The RNA Pol II elongation factor Ell3 marks enhancers in ES cells and primes future gene activation

Cell

Volumn 152, Issue 1-2, 2013, Pages 144-156

  Lin, Chengqi ^a   Garruss, Alexander S ^a   Luo, Zhuojuan ^a   Guo, Fengli ^a   Shilatifard, Ali ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; RNA POLYMERASE II ELONGATION FACTOR ELL3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE ACTIVATION; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 84872605250     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.12.015     Document Type: Article

References (67)

1. B.E. Bernstein, T.S. Mikkelsen, X. Xie, M. Kamal, D.J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, and K. Plath A bivalent chromatin structure marks key developmental genes in embryonic stem cells Cell 125 2006 315 326
2. M. Bulger, and M. Groudine Functional and mechanistic diversity of distal transcription enhancers Cell 144 2011 327 339
3. L.J. Core, J.J. Waterfall, and J.T. Lis Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters Science 322 2008 1845 1848
4. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, and P.A. Sharp Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
5. K. Cui, C. Zang, T.Y. Roh, D.E. Schones, R.W. Childs, W. Peng, and K. Zhao Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation Cell Stem Cell 4 2009 80 93
6. M.A. Dawson, R.K. Prinjha, A. Dittmann, G. Giotopoulos, M. Bantscheff, W.I. Chan, S.C. Robson, C.W. Chung, C. Hopf, and M.M. Savitski Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia Nature 478 2011 529 533
7. W. Deng, and G.A. Blobel Do chromatin loops provide epigenetic gene expression states? Curr. Opin. Genet. Dev. 20 2010 548 554
8. J.R. Dixon, S. Selvaraj, F. Yue, A. Kim, Y. Li, Y. Shen, M. Hu, J.S. Liu, and B. Ren Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature 485 2012 376 380
9. D. Dorsett Cohesin: genomic insights into controlling gene transcription and development Curr. Opin. Genet. Dev. 21 2011 199 206
10. B.J. Elmendorf, A. Shilatifard, Q. Yan, J.W. Conaway, and R.C. Conaway Transcription factors TFIIF, ELL, and Elongin negatively regulate SII-induced nascent transcript cleavage by non-arrested RNA polymerase II elongation intermediates J. Biol. Chem. 276 2001 23109 23114
11. N. Engel, A.G. West, G. Felsenfeld, and M.S. Bartolomei Antagonism between DNA hypermethylation and enhancer-blocking activity at the H19 DMD is uncovered by CpG mutations Nat. Genet. 36 2004 883 888 (Pubitemid 39014108)
12. M.B. Gerstein, Z.J. Lu, E.L. Van Nostrand, C. Cheng, B.I. Arshinoff, T. Liu, K.Y. Yip, R. Robilotto, A. Rechtsteiner, K. Ikegami modENCODE Consortium Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project Science 330 2010 1775 1787
13. M.G. Guenther, S.S. Levine, L.A. Boyer, R. Jaenisch, and R.A. Young A chromatin landmark and transcription initiation at most promoters in human cells Cell 130 2007 77 88 (Pubitemid 47031323)
14. S. Hadjur, L.M. Williams, N.K. Ryan, B.S. Cobb, T. Sexton, P. Fraser, A.G. Fisher, and M. Merkenschlager Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus Nature 460 2009 410 413
15. H. Hagège, P. Klous, C. Braem, E. Splinter, J. Dekker, G. Cathala, W. de Laat, and T. Forné Quantitative analysis of chromosome conformation capture assays (3C-qPCR) Nat. Protoc. 2 2007 1722 1733
16. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, and B.R. Cairns Distinctive chromatin in human sperm packages genes for embryo development Nature 460 2009 473 478
17. M.M. Harrison, X.Y. Li, T. Kaplan, M.R. Botchan, and M.B. Eisen Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition PLoS Genet. 7 2011 e1002266
18. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, and C.W. Ching Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
19. H.M. Herz, M. Mohan, A.S. Garruss, K. Liang, Y.H. Takahashi, K. Mickey, O. Voets, C.P. Verrijzer, and A. Shilatifard Enhancer-associated H3K4 monomethylation by Trithorax-related, the Drosophila homolog of mammalian Mll3/Mll4 Genes Dev. 26 2012 2604 2620
20. C. Hou, R. Dale, and A. Dean Cell type specificity of chromatin organization mediated by CTCF and cohesin Proc. Natl. Acad. Sci. USA 107 2010 3651 3656
21. M.H. Kagey, J.J. Newman, S. Bilodeau, Y. Zhan, D.A. Orlando, N.L. van Berkum, C.C. Ebmeier, J. Goossens, P.B. Rahl, and S.S. Levine Mediator and cohesin connect gene expression and chromatin architecture Nature 467 2010 430 435
22. P. Khoueiry, U. Rothbächer, Y. Ohtsuka, F. Daian, E. Frangulian, A. Roure, I. Dubchak, and P. Lemaire A cis-regulatory signature in ascidians and flies, independent of transcription factor binding sites Curr. Biol. 20 2010 792 802
23. A.V. Krivtsov, and S.A. Armstrong MLL translocations, histone modifications and leukaemia stem-cell development Nat. Rev. Cancer 7 2007 823 833 (Pubitemid 350006257)
24. H. Kurosawa Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells J. Biosci. Bioeng. 103 2007 389 398 (Pubitemid 46991394)
25. E.Z. Kvon, G. Stampfel, J.O. Yáñez-Cuna, B.J. Dickson, and A. Stark HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature Genes Dev. 26 2012 908 913
26. H. Lee, K.W. Kraus, M.F. Wolfner, and J.T. Lis DNA sequence requirements for generating paused polymerase at the start of hsp70 Genes Dev. 6 1992 284 295
27. T.I. Lee, S.E. Johnstone, and R.A. Young Chromatin immunoprecipitation and microarray-based analysis of protein location Nat. Protoc. 1 2006 729 748
28. M. Levine Paused RNA polymerase II as a developmental checkpoint Cell 145 2011 502 511
29. G. Li, X. Ruan, R.K. Auerbach, K.S. Sandhu, M. Zheng, P. Wang, H.M. Poh, Y. Goh, J. Lim, and J. Zhang Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation Cell 148 2012 84 98
30. H.L. Liang, C.Y. Nien, H.Y. Liu, M.M. Metzstein, N. Kirov, and C. Rushlow The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila Nature 456 2008 400 403
31. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, and M.O. Dorschner Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
32. C. Lin, E.R. Smith, H. Takahashi, K.C. Lai, S. Martin-Brown, L. Florens, M.P. Washburn, J.W. Conaway, R.C. Conaway, and A. Shilatifard AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia Mol. Cell 37 2010 429 437
33. C. Lin, A.S. Garrett, B. De Kumar, E.R. Smith, M. Gogol, C. Seidel, R. Krumlauf, and A. Shilatifard Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC) Genes Dev. 25 2011 1486 1498
34. Z. Luo, C. Lin, and A. Shilatifard The super elongation complex (SEC) family in transcriptional control Nat. Rev. Mol. Cell Biol. 13 2012 543 547
35. M. Markstein, and M. Levine Decoding cis-regulatory DNAs in the Drosophila genome Curr. Opin. Genet. Dev. 12 2002 601 606 (Pubitemid 35013542)
36. A. Marson, S.S. Levine, M.F. Cole, G.M. Frampton, T. Brambrink, S. Johnstone, M.G. Guenther, W.K. Johnston, M. Wernig, and J. Newman Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells Cell 134 2008 521 533
37. C.Y. McLean, D. Bristor, M. Hiller, S.L. Clarke, B.T. Schaar, C.B. Lowe, A.M. Wenger, and G. Bejerano GREAT improves functional interpretation of cis-regulatory regions Nat. Biotechnol. 28 2010 495 501
38. T.S. Mikkelsen, M. Ku, D.B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T.K. Kim, and R.P. Koche Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448 2007 553 560 (Pubitemid 47206934)
39. T. Miller, K. Williams, R.W. Johnstone, and A. Shilatifard Identification, cloning, expression, and biochemical characterization of the testis-specific RNA polymerase II elongation factor ELL3 J. Biol. Chem. 275 2000 32052 32056
40. T. Mishiro, K. Ishihara, S. Hino, S. Tsutsumi, H. Aburatani, K. Shirahige, Y. Kinoshita, and M. Nakao Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster EMBO J. 28 2009 1234 1245
41. M. Mohan, C. Lin, E. Guest, and A. Shilatifard Licensed to elongate: a molecular mechanism for MLL-based leukaemogenesis Nat. Rev. Cancer 10 2010 721 728
42. T. Montavon, N. Soshnikova, B. Mascrez, E. Joye, L. Thevenet, E. Splinter, W. de Laat, F. Spitz, and D. Duboule A regulatory archipelago controls Hox genes transcription in digits Cell 147 2011 1132 1145
43. C. Moorman, L.V. Sun, J. Wang, E. de Wit, W. Talhout, L.D. Ward, F. Greil, X.J. Lu, K.P. White, H.J. Bussemaker, and B. van Steensel Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster Proc. Natl. Acad. Sci. USA 103 2006 12027 12032 (Pubitemid 44215805)
44. R. Nativio, K.S. Wendt, Y. Ito, J.E. Huddleston, S. Uribe-Lewis, K. Woodfine, C. Krueger, W. Reik, J.M. Peters, and A. Murrell Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus PLoS Genet. 5 2009 e1000739
45. J.J. Newman, and R.A. Young Connecting transcriptional control to chromosome structure and human disease Cold Spring Harb. Symp. Quant. Biol. 75 2010 227 235
46. C.Y. Nien, H.L. Liang, S. Butcher, Y. Sun, S. Fu, T. Gocha, N. Kirov, J.R. Manak, and C. Rushlow Temporal coordination of gene networks by Zelda in the early Drosophila embryo PLoS Genet. 7 2011 e1002339
47. J.P. Noonan, and A.S. McCallion Genomics of long-range regulatory elements Annu. Rev. Genomics Hum. Genet. 11 2010 1 23
48. A. Rada-Iglesias, R. Bajpai, T. Swigut, S.A. Brugmann, R.A. Flynn, and J. Wysocka A unique chromatin signature uncovers early developmental enhancers in humans Nature 470 2011 279 283
49. P.B. Rahl, C.Y. Lin, A.C. Seila, R.A. Flynn, S. McCuine, C.B. Burge, P.A. Sharp, and R.A. Young c-Myc regulates transcriptional pause release Cell 141 2010 432 445
50. E.E. Raschke, T. Albert, and D. Eick Transcriptional regulation of the Ig kappa gene by promoter-proximal pausing of RNA polymerase II J. Immunol. 163 1999 4375 4382 (Pubitemid 29474505)
51. A. Shilatifard, R.C. Conaway, and J.W. Conaway The RNA polymerase II elongation complex Annu. Rev. Biochem. 72 2003 693 715 (Pubitemid 36930457)
52. R.J. Sims III, R. Belotserkovskaya, and D. Reinberg Elongation by RNA polymerase II: the short and long of it Genes Dev. 18 2004 2437 2468 (Pubitemid 39362887)
53. E. Smith, and A. Shilatifard The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes Mol. Cell 40 2010 689 701
54. E. Smith, C. Lin, and A. Shilatifard The super elongation complex (SEC) and MLL in development and disease Genes Dev. 25 2011 661 672
55. E.R. Smith, C. Lin, A.S. Garrett, J. Thornton, N. Mohaghegh, D. Hu, J. Jackson, A. Saraf, S.K. Swanson, and C. Seidel The little elongation complex regulates small nuclear RNA transcription Mol. Cell 44 2011 954 965
56. H. Takahashi, T.J. Parmely, S. Sato, C. Tomomori-Sato, C.A. Banks, S.E. Kong, H. Szutorisz, S.K. Swanson, S. Martin-Brown, and M.P. Washburn Human mediator subunit MED26 functions as a docking site for transcription elongation factors Cell 146 2011 92 104
57. K.S. Wendt, and J.M. Peters How cohesin and CTCF cooperate in regulating gene expression Chromosome Res. 17 2009 201 214
58. A. Yokoyama, M. Lin, A. Naresh, I. Kitabayashi, and M.L. Cleary A higher-order complex containing AF4 and ENL family proteins with P-TEFb facilitates oncogenic and physiologic MLL-dependent transcription Cancer Cell 17 2010 198 212
59. J.A. Zhang, A. Mortazavi, B.A. Williams, B.J. Wold, and E.V. Rothenberg Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity Cell 149 2012 467 482
60. Huang, W.; Sherman, B.T.; and Lempicki, R.A. (2009a). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13.
61. Huang, W.; Sherman, B.T.; and Lempicki, R.A. (2009b). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
62. 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.
63. Smith, E.R.; Lin, C.; Garrett, A.S.; Thornton, J.; Mohaghegh, N.; Hu, D.; Jackson, J.; Saraf, A.; Swanson, S.K.; Seidel, C.; et al. (2011b). The little elongation complex regulates small nuclear RNA transcription. Mol. Cell 44, 954-965.
64. Trapnell, C.; Pachter, L.; and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
65. 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.
66. Zang, C.; Schones, D.E.; Zeng, C.; Cui, K.; Zhao, K.; and Peng, W. (2009). A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25, 1952-1958.
67. Zhang, Y.; Liu, T.; Meyer, C.A.; Eeckhoute, J.; Johnson, D.S.; Bernstein, B.E.; Nusbaum, C.; Myers, R.M.; Brown, M.; Li, W.; et al. (2008). Model-based analysis of ChIP-Seq (MACS). Gen. Biol. 9, R137.