An overview of microRNAs

Advanced Drug Delivery Reviews - Tập 87 - Trang 3-14 - 2015
Scott M. Hammond1
1Department of Cell Biology and Physiology, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC 27599, USA

Tài liệu tham khảo

Horvitz, 1980, Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans, Genetics, 96, 435, 10.1093/genetics/96.2.435 Lee, 1993, The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14, Cell, 75, 843, 10.1016/0092-8674(93)90529-Y Wightman, 1993, Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans, Cell, 75, 855, 10.1016/0092-8674(93)90530-4 Reinhart, 2000, The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans, Nature, 403, 901, 10.1038/35002607 Pasquinelli, 2000, Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA, Nature, 408, 86, 10.1038/35040556 Fire, 1998, Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 391, 806, 10.1038/35888 Hamilton, 1999, A species of small antisense RNA in posttranscriptional gene silencing in plants, Science, 286, 950, 10.1126/science.286.5441.950 Zamore, 2000, RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals, Cell, 101, 25, 10.1016/S0092-8674(00)80620-0 Hammond, 2000, An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells, Nature, 404, 293, 10.1038/35005107 Hutvagner, 2001, A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA, Science, 293, 834, 10.1126/science.1062961 Grishok, 2001, Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing, Cell, 106, 23, 10.1016/S0092-8674(01)00431-7 Ketting, 2001, Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans, Genes Dev., 15, 2654, 10.1101/gad.927801 Griffiths-Jones, 2006, miRBase: microRNA sequences, targets and gene nomenclature, Nucleic Acids Res., 34, D140, 10.1093/nar/gkj112 Bartel, 2004, MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 116, 281, 10.1016/S0092-8674(04)00045-5 Rodriguez, 2004, Identification of mammalian microRNA host genes and transcription units, Genome Res., 14, 1902, 10.1101/gr.2722704 Poliseno, 2010, Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation, Sci. Signal., 3, ra29, 10.1126/scisignal.2000594 Ventura, 2008, Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters, Cell, 132, 875, 10.1016/j.cell.2008.02.019 Lagos-Quintana, 2001, Identification of novel genes coding for small expressed RNAs, Science, 294, 853, 10.1126/science.1064921 Lau, 2001, An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans, Science, 294, 858, 10.1126/science.1065062 Lee, 2001, An extensive class of small RNAs in Caenorhabditis elegans, Science, 294, 862, 10.1126/science.1065329 Papadopoulos, 2009, The database of experimentally supported targets: a functional update of TarBase, Nucleic Acids Res., 37, D155, 10.1093/nar/gkn809 Lee, 2004, MicroRNA genes are transcribed by RNA polymerase II, EMBO J., 23, 4051, 10.1038/sj.emboj.7600385 Bortolin-Cavaille, 2009, C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts, Nucleic Acids Res., 37, 3464, 10.1093/nar/gkp205 Cai, 2004, Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs, RNA, 10, 1957, 10.1261/rna.7135204 O'Donnell, 2005, c-Myc-regulated microRNAs modulate E2F1 expression, Nature, 435, 839, 10.1038/nature03677 Woods, 2007, Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors, J. Biol. Chem., 282, 2130, 10.1074/jbc.C600252200 Marson, 2008, Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells, Cell, 134, 521, 10.1016/j.cell.2008.07.020 Chang, 2007, Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis, Mol. Cell, 26, 745, 10.1016/j.molcel.2007.05.010 Raver-Shapira, 2007, Transcriptional activation of miR-34a contributes to p53-mediated apoptosis, Mol. Cell, 26, 731, 10.1016/j.molcel.2007.05.017 He, 2007, A microRNA component of the p53 tumour suppressor network, Nature, 447, 1130, 10.1038/nature05939 Georgakilas, 2014, MicroTSS: accurate microRNA transcription start site identification reveals a significant number of divergent pri-miRNAs, Nat. Commun., 5, 5700, 10.1038/ncomms6700 Bhattacharyya, 2012, MicroRNA transcription start site prediction with multi-objective feature selection, Stat. Appl. Genet. Mol. Biol., 11, 10.2202/1544-6115.1743 Ozsolak, 2008, Chromatin structure analyses identify miRNA promoters, Genes Dev., 22, 3172, 10.1101/gad.1706508 Kim, 2009, Biogenesis of small RNAs in animals, Nat. Rev. Mol. Cell Biol., 10, 126, 10.1038/nrm2632 Lee, 2003, The nuclear RNase III Drosha initiates microRNA processing, Nature, 425, 415, 10.1038/nature01957 Lee, 2002, MicroRNA maturation: stepwise processing and subcellular localization, EMBO J., 21, 4663, 10.1093/emboj/cdf476 Ballarino, 2009, Coupled RNA processing and transcription of intergenic primary microRNAs, Mol. Cell. Biol., 29, 5632, 10.1128/MCB.00664-09 Morlando, 2008, Primary microRNA transcripts are processed co-transcriptionally, Nat. Struct. Mol. Biol., 15, 902, 10.1038/nsmb.1475 Han, 2004, The Drosha–DGCR8 complex in primary microRNA processing, Genes Dev., 18, 3016, 10.1101/gad.1262504 Gregory, 2004, The microprocessor complex mediates the genesis of microRNAs, Nature, 432, 235, 10.1038/nature03120 Denli, 2004, Processing of primary microRNAs by the microprocessor complex, Nature, 432, 231, 10.1038/nature03049 Yi, 2003, Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs, Genes Dev., 17, 3011, 10.1101/gad.1158803 Lund, 2004, Nuclear export of microRNA precursors, Science, 303, 95, 10.1126/science.1090599 Bohnsack, 2004, Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs, RNA, 10, 185, 10.1261/rna.5167604 Bernstein, 2001, Role for a bidentate ribonuclease in the initiation step of RNA interference, Nature, 409, 363, 10.1038/35053110 Maniataki, 2005, A human ATP-independent, RISC assembly machine fueled by pre-miRNA, Genes Dev., 19, 2979, 10.1101/gad.1384005 Gregory, 2005, Human RISC couples microRNA biogenesis and posttranscriptional gene silencing, Cell, 123, 631, 10.1016/j.cell.2005.10.022 Gatignol, 2005, Dual role of TRBP in HIV replication and RNA interference: viral diversion of a cellular pathway or evasion from antiviral immunity?, Retrovirology, 2, 65, 10.1186/1742-4690-2-65 Haase, 2005, TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing, EMBO Rep., 6, 961, 10.1038/sj.embor.7400509 Chendrimada, 2005, TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing, Nature, 436, 740, 10.1038/nature03868 Yang, 2011, Widespread regulatory activity of vertebrate microRNA* species, RNA, 17, 312, 10.1261/rna.2537911 Ohanian, 2013, A heterozygous variant in the human cardiac miR-133 gene, MIR133A2, alters miRNA duplex processing and strand abundance, BMC Genet., 14, 18, 10.1186/1471-2156-14-18 Lee, 2010, Complexity of the microRNA repertoire revealed by next-generation sequencing, RNA, 16, 2170, 10.1261/rna.2225110 Marti, 2010, A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing, Nucleic Acids Res., 38, 7219, 10.1093/nar/gkq575 Baran-Gale, 2013, Beta cell 5′-shifted isomiRs are candidate regulatory hubs in type 2 diabetes, PLoS ONE, 8, e73240, 10.1371/journal.pone.0073240 Vickers, 2013, Complexity of microRNA function and the role of isomiRs in lipid homeostasis, J. Lipid Res., 54, 1182, 10.1194/jlr.R034801 Hammond, 2001, Argonaute2, a link between genetic and biochemical analyses of RNAi, Science, 293, 1146, 10.1126/science.1064023 Tabara, 1999, The rde-1 gene, RNA interference, and transposon silencing in C. elegans, Cell, 99, 123, 10.1016/S0092-8674(00)81644-X Matranga, 2005, Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes, Cell, 123, 607, 10.1016/j.cell.2005.08.044 Shin, 2008, Cleavage of the star strand facilitates assembly of some microRNAs into Ago2-containing silencing complexes in mammals, Mol. Cell, 26, 308 Liu, 2009, C3PO, an endoribonuclease that promotes RNAi by facilitating RISC activation, Science, 325, 750, 10.1126/science.1176325 Ye, 2011, Structure of C3PO and mechanism of human RISC activation, Nat. Struct. Mol. Biol., 18, 650, 10.1038/nsmb.2032 Tomari, 2004, RISC assembly defects in the Drosophila RNAi mutant armitage, Cell, 116, 831, 10.1016/S0092-8674(04)00218-1 Meister, 2005, Identification of novel argonaute-associated proteins, Curr. Biol., 15, 2149, 10.1016/j.cub.2005.10.048 Nykanen, 2001, ATP requirements and small interfering RNA structure in the RNA interference pathway, Cell, 107, 309, 10.1016/S0092-8674(01)00547-5 Robb, 2007, RNA helicase A interacts with RISC in human cells and functions in RISC loading, Mol. Cell, 26, 523, 10.1016/j.molcel.2007.04.016 Liu, 2012, Precursor microRNA-programmed silencing complex assembly pathways in mammals, Mol. Cell, 46, 507, 10.1016/j.molcel.2012.03.010 Lai, 2005, Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs, Genes Dev., 19, 1067, 10.1101/gad.1291905 Lewis, 2003, Prediction of mammalian microRNA targets, Cell, 115, 787, 10.1016/S0092-8674(03)01018-3 Jackson, 2003, Expression profiling reveals off-target gene regulation by RNAi, Nat. Biotechnol., 21, 635, 10.1038/nbt831 Grimson, 2007, MicroRNA targeting specificity in mammals: determinants beyond seed pairing, Mol. Cell, 27, 91, 10.1016/j.molcel.2007.06.017 Shin, 2010, Expanding the microRNA targeting code: functional sites with centered pairing, Mol. Cell, 38, 789, 10.1016/j.molcel.2010.06.005 Helwak, 2013, Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding, Cell, 153, 654, 10.1016/j.cell.2013.03.043 Miranda, 2006, A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes, Cell, 126, 1203, 10.1016/j.cell.2006.07.031 Liu, 2004, Argonaute2 is the catalytic engine of mammalian RNAi, Science, 305, 1437, 10.1126/science.1102513 Doench, 2003, siRNAs can function as miRNAs, Genes Dev., 17, 438, 10.1101/gad.1064703 Pfaff, 2013, Argonaute and GW182 proteins: an effective alliance in gene silencing, Biochem. Soc. Trans., 41, 855, 10.1042/BST20130047 Braun, 2013, The role of GW182 proteins in miRNA-mediated gene silencing, Adv. Exp. Med. Biol., 768, 147, 10.1007/978-1-4614-5107-5_9 Fabian, 2012, The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC, Nat. Struct. Mol. Biol., 19, 586, 10.1038/nsmb.2296 Ruby, 2007, Intronic microRNA precursors that bypass Drosha processing, Nature, 448, 83, 10.1038/nature05983 Berezikov, 2007, Mammalian mirtron genes, Mol. Cell, 28, 328, 10.1016/j.molcel.2007.09.028 Okamura, 2007, The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila, Cell, 130, 89, 10.1016/j.cell.2007.06.028 Babiarz, 2008, Mouse ES cells express endogenous shRNAs, siRNAs, and other microprocessor-independent, Dicer-dependent small RNAs, Genes Dev., 22, 2773, 10.1101/gad.1705308 Cheloufi, 2010, A dicer-independent miRNA biogenesis pathway that requires Ago catalysis, Nature, 465, 584, 10.1038/nature09092 Cifuentes, 2010, A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity, Science, 328, 1694, 10.1126/science.1190809 Yang, 2010, Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates, Cell Cycle, 9, 4455, 10.4161/cc.9.22.13958 Diederichs, 2007, Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression, Cell, 131, 1097, 10.1016/j.cell.2007.10.032 Garcia-Silva, 2012, Hints of tRNA-derived small RNAs role in RNA silencing mechanisms, Genes (Basel), 3, 603, 10.3390/genes3040603 Haussecker, 2010, Human tRNA-derived small RNAs in the global regulation of RNA silencing, RNA, 16, 673, 10.1261/rna.2000810 Lee, 2009, A novel class of small RNAs: tRNA-derived RNA fragments (tRFs), Genes Dev., 23, 2639, 10.1101/gad.1837609 Janas, 2012, Alternative RISC assembly: binding and repression of microRNA–mRNA duplexes by human Ago proteins, RNA, 18, 2041, 10.1261/rna.035675.112 Eiring, 2010, miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts, Cell, 140, 652, 10.1016/j.cell.2010.01.007 Paduano, 2013, Protein tyrosine phosphatase PTPRJ is negatively regulated by microRNA-328, FEBS J., 280, 401, 10.1111/j.1742-4658.2012.08624.x Turrini, 2012, MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression, Pharmacogenet. Genomics, 22, 198, 10.1097/FPC.0b013e328350012b Boissonneault, 2009, MicroRNA-298 and microRNA-328 regulate expression of mouse beta-amyloid precursor protein-converting enzyme 1, J. Biol. Chem., 284, 1971, 10.1074/jbc.M807530200 Wang, 2008, MicroRNA miR-328 regulates zonation morphogenesis by targeting CD44 expression, PLoS ONE, 3, e2420, 10.1371/journal.pone.0002420 Chen, 2012, MicroRNA-328 may influence myopia development by mediating the PAX6 gene, Invest. Ophthalmol. Vis. Sci., 53, 2732, 10.1167/iovs.11-9272 Ekimler, 2014, Computational methods for microRNA target prediction, Genes (Basel), 5, 671, 10.3390/genes5030671 Friedman, 2009, Most mammalian mRNAs are conserved targets of microRNAs, Genome Res., 19, 92, 10.1101/gr.082701.108 John, 2004, Human microRNA targets, PLoS Biol., 2, e363, 10.1371/journal.pbio.0020363 Grun, 2005, MicroRNA target predictions across seven Drosophila species and comparison to mammalian targets, PLoS Comput. Biol., 1, e13, 10.1371/journal.pcbi.0010013 Thomas, 2010, Desperately seeking microRNA targets, Nat. Struct. Mol. Biol., 17, 1169, 10.1038/nsmb.1921 Huang, 2010, A study of miRNAs targets prediction and experimental validation, Protein Cell, 1, 979, 10.1007/s13238-010-0129-4 Hafner, 2010, Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP, Cell, 141, 129, 10.1016/j.cell.2010.03.009 Chi, 2009, Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps, Nature, 460, 479, 10.1038/nature08170 Karginov, 2007, A biochemical approach to identifying microRNA targets, Proc. Natl. Acad. Sci. U. S. A., 104, 19291, 10.1073/pnas.0709971104 Leung, 2011, Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs, Nat. Struct. Mol. Biol., 18, 237, 10.1038/nsmb.1991 Riley, 2012, Association of Argonaute proteins and microRNAs can occur after cell lysis, RNA, 18, 1581, 10.1261/rna.034934.112 Orom, 2008, MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation, Mol. Cell, 30, 460, 10.1016/j.molcel.2008.05.001 Lal, 2011, Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling, PLoS Genet., 7, e1002363, 10.1371/journal.pgen.1002363 Eichhorn, 2014, mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues, Mol. Cell, 56, 104, 10.1016/j.molcel.2014.08.028 van Dongen, 2008, Detecting microRNA binding and siRNA off-target effects from expression data, Nat. Methods, 5, 1023, 10.1038/nmeth.1267 Rasmussen, 2013, cWords — systematic microRNA regulatory motif discovery from mRNA expression data, Silence, 4, 2, 10.1186/1758-907X-4-2 Diao, 2014, MixMir: microRNA motif discovery from gene expression data using mixed linear models, Nucleic Acids Res., 42, e135, 10.1093/nar/gku672 Sood, 2006, Cell-type-specific signatures of microRNAs on target mRNA expression, Proc. Natl. Acad. Sci. U. S. A., 103, 2746, 10.1073/pnas.0511045103 Baek, 2008, The impact of microRNAs on protein output, Nature, 455, 64, 10.1038/nature07242 Baskerville, 2005, Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes, RNA, 11, 241, 10.1261/rna.7240905 Sylvestre, 2007, An E2F/miR-20a autoregulatory feedback loop, J. Biol. Chem., 282, 2135, 10.1074/jbc.M608939200 Chen, 2006, The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation, Nat. Genet., 38, 228, 10.1038/ng1725 Niu, 2008, Serum response factor orchestrates nascent sarcomerogenesis and silences the biomineralization gene program in the heart, Proc. Natl. Acad. Sci. U. S. A., 105, 17824, 10.1073/pnas.0805491105 Zhao, 2005, Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis, Nature, 436, 214, 10.1038/nature03817 Liu, 2007, An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133, Proc. Natl. Acad. Sci. U. S. A., 104, 20844, 10.1073/pnas.0710558105 Sweetman, 2008, Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133, Dev. Biol., 321, 491, 10.1016/j.ydbio.2008.06.019 Thomson, 2006, Extensive post-transcriptional regulation of microRNAs and its implications for cancer, Genes Dev., 20, 2202, 10.1101/gad.1444406 Newman, 2008, Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing, RNA, 14, 1539, 10.1261/rna.1155108 Viswanathan, 2008, Selective blockade of microRNA processing by Lin28, Science, 320, 97, 10.1126/science.1154040 Rybak, 2008, A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment, Nat. Cell Biol., 10, 987, 10.1038/ncb1759 Nam, 2011, Molecular basis for interaction of let-7 microRNAs with Lin28, Cell, 147, 1080, 10.1016/j.cell.2011.10.020 Ali, 2012, Recognition of the let-7g miRNA precursor by human Lin28B, FEBS Lett., 586, 3986, 10.1016/j.febslet.2012.09.034 Lightfoot, 2011, A LIN28-dependent structural change in pre-let-7g directly inhibits dicer processing, Biochemistry, 50, 7514, 10.1021/bi200851d Heo, 2009, TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation, Cell, 138, 696, 10.1016/j.cell.2009.08.002 Hagan, 2009, Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells, Nat. Struct. Mol. Biol., 16, 1021, 10.1038/nsmb.1676 Heo, 2008, Lin28 mediates the terminal uridylation of let-7 precursor microRNA, Mol. Cell, 32, 276, 10.1016/j.molcel.2008.09.014 Lehrbach, 2009, LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans, Nat. Struct. Mol. Biol., 16, 1016, 10.1038/nsmb.1675 Towbin, 2013, Systematic screens of proteins binding to synthetic microRNA precursors, Nucleic Acids Res., 41, e47, 10.1093/nar/gks1197 Trabucchi, 2009, The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs, Nature, 459, 1010, 10.1038/nature08025 Guil, 2007, The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a, Nat. Struct. Mol. Biol., 14, 591, 10.1038/nsmb1250 Newman, 2010, Emerging paradigms of regulated microRNA processing, Genes Dev., 24, 1086, 10.1101/gad.1919710 Krol, 2010, The widespread regulation of microRNA biogenesis, function and decay, Nat. Rev. Genet., 11, 597, 10.1038/nrg2843 Bernstein, 2003, Dicer is essential for mouse development, Nat. Genet., 35, 215, 10.1038/ng1253 Wang, 2007, DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal, Nat. Genet., 39, 380, 10.1038/ng1969 Park, 2010, Analysis of microRNA knockouts in mice, Hum. Mol. Genet., 19, R169, 10.1093/hmg/ddq367 Vidigal, 2014, The biological functions of miRNAs: lessons from in vivo studies, Trends Cell Biol., 25, 137, 10.1016/j.tcb.2014.11.004 van Rooij, 2007, Control of stress-dependent cardiac growth and gene expression by a microRNA, Science, 316, 575, 10.1126/science.1139089 van Rooij, 2009, A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance, Dev. Cell, 17, 662, 10.1016/j.devcel.2009.10.013 Kole, 2011, miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis, Genes Dev., 25, 125, 10.1101/gad.1975411 Somel, 2011, MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates, PLoS Biol., 9, e1001214, 10.1371/journal.pbio.1001214 Schratt, 2006, A brain-specific microRNA regulates dendritic spine development, Nature, 439, 283, 10.1038/nature04367 Griggs, 2013, MicroRNA-182 regulates amygdala-dependent memory formation, J. Neurosci., 33, 1734, 10.1523/JNEUROSCI.2873-12.2013 Fazi, 2005, A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis, Cell, 123, 819, 10.1016/j.cell.2005.09.023 Zhou, 2007, miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely, Proc. Natl. Acad. Sci. U. S. A., 104, 7080, 10.1073/pnas.0702409104 Vigorito, 2007, MicroRNA-155 regulates the generation of immunoglobulin class-switched plasma cells, Immunity, 27, 847, 10.1016/j.immuni.2007.10.009 Thai, 2007, Regulation of the germinal center response by microRNA-155, Science, 316, 604, 10.1126/science.1141229 Xiao, 2007, MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb, Cell, 131, 146, 10.1016/j.cell.2007.07.021 Lu, 2008, MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors, Dev. Cell, 14, 843, 10.1016/j.devcel.2008.03.012 Ben-Ami, 2009, A regulatory interplay between miR-27a and Runx1 during megakaryopoiesis, Proc. Natl. Acad. Sci. U. S. A., 106, 238, 10.1073/pnas.0811466106 Dore, 2008, A GATA-1-regulated microRNA locus essential for erythropoiesis, Proc. Natl. Acad. Sci. U. S. A., 105, 3333, 10.1073/pnas.0712312105 Felli, 2005, MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation, Proc. Natl. Acad. Sci. U. S. A., 102, 18081, 10.1073/pnas.0506216102 Johnnidis, 2008, Regulation of progenitor cell proliferation and granulocyte function by microRNA-223, Nature, 451, 1125, 10.1038/nature06607 Taganov, 2006, NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses, Proc. Natl. Acad. Sci. U. S. A., 103, 12481, 10.1073/pnas.0605298103 Garzon, 2006, MicroRNA fingerprints during human megakaryocytopoiesis, Proc. Natl. Acad. Sci. U. S. A., 103, 5078, 10.1073/pnas.0600587103 Thomson, 2004, A custom microarray platform for analysis of microRNA gene expression, Nat. Methods, 1, 47, 10.1038/nmeth704 Liu, 2004, An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues, Proc. Natl. Acad. Sci. U. S. A., 101, 9740, 10.1073/pnas.0403293101 Lu, 2005, MicroRNA expression profiles classify human cancers, Nature, 435, 834, 10.1038/nature03702 Chen, 2005, Real-time quantification of microRNAs by stem–loop RT-PCR, Nucleic Acids Res., 33, e179, 10.1093/nar/gni178 Calin, 2002, Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia, Proc. Natl. Acad. Sci. U. S. A., 99, 15524, 10.1073/pnas.242606799 Esquela-Kerscher, 2006, Oncomirs — microRNAs with a role in cancer, Nat. Rev. Cancer, 6, 259, 10.1038/nrc1840 Kutay, 2006, Downregulation of miR-122 in the rodent and human hepatocellular carcinomas, J. Cell. Biochem., 99, 671, 10.1002/jcb.20982 Girard, 2008, miR-122, a paradigm for the role of microRNAs in the liver, J. Hepatol., 48, 648, 10.1016/j.jhep.2008.01.019 Ota, 2004, Identification and characterization of a novel gene, C13orf25, as a target for 13q31–q32 amplification in malignant lymphoma, Cancer Res., 64, 3087, 10.1158/0008-5472.CAN-03-3773 He, 2005, A microRNA polycistron as a potential human oncogene, Nature, 435, 828, 10.1038/nature03552 Dews, 2006, Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster, Nat. Genet., 38, 1060, 10.1038/ng1855 Lu, 2007, Transgenic over-expression of the microRNA miR-17–92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells, Dev. Biol., 310, 442, 10.1016/j.ydbio.2007.08.007 Bonauer, 2009, The microRNA-17–92 cluster: still a miRacle?, Cell Cycle, 8, 3866, 10.4161/cc.8.23.9994 He, 2007, MicroRNAs join the p53 network—another piece in the tumour-suppression puzzle, Nat. Rev. Cancer, 7, 819, 10.1038/nrc2232 Berindan-Neagoe, 2014, MicroRNAome genome: a treasure for cancer diagnosis and therapy, CA Cancer J. Clin., 64, 311, 10.3322/caac.21244 Barbarotto, 2008, MicroRNAs and cancer: profile, profile, profile, Int. J. Cancer, 122, 969, 10.1002/ijc.23343 Fernandez-Hernando, 2013, MicroRNAs in metabolic disease, Arterioscler. Thromb. Vasc. Biol., 33, 178, 10.1161/ATVBAHA.112.300144 Hsu, 2012, Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver, J. Clin. Invest., 122, 2871, 10.1172/JCI63539 Tsai, 2012, MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis, J. Clin. Invest., 122, 2884, 10.1172/JCI63455 Esau, 2006, miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting, Cell Metab., 3, 87, 10.1016/j.cmet.2006.01.005 Krutzfeldt, 2005, Silencing of microRNAs in vivo with ‘antagomirs’, Nature, 438, 685, 10.1038/nature04303 Marquart, 2010, miR-33 links SREBP-2 induction to repression of sterol transporters, Proc. Natl. Acad. Sci. U. S. A., 107, 12228, 10.1073/pnas.1005191107 Najafi-Shoushtari, 2010, MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis, Science, 328, 1566, 10.1126/science.1189123 Rayner, 2010, MiR-33 contributes to the regulation of cholesterol homeostasis, Science, 328, 1570, 10.1126/science.1189862 Horie, 2010, MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo, Proc. Natl. Acad. Sci. U. S. A., 107, 17321, 10.1073/pnas.1008499107 Poy, 2004, A pancreatic islet-specific microRNA regulates insulin secretion, Nature, 432, 226, 10.1038/nature03076 Poy, 2009, miR-375 maintains normal pancreatic alpha- and beta-cell mass, Proc. Natl. Acad. Sci. U. S. A., 106, 5813, 10.1073/pnas.0810550106 Frost, 2011, Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs, Proc. Natl. Acad. Sci. U. S. A., 108, 21075, 10.1073/pnas.1118922109 Zhu, 2011, The Lin28/let-7 axis regulates glucose metabolism, Cell, 147, 81, 10.1016/j.cell.2011.08.033 Trajkovski, 2011, MicroRNAs 103 and 107 regulate insulin sensitivity, Nature, 474, 649, 10.1038/nature10112 Cullen, 2011, Herpesvirus microRNAs: phenotypes and functions, Curr Opin Virol, 1, 211, 10.1016/j.coviro.2011.04.003 Jopling, 2005, Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA, Science, 309, 1577, 10.1126/science.1113329 Jopling, 2008, Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome, Cell Host Microbe, 4, 77, 10.1016/j.chom.2008.05.013 Shimakami, 2012, Base pairing between hepatitis C virus RNA and microRNA 122 3′ of its seed sequence is essential for genome stabilization and production of infectious virus, J. Virol., 86, 7372, 10.1128/JVI.00513-12 Nelson, 2006, RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain, RNA, 12, 187, 10.1261/rna.2258506 Xi, 2007, Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples, RNA, 13, 1668, 10.1261/rna.642907 Lehmann, 2010, MicroRNA-profiling in formalin-fixed paraffin-embedded specimens, Methods Mol. Biol., 667, 113, 10.1007/978-1-60761-811-9_8 Hayes, 2014, MicroRNAs in cancer: biomarkers, functions and therapy, Trends Mol. Med., 20, 460, 10.1016/j.molmed.2014.06.005 Li, 2013, MicroRNA profile of paclitaxel-resistant serous ovarian carcinoma based on formalin-fixed paraffin-embedded samples, BMC Cancer, 13, 216, 10.1186/1471-2407-13-216 Vecchione, 2013, A microRNA signature defines chemoresistance in ovarian cancer through modulation of angiogenesis, Proc. Natl. Acad. Sci. U. S. A., 110, 9845, 10.1073/pnas.1305472110 Dai, 2011, MicroRNA expression profiles of head and neck squamous cell carcinoma with docetaxel-induced multidrug resistance, Head Neck, 33, 786, 10.1002/hed.21540 Salter, 2008, An integrated approach to the prediction of chemotherapeutic response in patients with breast cancer, PLoS ONE, 3, e1908, 10.1371/journal.pone.0001908 Du, 2013, A high-throughput screen identifies miRNA inhibitors regulating lung cancer cell survival and response to paclitaxel, RNA Biol., 10, 10.4161/rna.26541 Du, 2012, miR-337-3p and its targets STAT3 and RAP1A modulate taxane sensitivity in non-small cell lung cancers, PLoS ONE, 7, e39167, 10.1371/journal.pone.0039167 Asuragen. RosettaGenomics. Pritchard, 2012, MicroRNA profiling: approaches and considerations, Nat. Rev. Genet., 13, 358, 10.1038/nrg3198 Kapranov, 2012, Profiling of short RNAs using Helicos single-molecule sequencing, Methods Mol. Biol., 822, 219, 10.1007/978-1-61779-427-8_15 Gu, 2012, Detection of miRNAs with a nanopore single-molecule counter, Expert. Rev. Mol. Diagn., 12, 573, 10.1586/erm.12.58 Hafner, 2011, RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries, RNA, 17, 1697, 10.1261/rna.2799511 Leshkowitz, 2013, Differences in microRNA detection levels are technology and sequence dependent, RNA, 19, 527, 10.1261/rna.036475.112 Knutsen, 2013, Performance comparison of digital microRNA profiling technologies applied on human breast cancer cell lines, PLoS ONE, 8, e75813, 10.1371/journal.pone.0075813 Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 Mitchell, 2008, Circulating microRNAs as stable blood-based markers for cancer detection, Proc. Natl. Acad. Sci. U. S. A., 105, 10513, 10.1073/pnas.0804549105 Kharaziha, 2012, Tumor cell-derived exosomes: a message in a bottle, Biochim. Biophys. Acta, 1826, 103 Hannafon, 2013, Intercellular communication by exosome-derived microRNAs in cancer, Int. J. Mol. Sci., 14, 14240, 10.3390/ijms140714240 Turchinovich, 2011, Characterization of extracellular circulating microRNA, Nucleic Acids Res., 39, 7223, 10.1093/nar/gkr254 Vickers, 2011, MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins, Nat. Cell Biol., 13, 423, 10.1038/ncb2210 Turchinovich, 2012, Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma, RNA Biol., 9, 1066, 10.4161/rna.21083 Kroh, 2010, Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR), Methods, 50, 298, 10.1016/j.ymeth.2010.01.032 Arroyo, 2011, Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma, Proc. Natl. Acad. Sci. U. S. A., 108, 5003, 10.1073/pnas.1019055108 Hergenreider, 2012, Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs, Nat. Cell Biol., 14, 249, 10.1038/ncb2441 Pegtel, 2010, Functional delivery of viral miRNAs via exosomes, Proc. Natl. Acad. Sci. U. S. A., 107, 6328, 10.1073/pnas.0914843107 Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat. Commun., 2, 282, 10.1038/ncomms1285 Koppers-Lalic, 2014, Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes, Cell Rep., 8, 1649, 10.1016/j.celrep.2014.08.027 Azmi, 2013, Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review, Cancer Metastasis Rev., 32, 623, 10.1007/s10555-013-9441-9 van Rooij, 2014, Development of microRNA therapeutics is coming of age, EMBO Mol. Med., 6, 851, 10.15252/emmm.201100899 Li, 2014, Therapeutic targeting of microRNAs: current status and future challenges, Nat. Rev. Drug Discov., 13, 622, 10.1038/nrd4359 Chen, 2015, In vivo delivery of miRNAs for cancer therapy: challenges and strategies, Adv. Drug Deliv. Rev., 81C, 128, 10.1016/j.addr.2014.05.009 Bader, 2012, miR-34 — a microRNA replacement therapy is headed to the clinic, Front. Genet., 3, 120, 10.3389/fgene.2012.00120 Montgomery, 2014, MicroRNA mimicry blocks pulmonary fibrosis, EMBO Mol. Med., 6, 1347, 10.15252/emmm.201303604 Monroig, 2015, Small molecule compounds targeting miRNAs for cancer therapy, Adv. Drug Deliv. Rev., 81C, 104, 10.1016/j.addr.2014.09.002 Xiao, 2014, A small-molecule modulator of the tumor-suppressor miR34a inhibits the growth of hepatocellular carcinoma, Cancer Res., 74, 6236, 10.1158/0008-5472.CAN-14-0855 Shi, 2013, AC1MMYR2, an inhibitor of dicer-mediated biogenesis of Oncomir miR-21, reverses epithelial–mesenchymal transition and suppresses tumor growth and progression, Cancer Res., 73, 5519, 10.1158/0008-5472.CAN-13-0280 Shum, 2012, An image-based biosensor assay strategy to screen for modulators of the microRNA 21 biogenesis pathway, Comb. Chem. High Throughput Screen., 15, 529, 10.2174/138620712801619131 Connelly, 2014, Identification of inhibitors of microRNA function from small molecule screens, Methods Mol. Biol., 1095, 147, 10.1007/978-1-62703-703-7_12 Gumireddy, 2008, Small-molecule inhibitors of microRNA miR-21 function, Angew. Chem. Int. Ed. Engl., 47, 7482, 10.1002/anie.200801555 Young, 2010, Small molecule modifiers of microRNA miR-122 function for the treatment of hepatitis C virus infection and hepatocellular carcinoma, J. Am. Chem. Soc., 132, 7976, 10.1021/ja910275u Cai, 2014, Targeted genome editing tools for disease modeling and gene therapy, Curr. Gene Ther., 14, 2, 10.2174/156652321402140318165450 Marraffini, 2010, CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea, Nat. Rev. Genet., 11, 181, 10.1038/nrg2749 Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 Jinek, 2013, RNA-programmed genome editing in human cells, Elife, 2, e00471, 10.7554/eLife.00471 Mali, 2013, RNA-guided human genome engineering via Cas9, Science, 339, 823, 10.1126/science.1232033 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 Doudna, 2014, Genome editing. The new frontier of genome engineering with CRISPR-Cas9, Science, 346, 1258096, 10.1126/science.1258096 Long, 2014, Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA, Science, 345, 1184, 10.1126/science.1254445