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The stability of mRNA secondary structure at the ribosomal entry site within the frameshifting stimulating elements (FSEs) determines the frameshifting efficiency. Here, we report the development of a programmable mRNA-based platform that detects specific mature microRNA (miRNA or miR) by converting their presence into a quantifiable protein output through miRNA-triggered \u22121 PRF. We designed a triplex-forming mRNA (TF-mRNA) platform to selectively trap target miRNAs through the formation of major-groove mRNA\u2013miRNA\u2013mRNA (miR\u2013mRNA2) triplexes. Biolayer interferometry and fluorescence binding studies confirmed that TF-mRNA forms stable complexes with cognate miRNAs with low nanomolar affinity and prolonged dissociation rate. Critically, the formation of miR\u2013mRNA2 triplex robustly stimulated ribosomal frameshifting in a cell-free dual-luciferase translation system, acting as a miRNA-dependent molecular switch. The generality of this TF-mRNA platform has been verified for several disease-associated purine-rich miRNAs, and it is suitable for targeting a wide range of other purine-enriched miRNAs. This programmable TF-mRNA platform establishes a foundation for developing novel diagnostic tools and synthetic biology circuits that convert the presence of miRNA into a quantifiable protein output.<\/jats:p>","DOI":"10.1021\/acssynbio.5c00883","type":"journal-article","created":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T06:51:02Z","timestamp":1784271062000},"page":"3158-3167","source":"Crossref","is-referenced-by-count":0,"title":["A Programmable\nmRNA Platform for miRNA Detection via\nmiRNA\u2013mRNA2 Triplex-Mediated Ribosomal Frameshifting"],"prefix":"10.1021","volume":"15","author":[{"given":"Yanyu","family":"Chen","sequence":"first","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanqi","family":"Zhao","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huizhen","family":"Chen","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]},{"name":"The Chinese University of Hong Kong , , Shatin, N.T. , ,","place":["Hong Kong SAR, P. R. China, 999077"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanting","family":"Zhou","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shijian","family":"Fan","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liping","family":"Xing","sequence":"additional","affiliation":[{"name":"Shenzhen Bay Laboratory , , , ,","place":["Shenzhen, Guangdong, P. R. China, 518132"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yun","family":"Lian","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongyu","family":"Duan","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuze","family":"Dai","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5536-0439","authenticated-orcid":true,"given":"Zheng","family":"Zhao","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rongguang","family":"Lu","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]},{"name":"Shenzhen Bay Laboratory , , , ,","place":["Shenzhen, Guangdong, P. R. China, 518132"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0486-4530","authenticated-orcid":true,"given":"Chenzhong","family":"Li","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4386-0740","authenticated-orcid":true,"given":"Cheng","family":"Jiang","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ho Yin Edwin","family":"Chan","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong , , Shatin, N.T. , ,","place":["Hong Kong SAR, P. R. China, 999077"]},{"name":"The Chinese University of Hong Kong , , Shatin, N.T. , ,","place":["Hong Kong SAR, P. R. China, 999077"]},{"name":"The Chinese University of Hong Kong , , Shatin, N.T. , ,","place":["Hong Kong SAR, P. R. China, 999077"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8772-9755","authenticated-orcid":true,"given":"Gang","family":"Chen","sequence":"additional","affiliation":[{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]},{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]},{"name":"The Chinese University of Hong Kong (Shenzhen) , , Longgang , , ,","place":["Shenzhen, Guangdong, P. R. China, 518172"]},{"name":"The Chinese University of Hong Kong (Shenzhen) Futian Biomedical Innovation R&D Center , , ,","place":["Shenzhen, Guangdong, P. R. China, 518031"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,7,17]]},"reference":[{"issue":"1","key":"2026082212130302900_cit1","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.virusres.2005.10.008","article-title":"Programmed ribosomal frameshifting in HIV-1 and the\nSARS\u2013CoV","volume":"119","author":"Brierley","year":"2006","journal-title":"Virus Res."},{"issue":"20","key":"2026082212130302900_cit2","doi-asserted-by":"publisher","first-page":"8952","DOI":"10.1093\/nar\/gkr579","article-title":"Stem-loop structures\ncan effectively substitute for an RNA pseudoknot in \u22121 ribosomal\nframeshifting","volume":"39","author":"Yu","year":"2011","journal-title":"Nucleic Acids Res."},{"issue":"7090","key":"2026082212130302900_cit3","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1038\/nature04735","article-title":"A mechanical explanation\nof RNA pseudoknot function in programmed ribosomal frameshifting","volume":"441","author":"Namy","year":"2006","journal-title":"Nature"},{"issue":"3","key":"2026082212130302900_cit4","doi-asserted-by":"publisher","first-page":"1901","DOI":"10.1093\/nar\/gks1254","article-title":"HIV-1 frameshift efficiency\nis primarily determined by the stability of base pairs positioned\nat the mRNA entrance channel of the ribosome","volume":"41","author":"Mouzakis","year":"2013","journal-title":"Nucleic Acids Res."},{"issue":"31","key":"2026082212130302900_cit5","doi-asserted-by":"publisher","first-page":"12706","DOI":"10.1073\/pnas.0905046106","article-title":"Triplex structures in\nan RNA pseudoknot enhance mechanical stability and increase efficiency\nof \u22121 ribosomal frameshifting","volume":"106","author":"Chen","year":"2009","journal-title":"Proc.\nNatl. Acad. Sci. U.S.A."},{"issue":"1","key":"2026082212130302900_cit6","doi-asserted-by":"publisher","DOI":"10.1038\/srep39549","article-title":"Mechanical unfolding\nkinetics of the SRV-1 gag-pro mRNA pseudoknot: possible implications\nfor \u2013 1 ribosomal frameshifting stimulation","volume":"6","author":"Zhong","year":"2016","journal-title":"Sci. Rep."},{"issue":"46","key":"2026082212130302900_cit7","doi-asserted-by":"publisher","first-page":"4429","DOI":"10.1021\/acs.biochem.0c00611","article-title":"Tertiary Base Triple\nFormation in the SRV-1 Frameshifting Pseudoknot Stabilizes Secondary\nStructure Components","volume":"59","author":"Yang","year":"2020","journal-title":"Biochemistry"},{"issue":"23","key":"2026082212130302900_cit8","doi-asserted-by":"publisher","first-page":"11435","DOI":"10.1021\/ac402497x","article-title":"Unusual \u2013 1 Ribosomal Frameshift Caused by Stable\nRNA G-Quadruplex in Open Reading Frame","volume":"85","author":"Endoh","year":"2013","journal-title":"Anal.\nChem."},{"issue":"3","key":"2026082212130302900_cit9","doi-asserted-by":"publisher","first-page":"1887","DOI":"10.1093\/nar\/gkt1022","article-title":"Stimulation of ribosomal frameshifting\nby RNA G-quadruplex structures","volume":"42","author":"Yu","year":"2014","journal-title":"Nucleic Acids\nRes."},{"issue":"40","key":"2026082212130302900_cit10","doi-asserted-by":"publisher","first-page":"16167","DOI":"10.1073\/pnas.1204114109","article-title":"Programmed \u2013 1 frameshifting\nefficiency correlates with RNA pseudoknot conformational plasticity,\nnot resistance to mechanical unfolding","volume":"109","author":"Ritchie","year":"2012","journal-title":"Proc.\nNatl. Acad. Sci. U.S.A."},{"issue":"39","key":"2026082212130302900_cit11","doi-asserted-by":"publisher","first-page":"19500","DOI":"10.1073\/pnas.1905258116","article-title":"Complex dynamics under\ntension in a high-efficiency frameshift stimulatory structure","volume":"116","author":"Halma","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"issue":"12","key":"2026082212130302900_cit12","doi-asserted-by":"publisher","first-page":"1302","DOI":"10.1021\/ar200098t","article-title":"The Molecular Interactions\nThat Stabilize RNA Tertiary\nStructure: RNA Motifs, Patterns, and Networks","volume":"44","author":"Butcher","year":"2011","journal-title":"Acc. Chem. Res."},{"issue":"1","key":"2026082212130302900_cit13","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1002\/wrna.1261","article-title":"RNA triplexes: from\nstructural principles to biological and biotech applications","volume":"6","author":"Devi","year":"2015","journal-title":"WIREs RNA"},{"issue":"6548","key":"2026082212130302900_cit14","doi-asserted-by":"publisher","first-page":"1306","DOI":"10.1126\/science.abf3546","article-title":"Structural basis of\nribosomal frameshifting during translation of the SARS-CoV-2 RNA genome","volume":"372","author":"Bhatt","year":"2021","journal-title":"Science"},{"issue":"5","key":"2026082212130302900_cit15","doi-asserted-by":"publisher","DOI":"10.1016\/j.xcrp.2026.103281","article-title":"Isoenergetic peptide nucleic acid probes for\ntargeting double-stranded RNAs via enhanced sequence-specific stacking\ninteractions","volume":"7","author":"Lu","year":"2026","journal-title":"Cell Rep. Phys. Sci."},{"key":"2026082212130302900_cit16","doi-asserted-by":"publisher","DOI":"10.1016\/j.xcrp.2024.102150","article-title":"Recognition of RNA secondary\nstructures with a programmable peptide nucleic acid-based platform","volume":"5","author":"Lu","year":"2024","journal-title":"Cell Rep. Phys. Sci."},{"issue":"1","key":"2026082212130302900_cit17","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1021\/acs.biochem.7b00744","article-title":"Selective Binding to mRNA Duplex Regions\nby Chemically Modified Peptide Nucleic Acids Stimulates Ribosomal\nFrameshifting","volume":"57","author":"Puah","year":"2018","journal-title":"Biochemistry"},{"issue":"6","key":"2026082212130302900_cit18","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.1261\/rna.1922410","article-title":"Stimulation\nof \u22121 programmed\nribosomal frameshifting by a metabolite-responsive RNA pseudoknot","volume":"16","author":"Chou","year":"2010","journal-title":"RNA"},{"issue":"18","key":"2026082212130302900_cit19","doi-asserted-by":"publisher","first-page":"9005","DOI":"10.1093\/nar\/gkw718","article-title":"Rational design of a synthetic mammalian riboswitch\nas a ligand-responsive \u22121 ribosomal frame-shifting stimulator","volume":"44","author":"Lin","year":"2016","journal-title":"Nucleic Acids Res."},{"issue":"19","key":"2026082212130302900_cit20","doi-asserted-by":"publisher","first-page":"7537","DOI":"10.1074\/jbc.REV119.006348","article-title":"Translational\nrecoding signals: Expanding the synthetic biology toolbox","volume":"294","author":"Dinman","year":"2019","journal-title":"J. Biol. Chem."},{"issue":"12","key":"2026082212130302900_cit21","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1038\/s41576-023-00611-y","article-title":"microRNAs in action: biogenesis, function\nand regulation","volume":"24","author":"Shang","year":"2023","journal-title":"Nat. Rev. Genet."},{"issue":"5","key":"2026082212130302900_cit22","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/0092-8674(93)90529-Y","article-title":"The C. elegans heterochronic gene\nlin-4 encodes small RNAs with antisense complementarity to lin-14","volume":"75","author":"Lee","year":"1993","journal-title":"Cell"},{"issue":"5","key":"2026082212130302900_cit23","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1016\/0092-8674(93)90530-4","article-title":"Posttranscriptional\nregulation of the heterochronic\ngene lin-14 by lin-4 mediates temporal pattern formation in C. elegans","volume":"75","author":"Wightman","year":"1993","journal-title":"Cell"},{"issue":"6808","key":"2026082212130302900_cit24","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1038\/35040556","article-title":"Conservation\nof the\nsequence and temporal expression of let-7 heterochronic regulatory\nRNA","volume":"408","author":"Pasquinelli","year":"2000","journal-title":"Nature"},{"issue":"3","key":"2026082212130302900_cit25","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/nrd.2016.246","article-title":"MicroRNA therapeutics:\ntowards a new era for the management\nof cancer and other diseases","volume":"16","author":"Rupaimoole","year":"2017","journal-title":"Nat. Rev. Drug\nDiscovery"},{"issue":"2","key":"2026082212130302900_cit26","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1016\/j.chom.2014.12.014","article-title":"miR-122 stimulates hepatitis\nC virus RNA synthesis by altering the balance of viral RNAs engaged\nin replication versus translation","volume":"17","author":"Masaki","year":"2015","journal-title":"Cell Host\nMicrobe"},{"issue":"3","key":"2026082212130302900_cit27","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2021.109839","article-title":"Role of\nmiR-2392 in\ndriving SARS-CoV-2 infection","volume":"37","author":"McDonald","year":"2021","journal-title":"Cell Rep."},{"issue":"4","key":"2026082212130302900_cit28","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/j.tibs.2024.01.002","article-title":"Pre-twisting\nfor improved genome modification and miRNA targeting","volume":"49","author":"Lu","year":"2024","journal-title":"Trends Biochem. Sci."},{"issue":"1","key":"2026082212130302900_cit29","doi-asserted-by":"publisher","DOI":"10.1016\/j.xcrm.2023.101354","article-title":"Antitumor efficacy of\na sequence-specific DNA-targeted gammaPNA-based c-Myc inhibitor","volume":"5","author":"Malik","year":"2024","journal-title":"Cell Rep. Med."},{"issue":"15","key":"2026082212130302900_cit30","doi-asserted-by":"publisher","first-page":"1999","DOI":"10.1039\/D3CC05409H","article-title":"Triplex-forming\npeptide nucleic acids\nas emerging ligands to modulate structure and function of complex\nRNAs","volume":"60","author":"Katkevics","year":"2024","journal-title":"Chem. Commun."},{"issue":"6","key":"2026082212130302900_cit31","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abq7459","article-title":"Anti-seed PNAs targeting\nmultiple oncomiRs for brain tumor therapy","volume":"9","author":"Wang","year":"2023","journal-title":"Sci.\nAdv."},{"issue":"10","key":"2026082212130302900_cit32","doi-asserted-by":"publisher","DOI":"10.1016\/j.xcrp.2023.101635","article-title":"DNA recognition and\ninduced genome modification by a hydroxymethyl-gamma tail-clamp peptide\nnucleic acid","volume":"4","author":"Oyaghire","year":"2023","journal-title":"Cell Rep. Phys. Sci."},{"issue":"15","key":"2026082212130302900_cit33","doi-asserted-by":"publisher","DOI":"10.1002\/cbic.202300291","article-title":"Nucleobase and Linker\nModification for Triple-Helical Recognition of Pyrimidines in RNA\nUsing Peptide Nucleic Acids","volume":"24","author":"Kumpina","year":"2023","journal-title":"ChemBioChem."},{"issue":"10","key":"2026082212130302900_cit34","doi-asserted-by":"publisher","DOI":"10.1016\/j.xcrp.2023.101584","article-title":"Head-to-head comparison\nof in vitro and in vivo efficacy of pHLIP-conjugated anti-seed gamma\npeptide nucleic acids","volume":"4","author":"Dhuri","year":"2023","journal-title":"Cell Rep. Phys. Sci."},{"issue":"6","key":"2026082212130302900_cit35","doi-asserted-by":"publisher","first-page":"4008","DOI":"10.1093\/nar\/gkt1367","article-title":"Incorporation of thio-pseudoisocytosine\ninto triplex-forming peptide nucleic acids for enhanced recognition\nof RNA duplexes","volume":"42","author":"Devi","year":"2014","journal-title":"Nucleic Acids Res."},{"issue":"2","key":"2026082212130302900_cit36","doi-asserted-by":"publisher","DOI":"10.1002\/bip.23476","article-title":"Mechanisms and applications of peptide\nnucleic acids selectively binding to double-stranded RNA","volume":"113","author":"Zhan","year":"2022","journal-title":"Biopolymers"},{"issue":"1","key":"2026082212130302900_cit37","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-31387-5","article-title":"Modified RNA triplexes: Thermodynamics,\nstructure and biological potential","volume":"8","author":"Szabat","year":"2018","journal-title":"Sci. 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