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Research Paper

MicroRNAs activate gene transcription epigenetically as an enhancer trigger

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Pages 1326-1334 | Received 22 Apr 2015, Accepted 19 Oct 2015, Published online: 30 May 2017

References

  • Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010; 79:351-79; PMID:20533884; https://doi.org/10.1146/annurev-biochem-060308-103103
  • Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012; 13:271-82; PMID:22411466; https://doi.org/10.1038/nrg3162
  • Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-97; PMID:14744438; https://doi.org/10.1016/S0092-8674(04)00045-5
  • Matsui M, Chu Y, Zhang H, Gagnon KT, Shaikh S, Kuchimanchi S, Manoharan M, Corey DR, Janowski BA. Promoter RNA links transcriptional regulation of inflammatory pathway genes. Nucleic Acids Res 2013; 41:10086-109; PMID:23999091; https://doi.org/10.1093/nar/gkt777
  • Majid S, Dar AA, Saini S, Yamamura S, Hirata H, Tanaka Y, Deng G, Dahiya R. MicroRNA-205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 2010; 116:5637-49; PMID:20737563; https://doi.org/10.1002/cncr.25488
  • Huang V, Place RF, Portnoy V, Wang J, Qi Z, Jia Z, Yu A, Shuman M, Yu J, Li LC. Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucleic Acids Res 2012; 40:1695-707; PMID:22053081; https://doi.org/10.1093/nar/gkr934
  • Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A 2008; 105:1608-13; PMID:18227514; https://doi.org/10.1073/pnas.0707594105
  • Guo D, Barry L, Lin SS, Huang V, Li LC. RNAa in action: from the exception to the norm. RNA Biol 2014; 11:1221-5; PMID:25602906; https://doi.org/10.4161/15476286.2014.972853
  • Turner MJ, Jiao AL, Slack FJ. Autoregulation of lin-4 microRNA transcription by RNA activation (RNAa) in C. elegans. Cell Cycle 2014; 13:772-81; PMID:24398561; https://doi.org/10.4161/cc.27679
  • Huang V, Zheng J, Qi Z, Wang J, Place RF, Yu J, Li H, Li LC. Ago1 Interacts with RNA polymerase II and binds to the promoters of actively transcribed genes in human cancer cells. PLoS Genet 2013; 9:e1003821; PMID:24086155; https://doi.org/10.1371/journal.pgen.1003821
  • Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. Interchromosomal associations between alternatively expressed loci. Nature 2005; 435:637-45; PMID:15880101; https://doi.org/10.1038/nature03574
  • Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, Chen Y, Zhao X, Schmidl C, Suzuki T, et al. An atlas of active enhancers across human cell types and tissues. Nature 2014; 507:455-61; PMID:24670763; https://doi.org/10.1038/nature12787
  • Nord AS, Blow MJ, Attanasio C, Akiyama JA, Holt A, Hosseini R, Phouanenavong S, Plajzer-Frick I, Shoukry M, Afzal V, et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 2013; 155:1521-31; PMID:24360275; https://doi.org/10.1016/j.cell.2013.11.033
  • Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013; 153:307-19; PMID:23582322; https://doi.org/10.1016/j.cell.2013.03.035
  • De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL, Natoli G. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 2010; 8:e1000384; PMID:20485488; https://doi.org/10.1371/journal.pbio.1000384
  • 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; PMID:20393465; https://doi.org/10.1038/nature09033
  • 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; PMID:23728302; https://doi.org/10.1038/nature12210
  • Lam MT, 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; PMID:23728303; https://doi.org/10.1038/nature12209
  • Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010; 143:46-58; PMID:20887892; https://doi.org/10.1016/j.cell.2010.09.001
  • 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; PMID:23417068; https://doi.org/10.1038/nature11884
  • Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA, Terragni J, Figueroa ME, De Figueiredo PL, Alberich-Jorda M, Zhang P, et al. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 2013; 503:371-6; PMID:24107992; https://doi.org/10.1038/nature12598
  • Garcia PB, Cai A, Bates JG, Nolla H, Schlissel MS. miR290-5p/292-5p activate the immunoglobulin kappa locus in B cell development. PLoS One 2012; 7:e43805; PMID:22928038; https://doi.org/10.1371/journal.pone.0043805
  • Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. Landscape of transcription in human cells. Nature 2012; 489:101-8; PMID:22955620; https://doi.org/10.1038/nature11233
  • Roberts TC. The MicroRNA biology of the mammalian nucleus. Mol Ther Nucleic Acids 2014; 3:e188; PMID:25137140; https://doi.org/10.1038/mtna.2014.40
  • Chen D, Fu LY, Zhang Z, Li G, Zhang H, Jiang L, Harrison AP, Shanahan HP, Klukas C, Zhang HY, et al. Dissecting the chromatin interactome of microRNA genes. Nucleic Acids Res 2014; 42:3028-43; PMID:24357409; https://doi.org/10.1093/nar/gkt1294
  • Dvinge H, Git A, Graf S, Salmon-Divon M, Curtis C, Sottoriva A, Zhao Y, Hirst M, Armisen J, Miska EA, et al. The shaping and functional consequences of the microRNA landscape in breast cancer. Nature 2013; 497:378-82; PMID:23644459; https://doi.org/10.1038/nature12108
  • Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, Poh HM, Goh Y, Lim J, Zhang J, et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 2012; 148:84-98; PMID:22265404; https://doi.org/10.1016/j.cell.2011.12.014
  • Sanjana NE, Cong L, Zhou Y, Cunniff MM, Feng G, Zhang F. A transcription activator-like effector toolbox for genome engineering. Nat Protoc 2012; 7:171-92; PMID:22222791; https://doi.org/10.1038/nprot.2011.431
  • Mulepati S, Heroux A, Bailey S. Structural biology. Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science 2014; 345:1479-84; PMID:25123481; https://doi.org/10.1126/science.1256996
  • Castanotto D, Lingeman R, Riggs AD, Rossi JJ. CRM1 mediates nuclear-cytoplasmic shuttling of mature microRNAs. Proc Natl Acad Sci U S A 2009; 106:21655-9; PMID:19955415; https://doi.org/10.1073/pnas.0912384106
  • Nishi K, Nishi A, Nagasawa T, Ui-Tei K. Human TNRC6A is an Argonaute-navigator protein for microRNA-mediated gene silencing in the nucleus. Rna 2013; 19:17-35; PMID:23150874; https://doi.org/10.1261/rna.034769.112
  • Tang R, Li L, Zhu D, Hou D, Cao T, Gu H, Zhang J, Chen J, Zhang CY, Zen K. Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res 2012; 22:504-15; PMID:21862971; https://doi.org/10.1038/cr.2011.137
  • Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE. Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 2012; 486:541-4; PMID:22722835; https://doi.org/10.1038/nature11134
  • Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen MU, Ohgi KA, et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 2011; 474:390-4; PMID:21572438; https://doi.org/10.1038/nature10006
  • 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. Proc Natl Acad Sci U S A 2010; 107:21931-6; PMID:21106759; https://doi.org/10.1073/pnas.1016071107
  • Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA. Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res 2012; 22:2497-506; PMID:22960375; https://doi.org/10.1101/gr.143008.112
  • Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009; 459:108-12; PMID:19295514; https://doi.org/10.1038/nature07829
  • Janowski BA, Younger ST, Hardy DB, Ram R, Huffman KE, Corey DR. Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat Chem Biol 2007; 3:166-73; PMID:17259978; https://doi.org/10.1038/nchembio860
  • Yue X, Schwartz JC, Chu Y, Younger ST, Gagnon KT, Elbashir S, Janowski BA, Corey DR. Transcriptional regulation by small RNAs at sequences downstream from 3′ gene termini. Nat Chem Biol 2010; 6:621-9; PMID:20581822; https://doi.org/10.1038/nchembio.400
  • Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, et al. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 2014; 158:607-19; PMID:25083871; https://doi.org/10.1016/j.cell.2014.05.047
  • Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-54; PMID:8252621; https://doi.org/10.1016/0092-8674(93)90529-Y
  • Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993; 75:855-62; PMID:8252622; https://doi.org/10.1016/0092-8674(93)90530-4
  • Ambros V. The functions of animal microRNAs. Nature 2004; 431:350-5; PMID:15372042; https://doi.org/10.1038/nature02871
  • Shenoy A, Blelloch RH. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat Rev Mol Cell Biol 2014; 15:565-76; PMID:25118717; https://doi.org/10.1038/nrm3854