.025.
43. Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L, Splinter E, de Laat W, Spitz F, Duboule D. 2011. A regulatory archipelago controls Hox genes transcription in digits. Cell 147: 1132-1145.
44. Morin RD, Mendez-Lago M, Mungall AJ, Goya R, Mungall KL, Corbett RD, Johnson NA, Severson TM, Chiu R, Field M, et al. 2011. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476: 298-303.
45. Ong CT, Corces VG. 2011. Enhancer function: New insights into the regulation of tissue-specific gene expression. Nat Rev Genet 12: 283-293.
46. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al. 2011. The genetic landscape of the childhood cancer medulloblastoma. Science 331: 435-439.
47. Pasini D, Malatesta M, Jung HR, Walfridsson J, Willer A, Olsson L, Skotte J, Wutz A, Porse B, Jensen ON, et al. 2010. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res 38: 4958-4969.
48. Patel SR, Kim D, Levitan I, Dressler GR. 2007. The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev Cell 13: 580-592.
49. Poux S, Horard B, Sigrist CJ, Pirrotta V. 2002. The Drosophila trithorax protein is a coactivator required to prevent reestablishment of polycomb silencing. Development 129: 2483-2493.
50. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
51. Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M, Aasland R, Stewart AF. 2001. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 20: 7137-7148.
52. Rollins RA, Morcillo P, Dorsett D. 1999. Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152: 577-593.
53. Rollins RA, Korom M, Aulner N, Martens A, Dorsett D. 2004. Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol 24: 3100-3111.
54. Schneider J, Wood A, Lee JS, Schuster R, Dueker J, Maguire C, Swanson SK, Florens L, Washburn MP, Shilatifard A. 2005. Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19: 849-856.
55. Schuettengruber B, Martinez AM, Iovino N, Cavalli G. 2011. Trithorax group proteins: Switching genes on and keeping them active. Nat Rev Mol Cell Biol 12: 799-814.
56. Sedkov Y, Benes JJ, Berger JR, Riker KM, Tillib S, Jones RS, Mazo A. 1999. Molecular genetic analysis of the Drosophila trithorax-related gene which encodes a novel SET domain protein. Mech Dev 82: 171-179.
57. Sedkov Y, Cho E, Petruk S, Cherbas L, Smith ST, Jones RS, Cherbas P, Canaani E, Jaynes JB, Mazo A. 2003. Methylation at lysine 4 of histone H3 in ecdysone-dependent development of Drosophila. Nature 426: 78-83.
58. Seenundun S, Rampalli S, Liu QC, Aziz A, Palii C, Hong S, Blais A, Brand M, Ge K, Dilworth FJ. 2010. UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J 29: 1401-1411.
59. Shilatifard A. 2012. The COMPASS family of histone H3K4 methylases: Mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81: 65-95.
60. Simon JA, Kingston RE. 2009. Mechanisms of polycomb gene silencing: Knowns and unknowns. Nat Rev Mol Cell Biol 10: 697-708.
61. Simon JA, Tamkun JW. 2002. Programming off and on states in chromatin: Mechanisms of Polycomb and trithorax group complexes. Curr Opin Genet Dev 12: 210-218.
62. Smith ER, Lee MG, Winter B, Droz NM, Eissenberg JC, Shiekhattar R, 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.
63. Steward MM, Lee JS, O'Donovan A, Wyatt M, Bernstein BE, Shilatifard A. 2006. Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nat Struct Mol Biol 13: 852-854.
64. Takahashi YH, Lee JS, Swanson SK, Saraf A, Florens L, Washburn MP, Trievel RC, Shilatifard A. 2009. Regulation of H3K4 trimethylation via Cps40 (Spp1) of COMPASS is monoubiquitination independent: Implication for a Phe/Tyr switch by the catalytic domain of Set1. Mol Cell Biol 29: 3478-3486.
65. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ. 2009. CBPmediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136: 3131-3141.
66. Tie F, Banerjee R, Conrad PA, Scacheri PC, Harte PJ. 2012. The histone demethylase UTX and chromatin remodeler BRM bind directly to CBP and modulate acetylation of histone H3 lysine 27. Mol Cell Biol 32: 2323-2334.
67. Vandamme J, Lettier G, Sidoli S, Di Schiavi E, Norregaard Jensen O, Salcini AE. 2012. The C. elegans H3K27 demethylase UTX-1 is essential for normal development, independent of its enzymatic activity. PLoS Genet 8: e1002647. doi: 10.1371/journal.pgen.1002647.
68. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, Edkins S, Hardy C, O'Meara S, Teague J, et al. 2009. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet 41: 521-523.
69. Vicent GP, Nacht AS, Font-Mateu J, Castellano G, Gaveglia L, Ballare C, Beato M. 2011. Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation. Genes Dev 25: 845-862.
70. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858.
71. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
72. Wang P, Lin C, Smith ER, Guo H, Sanderson BW, Wu M, Gogol M, Alexander T, Seidel C, Wiedemann LM, 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.
73. Wang C, Lee JE, Cho YW, Xiao Y, Jin Q, Liu C, Ge K. 2012. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc Natl Acad Sci 109: 15324-15329.
74. Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A. 2008. Molecular regulation of H3K4 trimethylation byWdr82, a component of human Set1/COMPASS. Mol Cell Biol 28: 7337-7344.
75. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, Herr W, Cleary ML. 2004. Leukemia protooncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 24: 5639-5649.
76. Zentner GE, Tesar PJ, Scacheri PC. 2011. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 21: 1273-1283.
77. Zhou Q, Li T, Price DH. 2012. RNA polymerase II elongation control. Annu Rev Biochem 81: 119-143.