eRNA binding produces tailored CBP activity profiles to regulate gene expression

References

• Kim TK, Shiekhattar R. Architectural and functional commonalities between enhancers and promoters. Cell. 2015;162:948–59. doi:10.1016/j.cell.2015.08.008.
   PubMed Web of Science ®Google Scholar
• Lam MTY, Cho H, Lesch HP, Gosselin D, Heinz S, Tanaka-Oishi Y, Benner C, Kaikkonen MU, Kim AS, Kosaka M, et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature. 2013;498:511–5. doi:10.1038/nature12209.
   PubMed Web of Science ®Google Scholar
• Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010;465:182–7. doi:10.1038/nature 09033.
   PubMed Web of Science ®Google Scholar
• Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA, Shiekhattar R. Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature. 2013;494:497–501. doi:10.1038/nature11884.
   PubMed Web of Science ®Google Scholar
• Li W, Notani D, Ma Q, Tanasa B, Nunez E, Chen AY, Merkurjev D, Zhang J, Ohgi K, Song X, et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 2013;498:516–20. doi:10.1038/nature12210.
   PubMed Web of Science ®Google Scholar
• Melo CA, Drost J, Wijchers PJ, van de Werken H, de Wit E, Oude Vrielink JAF, Elkon R, Melo SA, Léveillé N, Kalluri R, et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell. 2013;49:524–35. doi:10.1016/j.molcel.2012.11.021.
   PubMed Web of Science ®Google Scholar
• Mousavi K, Zare H, Dell'Orso S, Grontved L, Gutierrez-Cruz G, Derfoul A, Hager GL, Sartorelli V. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol Cell. 2013;51:606–17. doi:10.1016/j.molcel.2013.07.022.
   PubMed Web of Science ®Google Scholar
• Hsieh CL, Fei T, Chen Y, Li T, Gao Y, Wang X, Sun T, Sweeney CJ, Lee GSM, Chen S, et al. Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. Proc Natl Acad Sci. 2014;111:7319–24. doi:10.1073/pnas.1324151111.
   PubMed Web of Science ®Google Scholar
• Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, Kim T-K. Enhancer RNA facilitates NELF release from immediate early genes. Mol Cell. 2014;56:29–42. doi:10.1016/j.molcel.2014.08.023.
   PubMed Web of Science ®Google Scholar
• Kaikkonen MU, Spann NJ, Heinz S, Romanoski CE, Allison KA, Stender JD, Chun HB, Tough DF, Prinjha RK, Benner C, et al. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol Cell. 2013;51:310–25. doi:10.1016/j.molcel.2013.07.010.
   PubMed Web of Science ®Google Scholar
• Wang L, Tang Y, Cole PA, Marmorstein R. Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: Implications for histone acetyltransferase evolution and function. Curr Opin Struct Biol. 2008;18:741–7. doi:10.1016/j.sbi.2008.09.004.
   PubMed Web of Science ®Google Scholar
• Delvecchio M, Gaucher J, Aguilar-Gurrieri C, Ortega E, Panne D. Structure of the p300 catalytic core and implications for chromatin targeting and HAT regulation. Nat Struct Biol. 2013;20:1040–6. doi:10.1038/nsmb.2642.
   Google Scholar
• Bedford DC, Kasper LH, Fukuyama T, Brindle PK. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics. 2010;5:9–15. doi:10.4161/epi.5.1.10449.
   PubMed Web of Science ®Google Scholar
• Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. PNAS. 2010;107:21931–6. doi:10.1073/pnas.1016071107.
   PubMed Web of Science ®Google Scholar
• May D, Blow MJ, Kaplan T, McCulley DJ, Jensen BC, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, et al. Large-scale discovery of enhancers from human heart tissue. Nat Genet. 2012;44:89–93. doi:10.1038/ng.1006
   Web of Science ®Google Scholar
• Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol. 2015;33:510–7. doi:10.1038/nbt.3199.
   PubMed Web of Science ®Google Scholar
• Jin Q, Yu LR, Wang L, Zhang Z, Kasper LH, Lee J-E, Wang C, Brindle PK, Dent SYR, Ge K. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 2011;30:249–62. doi:10.1038/emboj.2010.318.
   PubMed Web of Science ®Google Scholar
• He C, Sidoli S, Warneford-Thomson R, Tatomer DC, Wilusz JE, Garcia BA, Bonasio R. High-resolution mapping of RNA-binding regions in the nuclear proteome of embryonic stem cells. Mol Cell. 2016;64:416–30. doi:10.1016/j.molcel.2016.09.034.
   PubMed Web of Science ®Google Scholar
• Castello A, Fischer B, Frese CK, Horos R, Alleaume A-M, Foehr S, Curk T, Krijgsveld J, Hentze MW. Comprehensive identification of RNA-binding domains in human cells. Mol Cell. 2016;63:696–710. doi:10.1016/j.molcel.2016.06.029.
   PubMed Web of Science ®Google Scholar
• G Hendrickson D, Kelley DR, Tenen D, Bernstein B, Rinn JL. Widespread RNA binding by chromatin-associated proteins. Genome Biol. 2016;17:28. doi:10.1186/s13059-016-0878-3.
   PubMed Web of Science ®Google Scholar
• Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA, Terragni J, Figueroa ME, De Figueiredo Pontes LL, Alberich-Jorda M, Zhang P, et al. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature. 2013;503:371–6. doi:10.1038/nature12598.
   PubMed Web of Science ®Google Scholar
• Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT. Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell. 2014;55:171–85. doi:10.1016/j.molcel.2014.05.009.
   PubMed Web of Science ®Google Scholar
• Davidovich C, Zheng L, Goodrich KJ, Cech TR. Promiscuous RNA binding by Polycomb repressive complex 2. Nat Struct Biol. 2013;20:1250–7. doi:10.1038/nsmb.2679.
   Google Scholar
• Kaneko S, Bonasio R, Saldaña-Meyer R, Yoshida T, Son J, Nishino K, Umezawa A, Reinberg D. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol Cell. 2014;53:290–300. doi:10.1016/j.molcel.2013.11.012.
   PubMed Web of Science ®Google Scholar
• Beltran M, Yates CM, Skalska L, Dawson M, Reis FP, Viiri K, Fisher CL, Sibley CR, Foster BM, Bartke T, et al. The interaction of PRC2 with RNA or chromatin is mutually antagonistic. Genome Res. 2016;26:896–907. doi:10.1101/gr.197632.115.
   PubMed Web of Science ®Google Scholar
• Kaneko S, Son J, Bonasio R, Shen SS, Reinberg D. Nascent RNA interaction keeps PRC2 activity poised and in check. Genes Dev. 2014;28:1983–8. doi:10.1101/gad.247940.114.
   PubMed Web of Science ®Google Scholar
• Wongtrakoongate P, Riddick G, Fucharoen S, Felsenfeld G. Association of the long non-coding RNA Steroid Receptor RNA Activator (SRA) with TrxG and PRC2 complexes. PLoS Genet. 2015;11:e1005615. doi:10.1371/journal.pgen.1005615.
   PubMed Web of Science ®Google Scholar
• Yang YW, Flynn RA, Chen Y, Qu K, Wan B, Wang KC, Lei M, Chang HY. Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. Elife. 2014;3:e02046. doi:10.7554/eLife.02046.
   PubMed Web of Science ®Google Scholar
• Bose DA, Donahue G, Reinberg D, Shiekhattar R, Bonasio R, Berger SL. RNA binding to CBP stimulates histone acetylation and transcription. Cell. 2017;168:135–149.e22. doi:10.1016/j.cell.2016.12.020.
   PubMed Web of Science ®Google Scholar
• Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp A-C, Munschauer M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141:129–41. doi:10.1016/j.cell.2010.03.009.
   PubMed Web of Science ®Google Scholar
• Huppertz I, Attig J, D'Ambrogio A, Easton LE, Sibley CR, Sugimoto Y, Tajnik M, König J, Ule J. iCLIP: Protein-RNA interactions at nucleotide resolution. Methods. 2014;65:274–87. doi:10.1016/j.ymeth.2013.10.011.
   PubMed Web of Science ®Google Scholar
• Thompson PR, Wang D, Wang L, Fulco M, Pediconi N, Zhang D, An W, Ge Q, Roeder RG, Wong J, et al. Regulation of the p300 HAT domain via a novel activation loop. Nat Struct Biol. 2004;11:308–15. doi:10.1038/nsmb740.
   Google Scholar
• Kasper LH, Qu C, Obenauer JC, McGoldrick DJ, Brindle PK. Genome-wide and single-cell analyses reveal a context dependent relationship between CBP recruitment and gene expression. NAR. 2014;42:11363–82. doi:10.1093/nar/gku827.
   PubMed Web of Science ®Google Scholar