Towards an understanding of cell-specific functions of signaldependent transcription factors

Journal of Molecular Endocrinology

Volumn 51, Issue 3, 2013, Pages

  Zhang, Dawn X ^a,b   Glass, Christopher K ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Cell specific; Genome wide analyses; Lineage determining transcription factors; Signal dependent transcription factors

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; CORE BINDING FACTOR BETA; E1A ASSOCIATED P300 PROTEIN; ESTROGEN RECEPTOR ALPHA; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; INTERFERON REGULATORY FACTOR 4; LIVER X RECEPTOR; MYOD1 PROTEIN; SERUM RESPONSE FACTOR; SIGNAL DEPENDENT TRANSCRIPTION FACTOR; SMAD3 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 3; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR ELF 1; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR JUNB; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

B LYMPHOCYTE; BINDING SITE; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL STRAIN LNCAP; CELL STRAIN MCF 7; CHROMATIN ASSEMBLY AND DISASSEMBLY; DENDRITIC CELL; DNA BINDING; EMBRYONIC STEM CELL; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GENETIC VARIABILITY; HEMATOPOIETIC STEM CELL; HUMAN; INNATE IMMUNITY; LYMPHOID PROGENITOR CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MYELOID PROGENITOR CELL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; RNA TRANSCRIPTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION;

CELL-SPECIFIC; GENOME-WIDE ANALYSES; LINEAGE DETERMINING TRANSCRIPTION FACTORS; SIGNAL DEPENDENT TRANSCRIPTION FACTORS;

ANIMALS; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84887729457     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-13-0216     Document Type: Review

References (96)

1. 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 Journal 30 2817-2828. (doi:10.1038/emboj. 2011.194)
2. Barish GD, Yu RT, Karunasiri M, Ocampo CB, Dixon J, Benner C, Dent AL, Tangirala RK & Evans RM 2010 Bcl-6 and NF-k B cistromes mediate opposing regulation of the innate immune response. Genes and Development 24 2760-2765. (doi:10.1101/gad.1998010)
3. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C & Snyder M 2012 An integrated encyclopedia of DNA elements in the human genome. Nature 489 57-74. (doi:10.1038/nature11247)
4. Biddie SC, John S, Sabo PJ, Thurman RE, Johnson TA, Schiltz RL, Miranda TB, Sung MH, Trump S, Lightman SL et al. 2011 Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Molecular Cell 43 145-155. (doi:10.1016/j.molcel. 2011.06.016)
5. Buryachkovskaya L, Sumarokov A & Lomakin N 2013 Historical overview of studies on inflammation in Russia. Inflammation Research 62 441-450. (doi:10.1007/s00011-013-0597-0)
6. Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, Mietton F, Matteoli G, Hiebert S & Natoli G 2012 Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. PNAS 109 E2865-E2874. (doi:10.1073/pnas.1121131109)
7. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, Di Tacchio L, Atkins AR, Glass CK et al. 2012 Regulation of circadian behaviour and metabolism by REV-ERB-a and REV-ERB-b. Nature 485 123-127. (doi:10.1038/nature11048)
8. Ciofani M, Madar A, Galan C, Sellars M, Mace K, Pauli F, Agarwal A, Huang W, Parkurst CN, Muratet M et al. 2012 A validated regulatory network for Th17 cell specification. Cell 151 289-303. (doi:10.1016/j.cell.2012. 09.016)
9. 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. PNAS 107 21931-21936. (doi:10.1073/ pnas.1016071107)
10. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W & Zhao K 2009 Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4 80-93. (doi:10.1016/j.stem.2008.11.011)
11. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G & Natoli G 2007 The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130 1083-1094. (doi:10.1016/j.cell.2007.08.019)
12. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL & Natoli G 2010 A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLo S Biology 8 e1000384. (doi:10.1371/journal.pbio.1000384)
13. Drexler SK & Foxwell BM 2010 The role of toll-like receptors in chronic inflammation. International Journal of Biochemistry & Cell Biology 42 506-518. (doi:10.1016/j.biocel.2009.10.009)
14. Escoubet-Lozach L, Benner C, Kaikkonen MU, Lozach J, Heinz S, Spann NJ, Crotti A, Stender J, Ghisletti S, Reichart D et al. 2011 Mechanisms establishing TLR4-responsive activation states of inflammatory response genes. PLo S Genetics 7 e1002401. (doi:10.1371/journal.pgen.1002401)
15. Fan W, Morinaga H, Kim JJ, Bae E, Spann NJ, Heinz S, Glass CK & Olefsky JM2010 Fox O1 regulates Tlr4 inflammatory pathway signalling in macrophages. EMBOJournal294223-4236. (doi:10.1038/emboj.2010.268)
16. Feng J, Bi C, Clark BS, Mady R, Shah P & Kohtz JD 2006 The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes and Development 20 1470-1484. (doi:10.1101/gad.1416106)
17. Foster SL, Hargreaves DC & Medzhitov R 2007 Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 972-978. (doi:10.1038/nature05836)
18. Friedman JR & Kaestner KH 2006 The Foxa family of transcription factors in development and metabolism. Cellular and Molecular Life Sciences 63 2317-2328. (doi:10.1007/s00018-006-6095-6)
19. Garber M, Yosef N, Goren A, Raychowdhury R, Thielke A, Guttman M, Robinson J, Minie B, Chevrier N, Itzhaki Z et al. 2012 A highthroughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Molecular Cell 47 810-822. (doi:10.1016/j.molcel.2012.07.030)
20. Ghisletti S, Barozzi I, Mietton F, Polletti S, De Santa F, Venturini E, Gregory L, Lonie L, Chew A, Wei CL et al. 2010 Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32 317-328. (doi:10.1016/j.immuni.2010.02.008)
21. Glass CK & Saijo K 2010 Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nature Reviews. Immunology 10 365-376. (doi:10.1038/nri2748)
22. Hallson G, Hollebakken RE, Li T, Syrzycka M, Kim I, Cotsworth S, Fitzpatrick KA, Sinclair DA & Honda BM 2012 d Set1 is the main H3K4 di-and tri-methyltransferase throughout Drosophila development. Genetics 190 91-100. (doi:10.1534/genetics.111.135863)
23. Hargreaves DC, Horng T & Medzhitov R 2009 Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138 129-145. (doi:10.1016/j.cell.2009.05.047)
24. He HH, Meyer CA, Shin H, Bailey ST, Wei G, Wang Q, Zhang Y, Xu K, Ni M, Lupien M et al. 2010 Nucleosome dynamics define transcriptional enhancers. Nature Genetics 42 343-347. (doi:10.1038/ng.545)
25. 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. Nature Genetics 39 311-318. (doi:10.1038/ng1966)
26. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CWet al. 2009 Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459 108-112. (doi:10.1038/nature07829)
27. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H & Glass CK 2010 Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell 38 576-589. (doi:10.1016/j.molcel.2010.05.004)
28. Heinz S, Romanoski CE, Benner C, Allison KA, Kaikkonen MU, Orozco LD & Glass CK 2013 Impact of natural genetic variation on enhancer selection and function. Nature [in press]. (doi:10.1038/nature12615)
29. Hettinger J, Richards DM, Hansson J, Barra MM, Joschko AC, Krijgsveld J & Feuerer M 2013 Origin of monocytes and macrophages in a committed progenitor. Nature Immunology 14 821-830. (doi:10.1038/ni.2638)
30. Hu G, Schones DE, Cui K, Ybarra R, Northrup D, Tang Q, Gattinoni L, Restifo NP, Huang S & Zhao K 2011 Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1. Genome Research 21 1650-1658. (doi:10.1101/gr.121145.111)
31. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D & Carroll JS 2011 FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nature Genetics 43 27-33. (doi:10.1038/ng.730)
32. Jeong KW, Kim K, Situ AJ, Ulmer TS, An W& Stallcup MR 2011 Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nature Structural & Molecular Biology 18 1358-1365. (doi:10.1038/nsmb.2153)
33. 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 Journal 30 249-262. (doi:10.1038/emboj.2010.318)
34. Kaikkonen MU, Spann NJ, Heinz S, Romanoski CE, Allison KA, Stender JD, Chun HB, Tough DF, Prinjha RK, Benner C et al. 2013 Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Molecular Cell 51 310-325. (doi:10.1016/ j.molcel.2013.07.010)
35. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, Waszak SM, Habegger L, Rozowsky J, Shi M, Urban AE et al. 2010 Variation in transcription factor binding among humans. Science 328 232-235. (doi:10.1126/science.1183621)
36. Kerenyi MA, Shao Z, Hsu YJ, Guo G, Luc S, O'Brien K, Fujiwara Y, Peng C, Nguyen M & Orkin SH 2013 Histone demethylase Lsd1 represses hematopoietic stem and progenitor cell signatures during blood cell maturation. e Life 2 e00633. (doi:10.7554/e Life.00633)
37. 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 activity-regulated enhancers. Nature 465 182-187. (doi:10.1038/nature09033)
38. Kowalczyk MS, Hughes JR, Garrick D, Lynch MD, Sharpe JA, Sloane-Stanley JA, McGowan SJ, De Gobbi M, Hosseini M, Vernimmen D et al. 2012 Intragenic enhancers act as alternative promoters. Molecular Cell45447-458. (doi:10.1016/j.molcel.2011.12.021)
39. Kueh HY, Champhekhar A, Nutt SL, Elowitz MB & Rothenberg EV 2013 Positive feedback between PU.1 and the cell cycle controls myeloid differentiation. Science 341 670-673. (doi:10.1126/science.1240831)
40. Lam MT, Cho H, Lesch HP, Gosselin D, Heinz S, Tanaka-Oishi Y, Benner C, Kaikkonen MU, Kim AS, Kosaka M et al. 2013 Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498 511-515. (doi:10.1038/nature12209)
41. Lawrence T & Natoli G 2011 Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nature Reviews. Immunology 11 750-761. (doi:10.1038/nri3088)
42. Lazar MA 2011 Mechanism of action of hormones that act on nuclear receptors. In Williams Textbook of Endocrinology, 12th edn, pp 52-61. Eds S Melmed & RH Williams. Philadelphia: Elsevier/Saunders.
43. Lefterova MI, Zhang Y, Steger DJ, Schupp M, Schug J, Cristancho A, Feng D, Zhuo D, Stoeckert CJ Jr, Liu XS et al. 2008 PPARg and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes and Development 22 2941-2952. (doi:10.1101/gad.1709008)
44. Li W, Notani D, Ma Q, Tanasa B, Nunez E, Chen AY, Merkurjev D, Zhang J, Ohgi K, Song X et al. 2013 Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498 516-520. (doi:10.1038/nature12210)
45. Liber D, Domaschenz R, Holmqvist PH, Mazzarella L, Georgiou A, Leleu M, Fisher AG, Labosky PA & Dillon N 2010 Epigenetic priming of a pre-B cell-specific enhancer through binding of Sox2 and Foxd3 at the ESC stage. Cell Stem Cell 7 114-126. (doi:10.1016/j.stem.2010.05.020)
46. Lickwar CR, Mueller F, Hanlon SE, McNally JG & Lieb JD 2012 Genomewide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function. Nature 484 251-255. (doi:10.1038/ nature10985)
47. Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J et al. 2010 A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nature Immunology 11 635-643. (doi:10.1038/ ni.1891)
48. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS & Brown M 2008 Fox A1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132 958-970. (doi:10.1016/j.cell.2008.01.018)
49. Maurya MR, Gupta S, Li X, Fahy E, Dinasarapu AR, Sud M, Brown HA, Glass CK, Murphy RC, Russell DW et al. 2013 Analysis of inflammatory and lipid metabolic networks across RAW264.7 and thioglycolate-elicited macrophages. Journal of Lipid Research542525-2542. (doi:10.1194/jlr.M040212)
50. Medzhitov R & Horng T 2009 Transcriptional control of the inflammatory response. Nature Reviews. Immunology 9 692-703. (doi:10.1038/nri2634)
51. Medzhitov R, Preston-Hurlburt P & Janeway CA Jr 1997 A human homologue of the Drosophila toll protein signals activation of adaptive immunity. Nature 388 394-397. (doi:10.1038/41131)
52. Medzhitov R, Shevach EM, Trinchieri G, Mellor AL, Munn DH, Gordon S, Libby P, Hansson GK, Shortman K, Dong C et al. 2011 Highlights of 10 years of immunology in Nature Reviews Immunology. Nature Reviews. Immunology 11 693-702. (doi:10.1038/nri3063)
53. Meissner F, Scheltema RA, Mollenkopf HJ & Mann M 2013 Direct proteomic quantification of the secretome of activated immune cells. Science 340 475-478. (doi:10.1126/science.1232578)
54. Melo CA, Drost J, Wijchers PJ, van de Werken H, de Wit E, Oude Vrielink JA, Elkon R, Melo SA, Leveille N, Kalluri R et al. 2013 e RNAs are required for p53-dependent enhancer activity and gene transcription. Molecular Cell 49 524-535. (doi:10.1016/j.molcel.2012.11.021)
55. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP et al. 2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 553-560. (doi:10.1038/nature06008)
56. Miranda-Carboni GA, Guemes M, Bailey S, Anaya E, Corselli M, Peault B & Krum SA 2011 GATA4 regulates estrogen receptor-a-mediated osteoblast transcription. Molecular Endocrinology 25 1126-1136. (doi:10.1210/me.2010-0463)
57. Mullen AC, Orlando DA, Newman JJ, Loven J, Kumar RM, Bilodeau S, Reddy J, Guenther MG, De Koter RP & Young RA 2011 Master transcription factors determine cell-type-specific responses to TGF-b signaling. Cell 147 565-576. (doi:10.1016/j.cell.2011.08.050)
58. Murray PJ & Wynn TA 2011 Protective and pathogenic functions of macrophage subsets. Nature Reviews. Immunology 11 723-737. (doi:10.1038/nri3073)
59. Nagy PL, Griesenbeck J, Kornberg RD & Cleary ML 2002 A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. PNAS 99 90-94. (doi:10.1073/pnas.221596698)
60. Nau GJ, Richmond JF, Schlesinger A, Jennings EG, Lander ES & Young RA 2002 Human macrophage activation programs induced by bacterial pathogens. PNAS 99 1503-1508. (doi:10.1073/pnas.022649799)
61. Nerlov C & Graf T 1998 PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes and Development 12 2403-2412. (doi:10.1101/gad.12.15.2403)
62. Ogawa S, Lozach J, Jepsen K, Sawka-Verhelle D, Perissi V, Sasik R, Rose DW, Johnson RS, Rosenfeld MG & Glass CK 2004 A nuclear receptor corepressor transcriptional checkpoint controlling activator protein 1-dependent gene networks required for macrophage activation. PNAS 101 14461-14466. (doi:10.1073/pnas.0405786101)
63. Olefsky JM & Glass CK 2010 Macrophages, inflammation, and insulin resistance. Annual Review of Physiology 72 219-246. (doi:10.1146/ annurev-physiol-021909-135846)
64. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q et al. 2010 Long noncoding RNAs with enhancer-like function in human cells. Cell 143 46-58. (doi:10.1016/j.cell.2010.09.001)
65. Ostuni R, Piccolo V, Barozzi I, Polletti S, Termanini A, Bonifacio S, Curina A, Prosperini E, Ghisletti S & Natoli G 2013 Latent enhancers activated by stimulation in differentiated cells. Cell 152 157-171. (doi:10.1016/ j.cell.2012.12.018)
66. 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 Research 38 4958-4969. (doi:10.1093/nar/gkq244)
67. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD et al. 2006 In vivo enhancer analysis of human conserved non-coding sequences. Nature 444 499-502. (doi:10.1038/nature05295)
68. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C et al. 1998a Defective LPS signaling in C3H/He J and C57BL/10Sc Cr mice: mutations in Tlr4 gene. Science 282 2085-2088. (doi:10.1126/science.282.5396.2085)
69. Poltorak A, Smirnova I, He X, Liu MY, Van Huffel C, McNally O, Birdwell D, Alejos E, Silva M, Du X et al. 1998b Genetic and physical mapping of the Lps locus: identification of the toll-4 receptor as a candidate gene in the critical region. Blood Cells, Molecules & Diseases 24 340-355. (doi:10.1006/bcmd.1998.0201)
70. 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. (doi:10.1038/nature09692)
71. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, Black JC, Hoffmann A, Carey M & Smale ST 2009 A unifying model for the selective regulation of inducible transcription by Cp G islands and nucleosome remodeling. Cell 138 114-128. (doi:10.1016/j.cell.2009. 04.020)
72. Saijo K & Glass CK 2011 Microglial cell origin and phenotypes in health and disease. Nature Reviews. Immunology 11 775-787. (doi:10.1038/ nri3086)
73. Samstein RM, Arvey A, Josefowicz SZ, Peng X, Reynolds A, Sandstrom R, Neph S, Sabo P, Kim JM, Liao Wet al. 2012 Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification. Cell 151 153-166. (doi:10.1016/j.cell.2012.06.053)
74. Scott EW, Simon MC, Anastasi J & Singh H 1994 Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265 1573-1577. (doi:10.1126/science.8079170)
75. Scott EW, Fisher RC, Olson MC, Kehrli EW, Simon MC & Singh H 1997 PU.1 functions in a cell-autonomous manner to control the differentiation of multipotential lymphoid-myeloid progenitors. Immunity 6 437-447. (doi:10.1016/S1074-7613(00)80287-3)
76. Shi C & Pamer EG 2011 Monocyte recruitment during infection and inflammation. Nature Reviews. Immunology 11 762-774. (doi:10.1038/ nri3070)
77. Sica A & Mantovani A 2012 Macrophage plasticity and polarization: in vivo veritas. Journal of Clinical Investigation 122 787-795. (doi:10.1172/JCI59643)
78. Smale ST 2010 Selective transcription in response to an inflammatory stimulus. Cell 140 833-844. (doi:10.1016/j.cell.2010.01.037)
79. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Graf S, Huss M, Keefe D et al. 2011 Open chromatin defined by DNase I and FAIRE identifies regulatory elements that shape cell-type identity. Genome Research 21 1757-1767. (doi:10.1101/gr.121541.111)
80. Spann NJ, Garmire LX, McDonald JG, Myers DS, Milne SB, Shibata N, Reichart D, Fox JN, Shaked I, Heudobler D et al. 2012 Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151 138-152. (doi:10.1016/j.cell. 2012.06.054)
81. Stefflova K, Thybert D, Wilson MD, Streeter I, Aleksic J, Karagianni P, Brazma A, Adams DJ, Talianidis I, Marioni JC et al. 2013 Cooperativity and rapid evolution of cobound transcription factors in closely related mammals. Cell 154 530-540. (doi:10.1016/j.cell.2013.07.007)
82. Stender JD, Pascual G, Liu W, Kaikkonen MU, Do K, Spann NJ, Boutros M, Perrimon N, Rosenfeld MG & Glass CK 2012 Control of proinflammatory gene programs by regulated trimethylation and demethylation of histone H4K20. Molecular Cell 48 28-38. (doi:10.1016/j.molcel.2012. 07.020)
83. Struhl K 2007 Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nature Structural & Molecular Biology 14 103-105. (doi:10.1038/nsmb0207-103)
84. Sullivan AL, Benner C, Heinz S, Huang W, Xie L, Miano JM& Glass CK 2011 Serum response factor utilizes distinct promoter-and enhancer-based mechanisms to regulate cytoskeletal gene expression in macrophages. Molecular and Cellular Biology 31 861-875. (doi:10.1128/MCB.00836-10)
85. Tan SK, Lin ZH, Chang CW, Varang V, Chng KR, Pan YF, Yong EL, Sung WK & Cheung E 2011 AP-2g regulates oestrogen receptor-mediated longrange chromatin interaction and gene transcription. EMBO Journal 30 2569-2581. (doi:10.1038/emboj.2011.151)
86. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC & Harte PJ 2009 CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136 3131-3141. (doi:10.1242/dev.037127)
87. Vahedi G, Takahashi H, Nakayamada S, Sun HW, Sartorelli V, Kanno Y & O'Shea JJ 2012 STATs shape the active enhancer landscape of T cell populations. Cell 151 981-993. (doi:10.1016/j.cell.2012.09.044)
88. Van Dyken SJ & Locksley RM 2013 Interleukin-4-and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annual Review of Immunology 31 317-343. (doi:10.1146/ annurev-immunol-032712-095906)
89. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Afzal V, Rubin EM & Pennacchio LA 2008 Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nature Genetics 40 158-160. (doi:10.1038/ ng.2007.55)
90. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK&Kurokawa R 2008 Induced nc RNAs allostericallymodify RNAbinding proteins in cis to inhibit transcription. Nature 454 126-130. (doi:10.1038/nature06992)
91. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen MU, Ohgi KA et al. 2011 Reprogramming transcription by distinct classes of enhancers functionally defined by e RNA. Nature 474 390-394. (doi:10.1038/nature10006)
92. Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, Foster CT, Cowley SM & Young RA 2012 Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482 221-225. (doi:10.1038/nature10805)
93. 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. Molecular and Cellular Biology 28 7337-7344. (doi:10.1128/MCB.00976-08)
94. Wynn TA, Chawla A & Pollard JW 2013 Macrophage biology in development, homeostasis and disease. Nature 496 445-455. (doi:10.1038/nature12034)
95. Zaret KS & Carroll JS 2011 Pioneer transcription factors: establishing competence for gene expression. Genes and Development 25 2227-2241. (doi:10.1101/gad.176826.111)
96. Zentner GE, Tesar PJ & Scacheri PC 2011 Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Research 21 1273-1283. (doi:10.1101/gr.122382.111)