Interactions between pluripotency factors specify cis-regulation in embryonic stem cells

Genome Research

Volumn 26, Issue 6, 2016, Pages 778-786

  Fiore, Chris ^a   Cohen, Barak A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYONIC STEM CELL; INVESTIGATIVE PROCEDURES; MOUSE; NONHUMAN; OBSERVATIONAL STUDY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; THERMODYNAMICS; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LIBRARY; MOUSE EMBRYONIC STEM CELL; PHYSIOLOGY; REGULATORY SEQUENCE;

ANIMALS; BINDING SITES; CELLS, CULTURED; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LIBRARY; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MODELS, GENETIC; MOUSE EMBRYONIC STEM CELLS; REGULATORY SEQUENCES, NUCLEIC ACID; THERMODYNAMICS; TRANSCRIPTION FACTORS;

EID: 84973401361     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.200733.115     Document Type: Article

References (58)

1. Akaike H. 1974. A new look at the statistical model identification. IEEE Trans Automat Contr 19: 716-723.
2. Ambrosetti DC, Schöler HR, Dailey L, Basilico C. 2000. Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J Biol Chem 275: 23387-23397.
3. Arnold CD, Gerlach D, Stelzer C, Boryn ŁM, Rath M, Stark A. 2013. Genomewide quantitative enhancer activity maps identified by STARR-seq. Science 339: 1074-1077.
4. Arnosti DN, Kulkarni MM. 2005. Transcriptional enhancers: intelligent enhanceosomes or flexible billboards? J Cell Biochem 94: 890-898.
5. Arnosti DN, Barolo S, Levine M, Small S. 1996. The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 122: 205-214.
6. Bates DM, Watts DG. 1988. Nonlinear regression analysis and its applications. John Wiley & Sons, New York.
7. Bintu L, Buchler NE, Garcia HG, Gerland U, Hwa T, Kondev J, Phillips R. 2005. Transcriptional regulation by the numbers: models. Curr Opin Genet Dev 15: 116-124.
8. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
9. Brewster RC, Jones DL, Phillips R. 2012. Tuning promoter strength through RNA polymerase binding site design in Escherichia coli. PLoS Comput Biol 8: e1002811.
10. Brewster RC, Weinert FM, Garcia HG, Song D, Rydenfelt M, Phillips R. 2014. The transcription factor titration effect dictates level of gene expression. Cell 156: 1312-1323.
11. Buchler NE, Gerland U, Hwa T. 2003. On schemes of combinatorial transcription logic. Proc Natl Acad Sci 100: 5136-5141.
12. Chen CT, Gottlieb DI, Cohen BA. 2008a. Ultraconserved elements in the Olig2 promoter. PLoS One 3: e3946.
13. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. 2008b. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
14. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, Yeap LS, Li P, Ang YS, Lim B, Robson P, et al. 2005. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25: 6031-6046.
15. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
16. Erceg J, Saunders TE, Girardot C, Devos DP, Hufnagel L, Furlong EE. 2014. Subtle changes in motif positioning cause tissue-specific effects on robustness of an enhancer's activity. PLoS Genet 10: e1004060.
17. Gertz J, Cohen BA. 2009. Environment-specific combinatorial cis-regulation in synthetic promoters. Mol Syst Biol 5: 244.
18. Gertz J, Siggia ED, Cohen BA. 2009. Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457: 215-218.
19. Goldwater MB, Markman AB, Stilwell CH. 2010. The empirical case for rolegoverned categories. Dev Cell 18: 359-376.
20. Gotea V, Visel A, Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I. 2010. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res 20: 565-577.
21. Grant CE, Bailey TL, Noble WS. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017-1018.
22. He X, Samee MA, Blatti C, Sinha S. 2010. Thermodynamics-based models of transcriptional regulation by enhancers: the roles of synergistic activation, cooperative binding and short-range repression. PLoS Comput Biol 6: e1000935.
23. Hutchins AP, Choo SH, Mistri TK, Rahmani M, Woon CT, Ng CKL, Jauch R, Robson P. 2013. Co-motif discovery identifies anesrrb-Sox2-DNA ternary complex as a mediator of transcriptional differences between mouse embryonic and epiblast stem cells. Stem Cells 31: 269-281.
24. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, Schafer X, Lun Y, Lemischka IR. 2006. Dissecting self-renewal instem cells with RNA interference. Nature 442: 533-538.
25. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, Robson P, Zhong S, Ng HH. 2008. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 10: 353-360.
26. Kim TK, Maniatis T. 1997. The mechanism of transcriptional synergy of an in vitro assembled interferon-β enhanceosome. Mol Cell 1: 119-129.
27. Kim J, Chu J, Shen X, Wang J, Orkin SH. 2008. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061.
28. Kinney JB, Murugan A, Callan CG, Cox EC. 2010. Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. Proc Natl Acad Sci 107: 9158-9163.
29. Kulkarni MM, Arnosti DN. 2003. Information display by transcriptional enhancers. Development 130: 6569-6575.
30. Kuroda T, Tada M, Kubota H, Kimura H, Hatano S, Suemori H, Nakatsuji N, Tada T. 2005. Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25: 2475-2485.
31. Kwasnieski JC, Mogno I, Myers CA, Corbo JC, Cohen BA. 2012. Complex effects of nucleotide variants in a mammalian cis-regulatory element. Proc Natl Acad Sci 109: 19498-19503.
32. Kwasnieski JC, Fiore C, Chaudhari HG, Cohen BA. 2014. High-throughput functional testing of ENCODE segmentation predictions. Genome Res 24: 1595-1602.
33. Levo M, Zalckvar E, Sharon E, Dantas Machado AC, Kalma Y, Lotam Pompan M, Weinberger A, Yakhini Z, Rohs R, Segal E. 2015. Unraveling determinants of transcription factor binding outside the core binding site. Genome Res 25: 1018-1029.
34. Liu F, Posakony JW. 2012. Role of architecture in the function and specificity of two notch-regulated transcriptional enhancer modules. PLoS Genet 8: e1002796.
35. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al. 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
36. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen CY, Chou A, Ienasescu H, et al. 2014. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 42: D142-D147.
37. Melnikov A, Murugan A, Zhang X, Tesileanu T, Wang L, Rogov P, Feizi S, Gnirke A, Callan CG, Kinney JB, et al. 2012. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat Biotechnol 30: 271-277.
38. Mogno I, Kwasnieski JC, Cohen BA. 2013. Massively parallel synthetic promoter assays reveal the in vivo effects of binding site variants. Genome Res 23: 1908-1915.
39. Nakatake Y, Fukui N, Iwamatsu Y, Masui S, Takahashi K, Yagi R, Yagi K, Miyazaki JI, Matoba R, Ko MSH, et al. 2006. Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Mol Cell Biol 26: 7772-7782.
40. Panne D, Maniatis T, Harrison SC. 2007. An atomic model of the interferonβ enhanceosome. Cell 129: 1111-1123.
41. Patwardhan RP, Hiatt JB, Witten DM, Kim MJ, Smith RP, May D, Lee C, Andrie JM, Lee SI, Cooper GM, et al. 2012. Massively parallel functional dissection of mammalian enhancers in vivo. Nat Biotechnol 30: 265-270.
42. Quinlan AR, Hall IM. 2010. BEDTools: aflexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
43. Reményi A, Lins K, Nissen LJ, Reinbold R, Schöler HR, Wilmanns M. 2003. Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 17: 2048-2059.
44. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P. 2005. Transcriptional regulation of Nanog by OCT4 and SOX2. J Biol Chem 280: 24731-24737.
45. Segal E, Raveh-Sadka T, Schroeder M, Unnerstall U, Gaul U. 2008. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451: 535-540.
46. Senger K, Armstrong GW, Rowell WJ, Kwan JM, Markstein M, Levine M. 2004. Immunity regulatory DNAs share common organizational features in Drosophila. Mol Cell 13: 19-32.
47. Sharon E, Kalma Y, Sharp A, Raveh-Sadka T, Levo M, Zeevi D, Keren L, Yakhini Z, Weinberger A, Segal E. 2012. Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat Biotechnol 30: 521-530.
48. R control system of bacteriophage λ. A physical-chemical model for gene regulation. J Mol Biol 181: 211-230.
49. Sherman MS, Cohen BA. 2012. Thermodynamic state ensemble models of cis-regulation. PLoS Comput Biol 8: e1002407.
50. Smith RP, Taher L, Patwardhan RP, Kim MJ, Inoue F, Shendure J, Ovcharenko I, Ahituv N. 2013. Massively parallel decoding of mammalian regulatory sequences supports a flexible organizational model. Nat Genet 45: 1021-1028.
51. Thanos D, Maniatis T. 1995. Virus induction of human IFNβ gene expression requires the assembly of an enhanceosome. Cell 83: 1091-1100.
52. van den Berg DL, Zhang W, Yates A, Engelen E, Takacs K, Bezstarosti K, Demmers J, Chambers I, Poot RA. 2008. Estrogen-related receptor β interacts with Oct4 to positively regulate Nanog gene expression. Mol Cell Biol 28: 5986-5995.
53. Wei Z, Yang Y, Zhang P, Andrianakos R, Hasegawa K, Lyu J, Chen X, Bai G, Liu C, Pera M, et al. 2009. Klf4 interacts directly with Oct4 and Sox2 to promote reprogramming. Stem Cells 27: 2969-2978.
54. White MA, Myers CA, Corbo JC, Cohen BA. 2013. Massively parallel in vivo enhancer assay reveals that highly local features determine the cisregulatory function of ChIP-seq peaks. Proc Natl Acad Sci 110: 11952-11957.
55. Xian HQ, Werth K, Gottlieb DI. 2005. Promoter analysis in ES cell-derived neural cells. Biochem Biophys Res Commun 327: 155-162.
56. Yáñez-Cuna JO, Dinh HQ, Kvon EZ, Shlyueva D, Stark A. 2012. Uncovering cis-regulatory sequence requirements for context-specific transcription factor binding. Genome Res 22: 2018-2030.
57. Zeigler RD, Cohen BA. 2014. Discrimination between thermodynamic models of cis-regulation using transcription factor occupancy data. Nucleic Acids Res 42: 2224-2234.
58. Zhang X, Zhang J, Wang T, Esteban MA, Pei D. 2008. Esrrb activates Oct4 transcription and sustains self-renewal and pluripotency in embryonic stem cells. J Biol Chem 283: 35825-35833.