The widespread regulation of microRNA biogenesis, function and decay (original) (raw)

• Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Carthew, R. W. & Sontheimer, E. J. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655 (2009).
  CAS PubMed PubMed Central Google Scholar
• Chekulaeva, M. & Filipowicz, W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21, 452–460 (2009).
  CAS PubMed Google Scholar
• Fabian, M. R., Sonenberg, N. & Filipowicz, W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351–379 (2010).
  CAS PubMed Google Scholar
• Kim, V. N., Han, J. & Siomi, M. C. Biogenesis of small RNAs in animals. Nature Rev. Mol. Cell Biol. 10, 126–139 (2009).
  CAS Google Scholar
• Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669–687 (2009).
  CAS PubMed Google Scholar
• Davis, B. N. & Hata, A. Regulation of microRNA biogenesis: a miRiad of mechanisms. Cell Commun. Signal 7, 18 (2009).
  PubMed PubMed Central Google Scholar
• Turner, M. J. & Slack, F. J. Transcriptional control of microRNA expression in C. elegans: promoting better understanding. RNA Biol. 6, 49–53 (2009).
  CAS PubMed Google Scholar
• Kim, J. et al. A microRNA feedback circuit in midbrain dopamine neurons. Science 317, 1220–1224 (2007).
  CAS PubMed PubMed Central Google Scholar
• Johnston, R. J. Jr, Chang, S., Etchberger, J. F., Ortiz, C. O. & Hobert, O. MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc. Natl Acad. Sci. USA 102, 12449–12454 (2005). Identified a double-negative feedback circuit between miRNAs and transcription factors that is essential for neuronal cell fate determination.
  CAS PubMed PubMed Central Google Scholar
• Stark, A. et al. A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev. 22, 8–13 (2008).
  CAS PubMed PubMed Central Google Scholar
• Tyler, D. M. et al. Functionally distinct regulatory RNAs generated by bidirectional transcription and processing of microRNA loci. Genes Dev. 22, 26–36 (2008).
  CAS PubMed PubMed Central Google Scholar
• Han, J. et al. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136, 75–84 (2009).
  CAS PubMed PubMed Central Google Scholar
• Triboulet, R., Chang, H. M., Lapierre, R. J. & Gregory, R. I. Post-transcriptional control of DGCR8 expression by the Microprocessor. RNA 15, 1005–1011 (2009). References 13 and 14 identified reciprocal co-regulation between Drosha and DGCR8 proteins.
  CAS PubMed PubMed Central Google Scholar
• Gregory, R. I. et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235–240 (2004).
  CAS PubMed Google Scholar
• Faller, M., Matsunaga, M., Yin, S., Loo, J. A. & Guo, F. Heme is involved in microRNA processing. Nature Struct. Mol. Biol. 14, 23–29 (2007).
  CAS Google Scholar
• Chendrimada, T. P. et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744 (2005).
  CAS PubMed PubMed Central Google Scholar
• Melo, S. A. et al. A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nature Genet. 41, 365–370 (2009).
  CAS PubMed Google Scholar
• Paroo, Z., Ye, X., Chen, S. & Liu, Q. Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 139, 112–122 (2009). Established the link between a major cell signalling pathway and the miRNA machinery, showing that mitogenic stimulation mediated by MAPK/ERK is associated with TRBP phosphorylation and leads to upregulation of growth-promoting miRNAs.
  CAS PubMed PubMed Central Google Scholar
• Forman, J. J., Legesse-Miller, A. & Coller, H. A. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl Acad. Sci. USA 105, 14879–14884 (2008).
  CAS PubMed PubMed Central Google Scholar
• Davalos, V. & Esteller, M. MicroRNAs and cancer epigenetics: a macrorevolution. Curr. Opin. Oncol. 22, 35–45 (2010).
  CAS PubMed Google Scholar
• Ma, E., MacRae, I. J., Kirsch, J. F. & Doudna, J. A. Autoinhibition of human dicer by its internal helicase domain. J. Mol. Biol. 380, 237–243 (2008).
  CAS PubMed PubMed Central Google Scholar
• Lugli, G., Larson, J., Martone, M. E., Jones, Y. & Smalheiser, N. R. Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. J. Neurochem. 94, 896–905 (2005).
  CAS PubMed Google Scholar
• Zhang, H., Kolb, F. A., Brondani, V., Billy, E. & Filipowicz, W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 21, 5875–5885 (2002).
  CAS PubMed PubMed Central Google Scholar
• Nakagawa, A., Shi, Y., Kage-Nakadai, E., Mitani, S. & Xue, D. Caspase-dependent conversion of Dicer ribonuclease into a death-promoting deoxyribonuclease. Science 328, 327–334 (2010).
  CAS PubMed PubMed Central Google Scholar
• Chiang, H. R. et al. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev. 24, 992–1009 (2010).
  CAS PubMed PubMed Central Google Scholar
• Frank, F., Sonenberg, N. & Nagar, B. Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818–822 (2010).
  CAS PubMed Google Scholar
• Krol, J. et al. Structural features of microRNA (miRNA) precursors and their relevance to miRNA biogenesis and small interfering RNA/short hairpin RNA design. J. Biol. Chem. 279, 42230–42239 (2004).
  CAS PubMed Google Scholar
• Ro, S., Park, C., Young, D., Sanders, K. M. & Yan, W. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res. 35, 5944–5953 (2007).
  CAS PubMed PubMed Central Google Scholar
• Winter, J., Jung, S., Keller, S., Gregory, R. I. & Diederichs, S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nature Cell Biol. 11, 228–234 (2009).
  CAS PubMed Google Scholar
• Viswanathan, S. R. & Daley, G. Q. Lin28: A microRNA regulator with a macro role. Cell 140, 445–459 (2010).
  CAS PubMed Google Scholar
• Rybak, A. et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nature Cell Biol. 10, 987–993 (2008).
  CAS PubMed Google Scholar
• Lehrbach, N. J. et al. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nature Struct. Mol. Biol. 16, 1016–1020 (2009).
  CAS Google Scholar
• Hagan, J. P., Piskounova, E. & Gregory, R. I. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nature Struct. Mol. Biol. 16, 1021–1025 (2009).
  CAS Google Scholar
• Heo, I. et al. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell 32, 276–284 (2008). Describes uridylation of pre-let-7 mediated by LIN-28. References 33, 36 and 37 identified TUTases involved in this process.
  CAS PubMed Google Scholar
• Heo, I. et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138, 696–708 (2009).
  CAS PubMed Google Scholar
• Jones, M. R. et al. Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nature Cell Biol. 11, 1157–1163 (2009).
  CAS PubMed Google Scholar
• Viswanathan, S. R., Daley, G. Q. & Gregory, R. I. Selective blockade of microRNA processing by Lin28. Science 320, 97–100 (2008).
  CAS PubMed PubMed Central Google Scholar
• Roush, S. & Slack, F. J. The let-7 family of microRNAs. Trends Cell Biol. 18, 505–516 (2008).
  CAS PubMed Google Scholar
• Viswanathan, S. R. et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nature Genet. 41, 843–848 (2009).
  CAS PubMed Google Scholar
• Fukuda, T. et al. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nature Cell Biol. 9, 604–611 (2007).
  CAS PubMed Google Scholar
• Suzuki, H. I. et al. Modulation of microRNA processing by p53. Nature 460, 529–533 (2009).
  CAS PubMed Google Scholar
• Davis, B. N., Hilyard, A. C., Lagna, G. & Hata, A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454, 56–61 (2008).
  CAS PubMed PubMed Central Google Scholar
• Yu, B. et al. The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc. Natl Acad. Sci. USA 105, 10073–10078 (2008).
  CAS PubMed PubMed Central Google Scholar
• Bracken, C. P. et al. Regulation of cyclin D1 RNA stability by SNIP1. Cancer Res. 68, 7621–7628 (2008).
  CAS PubMed PubMed Central Google Scholar
• Pawlicki, J. M. & Steitz, J. A. Nuclear networking fashions pre-messenger RNA and primary microRNA transcripts for function. Trends Cell Biol. 20, 52–61 (2010).
  CAS PubMed Google Scholar
• Gruber, J. J. et al. Ars2 links the nuclear cap-binding complex to RNA interference and cell proliferation. Cell 138, 328–339 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sabin, L. R. et al. Ars2 regulates both miRNA- and siRNA- dependent silencing and suppresses RNA virus infection in Drosophila. Cell 138, 340–351 (2009).
  CAS PubMed PubMed Central Google Scholar
• Laubinger, S. et al. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 105, 8795–8800 (2008).
  CAS PubMed PubMed Central Google Scholar
• Wu, H. et al. A splicing-independent function of SF2/ASF in microRNA processing. Mol. Cell 38, 67–77 (2010).
  CAS PubMed PubMed Central Google Scholar
• Michlewski, G., Guil, S., Semple, C. A. & Caceres, J. F. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol. Cell 32, 383–393 (2008).
  CAS PubMed PubMed Central Google Scholar
• Trabucchi, M. et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459, 1010–1014 (2009). References 51 and 52 identified regulators that bind to miRNA precursors and stimulate their processing.
  CAS PubMed PubMed Central Google Scholar
• Scadden, A. D. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nature Struct. Mol. Biol. 12, 489–496 (2005).
  CAS Google Scholar
• Kawahara, Y., Zinshteyn, B., Chendrimada, T. P., Shiekhattar, R. & Nishikura, K. RNA editing of the microRNA-151 precursor blocks cleavage by the Dicer–TRBP complex. EMBO Rep. 8, 763–769 (2007).
  CAS PubMed PubMed Central Google Scholar
• Kawahara, Y. et al. Frequency and fate of microRNA editing in human brain. Nucleic Acids Res. 36, 5270–5280 (2008).
  CAS PubMed PubMed Central Google Scholar
• Heale, B. S. et al. Editing independent effects of ADARs on the miRNA/siRNA pathways. EMBO J. 28, 3145–3156 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kawahara, Y. et al. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 315, 1137–1140 (2007). Describes a change in targeting specificity of miRNA induced by pre-miRNA editing.
  CAS PubMed PubMed Central Google Scholar
• Ghildiyal, M., Xu, J., Seitz, H., Weng, Z. & Zamore, P. D. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 16, 43–56 (2010).
  CAS PubMed PubMed Central Google Scholar
• Czech, B. et al. Hierarchical rules for Argonaute loading in Drosophila. Mol. Cell 36, 445–456 (2009).
  CAS PubMed PubMed Central Google Scholar
• Okamura, K., Liu, N. & Lai, E. C. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol. Cell 36, 431–444 (2009).
  CAS PubMed PubMed Central Google Scholar
• Iwasaki, S., Kawamata, T. & Tomari, Y. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol. Cell 34, 58–67 (2009).
  CAS PubMed Google Scholar
• Su, H., Trombly, M. I., Chen, J. & Wang, X. Essential and overlapping functions for mammalian Argonautes in microRNA silencing. Genes Dev. 23, 304–317 (2009).
  CAS PubMed PubMed Central Google Scholar
• Azuma-Mukai, A. et al. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc. Natl Acad. Sci. USA 105, 7964–7969 (2008).
  CAS PubMed PubMed Central Google Scholar
• Ender, C. et al. A human snoRNA with microRNA-like functions. Mol. Cell 32, 519–528 (2008).
  CAS PubMed Google Scholar
• Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129–141 (2010).
  CAS PubMed PubMed Central Google Scholar
• Cheloufi, S., Dos Santos, C. O., Chong, M. M. & Hannon, G. J. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465, 584–589 (2010).
  CAS PubMed PubMed Central Google Scholar
• Cifuentes, D. et al. A Novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328, 1694–1698 (2010).
  CAS PubMed PubMed Central Google Scholar
• O'Carroll, D. et al. A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev. 21, 1999–2004 (2007).
  CAS PubMed PubMed Central Google Scholar
• Wu, L., Fan, J. & Belasco, J. G. Importance of translation and nonnucleolytic ago proteins for on-target RNA interference. Curr. Biol. 18, 1327–1332 (2008).
  CAS PubMed PubMed Central Google Scholar
• Diederichs, S. & Haber, D. A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 131, 1097–1108 (2007).
  CAS PubMed Google Scholar
• Johnston, M., Geoffroy, M. C., Sobala, A., Hay, R. & Hutvagner, G. HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells. Mol. Biol. Cell 21, 1462–1469 (2010).
  CAS PubMed PubMed Central Google Scholar
• Tahbaz, N., Carmichael, J. B. & Hobman, T. C. GERp95 belongs to a family of signal-transducing proteins and requires Hsp90 activity for stability and Golgi localization. J. Biol. Chem. 276, 43294–43299 (2001).
  CAS PubMed Google Scholar
• Qi, H. H. et al. Prolyl 4-hydroxylation regulates Argonaute 2 stability. Nature 455, 421–424 (2008).
  CAS PubMed PubMed Central Google Scholar
• Rybak, A. et al. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nature Cell Biol. 11, 1411–1420 (2009).
  CAS PubMed Google Scholar
• Zeng, Y., Sankala, H., Zhang, X. & Graves, P. R. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J. 413, 429–436 (2008).
  CAS PubMed Google Scholar
• Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I. & Filipowicz, W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111–1124 (2006). This paper and reference 97 were the first studies to show that RBPs interacting with the mRNA 3′-UTR can relieve or prevent miRNA-mediated repression.
  CAS PubMed Google Scholar
• Leung, A. K. & Sharp, P. A. microRNAs: a safeguard against turmoil? Cell 130, 581–585 (2007).
  CAS PubMed Google Scholar
• Djuranovic, S. et al. Allosteric regulation of Argonaute proteins by miRNAs. Nature Struct. Mol. Biol. 17, 144–150 (2010).
  CAS Google Scholar
• Kiriakidou, M. et al. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 129, 1141–1151 (2007).
  CAS PubMed Google Scholar
• Eulalio, A., Huntzinger, E. & Izaurralde, E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nature Struct. Mol. Biol. 15, 346–353 (2008).
  CAS Google Scholar
• Wang, Y. et al. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754–761 (2009).
  CAS PubMed PubMed Central Google Scholar
• Eulalio, A., Tritschler, F. & Izaurralde, E. The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA 15, 1433–1442 (2009).
  CAS PubMed PubMed Central Google Scholar
• Li, S. et al. Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago2-mediated silencing. J. Cell Sci. 121, 4134–4144 (2008).
  CAS PubMed Google Scholar
• Eystathioy, T. et al. A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol. Biol. Cell 13, 1338–1351 (2002).
  CAS PubMed PubMed Central Google Scholar
• Yang, Z. et al. GW182 is critical for the stability of GW bodies expressed during the cell cycle and cell proliferation. J. Cell Sci. 117, 5567–5578 (2004).
  CAS PubMed Google Scholar
• Gibbings, D. J., Ciaudo, C., Erhardt, M. & Voinnet, O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nature Cell Biol. 11, 1143–1149 (2009). References 86 and 107 identified MVBs as organelles contributing to the miRISC function, possibly by promoting miRISC loading or turnover.
  CAS PubMed Google Scholar
• Hilbert, M., Karow, A. R. & Klostermeier, D. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol. Chem. 390, 1237–1250 (2009).
  CAS PubMed Google Scholar
• Robb, G. B. & Rana, T. M. RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol. Cell 26, 523–537 (2007).
  CAS PubMed Google Scholar
• Tomari, Y. et al. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116, 831–841 (2004).
  CAS PubMed Google Scholar
• Hammell, C. M., Lubin, I., Boag, P. R., Blackwell, T. K. & Ambros, V. nhl-2 modulates microRNA activity in Caenorhabditis elegans. Cell 136, 926–938 (2009). References 74 and 90–92 identified the TRIM-NHL family of ubiquitin ligases as miRNA regulators in mammals, flies and worms. They also provide evidence that different TRIM-NHL proteins may act through different mechanisms.
  CAS PubMed PubMed Central Google Scholar
• Neumuller, R. A. et al. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454, 241–245 (2008).
  PubMed PubMed Central Google Scholar
• Schwamborn, J. C., Berezikov, E. & Knoblich, J. A. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913–925 (2009).
  CAS PubMed PubMed Central Google Scholar
• Weinmann, L. et al. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 136, 496–507 (2009).
  CAS PubMed Google Scholar
• Pare, J. M. et al. Hsp90 regulates the function of argonaute 2 and its recruitment to stress granules and P-bodies. Mol. Biol. Cell 20, 3273–3284 (2009).
  CAS PubMed PubMed Central Google Scholar
• Iki, T. et al. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 3 Jun 2010 (doi:10.1016/j.molcel.2010.05.014).
  CAS PubMed Google Scholar
• Iwasaki, S. et al. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 3 Jun 2010 (doi:10.1016/j.molcel.2010.05.015).
  CAS PubMed Google Scholar
• Kedde, M. et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273–1286 (2007).
  CAS PubMed Google Scholar
• Mishima, Y. et al. Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr. Biol. 16, 2135–2142 (2006).
  CAS PubMed PubMed Central Google Scholar
• Nolde, M. J., Saka, N., Reinert, K. L. & Slack, F. J. The Caenorhabditis elegans pumilio homolog, puf-9, is required for the 3′UTR-mediated repression of the let-7 microRNA target gene, hbl-1. Dev. Biol. 305, 551–563 (2007).
  CAS PubMed PubMed Central Google Scholar
• Galgano, A. et al. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS One 3, e3164 (2008).
  PubMed PubMed Central Google Scholar
• Kim, H. H. et al. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743–1748 (2009).
  CAS PubMed PubMed Central Google Scholar
• Eiring, A. M. et al. miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140, 652–665 (2010).
  CAS PubMed PubMed Central Google Scholar
• Vasudevan, S. & Steitz, J. A. A U-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128, 1105–1118 (2007).
  CAS PubMed PubMed Central Google Scholar
• Vasudevan, S., Tong, Y. & Steitz, J. A. Switching from repression to activation: microRNAs can up-regulate translation. Science 318, 1931–1934 (2007).
  CAS PubMed Google Scholar
• Orom, U. A., Nielsen, F. C. & Lund, A. H. MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30, 460–471 (2008).
  PubMed Google Scholar
• Henke, J. I. et al. microRNA-122 stimulates translation of hepatitis C virus RNA. Embo J. 27, 3300–3310 (2008).
  CAS PubMed PubMed Central Google Scholar
• Lee, Y. S. et al. Silencing by small RNAs is linked to endosomal trafficking. Nature Cell Biol. 11, 1150–1156 (2009).
  CAS PubMed Google Scholar
• Cikaluk, D. E. et al. GERp95, a membrane-associated protein that belongs to a family of proteins involved in stem cell differentiation. Mol. Biol. Cell 10, 3357–3372 (1999).
  CAS PubMed PubMed Central Google Scholar
• Tahbaz, N. et al. Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO Rep. 5, 189–194 (2004).
  CAS PubMed PubMed Central Google Scholar
• Carlsbecker, A. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316–321 (2010).
  CAS PubMed PubMed Central Google Scholar
• Rechavi, O. et al. Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev. 23, 1971–1979 (2009).
  CAS PubMed PubMed Central Google Scholar
• Meister, G. et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185–197 (2004).
  CAS PubMed Google Scholar
• Robb, G. B., Brown, K. M., Khurana, J. & Rana, T. M. Specific and potent RNAi in the nucleus of human cells. Nature Struct. Mol. Biol. 12, 133–137 (2005).
  CAS Google Scholar
• Rudel, S., Flatley, A., Weinmann, L., Kremmer, E. & Meister, G. A multifunctional human Argonaute2-specific monoclonal antibody. Rna 14, 1244–1253 (2008).
  PubMed PubMed Central Google Scholar
• Castanotto, D., Lingeman, R., Riggs, A. D. & Rossi, J. J. CRM1 mediates nuclear-cytoplasmic shuttling of mature microRNAs. Proc. Natl Acad. Sci. USA 106, 21655–21659 (2009).
  CAS PubMed PubMed Central Google Scholar
• Till, S. et al. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nature Struct. Mol. Biol. 14, 897–903 (2007).
  CAS Google Scholar
• Khraiwesh, B. et al. Transcriptional control of gene expression by microRNAs. Cell 140, 111–122 (2010).
  CAS PubMed Google Scholar
• Bao, N., Lye, K. W. & Barton, M. K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell 7, 653–662 (2004).
  CAS PubMed Google Scholar
• Wu, L. et al. DNA methylation mediated by a microRNA pathway. Mol. Cell 38, 465–475 (2010).
  CAS PubMed Google Scholar
• Kim, D. H., Saetrom, P., Snove, O. & Rossi, J. J. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc. Natl Acad. Sci. USA 105, 16230–16235 (2008).
  CAS PubMed PubMed Central Google Scholar
• Ashraf, S. I., McLoon, A. L., Sclarsic, S. M. & Kunes, S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124, 191–205 (2006).
  CAS PubMed Google Scholar
• Banerjee, S., Neveu, P. & Kosik, K. S. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64, 871–884 (2009).
  CAS PubMed Google Scholar
• Schratt, G. M. et al. A brain-specific microRNA regulates dendritic spine development. Nature 439, 283–289 (2006).
  CAS PubMed Google Scholar
• Siegel, G. et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nature Cell Biol. 11, 705–716 (2009). References 121–124 demonstrated that neuronal activation triggers the local relief of miRNA-meditated repression of translation at dendritic spines, contributing to synaptic plasticity and long-term potentiation.
  CAS PubMed Google Scholar
• Barbee, S. A. et al. Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52, 997–1009 (2006).
  CAS PubMed PubMed Central Google Scholar
• Cougot, N. et al. Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J. Neurosci. 28, 13793–13804 (2008).
  CAS PubMed PubMed Central Google Scholar
• Zeitelhofer, M. et al. Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J. Neurosci. 28, 7555–7562 (2008).
  CAS PubMed PubMed Central Google Scholar
• Lugli, G., Torvik, V. I., Larson, J. & Smalheiser, N. R. Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J. Neurochem. 106, 650–661 (2008).
  CAS PubMed PubMed Central Google Scholar
• Li, X. & Jin, P. Macro role(s) of microRNAs in fragile X syndrome? Neuromolecular Med. 11, 200–207 (2009).
  CAS PubMed Google Scholar
• Edbauer, D. et al. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65, 373–84.
• Jin, P. et al. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neurosci. 7, 113–117 (2004).
  CAS PubMed Google Scholar
• van Rooij, E. et al. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575–579 (2007).
  CAS PubMed Google Scholar
• Gatfield, D. et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 23, 1313–1326 (2009).
  CAS PubMed PubMed Central Google Scholar
• Krol, J. et al. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141, 618–631 (2010). Reports that many miRNAs in neurons have a very rapid turnover, which is regulated by neuronal activity.
  CAS PubMed Google Scholar
• Hwang, H. W., Wentzel, E. A. & Mendell, J. T. A hexanucleotide element directs microRNA nuclear import. Science 315, 97–100 (2007).
  CAS PubMed Google Scholar
• Buck, A. H. et al. Post-transcriptional regulation of miR-27 in murine cytomegalovirus infection. RNA 16, 307–315 (2010).
  CAS PubMed PubMed Central Google Scholar
• Sethi, P. & Lukiw, W. J. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neocortex. Neurosci. Lett. 459, 100–104 (2009).
  CAS PubMed Google Scholar
• Rajasethupathy, P. et al. Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803–817 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kocerha, J. et al. MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc. Natl Acad. Sci. USA 106, 3507–3512 (2009).
  CAS PubMed PubMed Central Google Scholar
• Wibrand, K. et al. Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. Eur. J. Neurosci. 31, 636–645 (2010).
  PubMed PubMed Central Google Scholar
• Flavell, S. W. & Greenberg, M. E. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31, 563–590 (2008).
  CAS PubMed PubMed Central Google Scholar
• Katoh, T. et al. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 23, 433–438 (2009).
  CAS PubMed PubMed Central Google Scholar
• Lu, S., Sun, Y. H. & Chiang, V. L. Adenylation of plant miRNAs. Nucleic Acids Res. 37, 1878–1885 (2009).
  CAS PubMed PubMed Central Google Scholar
• Li, J., Yang, Z., Yu, B., Liu, J. & Chen, X. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol. 15, 1501–1507 (2005).
  CAS PubMed PubMed Central Google Scholar
• Ramachandran, V. & Chen, X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321, 1490–1492 (2008).
  CAS PubMed PubMed Central Google Scholar
• Chatterjee, S. & Grosshans, H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature 461, 546–549 (2009). References 145 and 146 identified the first exoribonucleases known to be involved in degradation of mature miRNAs.
  CAS PubMed Google Scholar
• Chi, S. W., Zang, J. B., Mele, A. & Darnell, R. B. Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps. Nature 460, 479–486 (2009).
  CAS PubMed PubMed Central Google Scholar
• Mayr, C. & Bartel, D. P. Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673–684 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sandberg, R., Neilson, J. R., Sarma, A., Sharp, P. A. & Burge, C. B. Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320, 1643–1647 (2008).
  CAS PubMed PubMed Central Google Scholar
• Edbauer, D. et al. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65, 373–384 (2010).
  CAS PubMed PubMed Central Google Scholar
• Chekulaeva, M., Filipowicz, W. & Parker, R. Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA 15, 794–803 (2009).
  CAS PubMed PubMed Central Google Scholar
• Ozsolak, F. et al. Chromatin structure analyses identify miRNA promoters. Genes Dev. 22, 3172–3183 (2008).
  CAS PubMed PubMed Central Google Scholar
• Corcoran, D. L. et al. Features of mammalian microRNA promoters emerge from polymerase II chromatin immunoprecipitation data. PLoS One 4, e5279 (2009).
  PubMed PubMed Central Google Scholar
• O'Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V. & Mendell, J. T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839–843 (2005).
  CAS PubMed Google Scholar
• Ma, L. et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nature Cell Biol. 12, 247–256 (2010).
  CAS PubMed Google Scholar
• Chang, T. C. et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nature Genet. 40, 43–50 (2008).
  CAS PubMed Google Scholar
• He, L. et al. A microRNA component of the p53 tumour suppressor network. Nature 447, 1130–1134 (2007).
  CAS PubMed PubMed Central Google Scholar
• Conaco, C., Otto, S., Han, J. J. & Mandel, G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl Acad. Sci. USA 103, 2422–2427 (2006).
  CAS PubMed PubMed Central Google Scholar
• Han, L., Witmer, P. D., Casey, E., Valle, D. & Sukumar, S. DNA methylation regulates microRNA expression. Cancer Biol. Ther. 6, 1284–1288 (2007).
  CAS PubMed Google Scholar
• Eulalio, A., Behm-Ansmant, I. & Izaurralde, E. P bodies: at the crossroads of post-transcriptional pathways. Nature Rev. Mol. Cell Biol. 8, 9–22 (2007).
  CAS Google Scholar
• Franks, T. M. & Lykke-Andersen, J. The control of mRNA decapping and P-body formation. Mol. Cell 32, 605–615 (2008).
  CAS PubMed PubMed Central Google Scholar
• Parker, R. & Sheth, U. P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635–646 (2007).
  CAS PubMed Google Scholar
• Chu, C. Y. & Rana, T. M. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 4, e210 (2006).
  PubMed PubMed Central Google Scholar
• Eulalio, A., Behm-Ansmant, I., Schweizer, D. & Izaurralde, E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27, 3970–3981 (2007).
  CAS PubMed PubMed Central Google Scholar
• Pauley, K. M. et al. Formation of GW bodies is a consequence of microRNA genesis. EMBO Rep. 7, 904–910 (2006).
  CAS PubMed PubMed Central Google Scholar
• Huang, J. et al. Derepression of microRNA-mediated protein translation inhibition by apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G (APOBEC3G) and its family members. J. Biol. Chem. 282, 33632–33640 (2007).
  CAS PubMed Google Scholar
• Liu, J., Valencia-Sanchez, M. A., Hannon, G. J. & Parker, R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nature Cell Biol. 7, 719–723 (2005).
  CAS PubMed Google Scholar
• Pillai, R. S. et al. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309, 1573–1576 (2005).
  CAS PubMed Google Scholar
• Nathans, R. et al. Cellular microRNA and P bodies modulate host–HIV-1 interactions. Mol. Cell 34, 696–709 (2009).
  CAS PubMed PubMed Central Google Scholar
• Ma, J. et al. MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 20, 265–270 (2010).
  CAS PubMed PubMed Central Google Scholar
• Suh, N. et al. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271–277 (2010).
  CAS PubMed PubMed Central Google Scholar
• Flemr, M., Ma, J., Schultz, R. M. & Svoboda, P. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes. Biol. Reprod. 82, 1008–1017 (2010).
  CAS PubMed PubMed Central Google Scholar
• Swetloff, A. et al. Dcp1-bodies in mouse oocytes. Mol. Biol. Cell 20, 4951–4961 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kedersha, N. et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169, 871–884 (2005).
  CAS PubMed PubMed Central Google Scholar
• Sakamoto, S. et al. The NF90–NF45 complex functions as a negative regulator in the microRNA processing pathway. Mol. Cell. Biol. 29, 3754–3769 (2009).
  CAS PubMed PubMed Central Google Scholar
• Watanabe, M. et al. A subfamily of RNA-binding DEAD-box proteins acts as an estrogen receptor alpha coactivator through the N-terminal activation domain (AF-1) with an RNA coactivator, SRA. EMBO J. 20, 1341–1352 (2001).
  CAS PubMed PubMed Central Google Scholar
• Yamagata, K. et al. Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell 36, 340–347 (2009).
  CAS PubMed Google Scholar