The MLL3/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers

Molecular and Cellular Biology

Volumn 33, Issue 23, 2013, Pages 4745-4754

  Hu, Deqing ^a   Gao, Xin ^a   Morgan, Marc A ^a   Herz, Hans Martin ^a   Smith, Edwin R ^a   Shilatifard, Ali ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HISTONE H3; HISTONE H3 LYSINE 4; HISTONE H3K4 MONOMETHYLASE; RNA POLYMERASE II; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HISTONE; MLL3 PROTEIN, HUMAN; MLL4 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL STRAIN HCT116; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYONIC STEM CELL; ENHANCER REGION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; LENTIVIRINAE; METHYLATION; MORPHOGENESIS; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ANIMAL; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; HCT116 CELL LINE; METABOLISM; NEOPLASM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ANIMALS; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; GENE EXPRESSION; HCT116 CELLS; HISTONES; HUMANS; METHYLATION; MICE; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 84891711796     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01181-13     Document Type: Article

References (40)

1. Bulger M, Groudine M. 2011. Functional and mechanistic diversity of distal transcription enhancers. Cell 144:327-339.
2. Ong CT, Corces VG. 2011. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet. 12:283-293.
3. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39:311-318.
4. 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.
5. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U. S. A. 107:21931-21936.
6. Pekowska A, Benoukraf T, Zacarias-Cabeza J, Belhocine M, Koch F, Holota H, Imbert J, Andrau JC, Ferrier P, Spicuglia S. 2011. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 30:4198-4210.
7. 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.
8. Zentner GE, Tesar PJ, Scacheri PC. 2011. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res. 21:1273-1283.
9. 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.
10. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326.
11. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77-88.
12. 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. U. S. A. 98:12902-12907.
13. 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.
14. 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.
15. Shilatifard A. 2012. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81:65-95.
16. 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.
17. 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.
18. Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A. 2008. Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol. Cell. Biol. 28:7337-7344.
19. Wang P, Lin C, Smith ER, Guo H, Sanderson BW, Wu M, Gogol M, Alexander T, Seidel C, Wiedemann LM, Ge K, Krumlauf R, Shilatifard A. 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.
20. Hu D, Garruss AS, Gao X, Morgan MA, Cook M, Smith ER, Shilatifard A. 2013. The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 20:1093-1097.
21. Herz HM, Mohan M, Garruss AS, Liang K, Takahashi YH, Mickey K, Voets O, Verrijzer CP, Shilatifard A. 2012. Enhancer-associated H3K4 monomethylation by Trithorax-related, the Drosophila homolog of mammalian Mll3/Mll4. Genes Dev. 26:2604-2620.
22. Guo C, Chang CC, Wortham M, Chen LH, Kernagis DN, Qin X, Cho YW, Chi JT, Grant GA, McLendon RE, Yan H, Ge K, Papadopoulos N, Bigner DD, He Y. 2012. Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 109:17603-17608.
23. Watanabe Y, Castoro RJ, Kim HS, North B, Oikawa R, Hiraishi T, Ahmed SS, Chung W, Cho MY, Toyota M, Itoh F, Estecio MR, Shen L, Jelinek J, Issa JP. 2011. Frequent alteration of MLL3 frameshift mutations in microsatellite deficient colorectal cancer. PLoS One 6:e23320. doi:10.1371/journal.pone.0023320.
24. Cleary SP, Jeck WR, Zhao X, Chen K, Selitsky SR, Savich GL, Tan TX, Wu MC, Getz G, Lawrence MS, Parker JS, Li J, Powers S, Kim H, Fischer S, Giundi M, Ghanekar A, Chiang DY. 31 May 2013. Identification of driver genes in hepatocellular carcinoma by exome sequencing. Hepatology [Epub ahead of print.] doi:10.1002/hep.26540.
25. Morin RD, Mendez-Lago M, Mungall AJ, Goya R, Mungall KL, Corbett RD, Johnson NA, Severson TM, Chiu R, Field M, Jackman S, Krzywinski M, Scott DW, Trinh DL, Tamura-Wells J, Li S, Firme MR, Rogic S, Griffith M, Chan S, Yakovenko O, Meyer IM, Zhao EY, Smailus D, Moksa M, Chittaranjan S, Rimsza L, Brooks-Wilson A, Spinelli JJ, Ben-Neriah S, Meissner B, Woolcock B, Boyle M, McDonald H, Tam A, Zhao Y, Delaney A, Zeng T, Tse K, Butterfield Y, Birol I, Holt R, Schein J, Horsman DE, Moore R, Jones SJ, Connors JM, Hirst M, Gascoyne RD, Marra MA. 2011. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476:298-303.
26. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, Gallia GL, Jallo GI, Binder ZA, Nikolsky Y, Hartigan J, Smith DR, Gerhard DS, Fults DW, VandenBerg S, Berger MS, Marie SK, Shinjo SM, Clara C, Phillips PC, Minturn JE, Biegel JA, Judkins AR, Resnick AC, Storm PB, Curran T, He Y, Rasheed BA, Friedman HS, Keir ST, McLendon R, Northcott PA, Taylor MD, Burger PC, Riggins GJ, Karchin R, Parmigiani G, Bigner DD, Yan H, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE. 2011. The genetic landscape of the childhood cancer medulloblastoma. Science 331:435-439.
27. Lee TI, Johnstone SE, Young RA. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1:729-748.
28. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
29. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952-1958.
30. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137. doi:10.1186/gb-2008-9-9-r137.
31. Huang DW, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
32. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
33. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560.
34. Frietze S, Wang R, Yao L, Tak YG, Ye Z, Gaddis M, Witt H, Farnham PJ, Jin VX. 2012. Cell type-specific binding patterns reveal that TCF7L2 can be tethered to the genome by association with GATA3. Genome Biol. 13:R52. doi:10.1186/gb-2012-13-9-r52.
35. Visel A, Rubin EM, Pennacchio LA. 2009. Genomic views of distantacting enhancers. Nature 461:199-205.
36. Calo E, Wysocka J. 2013. Modification of enhancer chromatin: what, how, and why? Mol. Cell 49:825-837.
37. 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.
38. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, Edkins S, Hardy C, O'Meara S, Teague J, Butler A, Hinton J, Latimer C, Andrews J, Barthorpe S, Beare D, Buck G, Campbell PJ, Cole J, Forbes S, Jia M, Jones D, Kok CY, Leroy C, Lin ML, McBride DJ, Maddison M, Maquire S, McLay K, Menzies A, Mironenko T, Mulderrig L, Mudie L, Pleasance E, Shepherd R, Smith R, Stebbings L, Stephens P, Tang G, Tarpey PS, Turner R, Turrell K, Varian J, West S, Widaa S, Wray P, Collins VP, Ichimura K, Law S, Wong J, Yuen ST, Leung SY, Tonon G, DePinho RA, Tai YT, Anderson KC, Kahnoski RJ, Massie A, Khoo SK, Teh BT, Stratton MR, Futreal PA. 2009. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat. Genet. 41:521-523.
39. Akhtar-Zaidi B, Cowper-Sal-lari R, Corradin O, Saiakhova A, Bartels CF, Balasubramanian D, Myeroff L, Lutterbaugh J, Jarrar A, Kalady MF, Willis J, Moore JH, Tesar PJ, Laframboise T, Markowitz S, Lupien M, Scacheri PC. 2012. Epigenomic enhancer profiling defines a signature of colon cancer. Science 336:736-739.
40. van Nuland R, Smits AH, Pallaki P, Jansen PW, Vermeulen M, Timmers HT. 2013. Quantitative dissection and stoichiometry determination of the human SET1/MLL histone methyltransferase complexes. Mol. Cell. Biol. 33:2067-2077.