High constitutive activity of a broad panel of housekeeping and tissue-specific cis-regulatory elements depends on a subset of ETS proteins

Genes and Development

Volumn 31, Issue 4, 2017, Pages 399-412

  Curina, Alessia ^a   Termanini, Alberto ^b   Barozzi, Iros ^a,d   Prosperini, Elena ^a   Simonatto, Marta ^a   Polletti, Sara ^a   Silvola, Alessio ^a   Soldi, Monica ^a   Austenaa, Liv ^a   Bonaldi, Tiziana ^a   Ghisletti, Serena ^b   Natoli, Gioacchino ^a,c  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c HUMANITAS UNIVERSITY   (Italy)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Enhancers; ETS; Housekeeping genes; Macrophages; Transcription

Indexed keywords

TRANSCRIPTION FACTOR ETS; CHROMATIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; BASE PAIRING; CHROMATIN; ENHANCER REGION; GENETIC TRANSCRIPTION; HOUSEKEEPING GENE; MACROPHAGE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY SEQUENCE; TRANSCRIPTION INITIATION; ANIMAL; C57BL MOUSE; ESSENTIAL GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CHROMATIN; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENES, ESSENTIAL; MACROPHAGES; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSCRIPTION FACTORS;

EID: 85015748301     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.293134.116     Document Type: Article

References (50)

1. Austenaa LM, Barozzi I, Simonatto M, Masella S, Della Chiara G, Ghisletti S, Curina A, de Wit E, Bouwman BA, de Pretis S, et al. 2015. Transcription of mammalian cis-regulatory elements is restrained by actively enforced early termination. Mol Cell 60: 460–474.
2. Barozzi I, Simonatto M, Bonifacio S, Yang L, Rohs R, Ghisletti S, Natoli G. 2014. Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers. Mol Cell 54: 844–857.
3. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10: 1213–1218.
4. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engstrom PG, Frith MC, et al. 2006. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 38: 626–635.
5. Core LJ, Martins AL, Danko CG, Waters CT, Siepel A, Lis JT. 2014. Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat Genet 46: 1311–1320.
6. 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. Proc Natl Acad Sci 107: 21931–21936.
7. Deng W, Roberts SG. 2005. A core promoter element downstream of the TATA box that is recognized by TFIIB. Genes Dev 19: 2418–2423.
8. 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. PLoS Biol 8: e1000384.
9. Farley EK, Olson KM, Zhang W, Brandt AJ, Rokhsar DS, Levine MS. 2015. Suboptimization of developmental enhancers. Science 350: 325–328.
10. Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ, Innocenti C, Ferrier P, Spicuglia S, Gut M, Gut I, et al. 2012. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res 22: 2399–2408.
11. FitzGerald PC, Shlyakhtenko A, Mir AA, Vinson C. 2004. Clustering of DNA sequences in human promoters. Genome Res 14: 1562–1574.
12. FitzGerald PC, Sturgill D, Shyakhtenko A, Oliver B, Vinson C. 2006. Comparative genomics of Drosophila and human core promoters. Genome Biol 7: R53.
13. Frith MC, Valen E, Krogh A, Hayashizaki Y, Carninci P, Sandelin A. 2008. A code for transcription initiation in mammalian genomes. Genome Res 18: 1–12.
14. Gallant S, Gilkeson G. 2006. ETS transcription factors and regulation of immunity. Arch Immunol Ther Exp (Warsz) 54: 149–163.
15. Gardini A, Baillat D, Cesaroni M, Hu D, Marinis JM, Wagner EJ, Lazar MA, Shilatifard A, Shiekhattar R. 2014. Integrator regulates transcriptional initiation and pause release following activation. Mol Cell 56: 128–139.
16. 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.
17. Gilmour J, Assi SA, Jaegle U, Kulu D, van de Werken H, Clarke D, Westhead DR, Philipsen S, Bonifer C. 2014. A crucial role for the ubiquitously expressed transcription factor Sp1 at early stages of hematopoietic specification. Development 141: 2391–2401.
18. Glass CK, Natoli G. 2016. Molecular control of activation and priming in macrophages. Nat Immunol 17: 26–33.
19. Goldberg ML. 1979. “Sequence analysis of Drosophila histone genes.” PhD thesis, Stanford University, San Francisco.
20. Goode DK, Obier N, Vijayabaskar MS, Lie ALM, Lilly AJ, Hannah R, Lichtinger M, Batta K, Florkowska M, Patel R, et al. 2016. Dynamic gene regulatory networks drive hematopoietic specification and differentiation. Dev Cell 36: 572–587.
21. Guzman-Ayala M, Sachs M, Koh FM, Onodera C, Bulut-Karslioglu A, Lin CJ, Wong P, Nitta R, Song JS, Ramalho-Santos M. 2015. Chd1 is essential for the high transcriptional output and rapid growth of the mouse epiblast. Development 142: 118–127.
22. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576–589.
23. Hollenhorst PC, McIntosh LP, Graves BJ. 2011. Genomic and biochemical insights into the specificity of ETS transcription factors. Annu Rev Biochem 80: 437–471.
24. Juven-Gershon T, Hsu JY, Kadonaga JT. 2006. Perspectives on the RNA polymerase II core promoter. Biochem Soc Trans 34: 1047–1050.
25. Kadonaga JT. 2012. Perspectives on the RNA polymerase II core promoter. Wiley Interdiscip Rev Dev Biol 1: 40–51.
26. 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. Mol Cell 51: 310–325.
27. 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.
28. Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH. 1998. New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12: 34–44.
29. Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E, Keren-Shaul H, Mildner A, Winter D, Jung S, et al. 2014. Immunogenetics. Chromatin state dynamics during blood formation. Science 345: 943–949.
30. Lichtinger M, Ingram R, Hannah R, Muller D, Clarke D, Assi SA, Lie ALM, Noailles L, Vijayabaskar MS, Wu M, et al. 2012. RUNX1 reshapes the epigenetic landscape at the onset of haematopoiesis. EMBO J 31: 4318–4333.
31. Lifton RP, Goldberg ML, Karp RW, Hogness DS. 1978. The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harb Symp Quant Biol 42: 1047–1051.
32. Mancino A, Termanini A, Barozzi I, Ghisletti S, Ostuni R, Prosperini E, Ozato K, Natoli G. 2015. A dual cis-regulatory code links IRF8 to constitutive and inducible gene expression in macrophages. Genes Dev 29: 394–408.
33. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28: 495–501.
34. 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.
35. Ponjavic J, Lenhard B, Kai C, Kawai J, Carninci P, Hayashizaki Y, Sandelin A. 2006. Transcriptional and structural impact of TATA-initiation site spacing in mammalian core promoters. Genome Biol 7: R78.
36. 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.
37. Sanjana NE, Shalem O, Zhang F. 2014. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods 11: 783–784.
38. Schumacher MA, Lau AO, Johnson PJ. 2003. Structural basis of core promoter recognition in a primitive eukaryote. Cell 115: 413–424.
39. Shlyueva D, Stampfel G, Stark A. 2014. Transcriptional enhancers: from properties to genome-wide predictions. Nat Rev Genet 15: 272–286.
40. Skene PJ, Hernandez AE, Groudine M, Henikoff S. 2014. The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. Elife 3: e02042.
41. Smale ST, Baltimore D. 1989. The ‘initiator’ as a transcription control element. Cell 57: 103–113.
42. Spitz F, Furlong EE. 2012. Transcription factors: from enhancer binding to developmental control. Nat Rev Genet 13: 613–626.
43. Stadelmayer B, Micas G, Gamot A, Martin P, Malirat N, Koval S, Raffel R, Sobhian B, Severac D, Rialle S, et al. 2014. Integrator complex regulates NELF-mediated RNA polymerase II pause/ release and processivity at coding genes. Nat Commun 5: 5531.
44. Tippmann SC, Ivanek R, Gaidatzis D, Scholer A, Hoerner L, van Nimwegen E, Stadler PF, Stadler MB, Schubeler D. 2012. Chromatin measurements reveal contributions of synthesis and decay to steady-state mRNA levels. Mol Syst Biol 8: 593.
45. 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 eRNA. Nature 474: 390–394.
46. Wei GH, Badis G, Berger MF, Kivioja T, Palin K, Enge M, Bonke M, Jolma A, Varjosalo M, Gehrke AR, et al. 2010. Genomewide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J 29: 2147–2160.
47. Weis L, Reinberg D. 1997. Accurate positioning of RNA polymerase II on a natural TATA-less promoter is independent of TATA-binding-protein-associated factors and initiator-binding proteins. Mol Cell Biol 17: 2973–2984.
48. ′ UTRs by comparison of several mammals. Nature 434: 338–345.
49. Yang C, Bolotin E, Jiang T, Sladek FM, Martinez E. 2007. Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters. Gene 389: 52–65.
50. Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227–2241.