In vitro and animal study showing that SARS-CoV-2 RNA-binding protein Nsp9 suppresses extracellular release of microRNA let-7b, potentially inhibiting antiviral responses mediated by Toll-like Receptor 7 (TLR7). Authors identify dual mechanism inhibition of let-7b-mediated TLR7 activation, which would normally trigger antiviral inflammatory responses. Authors validated these findings in a Drosophila model, where Nsp9 expression induced an innate immune response that was suppressed by human let-7b co-expression. The study reveals a novel mechanism by which SARS-CoV-2 evades host immune responses and suggests that targeting the Nsp9-let-7b interaction could be a potential therapeutic strategy for COVID-19.
Mun et al., 7 Jul 2025, USA, peer-reviewed, 24 authors.
Contact: skang34@jhmi.edu, jehyun-yoon@ouhsc.edu, woonghee.lee@ucdenver.edu.
In vitro studies are an important part of preclinical research, however results may be very different in vivo.
SARS-CoV-2 RNA-binding protein suppresses extracellular miRNA release
RNA Biology, doi:10.1080/15476286.2025.2527494
SARS-CoV-2 is the betacoronavirus causing the COVID-19 pandemic. Although the SARS-CoV-2 genome and transcriptome were reported previously, the function of individual viral proteins is largely unknown. Utilizing biochemical and molecular biology methods, we identified that four SARS-CoV-2 RNA-binding proteins (RBPs) regulate the host RNA metabolism by direct interaction with mature miRNA let-7b revealed by Nuclear Magnetic Resonance spectroscopy (NMR). SARS-CoV-2 RBP Nsp9 primarily binds mature miRNA let-7b, a direct ligand of the Toll-like Receptor 7 (TLR7), one of the potential SARS-CoV-2 therapeutics. Nsp9 suppresses host gene expression possibly by promoting let-7b-mediated silencing of a cellular RNA polymerase, POLR2D. In addition, Nsp9 inhibits extracellular release of let-7b and subsequent antiviral activity via TLR7. These results demonstrate that SARS-CoV-2 hijacks the host RNA metabolism to suppress antiviral responses and to shut down cellular transcription. Our findings of how a natural ligand of TLR7, miRNA let-7b, is suppressed by SARS-CoV-2 RBPs will advance our understanding of COVID-19 and SARS-CoV-2 therapeutics.
Disclosure statement No potential conflict of interest was reported by the author(s).
Author contributions
References
Arunachalam, Wimmers, Mok, Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans, Science, doi:10.1126/science.abc6261
Biegel, Henderson, Cox, Cellular DEAD-box RNA helicase DDX6 modulates interaction of miR-122 with the 5′ untranslated region of hepatitis C virus RNA, Virology, doi:10.1016/j.virol.2017.04.014
Chatterjee, Ade, Nurik, Phosphorylation induces conformational rigidity at the C-terminal domain of AMPA receptors, J Phys Chem B, doi:10.1021/acs.jpcb.8b10749
Chen, Xiong, Bao, Convalescent plasma as a potential therapy for COVID-19, Lancet Infect Dis, doi:10.1016/S1473-3099(20)30141-9
Croce, Causes and consequences of microRNA dysregulation in cancer, Nat Rev Genet, doi:10.1038/nrg2634
Cullen, Viral and cellular messenger RNA targets of viral microRNAs, Nature, doi:10.1038/nature07757
Delaglio, Grzesiek, Vuister, Nmrpipe: a multidimensional spectral processing system based on UNIX pipes, J Biomol NMR, doi:10.1007/bf00197809
Diebold, Kaisho, Hemmi, Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA, Science, doi:10.1126/science.1093616
Dudás, Puglisi, Korn, Backbone chemical shift spectral assignments of SARS coronavirus-2 non-structural protein nsp9, Biomol NMR Assign, doi:10.1007/s12104-021-10011-0
Dunckley, Parker, The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif, Embo J, doi:10.1093/emboj/18.19.5411
Eastman, Swails, Chodera, OpenMM 7: rapid development of high performance algorithms for molecular dynamics, PLOS Comput Biol, doi:10.1371/journal.pcbi.1005659
Egloff, Ferron, Campanacci, The severe acute respiratory syndrome-coronavirus replicative protein nsp9 is a single-stranded RNA-binding subunit unique in the RNA virus world, Proc Natl Acad Sci, doi:10.1073/pnas.0307877101
Furuichi, Lafiandra, Shatkin, 5′-terminal structure and mRNA stability, Nature, doi:10.1038/266235a0
Gao, Tian, Yang, Breakthrough: chloroquine phosphate has shown apparent efficacy in treatment of COVID-19 associated pneumonia in clinical studies, Biosci Trends, doi:10.5582/bst.2020.01047
Gautret, Lagier, Parola, Hydroxychloroquine and azithromycin as a treatment of COVID-19: results of an open-label non-randomized clinical trial, Int J Antimicrob Agents, doi:10.1016/j.ijantimicag.2020.105949
Gomez-Carballa, Pardo-Seco, Pischedda, Sex-biased expression of the TLR7 gene in severe COVID-19 patients: insights from transcriptomics and epigenomics, Environ Res, doi:10.1016/j.envres.2022.114288
Gordon, Jang, Bouhaddou, A SARS-CoV-2 protein interaction map reveals targets for drug repurposing, Nature, doi:10.1038/s41586-020-2286-9
Groban, Narayanan, Jacobson, Conformational changes in protein loops and helices induced by post-translational phosphorylation, PLOS Comput Biol, doi:10.1371/journal.pcbi.0020032
Guichard, Lu, Kanca, A comprehensive Drosophila resource to identify key functional interactions between SARS-CoV-2 factors and host proteins, Cell Rep, doi:10.1016/j.celrep.2023.112842
Guo, Price, RNA polymerase II transcription elongation control, Chem Rev, doi:10.1021/cr400105n
Gómez-Carballa, Pardo-Seco, Pischedda, Sex-biased expression of the TLR7 gene in severe COVID-19 patients: insights from transcriptomics and epigenomics, Environ Res, doi:10.1016/j.envres.2022.114288
Hossein-Khannazer, Shokoohian, Shpichka, Novel therapeutic approaches for treatment of COVID-19, J Mol Med, doi:10.1007/s00109-020-01927-6
Hu, Xie, Onishi, Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling, Cell, doi:10.1016/j.cell.2009.08.037
Huang Da, Sherman, Lempicki, Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists, Nucleic Acids Res, doi:10.1093/nar/gkn923
Huang Da, Sherman, Lempicki, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat Protoc, doi:10.1038/nprot.2008.211
Jeong, Jiang, Albino, Rapid identification of monospecific monoclonal antibodies using a human proteome microarray, Mol Cell Proteomics, doi:10.1074/mcp.O111.016253
Khushman, Bhardwaj, Patel, Exosomal markers (CD63 and CD9) expression pattern using immunohistochemistry in resected malignant and nonmalignant pancreatic specimens, Pancrease, doi:10.1097/MPA.0000000000000847
Kim, Chung, Jo, Identification of coronavirus isolated from a patient in Korea with COVID-19, Osong Public Health Res Perspect, doi:10.24171/j.phrp.2020.11.1.02
Kim, Kuwano, Srikantan, HuR recruits let-7/RISC to repress c-Myc expression, Genes Dev, doi:10.1101/gad.1812509
Kim, Lee, Yang, The architecture of SARS-CoV-2 transcriptome, Cell, doi:10.1016/j.cell.2020.04.011
Kincaid, Sullivan, Hobman, Virus-encoded microRNAs: an overview and a look to the future, PLoS Pathog, doi:10.1371/journal.ppat.1003018
Kwon, Liu, Mostov, Intercellular transfer of GPRC5B via exosomes drives HGF-mediated outward growth, Curr Biol, doi:10.1016/j.cub.2013.12.010
Lee, Cornilescu, Dashti, Integrative NMR for biomolecular research, J Biomol NMR, doi:10.1007/s10858-016-0029-x
Lee, Rahimi, Lee, POKY: a software suite for multidimensional NMR and 3D structure calculation of biomolecules, Bioinformatics, doi:10.1093/bioinformatics/btab180
Lehmann, Krüger, Park, An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration, Nat Neurosci, doi:10.1038/nn.3113
Li, Lian, Moser, Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago2-mediated silencing, J Cell Sci, doi:10.1242/jcs.036905
Lin, Zhang, Xiang, Exosomes derived from HeLa cells break down vascular integrity by triggering endoplasmic reticulum stress in endothelial cells, J Extracell Vesicles, doi:10.1080/20013078.2020.1722385
Littler, Gully, Colson, Crystal structure of the SARS-CoV-2 non-structural protein 9, Nsp9, Iscience, doi:10.1016/j.isci.2020.101258
Maeta, Kataoka, Nishiya, RNA polymerase II subunit D is essential for zebrafish development, Sci Rep, doi:10.1038/s41598-020-70110-1
Mantovani, Daga, Fallerini, Rare variants in Toll-like receptor 7 results in functional impairment and downregulation of cytokine-mediated signaling in COVID-19 patients, Genes Immun, doi:10.1038/s41435-021-00157-1
Mcnab, Mayer-Barber, Sher, Type I interferons in infectious disease, Nat Rev Immunol, doi:10.1038/nri3787
Menachery, Graham, Baric, Jumping species-a mechanism for coronavirus persistence and survival, Curr Opin Virol, doi:10.1016/j.coviro.2017.01.002
Merino, Raad, Bugnon, Novel SARS-CoV-2 encoded small RNAs in the passage to humans, Bioinformatics, doi:10.1093/bioinformatics/btaa1002
Miknis, Donaldson, Umland, Severe acute respiratory syndrome coronavirus nsp9 dimerization is essential for efficient viral growth, J Virol, doi:10.1128/JVI.01505-08
Min, Choi, Mun, Mature microRNA-binding protein QKI suppresses extracellular microRNA let-7b release, J Cell Sci, doi:10.1242/jcs.261575
Min, Davila, Zealy, eIF4E phosphorylation by MST1 reduces translation of a subset of mRNAs, but increases lncRNA translation, Biochim Biophys Acta Gene Regul Mech, doi:10.1016/j.bbagrm.2017.05.002
Min, Jo, Shin, AUF1 facilitates microRNA-mediated gene silencing, Nucleic Acids Res, doi:10.1093/nar/gkx149
Min, Zealy, Davila, Profiling of m6A RNA modifications identified an age-associated regulation of AGO 2 mRNA stability, Aging Cell, doi:10.1111/acel.12753
Minakhina, Steward, Melanotic mutants in Drosophila: pathways and phenotypes, Genetics, doi:10.1534/genetics.106.061978
Mizrahi, Nachshon, Shitrit, Virus-induced changes in mRNA secondary structure uncover cis-regulatory elements that directly control gene expression, Mol Cell, doi:10.1016/j.molcel.2018.09.003
Mun, Lee, Choi, Targeting of CYP2E1 by miRnas in alcohol-induced intestine injury, Mol Cells, doi:10.1016/j.mocell.2024.100074
Nikolov, Burley, RNA polymerase II transcription initiation: a structural view, Proc Natl Acad Sci, doi:10.1073/pnas.94.1.15
O'boyle, Banck, James, Open babel: an open chemical toolbox, J Cheminform, doi:10.1186/1758-2946-3-33
O'connell, Kahn, Gibson, MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development, Immunity, doi:10.1016/j.immuni.2010.09.009
Park, Osinski, Hernandez, The mechanism of RNA capping by SARS-CoV-2, Nature, doi:10.1038/s41586-022-05185-z
Rahimi, Chiu, Lopez Giraldo, REDEN: interactive multi-fitting decomposition-based NMR peak picking assistant, J Magn Reson, doi:10.1016/j.jmr.2023.107600
Rüdel, Wang, Lenobel, Phosphorylation of human argonaute proteins affects small RNA binding, Nucleic Acids Res, doi:10.1093/nar/gkq1032
Shen, Bax, Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks, J Biomol NMR, doi:10.1007/s10858-013-9741-y
Snijder, Decroly, Ziebuhr, The nonstructural proteins directing coronavirus RNA synthesis and processing, Adv Virus Res
Sola, Almazán, Zúñiga, Continuous and discontinuous RNA synthesis in coronaviruses, Annu Rev Virol, doi:10.1146/annurev-virology-100114-055218
Sonoda, Lee, Park, miRNA profiling of urinary exosomes to assess the progression of acute kidney injury, Sci Rep, doi:10.1038/s41598-019-40747-8
Stevens, mRNA-decapping enzyme from Saccharomyces cerevisiae: purification and unique specificity for long RNA chains, Mol Cell Biol, doi:10.1128/MCB.8.5.2005
Thapar, Structural basis for regulation of RNA-binding proteins by phosphorylation, ACS Chem Biol, doi:10.1021/cb500860x
Titos, Juginović, Vaccaro, A gut-secreted peptide suppresses arousability from sleep, Cell, doi:10.1016/j.cell.2023.02.022
Trott, Olson, AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading, J Comput Chem, doi:10.1002/jcc.21334
Yoon, Abdelmohsen, Kim, Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination, Nat Commun, doi:10.1038/ncomms3939
Yoon, Abdelmohsen, Srikantan, LincRNA-p21 suppresses target mRNA translation, Mol Cell, doi:10.1016/j.molcel.2012.06.027
Yoon, Jo, White, AUF1 promotes let-7b loading on argonaute 2, Genes Dev, doi:10.1101/gad.263749.115
Zealy, Wrenn, Davila, microRNA-binding proteins: specificity and function, Wiley Interdiscip Rev: RNA, doi:10.1002/wrna.1414
Zhang, Amahong, Sun, The miRNA: a small but powerful RNA for COVID-19, Brief Bioinform, doi:10.1093/bib/bbab062
Zhou, Yang, Wang, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, doi:10.1038/s41586-020-2012-7
Zhu, Zhang, Song, SARS-CoV-2-encoded MiRNAs inhibit host type I interferon pathway and mediate allelic differential expression of susceptible gene, Front Immunol, doi:10.3389/fimmu.2021.767726
Zhu, Zhang, Wang, A novel coronavirus from patients with pneumonia in China, N Engl J Med, doi:10.1056/NEJMoa2001017
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