1,609
Views
35
CrossRef citations to date
0
Altmetric
Review Articles

AGO2 and its partners: a silencing complex, a chromatin modulator, and new features

, , & ORCID Icon
Pages 33-53 | Received 17 Dec 2019, Accepted 02 Mar 2020, Published online: 13 Mar 2020

References

  • Alcid EA, Tsukiyama T. 2016. Expansion of antisense lncRNA transcriptomes in budding yeast species since the loss of RNAi. Nat Struct Mol Biol. 23:450–455.
  • Ameyar-Zazoua M, Rachez C, Souidi M, Robin P, Fritsch L, Young R, Morozova N, Fenouil R, Descostes N, Andrau JC, et al. 2012. Argonaute proteins couple chromatin silencing to alternative splicing. Nat Struct Mol Biol. 19:998–1004.
  • An JD, Zhu XD, Wang HW, Jin XD. 2013. A dynamic interplay between alternative polyadenylation and microRNA regulation: implications for cancer. Int J Oncol. 43:995–1001.
  • Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA. 11:717–727.
  • Ara T, Lopez F, Ritchie W, Benech P, Gautheret D. 2006. Conservation of alternative polyadenylation patterns in mammalian genes. BMC Genomics. 7:189.
  • Batsche E, Ameyar-Zazoua M. 2015. The influence of Argonaute proteins on alternative RNA splicing. Wiley Interdiscip Rev RNA. 6:141–156.
  • Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. 2006. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20:1885–1898.
  • Bernstein BE, Meissner A, Lander ES. 2007. The mammalian epigenome. Cell. 128:669–681.
  • Berrens RV, Andrews S, Spensberger D, Santos F, Dean W, Gould P, Sharif J, Olova N, Chandra T, Koseki H, et al. 2017. An endosiRNA-based repression mechanism counteracts transposon activation during global DNA demethylation in embryonic stem cells. Cell Stem Cell. 21:694–703 e7.
  • Blumenstiel JP. 2011. Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet. 27:23–31.
  • Boland A, Tritschler F, Heimstadt S, Izaurralde E, Weichenrieder O. 2010. Crystal structure and ligand binding of the MID domain of a eukaryotic Argonaute protein. EMBO Rep. 11:522–527.
  • Borchert GM, Holton NW, Williams JD, Hernan WL, Bishop IP, Dembosky JA, Elste JE, Gregoire NS, Kim JA, Koehler WW, et al. 2011. Comprehensive analysis of microRNA genomic loci identifies pervasive repetitive-element origins. Mob Genet Elements. 1:8–17.
  • Bukhari SIA, Truesdell SS, Lee S, Kollu S, Classon A, Boukhali M, Jain E, Mortensen RD, Yanagiya A, Sadreyev RI, et al. 2016. A specialized mechanism of translation mediated by FXR1a-associated MicroRNP in cellular quiescence. Mol Cell. 61:760–773.
  • Carissimi C, Laudadio I, Cipolletta E, Gioiosa S, Mihailovich M, Bonaldi T, Macino G, Fulci V. 2015. ARGONAUTE2 cooperates with SWI/SNF complex to determine nucleosome occupancy at human Transcription Start Sites. Nucleic Acids Res. 43:1498–1512.
  • Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. 2002. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16:2733–2742.
  • Caudy AA, Ketting RF, Hammond SM, Denli AM, Bathoorn AMP, Tops BBJ, Silva JM, Myers MM, Hannon GJ, Plasterk RHA, et al. 2003. A micrococcal nuclease homologue in RNAi effector complexes. Nature. 425:411–414.
  • Caudy AA, Myers M, Hannon GJ, Hammond SM. 2002. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16:2491–2496.
  • Cernilogar FM, Onorati MC, Kothe GO, Burroughs AM, Parsi KM, Breiling A, Sardo FL, Saxena A, Miyoshi K, Siomi H, et al. 2011. Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature. 480:391–U151.
  • Charroux B, Pellizzoni L, Perkinson RA, Yong J, Shevchenko A, Mann M, Dreyfuss G. 2000. Gemin4. A novel component of the SMN complex that is found in both gems and nucleoli. J Cell Biol. 148:1177–1186.
  • Chen L, Dahlstrom JE, Lee SH, Rangasamy D. 2012. Naturally occurring endo-siRNA silences LINE-1 retrotransposons in human cells through DNA methylation. Epigenetics. 7:758–771.
  • Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol. 10:741–754.
  • Chen Y, Boland A, Kuzuoğlu-Öztürk D, Bawankar P, Loh B, Chang CT, Weichenrieder O, Izaurralde E. 2014. A DDX6-CNOT1 complex and W-binding pockets in CNOT9 reveal direct links between miRNA target recognition and silencing. Mol Cell. 54:737–750.
  • Chendrimada TP, Finn KJ, Ji X, Baillat D, Gregory RI, Liebhaber SA, Pasquinelli AE, Shiekhattar R. 2007. MicroRNA silencing through RISC recruitment of eIF6. Nature. 447:823–828.
  • Cho S, Park JS, Kang YK. 2014. AGO2 and SETDB1 cooperate in promoter-targeted transcriptional silencing of the androgen receptor gene. Nucleic Acids Res. 42:13545–13556.
  • Christie M, Boland A, Huntzinger E, Weichenrieder O, Izaurralde E. 2013. Structure of the PAN3 pseudokinase reveals the basis for interactions with the PAN2 deadenylase and the GW182 proteins. Mol Cell. 51:360–373.
  • Chu Y, Yue X, Younger ST, Janowski BA, Corey DR. 2010. Involvement of argonaute proteins in gene silencing and activation by RNAs complementary to a non-coding transcript at the progesterone receptor promoter. Nucleic Acids Res. 38:7736–7748.
  • Conrad KD, Giering F, Erfurth C, Neumann A, Fehr C, Meister G, Niepmann M. 2013. MicroRNA-122 dependent binding of Ago2 protein to hepatitis C virus RNA is associated with enhanced RNA stability and translation stimulation. PLoS One. 8:e56272.
  • Daboussi F, Dumay A, Delacote F, Lopez BS. 2002. DNA double-strand break repair signalling: the case of RAD51 post-translational regulation. Cell Signal. 14:969–975.
  • Derti A, Garrett-Engele P, MacIsaac KD, Stevens RC, Sriram S, Chen R, Rohl CA, Johnson JM, Babak T. 2012. A quantitative atlas of polyadenylation in five mammals. Genome Res. 22:1173–1183.
  • Ding XC, Großhans H. 2009. Repression of C-elegans microRNA targets at the initiation level of translation requires GW182 proteins. Embo J. 28:213–222.
  • Dunckley T, Tucker M, Parker R. 2001. Two related proteins, Edc1p and Edc2p, stimulate mRNA decapping in Saccharomyces cerevisiae. Genetics. 157:27–37.
  • El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, Hakimi MA, Jacobsen SE, Cooke R, Lagrange T. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21:2539–2544.
  • Fabian MR, Cieplak MK, Frank F, Morita M, Green J, Srikumar T, Nagar B, Yamamoto T, Raught B, Duchaine TF, et al. 2011. miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat Struct Mol Biol. 18:1211–1217.
  • Fabian MR, Mathonnet G, Sundermeier T, Mathys H, Zipprich JT, Svitkin YV, Rivas F, Jinek M, Wohlschlegel J, Doudna JA, et al. 2009. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol Cell. 35:868–880.
  • Faehnle CR, Joshua-Tor L. 2010. Argonaute MID domain takes centre stage. EMBO Rep. 11:564–565.
  • Fagegaltier D, Bougé AL, Berry B, Poisot É, Sismeiro O, Coppée JY, Théodore L, Voinnet O, Antoniewski C. 2009. The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. Proc Natl Acad Sci USA. 106:21258–21263.
  • Francia S, Michelini F, Saxena A, Tang D, de Hoon M, Anelli V, Mione M, Carninci P, d’Adda di Fagagna F. 2012. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature. 488:231–235.
  • Frank F, Fabian MR, Stepinski J, Jemielity J, Darzynkiewicz E, Sonenberg N, Nagar B. 2011. Structural analysis of 5’-mRNA-cap interactions with the human AGO2 MID domain. EMBO Rep. 12:415–420.
  • Frank F, Sonenberg N, Nagar B. 2010. Structural basis for 5’-nucleotide base-specific recognition of guide RNA by human AGO2. Nature. 465:818–822.
  • Friend K, Campbell ZT, Cooke A, Kroll-Conner P, Wickens MP, Kimble J. 2012. A conserved PUF-Ago-eEF1A complex attenuates translation elongation. Nat Struct Mol Biol. 19:176–183.
  • Frohn A, Eberl HC, Stohr J, Glasmacher E, Rudel S, Heissmeyer V, Mann M, Meister G. 2012. Dicer-dependent and -independent Argonaute2 protein interaction networks in mammalian cells. Mol Cell Proteomics. 11:1442–1456.
  • Fu Y, Chen L, Chen C, Ge Y, Kang M, Song Z, Li J, Feng Y, Huo Z, He G, et al. 2018. Crosstalk between alternative polyadenylation and miRNAs in the regulation of protein translational efficiency. Genome Res. 28:1656–1663.
  • Gao M, Wei W, Li MM, Wu YS, Ba Z, Jin KX, Li MM, Liao YQ, Adhikari S, Chong Z, et al. 2014. Ago2 facilitates Rad51 recruitment and DNA double-strand break repair by homologous recombination. Cell Res. 24:532–541.
  • Garneau NL, Wilusz J, Wilusz CJ. 2007. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol. 8:113–126.
  • Ghosh S, Jacobson A. 2010. RNA decay modulates gene expression and controls its fidelity. Wiley Interdiscip Rev RNA. 1:351–361.
  • Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 442:199–202.
  • Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y, Livingston DM. 2006. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20:34–46.
  • Gu S, Jin L, Huang Y, Zhang F, Kay MA. 2012. Slicing-independent RISC activation requires the argonaute PAZ domain. Curr Biol. 22:1536–1542.
  • Gu S, Kay MA. 2010. How do miRNAs mediate translational repression? Silence. 1:11.
  • Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science. 293:1146–1150.
  • Hauptmann J, Dueck A, Harlander S, Pfaff J, Merkl R, Meister G. 2013. Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nat Struct Mol Biol. 20:814.
  • Hawkins PG, Santoso S, Adams C, Anest V, Morris KV. 2009. Promoter targeted small RNAs induce long-term transcriptional gene silencing in human cells. Nucleic Acids Res. 37:2984–2995.
  • Hock J, Meister G. 2008. The Argonaute protein family. Genome Biol. 9:210.
  • Horman SR, Janas MM, Litterst C, Wang B, MacRae IJ, Sever MJ, Morrissey DV, Graves P, Luo B, Umesalma S, et al. 2013. Akt-mediated phosphorylation of argonaute 2 downregulates cleavage and upregulates translational repression of MicroRNA targets. Mol Cell. 50:356–367.
  • Horvathova I, Voigt F, Kotrys AV, Zhan Y, Artus-Revel CG, Eglinger J, Stadler MB, Giorgetti L, Chao JA. 2017. The dynamics of mRNA turnover revealed by single-molecule imaging in single cells. Mol Cell. 68:615–625 e9.
  • Hu J, Chen Z, Xia D, Wu J, Xu H, Ye ZQ. 2012. Promoter-associated small double-stranded RNA interacts with heterogeneous nuclear ribonucleoprotein A2/B1 to induce transcriptional activation. Biochem J. 447:407–416.
  • Huang V, Qin Y, Wang J, Wang XL, Place RF, Lin GT. 2010. RNAa is conserved in mammalian cells. PLoS One. 5: e8848.
  • Hutvagner G, Zamore PD. 2002. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 297:2056–2060.
  • Ip JY, Schmidt D, Pan Q, Ramani AK, Fraser AG, Odom DT, Blencowe BJ. 2011. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res. 21:390–401.
  • Ishizuka A, Siomi MC, Siomi H. 2002. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16:2497–2508.
  • Iwakawa HO, Tomari Y. 2015. The functions of MicroRNAs: mRNA decay and translational repression. Trends Cell Biol. 25:651–665.
  • Iwasaki S, Tomari Y. 2009. Argonaute-mediated translational repression (and activation). Fly. 3:205–206.
  • Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 11:113–127.
  • Jaehning JA. 2010. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim Biophys Acta. 1799:379–388.
  • Janowski BA, Huffman KE, Schwartz JC, Ram R, Nordsell R, Shames DS. 2006. Involvement of AGO1 and AGO2 in mammalian transcriptional silencing. Nat Struct Mol Biol. 13:787–792.
  • Janowski BA, Younger ST, Hardy DB, Ram R, Huffman KE, Corey DR. 2007. Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat Chem Biol. 3:166–173.
  • Jee D, Lai EC. 2014. Alteration of miRNA activity via context-specific modifications of Argonaute proteins. Trends Cell Biol. 24:546–553.
  • Jiao AL, Slack FJ. 2014. RNA-mediated gene activation. Epigenetics. 9:27–36.
  • Jinek M, Doudna JA. 2009. A three-dimensional view of the molecular machinery of RNA interference. Nature. 457:405–412.
  • Johnsson P, Ackley A, Vidarsdottir L, Lui WO, Corcoran M, Grander D, Morris KV. 2013. A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells. Nat Struct Mol Biol. 20:440–446.
  • Johnston M, Geoffroy MC, Sobala A, Hay R, Hutvagner G. 2010. HSP90 protein stabilizes unloaded Argonaute complexes and microscopic P-bodies in human cells. MBoC. 21:1462–1469.
  • Kandeel M, Al-Taher A, Nakashima R, Sakaguchi T, Kandeel A, Nagaya Y, Kitamura Y, Kitade Y. 2014. Bioenergetics and gene silencing approaches for unraveling nucleotide recognition by the human EIF2C2/Ago2 PAZ domain. PLoS One. 9:e94538.
  • Kang YK. 2018. Surveillance of retroelement expression and nucleic-acid immunity by histone methyltransferase SETDB1. BioEssays. 40:e1800058.
  • Karginov FV, Cheloufi S, Chong MMW, Stark A, Smith AD, Hannon GJ. 2010. Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon MicroRNAs, Drosha, and additional nucleases. Mol Cell. 38:781–788.
  • Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, et al.; FANTOM Consortium. 2005. Antisense transcription in the mammalian transcriptome. Science. 309:1564–1566.
  • Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T, Okada TN, Siomi MC, Siomi H. 2008. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature. 453:793–797.
  • Kedzierska H, Piekielko-Witkowska A. 2017. Splicing factors of SR and hnRNP families as regulators of apoptosis in cancer. Cancer Lett. 396:53–65.
  • Kenny PJ, Zhou H, Kim M, Skariah G, Khetani RS, Drnevich J, Arcila ML, Kosik KS, Ceman S. 2014. MOV10 and FMRP regulate AGO2 association with microRNA recognition elements. Cell Rep. 9:1729–1741.
  • Kerwitz Y, Kuhn U, Lilie H, Knoth A, Scheuermann T, Friedrich H, Schwarz E, Wahle E. 2003. Stimulation of poly(A) polymerase through a direct interaction with the nuclear poly(A) binding protein allosterically regulated by RNA. Embo J. 22:3705–3714.
  • Kim DH, Saetrom P, Snove O Jr, Rossi JJ. 2008. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA. 105:16230–16235.
  • Kim J, Guermah M, Roeder RG. 2010. The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell. 140:491–503.
  • Kiriakidou M, Tan GS, Lamprinaki S, De Planell-Saguer M, Nelson PT, Mourelatos Z. 2007. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell. 129:1141–1151.
  • Kouzarides T. 2007. Chromatin modifications and their function. Cell. 128:693–705.
  • Kuhn U, Gundel M, Knoth A, Kerwitz Y, Rudel S, Wahle E. 2009. Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J Biol Chem. 284:22803–22814.
  • Kute PM, Ramakrishna S, Neelagandan N, Chattarji S, Muddashetty RS. 2019. NMDAR mediated translation at the synapse is regulated by MOV10 and FMRP. Mol Brain. 12:65.
  • Kuzuoglu-Ozturk D, Bhandari D, Huntzinger E, Fauser M, Helms S, Izaurralde E. 2016. miRISC and the CCR4-NOT complex silence mRNA targets independently of 43S ribosomal scanning. Embo J. 35:1186–1203.
  • Kwak PB, Tomari Y. 2012. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat Struct Mol Biol. 19:145–151.
  • Laham-Karam N, Laitinen P, Turunen TA, Yla-Herttuala S. 2018. Activating the chromatin by noncoding RNAs. Antioxid Redox Sign. 29:813–831.
  • Lam JKW, Chow MYT, Zhang Y, Leung S. 2015. siRNA versus miRNA as therapeutics for gene silencing. Mol Ther-Nucl Acids. 4:e252.
  • Lang F, Li X, Zheng W, Li Z, Lu D, Chen G, Gong D, Yang L, Fu J, Shi P, et al. 2017. CTCF prevents genomic instability by promoting homologous recombination-directed DNA double-strand break repair. Proc Natl Acad Sci USA. 114:10912–10917.
  • Legendre M, Gautheret D. 2003. Sequence determinants in human polyadenylation site selection. BMC Genomics. 4:7.
  • Leuschner PJ, Ameres SL, Kueng S, Martinez J. 2006. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 7:314–320.
  • Li Y, Tang W, Zhang LR, Zhang CY. 2014. FMRP regulates miR196a-mediated repression of HOXB8 via interaction with the AGO2 MID domain. Mol Biosyst. 10:1757–1764.
  • Lim JW, Snider L, Yao Z, Tawil R, Van Der Maarel SM, Rigo F, Bennett CF, Filippova GN, Tapscott SJ. 2015. DICER/AGO-dependent epigenetic silencing of D4Z4 repeats enhanced by exogenous siRNA suggests mechanisms and therapies for FSHD. Hum Mol Genet. 24:4817–4828.
  • Lima WF, De Hoyos CL, Liang XH, Crooke ST. 2016. RNA cleavage products generated by antisense oligonucleotides and siRNAs are processed by the RNA surveillance machinery. Nucleic Acids Res. 44:3351–3363.
  • Listerman I, Sapra AK, Neugebauer KM. 2006. Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat Struct Mol Biol. 13:815–822.
  • Liu T, Zhang H, Fang J, Yang Z, Chen R, Wang Y, Zhao X, Ge S, Yu J, Huang J, et al. 2020. AGO2 phosphorylation by c-Src kinase promotes tumorigenesis. Neoplasia. 22:129–141.
  • Long JC, Caceres JF. 2009. The SR protein family of splicing factors: master regulators of gene expression. Biochem J. 417:15–27.
  • Luo S, Lu J. 2017. Silencing of transposable elements by piRNAs in Drosophila: an evolutionary perspective. Genom Proteom Bioinform. 15:164–176.
  • Ma JB, Ye K, Patel DJ. 2004. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature. 429:318–322.
  • Maksakova IA, Romanish MT, Gagnier L, Dunn CA, de Lagemaat LNV, Mager DL. 2006. Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet. 2:e2–e10.
  • Maroney PA, Yu Y, Fisher J, Nilsen TW. 2006. Evidence that microRNAs are associated with translating messenger RNAs in human cells. Nat Struct Mol Biol. 13:1102–1107.
  • Matsui M, Chu Y, Zhang H, Gagnon KT, Shaikh S, Kuchimanchi S, Manoharan M, Corey DR, Janowski BA. 2013. Promoter RNA links transcriptional regulation of inflammatory pathway genes. Nucleic Acids Res. 41:10086–10109.
  • Mazumder A, Bose M, Chakraborty A, Chakrabarti S, Bhattacharyya SN. 2013. A transient reversal of miRNA-mediated repression controls macrophage activation. EMBO Rep. 14:1008–1016.
  • Meister G. 2013. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 14:447–459.
  • Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Lührmann R, Tuschl T. 2005. Identification of novel argonaute-associated proteins. Curr Biol. 15:2149–2155.
  • Mengardi C, Limousin T, Ricci EP, Soto-Rifo R, Decimo D, Ohlmann T. 2017. microRNAs stimulate translation initiation mediated by HCV-like IRESes. Nucleic Acids Res. 45:4810–4824.
  • Modarresi F, Faghihi MA, Lopez-Toledano MA, Fatemi RP, Magistri M, Brothers SP, van der Brug MP, Wahlestedt C. 2012. Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation. Nat Biotechnol. 30:453–459.
  • Moretti F, Kaiser C, Zdanowicz-Specht A, Hentze MW. 2012. PABP and the poly(A) tail augment microRNA repression by facilitated miRISC binding. Nat Struct Mol Biol. 19:603–608.
  • Morris KV, Chan SWL, Jacobsen SE, Looney DJ. 2004. Small interfering RNA-induced transcriptional gene silencing in human cells. Science. 305:1289–1292.
  • Morris KV, Santoso S, Turner AM, Pastori C, Hawkins PG. 2008. Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet. 4:e1000258.
  • Morris KV. 2008. RNA-mediated transcriptional gene silencing in human cells. Curr Top Microbiol Immunol. 320:211–224.
  • Morris KV. 2009. Long antisense non-coding RNAs function to direct epigenetic complexes that regulate transcription in human cells. Epigenetics. 4:296–301.
  • Mortensen RD, Serra M, Steitz JA, Vasudevan S. 2011. Posttranscriptional activation of gene expression in Xenopus laevis oocytes by microRNA-protein complexes (microRNPs). Proc Natl Acad Sci U S A. 108:8281–8286.
  • Moshkovich N, Nisha P, Boyle PJ, Thompson BA, Dale RK, Lei EP. 2011. RNAi-independent role for Argonaute2 in CTCF/CP190 chromatin insulator function. Genes Dev. 25:1686–1701.
  • Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G. 2002. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 16:720–728.
  • Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L, Laur O, Warren ST, Bassell GJ. 2011. Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol Cell. 42:673–688.
  • Muotri AR, Marchetto MC, Coufal NG, Gage FH. 2007. The necessary junk: new functions for transposable elements. Hum Mol Genet. 16:R159–R167.
  • Napoli S, Pastori C, Magistri M, Carbone GM, Catapano CV. 2009. Promoter-specific transcriptional interference and c-myc gene silencing by siRNAs in human cells. EMBO J. 28:1708–1719.
  • Nazer E, Dale RK, Chinen M, Radmanesh B, Lei EP. 2018. Argonaute2 and LaminB modulate gene expression by controlling chromatin topology. PLoS Genet. 14:e1007276.
  • Nykanen A, Haley B, Zamore PD. 2001. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell. 107:309–321.
  • Orban TI, Izaurralde E. 2005. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA. 11:459–469.
  • Parker JS, Roe SM, Barford D. 2005. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature. 434:663–666.
  • Parker R. 2012. RNA degradation in Saccharomyces cerevisae. Genetics. 191:671–702.
  • Pei H, Zhang L, Luo K, Qin Y, Chesi M, Fei F, Bergsagel PL, Wang L, You Z, Lou Z, et al. 2011. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature. 470:124–128.
  • Perez Canadillas JM, Varani G. 2003. Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. EMBO J. 22:2821–2830.
  • Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. 2006. Short RNAs repress translation after initiation in mammalian cells. Mol Cell. 21:533–542.
  • Petri R, Brattås PL, Sharma Y, Jönsson ME, Pircs K, Bengzon J, Jakobsson J. 2019. LINE-2 transposable elements are a source of functional human microRNAs and target sites. PLoS Genet. 15:e1008036.
  • Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W. 2005. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 309:1573–1576.
  • Pillai RS, Bhattacharyya SN, Filipowicz W. 2007. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 17:118–126.
  • Piriyapongsa J, Marino-Ramirez L, Jordan IK. 2007. Origin and evolution of human microRNAs from transposable elements. Genetics. 176:1323–1337.
  • Portnoy V, Huang V, Place RF, Li LC. 2011. Small RNA and transcriptional upregulation. Wiley Interdiscip Rev RNA. 2:748–760.
  • Portnoy V, Lin SHS, Li KH, Burlingame A, Hu ZH, Li H, Li LC. 2016. saRNA-guided Ago2 targets the RITA complex to promoters to stimulate transcription. Cell Res. 26:320–335.
  • Price BD, D’Andrea AD. 2013. Chromatin remodeling at DNA double-strand breaks. Cell. 152:1344–1354.
  • Qin S, Jin P, Zhou X, Chen L, Ma F. 2015. The role of transposable elements in the origin and evolution of MicroRNAs in human. PLoS One. 10:e0131365.
  • Rehwinkel J, Behm-Ansmant I, Gatfield D, Izaurralde E. 2005. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA. 11:1640–1647.
  • Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L. 2005. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol. 12:340–349.
  • Robb GB, Brown KM, Khurana J, Rana TM. 2005. Specific and potent RNAi in the nucleus of human cells. Nat Struct Mol Biol. 12:133–137.
  • Robb GB, Rana TM. 2007. RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol Cell. 26:523–537.
  • Robert VJ, Sijen T, van Wolfswinkel J, Plasterk RH. 2005. Chromatin and RNAi factors protect the C. elegans germline against repetitive sequences. Genes Dev. 19:782–787.
  • Romero-Cordoba SL, Salido-Guadarrama I, Rodriguez-Dorantes M, Hidalgo-Miranda A. 2014. miRNA biogenesis: biological impact in the development of cancer. Cancer Biol Ther. 15:1444–1455.
  • Rowe HM, Trono D. 2011. Dynamic control of endogenous retroviruses during development. Virology. 411:273–287.
  • Rudel S, Flatley A, Weinmann L, Kremmer E, Meister G. 2008. A multifunctional human Argonaute2-specific monoclonal antibody. RNA. 14:1244–1253.
  • Rudel S, Wang Y, Lenobel R, Korner R, Hsiao HH, Urlaub H, Patel D, Meister G. 2011. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res. 39:2330–2343.
  • San Filippo J, Sung P, Klein H. 2008. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem. 77:229–257.
  • Sasaki T, Shiohama A, Minoshima S, Shimizu N. 2003. Identification of eight members of the Argonaute family in the human genome. Genomics. 82:323–330.
  • Schirle NT, MacRae IJ. 2012. The crystal structure of human Argonaute2. Science. 336:1037–1040.
  • Schoenberg DR. 2011. Mechanisms of endonuclease-mediated mRNA decay. Wiley Interdiscip Rev RNA. 2:582–600.
  • Shekar PC, Naim A, Sarathi DP, Kumar S. 2011. Argonaute-2-null embryonic stem cells are retarded in self-renewal and differentiation. J Biosci. 36:649–657.
  • Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, Du Y, Wang Y, Chang WC, Chen CH, et al. 2013. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature. 497:383–387.
  • Sheu-Gruttadauria J, MacRae IJ. 2018. Phase transitions in the assembly and function of human miRISC. Cell. 173:946–957 e16.
  • Siomi MC, Saito K, Siomi H. 2008. How selfish retrotransposons are silenced in Drosophila germline and somatic cells. Febs Lett. 582:2473–2478.
  • Skourti-Stathaki K, Kamieniarz-Gdula K, Proudfoot NJ. 2014. R-loops induce repressive chromatin marks over mammalian gene terminators. Nature. 516:436–439.
  • Song JJ, Liu J, Tolia NH, Schneiderman J, Smith SK, Martienssen RA, Hannon GJ, Joshua-Tor L. 2003. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat Struct Mol Biol. 10:1026–1032.
  • Song JJ, Smith SK, Hannon GJ, Joshua-Tor L. 2004. Crystal structure of argonaute and its implications for RISC slicer activity. Science. 305:1434–1437.
  • Sun M, Ding J, Li D, Yang G, Cheng Z, Zhu Q. 2017. NUDT21 regulates 3’-UTR length and microRNA-mediated gene silencing in hepatocellular carcinoma. Cancer Lett. 410:158–168.
  • Sun Y, Zhang Y, Hamilton K, Manley JL, Shi Y, Walz T, Tong L. 2018. Molecular basis for the recognition of the human AAUAAA polyadenylation signal. Proc Natl Acad Sci USA. 115:E1419–E28.
  • Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet. 45:247–271.
  • Tang GL. 2005. siRNA and miRNA: an insight into RISCs. Trends Biochem Sci. 30:106–114.
  • Tang W, You W, Shi F, Qi T, Wang L, Djouder Z, Liu W, Zeng X. 2009. RNA helicase A acts as a bridging factor linking nuclear beta-actin with RNA polymerase II. Biochem J. 420:421–428.
  • Taniho K, Nakashima R, Kandeel M, Kitamura Y, Kitade Y. 2012. Synthesis and biological properties of chemically modified siRNAs bearing 1-deoxy-D-ribofuranose in their 3’-overhang region. Bioorg Med Chem Lett. 22:2518–2521.
  • Ting AH, Schuebel KE, Herman JG, Baylin SB. 2005. Short double-stranded RNA induces transcriptional gene silencing in human cancer cells in the absence of DNA methylation. Nat Genet. 37:906–910.
  • Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol. 160:823–831.
  • Truesdell SS, Mortensen RD, Seo M, Schroeder JC, Lee JH, LeTonqueze O, Vasudevan S. 2012. MicroRNA-mediated mRNA translation activation in quiescent cells and oocytes involves recruitment of a nuclear microRNP. Sci Rep. 2:842.
  • Tufarelli C, Stanley JAS, Garrick D, Sharpe JA, Ayyub H, Wood WG, Higgs DR. 2003. Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat Genet. 34:157–165.
  • Ueno Y, Kawada K, Shibata A, Yoshikawa K, Wataya Y, Kitade Y. 2008. Synthesis and silencing properties of siRNAs possessing lipophilic groups at their 3’-termini. Nucleic Acids Symp Ser. 52:503–504. :
  • Vasudevan S, Steitz JA. 2007. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell. 128:1105–1118.
  • Wahl MC, Will CL, Luhrmann R. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell. 136:701–718.
  • Wakiyama M, Ogami K, Iwaoka R, Aoki K, Hoshino SI. 2018. MicroRNP-mediated translational activation of nonadenylated mRNAs in a mammalian cell-free system. Genes Cells. 23:332–344.
  • Wang Q, Goldstein M. 2016. Small RNAs recruit chromatin-modifying enzymes MMSET and Tip60 to reconfigure damaged DNA upon double-strand break and facilitate repair. Cancer Res. 76:1904–1915.
  • Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Rendtlew Danielsen JM, Yang YG, Qi Y, et al. 2012. A role for small RNAs in DNA double-strand break repair. Cell. 149:101–112.
  • West S, Proudfoot NJ. 2008. Human Pcf11 enhances degradation of RNA polymerase II-associated nascent RNA and transcriptional termination. Nucleic Acids Res. 36:905–914.
  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, et al. 2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 8:973–982.
  • Wyman C, Kanaar R. 2006. DNA double-strand break repair: all’s well that ends well. Annu Rev Genet. 40:363–383.
  • Yamanaka S, Siomi H. 2014. diRNA-Ago2-RAD51 complexes at double-strand break sites. Cell Res. 24:511–512.
  • Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol. 12:1054–1063.
  • Ye X, Huang N, Liu Y, Paroo Z, Huerta C, Li P, Chen S, Liu Q, Zhang H. 2011. Structure of C3PO and mechanism of human RISC activation. Nat Struct Mol Biol. 18:650–657.
  • Ye Z, Jin H, Qian Q. 2015. Argonaute 2: a novel rising star in cancer research. J Cancer. 6:877–882.
  • Yen CY, Huang HW, Shu CW, Hou MF, Yuan SSF, Wang HR, Chang YT, Farooqi AA, Tang JY, Chang HW. 2016. DNA methylation, histone acetylation and methylation of epigenetic modifications as a therapeutic approach for cancers. Cancer Lett. 373:185–192.
  • Yi T, Arthanari H, Akabayov B, Song H, Papadopoulos E, Qi HH, Jedrychowski M, Güttler T, Guo C, Luna RE, et al. 2015. eIF1A augments Ago2-mediated Dicer-independent miRNA biogenesis and RNA interference. Nat Commun. 6:7194.
  • Yigit E, Batista PJ, Bei Y, Pang KM, Chen CCG, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC, et al. 2006. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell. 127:747–757.
  • Younger ST, Corey DR. 2011. Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucleic Acids Res. 39:5682–5691.
  • Zekri L, Huntzinger E, Heimstadt S, Izaurralde E. 2009. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol Cell Biol. 29:6220–6231.
  • Zekri L, Kuzuoğlu-Öztürk D, Izaurralde E. 2013. GW182 proteins cause PABP dissociation from silenced miRNA targets in the absence of deadenylation. Embo J. 32:1052–1065.
  • Zeng Y, Sankala H, Zhang X, Graves PR. 2008. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem J. 413:429–436.
  • Zhang H, Sheng C, Yin Y, Wen S, Yang G, Cheng Z, Zhu Q. 2015. PABPC1 interacts with AGO2 and is responsible for the microRNA mediated gene silencing in high grade hepatocellular carcinoma. Cancer Lett. 367:49–57.
  • Zheng D, Tian B. 2014. RNA-binding proteins in regulation of alternative cleavage and polyadenylation. Adv Exp Med Biol. 825:97–127.
  • Zhu R, Zhang Z, Li Y, Hu Z, Xin D, Qi Z, Chen Q. 2016. Discovering numerical differences between animal and plant microRNAs. PLoS One. 11:e0165152.
  • Zhu Y, Wang X, Forouzmand E, Jeong J, Qiao F, Sowd GA, Engelman AN, Xie X, Hertel KJ, Shi Y, et al. 2018. Molecular mechanisms for CFIm-mediated regulation of mRNA alternative polyadenylation. Mol Cell. 69:62–74 e4.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.