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Review

Recent progress in miRNA biogenesis and decay

& ORCID Icon
Pages 1-8 | Accepted 17 Nov 2023, Published online: 29 Nov 2023

References

  • Conrad T, Marsico A, Gehre M, et al. Microprocessor activity controls differential miRNA biogenesis in vivo. Cell Rep. 2014;9(2):542–554. doi: 10.1016/j.celrep.2014.09.007
  • Georgakilas G, Vlachos IS, Paraskevopoulou MD, et al. microTSS: accurate microRNA transcription start site identification reveals a significant number of divergent pri-miRNAs. Nat Commun. 2014;5:5700. doi: 10.1038/ncomms6700
  • Gregory RI, Yan KP, Amuthan G, et al. The Microprocessor complex mediates the genesis of microRnas. Nature. 2004;432(7014):235–240. doi: 10.1038/nature03120
  • Yi R, Qin Y, Macara IG, et al. Exportin-5 mediates the nuclear export of pre-microRnas and short hairpin RNAs. Genes Dev. 2003;17(24):3011–3016. doi: 10.1101/gad.1158803
  • Bartel DP. Metazoan MicroRNAs. Cell. 2018;173(1):20–51. doi: 10.1016/j.cell.2018.03.006
  • McGeary SE, Lin KS, Shi CY, et al. The biochemical basis of microRNA targeting efficacy. Science. 2019;366(6472):eaav1741. doi: 10.1126/science.aav1741
  • Suzuki HI, Young RA, Sharp PA. Super-enhancer-mediated RNA processing revealed by integrative MicroRNA network analysis. Cell. 2017;168(6):1000–1014.e15. doi: 10.1016/j.cell.2017.02.015
  • Wang S, Talukder A, Cha M, et al. Computational annotation of miRNA transcription start sites. Brief Bioinform. 2021;22(1):380–392. doi: 10.1093/bib/bbz178
  • Perdikopanis N, Georgakilas GK, Grigoriadis D, et al. DIANA-miRgen v4: indexing promoters and regulators for more than 1500 microRnas. Nucleic Acids Res. 2021;49(D1):D151–9. doi: 10.1093/nar/gkaa1060
  • Cha M, Zheng H, Talukder A, et al. A two-stream convolutional neural network for microRNA transcription start site feature integration and identification. Sci Rep. 2021;11(1):5625. doi: 10.1038/s41598-021-85173-x
  • Ballarino M, Pagano F, Girardi E, et al. Coupled RNA processing and transcription of intergenic primary microRnas. Mol Cell Biol. 2009;29(20):5632–5638. doi: 10.1128/MCB.00664-09
  • Lee Y, Ahn C, Han J, et al. The nuclear RNase III drosha initiates microRNA processing. Nature. 2003;425(6956):415–419. doi: 10.1038/nature01957
  • Denli AM, Tops BBJ, Plasterk RHA, et al. Processing of primary microRnas by the Microprocessor complex. Nature. 2004;432(7014):231–235. doi: 10.1038/nature03049
  • Landthaler M, Yalcin A, Tuschl T. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol. 2004;14(23):2162–2167. doi: 10.1016/j.cub.2004.11.001
  • Han J, Lee Y, Yeom K-H, et al. The drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004;18(24):3016–3027. doi: 10.1101/gad.1262504
  • Auyeung VC, Ulitsky I, McGeary SE, et al. Beyond secondary structure: primary-sequence determinants license pri-miRNA hairpins for processing. Cell 2013;
  • Nguyen TA, Jo MH, Choi Y-G, et al. Functional anatomy of the human Microprocessor. Cell. 2015;161(6):1374–1387. doi: 10.1016/j.cell.2015.05.010
  • Jin W, Wang J, Liu C-P, et al. Structural basis for pri-miRNA recognition by Drosha. Mol Cell. 2020;78(3):423–433.e5. doi: 10.1016/j.molcel.2020.02.024
  • Partin AC, Zhang K, Jeong B-C, et al. Cryo-EM structures of human drosha and DGCR8 in complex with primary MicroRNA. Mol Cell. 2020;78(3):411–422.e4. doi: 10.1016/j.molcel.2020.02.016
  • Kang W, Fromm B, Houben AJ, et al. MapToCleave: high-throughput profiling of microRNA biogenesis in living cells. Cell Rep. 2021;37(7):110015. doi: 10.1016/j.celrep.2021.110015
  • Conrad T, Ntini E, Lang B, et al. Determination of primary microRNA processing in clinical samples by targeted pri-miR-sequencing. RNA. 2020;26(11):1726–1730. doi: 10.1261/rna.076240.120
  • Kim K, Baek SC, Lee Y-Y, et al. A quantitative map of human primary microRNA processing sites. Mol Cell. 2021;81(16):3422–3439.e11. doi: 10.1016/j.molcel.2021.07.002
  • Rice GM, Shivashankar V, Ma EJ, et al. Functional atlas of primary miRNA maturation by the Microprocessor. Mol Cell. 2020;80(5):892–902.e4. doi: 10.1016/j.molcel.2020.10.028
  • Fóthi Á, Biró O, Erdei Z, et al. Tissue-specific and transcription-dependent mechanisms regulate primary microRNA processing efficiency of the human chromosome 19 MicroRNA cluster. RNA Biol. 2021;18(8):1170–1180. doi: 10.1080/15476286.2020.1836457
  • Shang R, Lai EC. Parameters of clustered suboptimal miRNA biogenesis. Proc Natl Acad Sci U S A. 2023;120(41):e2306727120. doi: 10.1073/pnas.2306727120
  • Kwon SC, Jang H, Shen S, et al. ERH facilitates microRNA maturation through the interaction with the N-terminus of DGCR8. Nucleic Acids Res. 2020;48(19):11097–11112. doi: 10.1093/nar/gkaa827
  • Fang W, Bartel DP. MicroRNA clustering assists processing of suboptimal MicroRNA hairpins through the action of the ERH protein. Mol Cell. 2020;78(2):289–302.e6. doi: 10.1016/j.molcel.2020.01.026
  • Shang R, Baek SC, Kim K, et al. Genomic clustering facilitates nuclear processing of suboptimal pri-miRNA loci. Mol Cell. 2020;78(2):303–316.e4. doi: 10.1016/j.molcel.2020.02.009
  • Hutter K, Lohmüller M, Jukic A, et al. SAFB2 enables the processing of suboptimal stem-Loop structures in clustered primary miRNA transcripts. Mol Cell. 2020;78(5):876–889.e6. doi: 10.1016/j.molcel.2020.05.011
  • Wang J, Lee JE, Riemondy K, et al. XPO5 promotes primary miRNA processing independently of RanGTP. Nat Commun. 2020;11(1):1845. doi: 10.1038/s41467-020-15598-x
  • Ruiz-Arroyo VM, Nam Y. Dynamic protein-RNA recognition in primary MicroRNA processing. Curr Opin Struct Biol. 2022;76:102442. doi: 10.1016/j.sbi.2022.102442
  • Pandey M, Luhur A, Sokol NS, et al. Molecular dissection of a conserved cluster of miRnas identifies critical structural determinants that mediate differential processing. Front Cell Dev Biol. 2022;10:909212. doi: 10.3389/fcell.2022.909212
  • Hecker M, Fitzner B, Putscher E, et al. Implication of genetic variants in primary microRNA processing sites in the risk of multiple sclerosis. EBioMedicine. 2022;80:104052. doi: 10.1016/j.ebiom.2022.104052
  • Liu Z, Wang J, Cheng H, et al. Cryo-EM structure of human Dicer and its complexes with a pre-miRNA substrate. Cell. 2018;173(5):1191–1203.e12. doi: 10.1016/j.cell.2018.03.080
  • Lee Y-Y, Lee H, Kim H, et al. Structure of the human DICER-pre-miRNA complex in a dicing state. Nature. 2023;615:331–338. doi: 10.1038/s41586-023-05723-3
  • Zapletal D, Taborska E, Pasulka J, et al. Structural and functional basis of mammalian microRNA biogenesis by Dicer. Mol Cell. 2022;82(21):4064–4079.e13. doi: 10.1016/j.molcel.2022.10.010
  • Jouravleva K, Golovenko D, Demo G, et al. Structural basis of microRNA biogenesis by Dicer-1 and its partner protein loqs-PB. Mol Cell. 2022;82(21):4049–4063.e6. doi: 10.1016/j.molcel.2022.09.002
  • Nguyen TD, Trinh TA, Bao S, et al. Secondary structure RNA elements control the cleavage activity of DICER. Nat Commun. 2022;13(1):2138. doi: 10.1038/s41467-022-29822-3
  • Lee Y-Y, Kim H, Kim VN. Sequence determinant of small RNA production by DICER. Nature. 2023;615(7951):323–330. doi: 10.1038/s41586-023-05722-4
  • Chendrimada TP, Gregory RI, Kumaraswamy E, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature. 2005;436(7051):740–744. doi: 10.1038/nature03868
  • Wilson RC, Tambe A, Kidwell MA, et al. Dicer-TRBP complex formation ensures accurate mammalian microRNA biogenesis. Mol Cell. 2015;57(3):397–407. doi: 10.1016/j.molcel.2014.11.030
  • Schwarz DS, Hutvágner G, Du T, et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 2003;115(2):199–208. doi: 10.1016/S0092-8674(03)00759-1
  • Fareh M, Yeom K-H, Haagsma AC, et al. TRBP ensures efficient Dicer processing of precursor microRNA in RNA-crowded environments. Nat Commun. 2016;7(1):13694. doi: 10.1038/ncomms13694
  • Schopp IM, Amaya Ramirez CC, Debeljak J, et al. Split-BioID a conditional proteomics approach to monitor the composition of spatiotemporally defined protein complexes. Nat Commun. 2017;8(1):15690. doi: 10.1038/ncomms15690
  • Nakanishi K. Anatomy of RISC: how do small RNAs and chaperones activate Argonaute proteins? Wiley Interdiscip Rev RNA. 2016;7(5):637–660. doi: 10.1002/wrna.1356
  • Medley JC, Panzade G, Zinovyeva AY. microRNA strand selection: unwinding the rules. Wiley Interdiscip Rev RNA. 2021;12:e1627. doi: 10.1002/wrna.1627
  • Frank F, Sonenberg N, Nagar B. Structural basis for 5’-nucleotide base-specific recognition of guide RNA by human AGO2. Nature. 2010;465:818–822. doi: 10.1038/nature09039
  • Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003;115(2):209–216. doi: 10.1016/S0092-8674(03)00801-8
  • Kim H, Kim J, Yu S, et al. A mechanism for microRNA arm switching regulated by Uridylation. Mol Cell. 2020;78(6):1224–1236.e5. doi: 10.1016/j.molcel.2020.04.030
  • Bofill-De Ros X, Hong Z, Birkenfeld B, et al. Flexible pri-miRNA structures enable tunable production of 5’ isomiRs. RNA Biol. 2022;19(1):279–289. doi: 10.1080/15476286.2022.2025680
  • Becker WR, Ober-Reynolds B, Jouravleva K, et al. High-throughput analysis reveals rules for target RNA binding and cleavage by AGO2. Mol Cell. 2019;75(4):741–755.e11. doi: 10.1016/j.molcel.2019.06.012
  • Helwak A, Kudla G, Dudnakova T, et al. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell. 2013;153(3):654–665. doi: 10.1016/j.cell.2013.03.043
  • Gu S, Jin L, Zhang F, et al. Biological basis for restriction of microRNA targets to the 3’ untranslated region in mammalian mRnas. Nat Struct Mol Biol. 2009;16:144–150. doi: 10.1038/nsmb.1552
  • Agarwal V, Bell GW, Nam J-W, et al. Predicting effective microRNA target sites in mammalian mRnas. Elife. 2015;4:4. doi: 10.7554/eLife.05005
  • Ruijtenberg S, Sonneveld S, Cui TJ, et al. mRNA structural dynamics shape Argonaute-target interactions. Nat Struct Mol Biol. 2020;27:790–801. doi: 10.1038/s41594-020-0461-1
  • Kim S, Kim S, Chang HR, et al. The regulatory impact of RNA-binding proteins on microRNA targeting. Nat Commun. 2021;12(1):5057. doi: 10.1038/s41467-021-25078-5
  • Baronti L, Guzzetti I, Ebrahimi P, et al. Base-pair conformational switch modulates miR-34a targeting of Sirt1 mRNA. Nature. 2020;583(7814):139–144. doi: 10.1038/s41586-020-2336-3
  • Willkomm S, Jakob L, Kramm K, et al. Single-molecule FRET uncovers hidden conformations and dynamics of human Argonaute 2. Nat Commun. 2022;13(1):3825. doi: 10.1038/s41467-022-31480-4
  • Kobayashi H, Singer RH. Single-molecule imaging of microRNA-mediated gene silencing in cells. Nat Commun. 2022;13(1):1435. doi: 10.1038/s41467-022-29046-5
  • Eisen TJ, Eichhorn SW, Subtelny AO, et al. MicroRNAs cause accelerated decay of short-tailed target mRnas. Mol Cell. 2020;77(4):775–785.e8. doi: 10.1016/j.molcel.2019.12.004
  • Subtelny AO, Eichhorn SW, Chen GR, et al. Poly(a)-tail profiling reveals an embryonic switch in translational control. Nature. 2014;508(7494):66–71. doi: 10.1038/nature13007
  • Dave P, Roth G, Griesbach E, et al. Single-molecule imaging reveals translation-dependent destabilization of mRnas. Mol Cell. 2023;83(4):589–606.e6. doi: 10.1016/j.molcel.2023.01.013
  • Iwakawa H-O, Tomari Y. Life of RISC: formation, action, and degradation of RNA-induced silencing complex. Mol Cell. 2022;82:30–43. doi: 10.1016/j.molcel.2021.11.026
  • Welte T, Goulois A, Stadler MB, et al. Convergence of multiple RNA-silencing pathways on GW182/TNRC6. Mol Cell. 2023;83(14):2478–2492.e8. doi: 10.1016/j.molcel.2023.06.001
  • Johnson ST, Chu Y, Liu J, et al. Impact of scaffolding protein TNRC6 paralogs on gene expression and splicing. RNA. 2021;27(9):1004–1016. doi: 10.1261/rna.078709.121
  • Sarshad AA, Juan AH, Muler AIC, et al. Argonaute-miRNA complexes silence target mRnas in the nucleus of mammalian stem cells. Mol Cell. 2018;71(6):1040–1050.e8. doi: 10.1016/j.molcel.2018.07.020
  • La Rocca G, King B, Shui B, et al. Inducible and reversible inhibition of miRNA-mediated gene repression in vivo. Elife. 2021;10:e70948. doi: 10.7554/eLife.70948
  • van Rooij E, Sutherland LB, Qi X, et al. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007;316(5824):575–579. doi: 10.1126/science.1139089
  • Rissland OS, Hong S-J, Bartel DP. MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol Cell. 2011;43(6):993–1004. doi: 10.1016/j.molcel.2011.08.021
  • Krol J, Busskamp V, Markiewicz I, et al. Characterizing light-regulated retinal microRnas reveals rapid turnover as a common property of neuronal microRnas. Cell. 2010;141(4):618–631. doi: 10.1016/j.cell.2010.03.039
  • Yang A, Shao T-J, Bofill-De Ros X, et al. AGO-bound mature miRnas are oligouridylated by TUTs and subsequently degraded by DIS3L2. Nat Commun. 2020;11(1):2765. doi: 10.1038/s41467-020-16533-w
  • Shukla S, Bjerke GA, Muhlrad D, et al. The RNase PARN controls the levels of specific miRnas that contribute to p53 regulation. Mol Cell. 2019;73(6):1204–1216.e4. doi: 10.1016/j.molcel.2019.01.010
  • Yu S, Kim VN. A tale of non-canonical tails: gene regulation by post-transcriptional RNA tailing. Nat Rev Mol Cell Biol. 2020;21(9):542–556. doi: 10.1038/s41580-020-0246-8
  • Morgan M, Much C, DiGiacomo M, et al. mRNA 3’ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome. Nature. 2017;548:347–351. doi: 10.1038/nature23318
  • Medhi R, Price J, Furlan G, et al. RNA uridyl transferases TUT4/7 differentially regulate miRNA variants depending on the cancer cell type. RNA. 2022;28(3):353–370. doi: 10.1261/rna.078976.121
  • Yang A, Bofill-De Ros X, Stanton R, et al. TENT2, TUT4, and TUT7 selectively regulate miRNA sequence and abundance. Nat Commun. 2022;13(1):5260. doi: 10.1038/s41467-022-32969-8
  • Mansur F, Ivshina M, Gu W, et al. Gld2-catalyzed 3’ monoadenylation of miRnas in the hippocampus has no detectable effect on their stability or on animal behavior. RNA. 2016;22:1492–1499. doi: 10.1261/rna.056937.116
  • Sheu-Gruttadauria J, Pawlica P, Klum SM, et al. Structural basis for target-directed MicroRNA degradation. Mol Cell. 2019;75(6):1243–1255.e7. doi: 10.1016/j.molcel.2019.06.019
  • Ameres SL, Horwich MD, Hung J-H, et al. Target RNA-directed trimming and tailing of small silencing RNAs. Science. 2010;328:1534–1539. doi: 10.1126/science.1187058
  • Elbarbary RA, Miyoshi K, Myers JR, et al. Tudor-SN-mediated endonucleolytic decay of human cell microRnas promotes G1/S phase transition. Science. 2017;356:859–862. doi: 10.1126/science.aai9372
  • Han J, LaVigne CA, Jones BT, et al. A ubiquitin ligase mediates target-directed microRNA decay independently of tailing and trimming. Science. 2020;370(6523):eabc9546. doi: 10.1126/science.abc9546
  • Shi CY, Kingston ER, Kleaveland B, et al. The ZSWIM8 ubiquitin ligase mediates target-directed microRNA degradation. Science. 2020;370(6523):eabc9359. doi: 10.1126/science.abc9359
  • Jones BT, Han J, Zhang H, et al. Target-directed microRNA degradation regulates developmental microRNA expression and embryonic growth in mammals. Genes Dev. 2023;37(13–14):661–674. doi: 10.1101/gad.350906.123
  • Shi CY, Elcavage LE, Chivukula RR, et al. ZSWIM8 destabilizes many murine microRnas and is required for proper embryonic growth and development. Genome Res. 2023;33(9):1482–1496. doi: 10.1101/gr.278073.123
  • Kingston ER, Blodgett LW, Bartel DP. Endogenous transcripts direct microRNA degradation in Drosophila, and this targeted degradation is required for proper embryonic development. Mol Cell. 2022;82(20):3872–3884.e9. doi: 10.1016/j.molcel.2022.08.029
  • Kleaveland B, Shi CY, Stefano J, et al. A network of noncoding regulatory RNAs acts in the mammalian Brain. Cell. 2018;174(2):350–362.e17. doi: 10.1016/j.cell.2018.05.022
  • Piwecka M, Glažar P, Hernandez-Miranda LR, et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science. 2017;357(6357):eaam8526. doi: 10.1126/science.aam8526
  • Hansen TB, Jensen TI, Clausen BH, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495(7441):384–388. doi: 10.1038/nature11993
  • Bitetti A, Mallory AC, Golini E, et al. MicroRNA degradation by a conserved target RNA regulates animal behavior. Nat Struct Mol Biol. 2018;25(3):244–251. doi: 10.1038/s41594-018-0032-x
  • Ghini F, Rubolino C, Climent M, et al. Endogenous transcripts control miRNA levels and activity in mammalian cells by target-directed miRNA degradation. Nat Commun. 2018;9(1):3119. doi: 10.1038/s41467-018-05182-9
  • Li L, Sheng P, Li T, et al. Widespread microRNA degradation elements in target mRnas can assist the encoded proteins. Genes Dev. 2021;35(23–24):1595–1609. doi: 10.1101/gad.348874.121
  • Sheng P, Li L, Li T, et al. Screening of drosophila microRNA-degradation sequences reveals Argonaute1 mRNA’s role in regulating miR-999. Nat Commun. 2023;14(1):2108. doi: 10.1038/s41467-023-37819-9
  • Han J, Mendell JT. MicroRNA turnover: a tale of tailing, trimming, and targets. Trends Biochem Sci. 2023;48(1):26–39. doi: 10.1016/j.tibs.2022.06.005
  • Wu P-H, Zamore PD. To Degrade a MicroRNA, Destroy Its Argonaute Protein. Mol Cell. 2021;81(2):223–225. doi: 10.1016/j.molcel.2020.12.043
  • Qi Y, Ding L, Zhang S, et al. A plant immune protein enables broad antitumor response by rescuing microRNA deficiency. Cell. 2022;185(11):1888–1904.e24. doi: 10.1016/j.cell.2022.04.030
  • Louloupi A, Ørom UAV. Inhibiting pri-miRNA processing with target site blockers. Methods Mol Biol. 2018;1823:63–68.
  • Yu A-M, Choi YH, Tu M-J, et al. RNA drugs and RNA targets for small molecules: principles, progress, and challenges. Pharmacol Rev. 2020;72(4):862–898. doi: 10.1124/pr.120.019554
  • Haniff HS, Liu X, Tong Y, et al. A structure-specific small molecule inhibits a miRNA-200 family member precursor and reverses a type 2 diabetes phenotype. Cell Chem Biol. 2021;29(2):300–311.e10. doi: 10.1016/j.chembiol.2021.07.006
  • Liu X, Haniff HS, Childs-Disney JL, et al. Targeted degradation of the oncogenic MicroRNA 17-92 cluster by Structure-Targeting Ligands. J Am Chem Soc. 2020;142(15):6970–6982. doi: 10.1021/jacs.9b13159
  • Golden RJ, Chen B, Li T, et al. An Argonaute phosphorylation cycle promotes microRNA-mediated silencing. Nature. 2017;542(7640):197–202. doi: 10.1038/nature21025
  • Quévillon Huberdeau M, Zeitler DM, Hauptmann J, et al. Phosphorylation of Argonaute proteins affects mRNA binding and is essential for microRNA-guided gene silencing in vivo. EMBO J. 2017;36(14):2088–2106. doi: 10.15252/embj.201696386
  • Bibel B, Elkayam E, Silletti S, et al. Target binding triggers hierarchical phosphorylation of human Argonaute-2 to promote target release. Elife. 2022;11:e76908. doi: 10.7554/eLife.76908
  • Sheu-Gruttadauria J, MacRae IJ. Phase transitions in the assembly and function of human miRISC. Cell. 2018;173(4):946–957.e16. doi: 10.1016/j.cell.2018.02.051
  • Gao Y, Zhu Y, Wang H, et al. Lipid-mediated phase separation of AGO proteins on the ER controls nascent-peptide ubiquitination. Mol Cell. 2022;82(7):1313–1328.e8. doi: 10.1016/j.molcel.2022.02.035