Direct GR Binding Sites Potentiate Clusters of TF Binding across the Human Genome

Cell

Volumn 166, Issue 5, 2016, Pages 1269-1281.e19

  Vockley, Christopher M ^a,b   D'Ippolito, Anthony M ^b   McDowell, Ian C ^b   Majoros, William H ^b   Safi, Alexias ^a,b   Song, Lingyun ^a,b   Crawford, Gregory E ^a,b   Reddy, Timothy E ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR CTCF; DEXAMETHASONE; NR3C1 PROTEIN, HUMAN; PROTEIN BINDING;

A549 CELL LINE; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING MOTIF; ENHANCER REGION; EPIGENETICS; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE INTERACTION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN GENOME; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY MECHANISM; REPORTER GENE; A-549 CELL LINE; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; METABOLISM; TRANSCRIPTION INITIATION;

A549 CELLS; BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; DEXAMETHASONE; GENES, REPORTER; GENOME, HUMAN; GLUCOCORTICOIDS; HUMANS; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84983801995     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.049     Document Type: Article

References (68)

1. Adey, A., Morrison, H.G., Asan, Xun, X., Kitzman, J.O., Turner, E.H., Stackhouse, B., MacKenzie, A.P., Caruccio, N.C., Zhang, X., Shendure, J., Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol., 11, 2010, R119.
2. Arnold, C.D., Gerlach, D., Stelzer, C., Boryń, L.M., Rath, M., Stark, A., Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 339 (2013), 1074–1077.
3. Bailey, T.L., Gribskov, M., Combining evidence using p-values: Application to sequence homology searches. Bioinformatics 14 (1998), 48–54.
4. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., Noble, W.S., MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 37 (2009), W202–W208.
5. Belikov, S., Astrand, C., Wrange, O., FoxA1 binding directs chromatin structure and the functional response of a glucocorticoid receptor-regulated promoter. Mol. Cell. Biol. 29 (2009), 5413–5425.
6. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57 (1995), 289–300.
7. Biddie, S.C., John, S., Sabo, P.J., Thurman, R.E., Johnson, T.A., Schiltz, R.L., Miranda, T.B., Sung, M.H., Trump, S., Lightman, S.L., et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol. Cell 43 (2011), 145–155.
8. Botta, M., Haider, S., Leung, I.X., Lio, P., Mozziconacci, J., Intra- and inter-chromosomal interactions correlate with CTCF binding genome wide. Mol. Syst. Biol., 6, 2010, 426.
9. Chandler, V.L., Maler, B.A., Yamamoto, K.R., DNA sequences bound specifically by glucocorticoid receptor in vitro render a heterologous promoter hormone responsive in vivo. Cell 33 (1983), 489–499.
10. Coleman, R.A., Pugh, B.F., Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J. Biol. Chem. 270 (1995), 13850–13859.
11. Devonshire, A.S., Elaswarapu, R., Foy, C.A., Evaluation of external RNA controls for the standardisation of gene expression biomarker measurements. BMC Genomics, 11, 2010, 662.
12. Diamond, M.I., Miner, J.N., Yoshinaga, S.K., Yamamoto, K.R., Transcription factor interactions: Selectors of positive or negative regulation from a single DNA element. Science 249 (1990), 1266–1272.
13. Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S., Ren, B., Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485 (2012), 376–380.
14. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
15. Feng, J., Liu, T., Qin, B., Zhang, Y., Liu, X.S., Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7 (2012), 1728–1740.
16. Fullwood, M.J., Liu, M.H., Pan, Y.F., Liu, J., Xu, H., Mohamed, Y.B., Orlov, Y.L., Velkov, S., Ho, A., Mei, P.H., et al. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462 (2009), 58–64.
17. Gao, X., Vockley, C.M., Pauli, F., Newberry, K.M., Xue, Y., Randell, S.H., Reddy, T.E., Hogan, B.L., Evidence for multiple roles for grainyhead-like 2 in the establishment and maintenance of human mucociliary airway epithelium. Proc. Natl. Acad. Sci. USA 110 (2013), 9356–9361.
18. Gertz, J., Varley, K.E., Davis, N.S., Baas, B.J., Goryshin, I.Y., Vaidyanathan, R., Kuersten, S., Myers, R.M., Transposase mediated construction of RNA-seq libraries. Genome Res. 22 (2012), 134–141.
19. Gertz, J., Savic, D., Varley, K.E., Partridge, E.C., Safi, A., Jain, P., Cooper, G.M., Reddy, T.E., Crawford, G.E., Myers, R.M., Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol. Cell 52 (2013), 25–36.
20. Gotea, V., Visel, A., Westlund, J.M., Nobrega, M.A., Pennacchio, L.A., Ovcharenko, I., Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res. 20 (2010), 565–577.
21. Harrow, J., Denoeud, F., Frankish, A., Reymond, A., Chen, C.K., Chrast, J., Lagarde, J., Gilbert, J.G., Storey, R., Swarbreck, D., et al. GENCODE: Producing a reference annotation for ENCODE. Genome Biol., 7(Suppl 1: S4 1–9), 2006.
22. Herrlich, P., Cross-talk between glucocorticoid receptor and AP-1. Oncogene 20 (2001), 2465–2475.
23. Hertel, K.J., Lynch, K.W., Maniatis, T., Common themes in the function of transcription and splicing enhancers. Curr. Opin. Cell Biol. 9 (1997), 350–357.
24. Hurtado, A., Holmes, K.A., Ross-Innes, C.S., Schmidt, D., Carroll, J.S., FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 43 (2011), 27–33.
25. Jiang, M., Anderson, J., Gillespie, J., Mayne, M., uShuffle: A useful tool for shuffling biological sequences while preserving the k-let counts. BMC Bioinformatics, 9, 2008, 192.
26. John, S., Sabo, P.J., Thurman, R.E., Sung, M.H., Biddie, S.C., Johnson, T.A., Hager, G.L., Stamatoyannopoulos, J.A., Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 43 (2011), 264–268.
27. Joseph, R., Orlov, Y.L., Huss, M., Sun, W., Kong, S.L., Ukil, L., Pan, Y.F., Li, G., Lim, M., Thomsen, J.S., et al. Integrative model of genomic factors for determining binding site selection by estrogen receptor-α. Mol. Syst. Biol., 6, 2010, 456.
28. Kheradpour, P., Ernst, J., Melnikov, A., Rogov, P., Wang, L., Zhang, X., Alston, J., Mikkelsen, T.S., Kellis, M., Systematic dissection of regulatory motifs in 2000 predicted human enhancers using a massively parallel reporter assay. Genome Res. 23 (2013), 800–811.
29. Kuznetsova, T., Wang, S.Y., Rao, N.A., Mandoli, A., Martens, J.H., Rother, N., Aartse, A., Groh, L., Janssen-Megens, E.M., Li, G., et al. Glucocorticoid receptor and nuclear factor kappa-b affect three-dimensional chromatin organization. Genome Biol., 16, 2015, 264.
30. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
31. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, 2009, R25.
32. Lee, D.H., Schleif, R.F., In vivo DNA loops in araCBAD: size limits and helical repeat. Proc. Natl. Acad. Sci. USA 86 (1989), 476–480.
33. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
34. Liu, X., Wang, L., Zhao, K., Thompson, P.R., Hwang, Y., Marmorstein, R., Cole, P.A., The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451 (2008), 846–850.
35. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
36. Luecke, H.F., Yamamoto, K.R., The glucocorticoid receptor blocks P-TEFb recruitment by NFkappaB to effect promoter-specific transcriptional repression. Genes Dev. 19 (2005), 1116–1127.
37. Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Chen, C.Y., Chou, A., Ienasescu, H., et al. JASPAR 2014: An extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 42 (2014), D142–D147.
38. Maurano, M.T., Humbert, R., Rynes, E., Thurman, R.E., Haugen, E., Wang, H., Reynolds, A.P., Sandstrom, R., Qu, H., Brody, J., et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 337 (2012), 1190–1195.
39. Melnikov, A., Murugan, A., Zhang, X., Tesileanu, T., Wang, L., Rogov, P., Feizi, S., Gnirke, A., Callan, C.G. Jr., Kinney, J.B., et al. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat. Biotechnol. 30 (2012), 271–277.
40. Mittal, R., Kumar, K.U., Pater, A., Pater, M.M., Differential regulation by c-jun and c-fos protooncogenes of hormone response from composite glucocorticoid response element in human papilloma virus type 16 regulatory region. Mol. Endocrinol. 8 (1994), 1701–1708.
41. Olansky, L., Welling, C., Giddings, S., Adler, S., Bourey, R., Dowse, G., Serjeantson, S., Zimmet, P., Permutt, M.A., A variant insulin promoter in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 89 (1992), 1596–1602.
42. Pearce, D., Matsui, W., Miner, J.N., Yamamoto, K.R., Glucocorticoid receptor transcriptional activity determined by spacing of receptor and nonreceptor DNA sites. J. Biol. Chem. 273 (1998), 30081–30085.
43. Quinlan, A.R., BEDTools: The Swiss-Army Tool for genome feature analysis. Curr. Protoc. Bioinformatics 47 (2014), 1–34.
44. R Development Core Team. R: A Language and Environment for Statistical Computing. 2016, R Foundation for Statistical Computing.
45. Ratman, D., Vanden Berghe, W., Dejager, L., Libert, C., Tavernier, J., Beck, I.M., De Bosscher, K., How glucocorticoid receptors modulate the activity of other transcription factors: A scope beyond tethering. Mol. Cell. Endocrinol. 380 (2013), 41–54.
46. Reddy, T.E., Pauli, F., Sprouse, R.O., Neff, N.F., Newberry, K.M., Garabedian, M.J., Myers, R.M., Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res. 19 (2009), 2163–2171.
47. Reddy, T.E., Gertz, J., Crawford, G.E., Garabedian, M.J., Myers, R.M., The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Mol. Cell. Biol. 32 (2012), 3756–3767.
48. Reddy, T.E., Gertz, J., Pauli, F., Kucera, K.S., Varley, K.E., Newberry, K.M., Marinov, G.K., Mortazavi, A., Williams, B.A., Song, L., et al. Effects of sequence variation on differential allelic transcription factor occupancy and gene expression. Genome Res. 22 (2012), 860–869.
49. Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.C., Müller, M., pROC: An open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics, 12, 2011, 77.
50. Rye, M., Sætrom, P., Håndstad, T., Drabløs, F., Clustered ChIP-Seq-defined transcription factor binding sites and histone modifications map distinct classes of regulatory elements. BMC Biol., 9, 2011, 80.
51. Sakai, D.D., Helms, S., Carlstedt-Duke, J., Gustafsson, J.A., Rottman, F.M., Yamamoto, K.R., Hormone-mediated repression: A negative glucocorticoid response element from the bovine prolactin gene. Genes Dev. 2 (1988), 1144–1154.
52. Salmon-Divon, M., Dvinge, H., Tammoja, K., Bertone, P., PeakAnalyzer: Genome-wide annotation of chromatin binding and modification loci. BMC Bioinformatics, 11, 2010, 415.
53. Sheppard, K.A., Phelps, K.M., Williams, A.J., Thanos, D., Glass, C.K., Rosenfeld, M.G., Gerritsen, M.E., Collins, T., Nuclear integration of glucocorticoid receptor and nuclear factor-kappaB signaling by CREB-binding protein and steroid receptor coactivator-1. J. Biol. Chem. 273 (1998), 29291–29294.
54. Slater, E.P., Rabenau, O., Karin, M., Baxter, J.D., Beato, M., Glucocorticoid receptor binding and activation of a heterologous promoter by dexamethasone by the first intron of the human growth hormone gene. Mol. Cell. Biol. 5 (1985), 2984–2992.
55. Smith, R.P., Taher, L., Patwardhan, R.P., Kim, M.J., Inoue, F., Shendure, J., Ovcharenko, I., Ahituv, N., Massively parallel decoding of mammalian regulatory sequences supports a flexible organizational model. Nat. Genet. 45 (2013), 1021–1028.
56. So, A.Y., Chaivorapol, C., Bolton, E.C., Li, H., Yamamoto, K.R., Determinants of cell- and gene-specific transcriptional regulation by the glucocorticoid receptor. PLoS Genet., 3, 2007, e94.
57. Soccio, R.E., Chen, E.R., Rajapurkar, S.R., Safabakhsh, P., Marinis, J.M., Dispirito, J.R., Emmett, M.J., Briggs, E.R., Fang, B., Everett, L.J., et al. Genetic variation determines PPARγ function and anti-diabetic drug response in vivo. Cell 162 (2015), 33–44.
58. Somma, M.P., Pisano, C., Lavia, P., The housekeeping promoter from the mouse CpG island HTF9 contains multiple protein-binding elements that are functionally redundant. Nucleic Acids Res. 19 (1991), 2817–2824.
59. Song, L., Crawford, G.E., DNase-seq: A high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harbor Protoc., 2010, 2010 pdb.prot5384.
60. Stadhouders, R., Aktuna, S., Thongjuea, S., Aghajanirefah, A., Pourfarzad, F., van Ijcken, W., Lenhard, B., Rooks, H., Best, S., Menzel, S., et al. HBS1L-MYB intergenic variants modulate fetal hemoglobin via long-range MYB enhancers. J. Clin. Invest. 124 (2014), 1699–1710.
61. Staller, M.V., Vincent, B.J., Bragdon, M.D., Lydiard-Martin, T., Wunderlich, Z., Estrada, J., DePace, A.H., Shadow enhancers enable Hunchback bifunctionality in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 112 (2015), 785–790.
62. Starick, S.R., Ibn-Salem, J., Jurk, M., Hernandez, C., Love, M.I., Chung, H.R., Vingron, M., Thomas-Chollier, M., Meijsing, S.H., ChIP-exo signal associated with DNA-binding motifs provides insight into the genomic binding of the glucocorticoid receptor and cooperating transcription factors. Genome Res. 25 (2015), 825–835.
63. Teurich, S., Angel, P., The glucocorticoid receptor synergizes with Jun homodimers to activate AP-1-regulated promoters lacking GR binding sites. Chem. Senses 20 (1995), 251–255.
64. Tyedmers, J., Brunke, M., Lechte, M., Sandholzer, U., Dierks, T., Schlotterhose, P., Schmidt, B., Zimmermann, R., Efficient folding of firefly luciferase after transport into mammalian microsomes in the absence of luminal chaperones and folding catalysts. J Biol Chem. 271 (1996), 19509–19513.
65. Vockley, C.M., Guo, C., Majoros, W.H., Nodzenski, M., Scholtens, D.M., Hayes, M.G., Lowe, W.L. Jr., Reddy, T.E., Massively parallel quantification of the regulatory effects of noncoding genetic variation in a human cohort. Genome Res. 25 (2015), 1206–1214.
66. Wang, Y., Zhang, J.J., Dai, W., Lei, K.Y., Pike, J.W., Dexamethasone potently enhances phorbol ester-induced IL-1beta gene expression and nuclear factor NF-kappaB activation. J. Immunol. 159 (1997), 534–537.
67. Wang, J.C., Derynck, M.K., Nonaka, D.F., Khodabakhsh, D.B., Haqq, C., Yamamoto, K.R., Chromatin immunoprecipitation (ChIP) scanning identifies primary glucocorticoid receptor target genes. Proc. Natl. Acad. Sci. USA 101 (2004), 15603–15608.
68. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., Liu, X.S., Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, 2008, R137.