A comparative survey of the influence of small self-cleaving ribozymes on gene expression in human cell culture

References

• Cech TR, Zaug AJ, Grabowski PJ. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell. 1981;27(3 Pt 2):487–496. doi: 10.1016/0092-8674(81)90390-1
   PubMed Web of Science ®Google Scholar
• Guerrier-Takada C, Gardiner K, Marsh T, et al. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 1983;35(3):849–857. doi: 10.1016/0092-8674(83)90117-4
   PubMed Web of Science ®Google Scholar
• Nissen P, Hansen J, Ban N, et al. The structural basis of ribosome activity in peptide bond synthesis. Science. 2000;289(5481):920–930. doi: 10.1126/science.289.5481.920
   PubMed Web of Science ®Google Scholar
• Herschlag D, Cech TR. Catalysis of RNA cleavage by the tetrahymena thermophila ribozyme. 1. Kinetic description of the reaction of an RNA substrate complementary to the active site. Biochemistry. 1990;29(44):10159–71. doi: 10.1021/bi00496a003
   PubMed Web of Science ®Google Scholar
• Peebles CL, Perlman PS, Mecklenburg KL, et al. A self-splicing RNA excises an intron lariat. Cell. 1986;44(2):213–223. doi: 10.1016/0092-8674(86)90755-5
   PubMed Web of Science ®Google Scholar
• Prody GA, Bakos JT, Buzayan JM, et al. Autolytic processing of dimeric plant virus satellite RNA. Science. 1986;231(4745):1577–1580. doi: 10.1126/science.231.4745.1577
   PubMed Web of Science ®Google Scholar
• Deng J, Wilson TJ, Wang J, et al. Structure and mechanism of a methyltransferase ribozyme. Nat Chem Biol. 2022;18(5):556–564. doi: 10.1038/s41589-022-00982-z
   PubMed Web of Science ®Google Scholar
• Weinberg CE, Weinberg Z, Hammann C. Novel ribozymes: discovery, catalytic mechanisms, and the quest to understand biological function. Nucleic Acids Res. 2019;47(18):9480–9494. doi: 10.1093/nar/gkz737
   PubMed Web of Science ®Google Scholar
• Jimenez RM, Polanco JA, Lupták A. Chemistry and Biology of self-cleaving ribozymes. Trends Biochem Sci. 2015;40(11):648–661. doi: 10.1016/j.tibs.2015.09.001
   PubMed Web of Science ®Google Scholar
• Peng H, Latifi B, Müller S, et al. Self-cleaving ribozymes: substrate specificity and synthetic biology applications. RSC Chem Biol. 2021;2(5):1370–1383. doi: 10.1039/D0CB00207K
   PubMedGoogle Scholar
• Chen Y, Qi F, Gao F, et al. Hovlinc is a recently evolved class of ribozyme found in human lncRNA. Nat Chem Biol. 2021;17(5):601–607. doi: 10.1038/s41589-021-00763-0
   PubMed Web of Science ®Google Scholar
• Forster AC, Symons RH. Self-cleavage of virusoid RNA is performed by the proposed 55-nucleotide active site. Cell. 1987;50(1):9–16. doi: 10.1016/0092-8674(87)90657-X
   PubMed Web of Science ®Google Scholar
• Buzayan JM, Gerlach WL, Bruening G. Satellite tobacco ringspot virus RNA: a subset of the RNA sequence is sufficient for autolytic processing. Proc Natl Acad Sci, USA. 1986;83(23):8859–8862. doi: 10.1073/pnas.83.23.8859
   PubMed Web of Science ®Google Scholar
• Sharmeen L, Kuo MY, Dinter-Gottlieb G, et al. Antigenomic RNA of human hepatitis delta virus can undergo self-cleavage. J Virol. 1988;62(8):2674–2679. doi: 10.1128/jvi.62.8.2674-2679.1988
   PubMed Web of Science ®Google Scholar
• Saville BJ, Collins RA. A site-specific self-cleavage reaction performed by a novel rna in Neurospora Mitochondria. Cell. 1990;61(4):685–696. doi: 10.1016/0092-8674(90)90480-3
   PubMed Web of Science ®Google Scholar
• Barrick JE, Corbino KA, Winkler WC, et al. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci, USA. 2004;101(17):6421–6426. doi: 10.1073/pnas.0308014101
   PubMed Web of Science ®Google Scholar
• Kolev NG, Hartland EI, Huber PW. A manganese-dependent ribozyme in the 3 ’-untranslated region of xenopus Vg1 mRNA. Nucleic Acids Res. 2008;36(17):5530–5539. doi: 10.1093/nar/gkn530
   PubMed Web of Science ®Google Scholar
• Roth A, Weinberg Z, Chen AGY, et al. A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat Chem Biol. 2014;10(1):56–60. doi: 10.1038/nchembio.1386
   PubMed Web of Science ®Google Scholar
• Weinberg Z, Kim PB, Chen TH, et al. New classes of self-cleaving ribozymes revealed by comparative genomics analysis. Nat Chem Biol. 2015;11(8):606–610. doi: 10.1038/nchembio.1846
   PubMed Web of Science ®Google Scholar
• Beilstein K, Wittmann A, Grez M, et al. Conditional control of mammalian gene expression by Tetracycline-Dependent Hammerhead Ribozymes. ACS Synth Biol. 2015;4(5):526–534. doi: 10.1021/sb500270h
   PubMed Web of Science ®Google Scholar
• Harris KA, Lünse CE, Li S, et al. Biochemical analysis of pistol self-cleaving ribozymes. RNA. 2015;21(11):1852–1858. doi: 10.1261/rna.052514.115
   PubMed Web of Science ®Google Scholar
• Hernandez AJ, Zovoilis A, Cifuentes-Rojas C, et al. B2 and ALU retrotransposons are self-cleaving ribozymes whose activity is enhanced by EZH2. Proc Natl Acad Sci, USA. 2020;117(1):415–425. doi: 10.1073/pnas.1917190117
   PubMed Web of Science ®Google Scholar
• Tang J, Breaker RR. Structural diversity of self-cleaving ribozymes. Proc Natl Acad Sci U S A. 2000;97(11):5784–9. doi: 10.1073/pnas.97.11.5784
   PubMed Web of Science ®Google Scholar
• Williams KP, Ciafré S, Tocchini-Valentini GP. Selection of novel Mg(2+)-dependent self-cleaving ribozymes. EMBO J. 1995;14(18):4551–4557. doi: 10.1002/j.1460-2075.1995.tb00134.x
   PubMed Web of Science ®Google Scholar
• Canny MD, Jucker FM, Kellogg E, et al. Fast cleavage kinetics of a natural hammerhead ribozyme. J Am Chem Soc. 2004;126(35):10848–10849. doi: 10.1021/ja046848v
   PubMed Web of Science ®Google Scholar
• Martick M, Scott WG. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell. 2006;126(2):309–320. doi: 10.1016/j.cell.2006.06.036
   PubMed Web of Science ®Google Scholar
• Ren A, Micura R, Patel DJ. Structure-based mechanistic insights into catalysis by small self-cleaving ribozymes. Curr Opin Chem Biol. 2017;41:71–83. doi: 10.1016/j.cbpa.2017.09.017
   PubMed Web of Science ®Google Scholar
• Emilsson GM, Nakamura S, Roth A, et al. Ribozyme speed limits. RNA. 2003;9(8):907–918. doi: 10.1261/rna.5680603
   PubMed Web of Science ®Google Scholar
• De La Peña M, Ceprián R, Casey JL, et al. Hepatitis delta virus-like circular RNAs from diverse metazoans encode conserved hammerhead ribozymes. Virus Evol. 2021;7(1). doi: 10.1093/ve/veab016
   PubMed Web of Science ®Google Scholar
• Eckert I, Friedrich R, Weinberg CE, et al. Discovery of natural non-circular permutations in non-coding RNAs. Nucleic Acids Res. 2023;51(6):2850–2861. doi: 10.1093/nar/gkad137
   PubMed Web of Science ®Google Scholar
• Weinberg CE, Olzog VJ, Eckert I, et al. Identification of over 200-fold more hairpin ribozymes than previously known in diverse circular RNAs. Nucleic Acids Res. 2021;49(11):6375–6388. doi: 10.1093/nar/gkab454
   PubMed Web of Science ®Google Scholar
• García-Robles I, Sánchez-Navarro J, De La Peña M. Intronic hammerhead ribozymes in mRNA biogenesis. Biol Chem. 2012;393(11):1317–1326. doi: 10.1515/hsz-2012-0223
   PubMed Web of Science ®Google Scholar
• Salehi-Ashtiani K, Lupták A, Litovchick A, et al. A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene. Science. 2006;313(5794):1788–1792. doi: 10.1126/science.1129308
   PubMed Web of Science ®Google Scholar
• Winkler WC, Nahvi A, Roth A, et al. Control of gene expression by a natural metabolite-responsive ribozyme. Nature. 2004;428(6980):281–286. doi: 10.1038/nature02362
   PubMed Web of Science ®Google Scholar
• Collins JA, Irnov I, Baker S, et al. Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev. 2007;21(24):3356–3368. doi: 10.1101/gad.1605307
   PubMed Web of Science ®Google Scholar
• Seith DD, Bingaman JL, Veenis AJ, et al. Elucidation of catalytic strategies of small nucleolytic ribozymes from comparative analysis of active sites. ACS Catal. 2018;8(1):314–327. doi: 10.1021/acscatal.7b02976
   PubMed Web of Science ®Google Scholar
• Yen L, Svendsen J, Lee J-S, et al. Exogenous control of mammalian gene expression through modulation of RNA self-cleavage. Nature. 2004;431(7007):471–476. doi: 10.1038/nature02844
   PubMed Web of Science ®Google Scholar
• Tickner ZJ, Farzan M. Riboswitches for controlled expression of therapeutic transgenes delivered by adeno-associated viral vectors. Pharmaceuticals. 2021;14(6):554. doi: 10.3390/ph14060554
   Web of Science ®Google Scholar
• Tang J, Breaker RR. Rational design of allosteric ribozymes. Chem Biol. 1997;4(6):453–459. doi: 10.1016/S1074-5521(97)90197-6
   PubMedGoogle Scholar
• Wieland M, Hartig JS. Improved aptazyme design and in vivo screening enable riboswitching in bacteria. Angew Chem Int Ed Engl. 2008;47(14):2604–7. doi: 10.1002/anie.200703700
   PubMed Web of Science ®Google Scholar
• Ceres P, Garst AD, Marcano-Velázquez JG, et al. Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth Biol. 2013;2(8):463–472. doi: 10.1021/sb4000096
   PubMed Web of Science ®Google Scholar
• Stifel J, Spöring M, Hartig JS. Expanding the toolbox of synthetic riboswitches with guanine-dependent aptazymes. Synth Biol (Oxf). 2019;4(1):ysy022. doi: 10.1093/synbio/ysy022
   PubMedGoogle Scholar
• Strobel B, Spöring M, Klein H, et al. High-throughput identification of synthetic riboswitches by barcode-free amplicon-sequencing in human cells. Nat Commun. 2020;11(1):11(1). doi: 10.1038/s41467-020-14491-x
   Web of Science ®Google Scholar
• Zhong GC, Wang H, Bailey CC, et al. Rational design of aptazyme riboswitches for efficient control of gene expression in mammalian cells. Elife. 2016;5:5. doi: 10.7554/eLife.18858
   Web of Science ®Google Scholar
• Ausländer S, Ketzer P, Hartig JS. A ligand-dependent hammerhead ribozyme switch for controlling mammalian gene expression. Mol Biosyst. 2010;6(5):807–814. doi: 10.1039/b923076a
   PubMedGoogle Scholar
• Xiang JS, Kaplan M, Dykstra P, et al. Massively parallel RNA device engineering in mammalian cells with RNA-Seq. Nat Commun. 2019;10(1):4327. doi: 10.1038/s41467-019-12334-y
   PubMedGoogle Scholar
• Chen YY, Jensen MC, Smolke CD. Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc Natl Acad Sci, USA. 2010;107(19):8531–8536. doi: 10.1073/pnas.1001721107
   PubMed Web of Science ®Google Scholar
• Nomura Y, Zhou L, Miu A, et al. Controlling mammalian gene expression by allosteric hepatitis delta virus ribozymes. ACS Synth Biol. 2013;2(12):684–689. doi: 10.1021/sb400037a
   PubMed Web of Science ®Google Scholar
• Mustafina K, Nomura Y, Rotrattanadumrong R, et al. Circularly-permuted pistol ribozyme: a synthetic ribozyme scaffold for mammalian riboswitches. ACS Synth Biol. 2021;10(8):2040–2048. doi: 10.1021/acssynbio.1c00213
   PubMed Web of Science ®Google Scholar
• Fukunaga K, Dhamodharan V, Miyahira N, et al. Small-molecule aptamer for regulating RNA functions in mammalian cells and animals. J Am Chem Soc. 2023;145(14):7820–7828. doi: 10.1021/jacs.2c12332
   PubMed Web of Science ®Google Scholar
• Mustafina K, Fukunaga K, Yokobayashi Y. Design of mammalian ON-Riboswitches based on tandemly fused aptamer and ribozyme. ACS Synth Biol. 2020;9(1):19–25. doi: 10.1021/acssynbio.9b00371
   PubMed Web of Science ®Google Scholar
• Felletti M, Stifel J, Wurmthaler LA, et al. Twister ribozymes as highly versatile expression platforms for artificial riboswitches. Nat Commun. 2016;7(1):7. doi: 10.1038/ncomms12834
   Google Scholar
• Ketzer P, Haas SF, Engelhardt S, et al. Synthetic riboswitches for external regulation of genes transferred by replication-deficient and oncolytic adenoviruses. Nucleic Acids Res. 2012;40(21):e167. doi: 10.1093/nar/gks734
   PubMed Web of Science ®Google Scholar
• Strobel B, Klauser B, Hartig JS, et al. Riboswitch-mediated attenuation of transgene cytotoxicity increases adeno-associated virus vector yields in HEK-293 cells. Mol Ther. 2015;23(10):1582–1591. doi: 10.1038/mt.2015.123
   PubMed Web of Science ®Google Scholar
• Reid CA, Nettesheim ER, Connor TB, et al. Development of an inducible anti-VEGF rAAV gene therapy strategy for the treatment of wet AMD. Sci Rep. 2018;8(1):11763. doi: 10.1038/s41598-018-29726-7
   PubMed Web of Science ®Google Scholar
• Zhong GC, Wang H, He W, et al. A reversible RNA on-switch that controls gene expression of AAV-delivered therapeutics in vivo. Nat Biotechnol. 2020;38(2):169–175. doi: 10.1038/s41587-019-0357-y
   PubMed Web of Science ®Google Scholar
• Ketzer P, Kaufmann JK, Engelhardt S, et al. Artificial riboswitches for gene expression and replication control of DNA and RNA viruses. Proc Natl Acad Sci U S A. 2014;111(5):E554–62. doi: 10.1073/pnas.1318563111
   PubMed Web of Science ®Google Scholar
• Lee ER, Baker JL, Weinberg Z, et al. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Sci. 2010;329(5993):845–848. doi: 10.1126/science.1190713
   PubMed Web of Science ®Google Scholar
• Panchapakesan SSS, Breaker RR. The case of the missing allosteric ribozymes. Nat Chem Biol. 2021;17(4):375–382. doi: 10.1038/s41589-020-00713-2
   PubMed Web of Science ®Google Scholar
• Ferre-D’Amare AR. The glmS ribozyme: use of a small molecule coenzyme by a gene-regulatory RNA. Q Rev Biophys. 2010;43(4):423–447. doi: 10.1017/S0033583510000144
   PubMed Web of Science ®Google Scholar
• Watson PY, Fedor MJ. The glmS riboswitch integrates signals from activating and inhibitory metabolites in vivo. Nat Struct Mol Biol. 2011;18(3):359–363. doi: 10.1038/nsmb.1989
   PubMed Web of Science ®Google Scholar
• Mayr C. Regulation by 3'-untranslated regions. Ann Rev Genet. 2017;51(1):171–194. doi: 10.1146/annurev-genet-120116-024704
   PubMedGoogle Scholar
• Ferre-D’Amare AR, Zhou K, Doudna JA. Crystal structure of a hepatitis delta virus ribozyme. Nature. 1998;395(6702):567–74. doi: 10.1038/26912
   PubMed Web of Science ®Google Scholar
• Chadalavada DM, Cerrone-Szakal AL, Bevilacqua PC. Wild-type is the optimal sequence of the HDV ribozyme under cotranscriptional conditions. RNA. 2007;13(12):2189–2201. doi: 10.1261/rna.778107
   PubMed Web of Science ®Google Scholar
• Lian Y, De Young MB, Siwkowski A, et al. The sCYMV1 hairpin ribozyme: targeting rules and cleavage of heterologous RNA. Gene Ther. 1999;6(6):1114–1119. doi: 10.1038/sj.gt.3300920
   PubMed Web of Science ®Google Scholar
• Kazakov SA, Balatskaya SV, Johnston BH. Ligation of the hairpin ribozyme in cis induced by freezing and dehydration. RNA. 2006;12(3):446–56. doi: 10.1261/rna.2123506
   PubMed Web of Science ®Google Scholar
• Fedor MJ. Tertiary structure stabilization promotes hairpin ribozyme ligation. Biochem. 1999;38(34):11040–11050. doi: 10.1021/bi991069q
   PubMed Web of Science ®Google Scholar
• DeYoung M, Siwkowski AM, Lian Y, et al. Catalytic properties of hairpin ribozymes derived from chicory yellow mottle virus and arabis mosaic virus satellite RNAs. Biochem. 1995;34(48):15785–91. doi: 10.1021/bi00048a024
   PubMed Web of Science ®Google Scholar
• Li S, Lünse CE, Harris KA, et al. Biochemical analysis of hatchet self-cleaving ribozymes. RNA. 2015;21(11):1845–1851. doi: 10.1261/rna.052522.115
   PubMed Web of Science ®Google Scholar
• Zheng L, Falschlunger C, Huang K, et al. Hatchet ribozyme structure and implications for cleavage mechanism. Proc Natl Acad Sci U S A. 2019;116(22):10783–10791. doi: 10.1073/pnas.1902413116
   PubMed Web of Science ®Google Scholar
• Nomura Y, Chien HC, Yokobayashi Y. Direct screening for ribozyme activity in mammalian cells. Chem Commun (Camb). 2017;53(93):12540–12543. doi: 10.1039/C7CC07815C
   PubMed Web of Science ®Google Scholar
• Eiler D, Wang J, Steitz TA. Structural basis for the fast self-cleavage reaction catalyzed by the twister ribozyme. Proc Natl Acad Sci U S A. 2014;111(36):13028–33. doi: 10.1073/pnas.1414571111
   PubMed Web of Science ®Google Scholar
• Hammann C, Luptak A, Perreault J, et al. The ubiquitous hammerhead ribozyme. RNA. RNA. 2012;18(5):871–885. doi: 10.1261/rna.031401.111
   PubMed Web of Science ®Google Scholar
• Perreault J, Weinberg Z, Roth A, et al. Identification of hammerhead ribozymes in all domains of life reveals novel structural variations. PLoS Comput Biol. 2011;7(5):e1002031. doi: 10.1371/journal.pcbi.1002031
   PubMed Web of Science ®Google Scholar
• Wurmthaler LA, Klauser B, Hartig JS. Highly motif- and organism-dependent effects of naturally occurring hammerhead ribozyme sequences on gene expression. RNA Biol. 2018;15(2):231–241. doi: 10.1080/15476286.2017.1397870
   PubMed Web of Science ®Google Scholar
• De La Peña M, García‐Robles I. Intronic hammerhead ribozymes are ultraconserved in the human genome. EMBO Rep. 2010;11(9):711–716. doi: 10.1038/embor.2010.100
   PubMed Web of Science ®Google Scholar
• Hull CM, Anmangandla A, Bevilacqua PC. Bacterial riboswitches and ribozymes potently activate the human innate immune sensor PKR. ACS Chem Biol. 2016;11(4):1118–1127. doi: 10.1021/acschembio.6b00081
   PubMed Web of Science ®Google Scholar
• Coumans JV, Gau D, Poljak A, et al. Green fluorescent protein expression triggers proteome changes in breast cancer cells. Exp Cell Res. 2014;320(1):33–45. doi: 10.1016/j.yexcr.2013.07.019
   PubMed Web of Science ®Google Scholar
• Tanguay RL, Gallie DR. Translational efficiency is regulated by the length of the 3' untranslated region. Mol Cell Biol. 1996;16(1):146–156. doi: 10.1128/MCB.16.1.146
   PubMed Web of Science ®Google Scholar