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Review Articles

Recent Development of Fluorescent Light-Up RNA Aptamers

ORCID Icon & ORCID Icon
Pages 1644-1661 | Published online: 18 Apr 2021

References

  • Moor, A. E.; Golan, M.; Massasa, E. E.; Lemze, D.; Weizman, T.; Shenhav, R.; Baydatch, S.; Mizrahi, O.; Winkler, R.; Golani, O.; et al. Global mRNA Polarization Regulates Translation Efficiency in the Intestinal Epithelium. Science 2017, 357, 1299–1303. DOI: 10.1126/science.aan2399.
  • Neueder, A.; Dumas, A. A.; Benjamin, A. C.; Bates, G. P. Regulatory Mechanisms of Incomplete Huntingtin mRNA Splicing. Nat. Commun. 2018, 9, 3955. DOI: 10.1038/s41467-018-06281-3.
  • Wu, L.; Belasco, J. G. Let Me Count the Ways: Mechanisms of Gene Regulation by miRNAs and siRNAs. Mol. Cell. 2008, 29, 1–7. DOI: 10.1016/j.molcel.2007.12.010.
  • Derrien, T.; Johnson, R.; Bussotti, G.; Tanzer, A.; Djebali, S.; Tilgner, H.; Guernec, G.; Martin, D.; Merkel, A.; Knowles, D. G.; et al. The GENCODE v7 Catalog of Human Long Noncoding RNAs: Analysis of Their Gene Structure, Evolution, and Expression. Genome Res. 2012, 22, 1775–1789. DOI: 10.1101/gr.132159.111.
  • Bertrand, E.; Chartrand, P.; Schaefer, M.; Shenoy, S. M.; Singer, R. H.; Long, R. M. Localization of ASH1 mRNA Particles in Living Yeast. Mol. Cell. 1998, 2, 437–445. DOI: 10.1016/S1097-2765(00)80143-4.
  • Daigle, N.; Ellenberg, J. LambdaN-GFP: An RNA Reporter System for Live-Cell Imaging. Nat. Methods 2007, 4, 633–636. DOI: 10.1038/nmeth1065.
  • Rackham, O.; Brown, C. M. Visualization of RNA-Protein Interactions in Living Cells: FMRP and IMP1 Interact on mRNAs. EMBO J. 2004, 23, 3346–3355. DOI: 10.1038/sj.emboj.7600341.
  • Ozawa, T.; Natori, Y.; Sato, M.; Umezawa, Y. Imaging Dynamics of Endogenous Mitochondrial RNA in Single Living Cells. Nat. Methods 2007, 4, 413–419. DOI: 10.1038/nmeth1030.
  • Tyagi, S. Imaging Intracellular RNA Distribution and Dynamics in Living Cells. Nat. Methods 2009, 6, 331–338. DOI: 10.1038/nmeth.1321.
  • Wang, Z.; Liu, W.; Fan, C.; Chen, N. Visualizing mRNA in Live Mammalian Cells. Methods 2019, 161, 16–23. DOI: 10.1016/j.ymeth.2019.03.008.
  • Wu, J.; Zaccara, S.; Khuperkar, D.; Kim, H.; Tanenbaum, M. E.; Jaffrey, S. R. Live Imaging of mRNA Using RNA-Stabilized Fluorogenic Proteins. Nat. Methods 2019, 16, 862–865. DOI: 10.1038/s41592-019-0531-7.
  • Wu, J.; Jaffrey, S. R. Imaging mRNA Trafficking in Living Cells Using Fluorogenic Proteins. Curr. Opin. Chem. Biol. 2020, 57, 177–183. DOI: 10.1016/j.cbpa.2020.07.007.
  • Okuda, M.; Fourmy, D.; Yoshizawa, S. Use of Baby Spinach and Broccoli for Imaging of Structured Cellular RNAs. Nucleic Acids Res. 2017, 45, 1404–1415. DOI: 10.1093/nar/gkw794.
  • Huang, K.; Doyle, F.; Wurz, Z. E.; Tenenbaum, S. A.; Hammond, R. K.; Caplan, J. L.; Meyers, B. C. FASTmiR: An RNA-Based Sensor for in Vitro Quantification and Live-Cell Localization of Small RNAs. Nucleic Acids Res. 2017, 45, e130. DOI: 10.1093/nar/gkx504.
  • Paige, J. S.; Nguyen-Duc, T.; Song, W.; Jaffrey, S. R. Fluorescence Imaging of Cellular Metabolites with RNA. Science 2012, 335, 1194–1194. DOI: 10.1126/science.1218298.
  • Strack, R. L.; Song, W.; Jaffrey, S. R. Using Spinach-Based Sensors for Fluorescence Imaging of Intracellular Metabolites and Proteins in Living Bacteria. Nat. Protoc. 2014, 9, 146–155. DOI: 10.1038/nprot.2014.001.
  • DasGupta, S.; Shelke, S. A.; Li, N-s.; Piccirilli, J. A. Spinach RNA Aptamer Detects Lead(ii) with High Selectivity. Chem. Commun. (Camb.) 2015, 51, 9034–9037. DOI: 10.1039/C5CC01526J.
  • Savage, J. C.; Shinde, P.; Bächinger, H. P.; Davare, M. A.; Shinde, U. A Ribose Modification of Spinach Aptamer Accelerates Lead(ii) Cation Association in Vitro. Chem. Commun. (Camb.) 2019, 55, 5882–5885. DOI: 10.1039/C9CC01697J.
  • Yu, Q.; Shi, J.; Mudiyanselage, A. P. K. K. K.; Wu, R.; Zhao, B.; Zhou, M.; You, M. Genetically Encoded RNA-Based Sensors for Intracellular Imaging of Silver Ions. Chem. Commun. (Camb.) 2019, 55, 707–710. DOI: 10.1039/c8cc08796b.
  • Zhang, K.; Yang, Q.; Huang, W.; Wang, K.; Zhu, X.; Xie, M. Detection of HIV-1 Ribonuclease H Activity in Single-Cell by Using RNA Mimics Green Fluorescent Protein Based Biosensor. Sens. Actuators B 2019, 281, 439–444. DOI: 10.1016/j.snb.2018.09.001.
  • Song, W.; Strack, R. L.; Jaffrey, S. R. Imaging Bacterial Protein Expression Using Genetically Encoded RNA Sensors. Nat. Methods 2013, 10, 873–875. DOI: 10.1038/nmeth.2568.
  • Sun, Z.; Nguyen, T.; McAuliffe, K.; You, M. Intracellular Imaging with Genetically Encoded RNA-Based Molecular Sensors. Nanomaterials 2019, 9, 233. DOI: 10.3390/nano9020233.
  • Karunanayake Mudiyanselage, A. P. K. K.; Wu, R.; Leon-Duque, M. A.; Ren, K.; You, M. "Second-Generation" Fluorogenic RNA-Based Sensors. Methods 2019, 161, 24–34. DOI: 10.1016/j.ymeth.2019.01.008.
  • Péresse, T.; Gautier, A. Next-Generation Fluorogen-Based Reporters and Biosensors for Advanced Bioimaging. IJMS. 2019, 20, 6142. DOI: 10.3390/ijms20246142.
  • Kolpashchikov, D. M.; Spelkov, A. Binary (Split) Light-Up Aptameric Sensors. Angew. Chem. Int. Ed. Engl. 2021, 60, 4988–4999. DOI: 10.1002/anie.201914919.
  • Su, Y.; Hammond, M. C. RNA-Based Fluorescent Biosensors for Live Cell Imaging of Small Molecules and RNAs. Curr. Opin. Biotechnol. 2020, 63, 157–166. DOI: 10.1016/j.copbio.2020.01.001.
  • You, M.; Jaffrey, S. R. Structure and Mechanism of RNA Mimics of Green Fluorescent Protein. Annu. Rev. Biophys. 2015, 44, 187–206. DOI: 10.1146/annurev-biophys-060414-033954.
  • Trachman, R. J.; Truong, L.; Ferré-D'Amaré, A. R. Structural Principles of Fluorescent RNA Aptamers. Trends Pharmacol. Sci. 2017, 38, 928–939. DOI: 10.1016/j.tips.2017.06.007.
  • Neubacher, S.; Hennig, S. RNA Structure and Cellular Applications of Fluorescent Light-Up Aptamers. Angew. Chem. Int. Ed. Engl. 2019, 58, 1266–1279. DOI: 10.1002/anie.201806482.
  • Trachman, R. J.; Ferre-D'Amare, A. R. Tracking RNA with Light: Selection, Structure, and Design of Fluorescence Turn-on RNA Aptamers. Q. Rev. Biophys. 2019, 52, e8. DOI: 10.1017/S0033583519000064.
  • Ryckelynck, M. Development and Applications of Fluorogen/Light-Up RNA Aptamer Pairs for RNA Detection and More. In RNA Tagging: Methods and Protocols; Heinlein, M. Ed.; Springer US: New York, NY, 2020; pp 73–102. DOI: 10.1007/978-1-0716-0712-1_5.
  • Zhou, H.; Rauch, S.; Dai, Q.; Cui, X.; Zhang, Z.; Nachtergaele, S.; Sepich, C.; He, C.; Dickinson, B. C. Evolution of a Reverse Transcriptase to Map N1-Methyladenosine in Human Messenger RNA. Nat. Methods 2019, 16, 1281–1288. DOI: 10.1038/s41592-019-0550-4.
  • Goldsworthy, V.; LaForce, G.; Abels, S.; Khisamutdinov, F. E. Fluorogenic RNA Aptamers: A Nano-Platform for Fabrication of Simple and Combinatorial Logic Gates. Nanomaterials 2018, 8, 984. DOI: 10.3390/nano8120984.
  • Ellington, A. D.; Szostak, J. W. In Vitro Selection of RNA Molecules That Bind Specific Ligands. Nature 1990, 346, 818–822. DOI: 10.1038/346818a0.
  • Tuerk, C.; Gold, L. Systematic Evolution of Ligands by Exponential Enrichment: RNA Ligands to Bacteriophage T4 DNA Polymerase. Science 1990, 249, 505–510. DOI: 10.1126/science.2200121.
  • Grate, D.; Wilson, C. Laser-Mediated, Site-Specific Inactivation of RNA Transcripts. Proc. Natl. Acad. Sci. U S A 1999, 96, 6131–6136. DOI: 10.1073/pnas.96.11.6131.
  • Babendure, J. R.; Adams, S. R.; Tsien, R. Y. Aptamers Switch on Fluorescence of Triphenylmethane Dyes. J. Am. Chem. Soc. 2003, 125, 14716–14717. DOI: 10.1021/ja037994o.
  • Novikova, I. V.; Afonin, K. A.; Leontis, N. B. New Ideas for in Vivo Detection of RNA. In Biosensors; Serra, P. A., Ed.; InTec europe: Rijeka, Croatia, 2010; pp 127–150. DOI: 10.5772/7207.
  • Olmsted, J.; Kearns, D. R. Mechanism of Ethidium Bromide Fluorescence Enhancement on Binding to Nucleic Acids. Biochemistry 1977, 16, 3647–3654. DOI: 10.1021/bi00635a022.
  • Sando, S.; Narita, A.; Aoyama, Y. Light-Up Hoechst-DNA Aptamer Pair: Generation of an Aptamer-Selective Fluorophore from a Conventional DNA-Staining Dye. Chembiochem 2007, 8, 1795–1803. DOI: 10.1002/cbic.200700325.
  • Paige, J. S.; Wu, K. Y.; Jaffrey, S. R. RNA Mimics of Green Fluorescent Protein. Science 2011, 333, 642–646. DOI: 10.1126/science.1207339.
  • Strack, R. L.; Disney, M. D.; Jaffrey, S. R. A Superfolding Spinach2 Reveals the Dynamic Nature of Trinucleotide repeat-containing RNA. Nat. Methods 2013, 10, 1219–1224. DOI: 10.1038/nmeth.2701.
  • Song, W.; Strack, R. L.; Svensen, N.; Jaffrey, S. R. Plug-and-Play Fluorophores Extend the Spectral Properties of Spinach. J. Am. Chem. Soc. 2014, 136, 1198–1201. DOI: 10.1021/ja410819x.
  • Warner, K. D.; Chen, M. C.; Song, W.; Strack, R. L.; Thorn, A.; Jaffrey, S. R.; Ferré-D'Amaré, A. R. Structural Basis for Activity of Highly Efficient RNA Mimics of Green Fluorescent Protein. Nat. Struct. Mol. Biol. 2014, 21, 658–663. DOI: 10.1038/nsmb.2865.
  • Huang, H.; Suslov, N. B.; Li, N.-S.; Shelke, S. A.; Evans, M. E.; Koldobskaya, Y.; Rice, P. A.; Piccirilli, J. A. A G-Quadruplex-Containing RNA Activates Fluorescence in a GFP-Like Fluorophore. Nat. Chem. Biol. 2014, 10, 686–691. DOI: 10.1038/nchembio.1561.
  • Autour, A.; Westhof, E.; Ryckelynck, M. iSpinach: A Fluorogenic RNA Aptamer Optimized for In Vitro Applications. Nucleic Acids Res. 2016, 44, 2491–2500. DOI: 10.1093/nar/gkw083.
  • Filonov, G. S.; Moon, J. D.; Svensen, N.; Jaffrey, S. R. Broccoli: Rapid Selection of an RNA Mimic of Green Fluorescent Protein by Fluorescence-Based Selection and Directed Evolution. J. Am. Chem. Soc. 2014, 136, 16299–16308. DOI: 10.1021/ja508478x.
  • Song, W.; Filonov, G. S.; Kim, H.; Hirsch, M.; Li, X.; Moon, J. D.; Jaffrey, S. R. Imaging RNA Polymerase III Transcription Using a Photostable RNA-Fluorophore Complex. Nat. Chem. Biol. 2017, 13, 1187–1194. DOI: 10.1038/nchembio.2477.
  • Warner, K. D.; Sjekloca, L.; Song, W.; Filonov, G. S.; Jaffrey, S. R.; Ferre-D'Amare, A. R. A Homodimer Interface without Base Pairs in an RNA Mimic of Red Fluorescent Protein. Nat. Chem. Biol. 2017, 13, 1195–1201. DOI: 10.1038/nchembio.2475.
  • Li, X.; Kim, H.; Litke, J. L.; Wu, J.; Jaffrey, S. R. Fluorophore-Promoted RNA Folding and Photostability Enables Imaging of Single Broccoli-Tagged mRNAs in Live Mammalian Cells. Angew. Chem. Int. Ed. Engl. 2020, 59, 4511–4518. DOI: 10.1002/anie.201914576.
  • Li, X.; Mo, L.; Litke, J. L.; Dey, S. K.; Suter, S. R.; Jaffrey, S. R. Imaging Intracellular S-Adenosyl Methionine Dynamics in Live Mammalian Cells with a Genetically Encoded Red Fluorescent RNA-Based Sensor. J. Am. Chem. Soc. 2020, 142, 14117–14124. DOI: 10.1021/jacs.0c02931.
  • Litke, J. L.; Jaffrey, S. R. Highly Efficient Expression of Circular RNA Aptamers in Cells Using Autocatalytic Transcripts. Nat. Biotechnol. 2019, 37, 667–675. DOI: 10.1038/s41587-019-0090-6.
  • Dolgosheina, E. V.; Jeng, S. C. Y.; Panchapakesan, S. S. S.; Cojocaru, R.; Chen, P. S. K.; Wilson, P. D.; Hawkins, N.; Wiggins, P. A.; Unrau, P. J. RNA Mango Aptamer-Fluorophore: A Bright, High-Affinity Complex for RNA Labeling and Tracking. ACS Chem. Biol. 2014, 9, 2412–2420. DOI: 10.1021/cb500499x.
  • Baugh, C.; Grate, D.; Wilson, C. 2.8 A Crystal Structure of the Malachite Green Aptamer. J. Mol. Biol. 2000, 301, 117–128. DOI: 10.1006/jmbi.2000.3951.
  • Fernandez-Millan, P.; Autour, A.; Ennifar, E.; Westhof, E.; Ryckelynck, M. Crystal Structure and Fluorescence Properties of the iSpinach Aptamer in Complex with DFHBI. RNA 2017, 23, 1788–1795. DOI: 10.1261/rna.063008.117.
  • Trachman, R. J.; Demeshkina, N. A.; Lau, M. W. L.; Panchapakesan, S. S. S.; Jeng, S. C. Y.; Unrau, P. J.; Ferré-D'Amaré, A. R. Structural Basis for High-Affinity Fluorophore Binding and Activation by RNA Mango. Nat. Chem. Biol. 2017, 13, 807–813. DOI: 10.1038/nchembio.2392.
  • Autour, A.; Jeng, C. Y.; Cawte, A. D.; Abdolahzadeh, A.; Galli, A.; Panchapakesan, S. S. S.; Rueda, D.; Ryckelynck, M.; Unrau, P. J. Fluorogenic RNA Mango Aptamers for Imaging Small Non-Coding RNAs in Mammalian Cells. Nat. Commun. 2018, 9, 656. DOI: 10.1038/s41467-018-02993-8.
  • Trachman, R. J.; Abdolahzadeh, A.; Andreoni, A.; Cojocaru, R.; Knutson, J. R.; Ryckelynck, M.; Unrau, P. J.; Ferré-D'Amaré, A. R. Crystal Structures of the Mango-II RNA Aptamer Reveal Heterogeneous Fluorophore Binding and Guide Engineering of Variants with Improved Selectivity and Brightness. Biochemistry 2018, 57, 3544–3548. DOI: 10.1021/acs.biochem.8b00399.
  • Trachman, R. J.; Autour, A.; Jeng, S. C. Y.; Abdolahzadeh, A.; Andreoni, A.; Cojocaru, R.; Garipov, R.; Dolgosheina, E. V.; Knutson, J. R.; Ryckelynck, M.; et al. Structure and Functional Reselection of the Mango-III Fluorogenic RNA Aptamer. Nat. Chem. Biol. 2019, 15, 472–479. DOI: 10.1038/s41589-019-0267-9.
  • Trachman, R. J.; Cojocaru, R.; Wu, D.; Piszczek, G.; Ryckelynck, M.; Unrau, P. J.; Ferré-D'Amaré, A. R. Structure-Guided Engineering of the Homodimeric Mango-IV Fluorescence Turn-on Aptamer Yields an RNA FRET Pair. Structure 2020, 28, 776–785.e3. DOI: 10.1016/j.str.2020.04.007.
  • Steinmetzger, C.; Palanisamy, N.; Gore, K. R.; Höbartner, C. A Multicolor Large Stokes Shift Fluorogen-Activating RNA Aptamer with Cationic Chromophores. Chemistry 2019, 25, 1931–1935. DOI: 10.1002/chem.201805882.
  • Chen, X.; Zhang, D.; Su, N.; Bao, B.; Xie, X.; Zuo, F.; Yang, L.; Wang, H.; Jiang, L.; Lin, Q.; et al. Visualizing RNA Dynamics in Live Cells with Bright and Stable Fluorescent RNAs. Nat. Biotechnol. 2019, 37, 1287–1293. DOI: 10.1038/s41587-019-0249-1.
  • Tan, X.; Constantin, T. P.; Sloane, K. L.; Waggoner, A. S.; Bruchez, M. P.; Armitage, B. A. Fluoromodules Consisting of a Promiscuous RNA Aptamer and Red or Blue Fluorogenic Cyanine Dyes: Selection, Characterization, and Bioimaging. J. Am. Chem. Soc. 2017, 139, 9001–9009. DOI: 10.1021/jacs.7b04211.
  • Shelke, S. A.; Shao, Y.; Laski, A.; Koirala, D.; Weissman, B. P.; Fuller, J. R.; Tan, X.; Constantin, T. P.; Waggoner, A. S.; Bruchez, M. P.; et al. Structural Basis for Activation of Fluorogenic Dyes by an RNA Aptamer Lacking a G-Quadruplex Motif. Nat. Commun. 2018, 9, 4542. DOI: 10.1038/s41467-018-06942-3.
  • Wirth, R.; Gao, P.; Nienhaus, G. U.; Sunbul, M.; Jäschke, A. SiRA: A Silicon Rhodamine-Binding Aptamer for Live-Cell Super-Resolution RNA Imaging. J. Am. Chem. Soc. 2019, 141, 7562–7571. DOI: 10.1021/jacs.9b02697.
  • Sunbul, M.; Jäschke, A. Contact-Mediated Quenching for RNA Imaging in Bacteria with a Fluorophore-Binding Aptamer. Angew. Chem. Int. Ed. Engl. 2013, 52, 13401–13404. DOI: 10.1002/anie.201306622.
  • Sunbul, M.; Jäschke, A. SRB-2: A Promiscuous Rainbow Aptamer for live-cell RNA imaging . Nucleic Acids Res. 2018, 46, e110. DOI: 10.1093/nar/gky543.
  • Arora, A.; Sunbul, M.; Jaschke, A. Dual-Colour Imaging of RNAs Using Quencher- and Fluorophore-Binding Aptamers. Nucleic Acids Res. 2015, 43, 9. DOI: 10.1093/nar/gkv718.
  • Murata, A.; Sato, S.-i.; Kawazoe, Y.; Uesugi, M. Small-Molecule Fluorescent Probes for Specific RNA Targets. Chem. Commun. (Camb). 2011, 47, 4712–4714. DOI: 10.1039/C1CC10393H.
  • Braselmann, E.; Wierzba, A. J.; Polaski, J. T.; Chromiński, M.; Holmes, Z. E.; Hung, S.-T.; Batan, D.; Wheeler, J. R.; Parker, R.; Jimenez, R.; et al. A Multicolor Riboswitch-Based Platform for Imaging of RNA in Live Mammalian Cells. Nat. Chem. Biol. 2018, 14, 964–971. DOI: 10.1038/s41589-018-0103-7.
  • Bouhedda, F.; Fam, K. T.; Collot, M.; Autour, A.; Marzi, S.; Klymchenko, A.; Ryckelynck, M. A Dimerization-Based Fluorogenic Dye-Aptamer Module for RNA Imaging in Live Cells. Nat. Chem. Biol. 2020, 16, 69–76. DOI: 10.1038/s41589-019-0381-8.
  • Ying, Z.-M.; Wu, Z.; Tu, B.; Tan, W.; Jiang, J.-H. Genetically Encoded Fluorescent RNA Sensor for Ratiometric Imaging of MicroRNA in Living Tumor Cells. J. Am. Chem. Soc. 2017, 139, 9779–9782. DOI: 10.1021/jacs.7b04527.
  • Yatsuzuka, K.; Sato, S.-i.; Pe, K. B.; Katsuda, Y.; Takashima, I.; Watanabe, M.; Uesugi, M. Live-Cell Imaging of Multiple Endogenous mRNAs Permits the Direct Observation of RNA Granule Dynamics. Chem. Commun. (Camb.) 2018, 54, 7151–7154. DOI: 10.1039/C8CC03805H.
  • Ying, Z.-M.; Yuan, Y.-Y.; Tu, B.; Tang, L.-J.; Yu, R.-Q.; Jiang, J.-H. A Single Promoter System co-Expressing RNA Sensor with Fluorescent Proteins for Quantitative mRNA Imaging in Living Tumor Cells. Chem. Sci. 2019, 10, 4828–4833. DOI: 10.1039/C9SC00458K.
  • Wu, R.; Karunanayake Mudiyanselage, A. P. K. K.; Shafiei, F.; Zhao, B.; Bagheri, Y.; Yu, Q.; McAuliffe, K.; Ren, K.; You, M. Genetically Encoded Ratiometric RNA-Based Sensors for Quantitative Imaging of Small Molecules in Living Cells. Angew. Chem. Int. Ed. Engl. 2019, 58, 18271–18275. DOI: 10.1002/anie.201911799.
  • Swetha, P.; Fan, Z.; Wang, F.; Jiang, J.-H. Genetically Encoded Light-Up RNA Aptamers and Their Applications for Imaging and Biosensing. J. Mater. Chem. B 2020, 8, 3382–3392. DOI: 10.1039/C9TB02668A.
  • Monici, M. Cell and Tissue Autofluorescence Research and Diagnostic Applications. In Biotechnology Annual Review; ElGewely, M. R., Ed.; Elsevier: Amsterdam, Netherlands, 2005; pp 227–256. DOI: 10.1016/S1387-2656(05)11007-2.
  • Braselmann, E.; Palmer, A. E. Chapter Fifteen - A Multicolor Riboswitch-Based Platform for Imaging of RNA in Live Mammalian Cells. In Methods in Enzymology; Chenoweth, D. M., Ed.; Academic Press: London, England, 2020; pp 343–372. DOI: 10.1016/bs.mie.2020.03.004.
  • Wang, P.; Querard, J.; Maurin, S.; Nath, S. S.; Le Saux, T.; Gautier, A.; Jullien, L. Photochemical Properties of Spinach and Its Use in Selective Imaging. Chem. Sci. 2013, 4, 2865–2873. DOI: 10.1039/c3sc50729g.
  • Han, K. Y.; Leslie, B. J.; Fei, J.; Zhang, J.; Ha, T. Understanding the Photophysics of the Spinach-DFHBI RNA Aptamer-Fluorogen Complex to Improve Live-Cell RNA Imaging. J. Am. Chem. Soc. 2013, 135, 19033–19038. DOI: 10.1021/ja411060p.
  • Cawte, A. D.; Unrau, P. J.; Rueda, D. S. Live Cell Imaging of Single RNA Molecules with Fluorogenic Mango II Arrays. Nat. Commun. 2020, 11, 1283. DOI: 10.1038/s41467-020-14932-7.
  • Brakemann, T.; Stiel, A. C.; Weber, G.; Andresen, M.; Testa, I.; Grotjohann, T.; Leutenegger, M.; Plessmann, U.; Urlaub, H.; Eggeling, C.; et al. A Reversibly Photoswitchable GFP-Like Protein with Fluorescence Excitation Decoupled from switching. Nat. Biotechnol. 2011, 29, 942–947. DOI: 10.1038/nbt.1952.
  • Warren, M. M.; Kaucikas, M.; Fitzpatrick, A.; Champion, P.; Timothy Sage, J.; van Thor, J. J. Ground-State Proton Transfer in the Photoswitching Reactions of the Fluorescent Protein Dronpa. Nat. Commun. 2013, 4, 1461. DOI: 10.1038/ncomms2460.
  • Yadav, D.; Lacombat, F.; Dozova, N.; Rappaport, F.; Plaza, P.; Espagne, A. Real-Time Monitoring of Chromophore Isomerization and Deprotonation during the Photoactivation of the Fluorescent Protein Dronpa. J. Phys. Chem. B 2015, 119, 2404–2414. DOI: 10.1021/jp507094f.
  • Bourgeois, D.; Adam, V. Reversible Photoswitching in Fluorescent Proteins: A Mechanistic View. IUBMB Life. 2012, 64, 482–491. DOI: 10.1002/iub.1023.
  • Duan, C.; Adam, V.; Byrdin, M.; Bourgeois, D. Structural Basis of Photoswitching in Fluorescent Proteins. In Photoswitching Proteins: Methods and Protocols; Cambridge, S., Ed.; Springer: New York, NY, 2014; pp 177–202. DOI: 10.1007/978-1-4939-0470-9_12.
  • Rasnik, I.; McKinney, S. A.; Ha, T. Nonblinking and Long-Lasting Single-Molecule Fluorescence Imaging. Nat. Methods 2006, 3, 891–893. DOI: 10.1038/nmeth934.
  • Richards, C. I.; Hsiang, J.-C.; Dickson, R. M. Synchronously Amplified Fluorescence Image Recovery (SAFIRe). J. Phys. Chem. B 2010, 114, 660–665. DOI: 10.1021/jp909167j.
  • Hsiang, J.-C.; Jablonski, A. E.; Dickson, R. M. Optically Modulated Fluorescence Bioimaging: Visualizing Obscured Fluorophores in High Background. Acc. Chem. Res. 2014, 47, 1545–1554. DOI: 10.1021/ar400325y.
  • Tian, Z.; Li, A. D. Q. Photoswitching-Enabled Novel Optical Imaging: Innovative Solutions for Real-World Challenges in Fluorescence Detections. Acc. Chem. Res. 2013, 46, 269–279. DOI: 10.1021/ar300108d.
  • Querard, J.; Gautier, A.; Le Saux, T.; Jullien, L. Expanding Discriminative Dimensions for Analysis and Imaging. Chem. Sci. 2015, 6, 2968–2978. DOI: 10.1039/C4SC03955F.
  • Chouket, R.; Pellissier-Tanon, A.; Lemarchand, A.; Espagne, A.; Le Saux, T.; Jullien, L. Dynamic Contrast with Reversibly Photoswitchable Fluorescent Labels for Imaging Living Cells. Chem. Sci. 2020, 11, 2882–2887. DOI: 10.1039/D0SC00182A.
  • Bouhedda, F.; Autour, A.; Ryckelynck, M. Light-Up RNA Aptamers and Their Cognate Fluorogens: From Their Development to Their Applications. IJMS. 2017, 19, 44. DOI: 10.3390/ijms19010044.
  • Zhang, J.; Fei, J.; Leslie, B. J.; Han, K. Y.; Kuhlman, T. E.; Ha, T. Tandem Spinach Array for mRNA Imaging in Living Bacterial Cells. Sci. Rep. 2015, 5, 17295. DOI: 10.1038/srep17295.
  • Strack, R. L.; Jaffrey, S. R. New Approaches for Sensing Metabolites and Proteins in Live Cells Using RNA. Curr. Opin. Chem. Biol. 2013, 17, 651–655. DOI: 10.1016/j.cbpa.2013.05.014.
  • Sato, S.-I.; Watanabe, M.; Katsuda, Y.; Murata, A.; Wang, D. O.; Uesugi, M. Live-Cell Imaging of Endogenous mRNAs with a Small Molecule. Angew. Chem. Int. Ed. Engl. 2015, 54, 1855–1858. DOI: 10.1002/anie.201410339.
  • Aw, S. S.; Tang, M. X.; Teo, Y. N.; Cohen, S. M. A Conformation-Induced Fluorescence Method for microRNA Detection. Nucleic Acids Res. 2016, 44, e92. DOI: 10.1093/nar/gkw108.
  • Wang, Z. J.; Luo, Y.; Xie, X. D.; Hu, X. J.; Song, H. Y.; Zhao, Y.; Shi, J. Y.; Wang, L. H.; Glinsky, G.; Chen, N.; et al. In Situ Spatial Complementation of Aptamer-Mediated Recognition Enables Live-Cell Imaging of Native RNA Transcripts in Real Time. Angew. Chem. Int. Ed. Engl. 2018, 57, 972–976. DOI: 10.1002/anie.201707795.
  • Karunanayake Mudiyanselage, A. P. K. K.; Yu, Q.; Leon-Duque, M. A.; Zhao, B.; Wu, R.; You, M. Genetically Encoded Catalytic Hairpin Assembly for Sensitive RNA Imaging in Live Cells. J. Am. Chem. Soc. 2018, 140, 8739–8745. DOI: 10.1021/jacs.8b03956.
  • Ren, K.; Wu, R.; Karunanayake Mudiyanselage, A. P. K. K.; Yu, Q.; Zhao, B.; Xie, Y.; Bagheri, Y.; Tian, Q.; You, M. In Situ Genetically Cascaded Amplification for Imaging RNA Subcellular Locations. J. Am. Chem. Soc. 2020, 142, 2968–2974. DOI: 10.1021/jacs.9b11748.
  • Kellenberger, C. A.; Wilson, S. C.; Sales-Lee, J.; Hammond, M. C. RNA-Based Fluorescent Biosensors for Live Cell Imaging of Second Messengers Cyclic di-GMP and Cyclic AMP-GMP. J. Am. Chem. Soc. 2013, 135, 4906–4909. DOI: 10.1021/ja311960g.
  • Kellenberger, C. A.; Chen, C.; Whiteley, A. T.; Portnoy, D. A.; Hammond, M. C. RNA-Based Fluorescent Biosensors for Live Cell Imaging of Second Messenger Cyclic di-AMP. J. Am. Chem. Soc. 2015, 137, 6432–6435. DOI: 10.1021/jacs.5b00275.
  • Wang, X. C.; Wilson, S. C.; Hammond, M. C. Next-Generation RNA-Based Fluorescent Biosensors Enable Anaerobic Detection of Cyclic di-GMP. Nucleic Acids Res. 2016, 44, e139. DOI: 10.1093/nar/gkw580.
  • Bose, D.; Su, Y.; Marcus, A.; Raulet, D. H.; Hammond, M. C. An RNA-Based Fluorescent Biosensor for High-Throughput Analysis of the cGAS-cGAMP-STING Pathway. Cell Chem. Biol. 2016, 23, 1539–1549. DOI: 10.1016/j.chembiol.2016.10.014.
  • Su, Y.; Hickey, S. F.; Keyser, S. G. L.; Hammond, M. C. In Vitro and In Vivo Enzyme Activity Screening via RNA-Based Fluorescent Biosensors for S-Adenosyl-l-Homocysteine (SAH). J. Am. Chem. Soc. 2016, 138, 7040–7047. DOI: 10.1021/jacs.6b01621.
  • Porter, E. B.; Polaski, J. T.; Morck, M. M.; Batey, R. T. Recurrent RNA Motifs as Scaffolds for Genetically Encodable Small-Molecule Biosensors. Nat. Chem. Biol. 2017, 13, 295–301. DOI: 10.1038/nchembio.2278.
  • Li, N.; Huang, X.; Zou, J.; Chen, G.; Liu, G.; Li, M.; Dong, J.; Du, F.; Cui, X.; Tang, Z. Evolution of Microbial Biosensor Based on Functional RNA through Fluorescence-Activated Cell Sorting. Sens. Actuators B 2018, 258, 550–557. DOI: 10.1016/j.snb.2017.11.015.
  • Truong, J.; Hsieh, Y.-F.; Truong, L.; Jia, G.; Hammond, M. C. Designing Fluorescent Biosensors Using Circular Permutations of Riboswitches. Methods 2018, 143, 102–109. DOI: 10.1016/j.ymeth.2018.02.014.
  • Kim, H.; Jaffrey, S. R. A Fluorogenic RNA-Based Sensor Activated by Metabolite-Induced RNA Dimerization. Cell Chem. Biol. 2019, 26, 1725–1731.e6. DOI: 10.1016/j.chembiol.2019.09.013.
  • You, M.; Litke, J. L.; Jaffrey, S. R. Imaging Metabolite Dynamics in Living Cells Using a Spinach-Based Riboswitch. Proc. Natl. Acad. Sci. U S A. 2015, 112, E2756–E2765. DOI: 10.1073/pnas.1504354112.
  • You, M.; Litke, J. L.; Wu, R.; Jaffrey, S. R. Detection of Low-Abundance Metabolites in Live Cells Using an RNA Integrator. Cell Chem. Biol. 2019, 26, 471–481.e3. DOI: 10.1016/j.chembiol.2019.01.005.
  • Jepsen, M. D. E.; Sparvath, S. M.; Nielsen, T. B.; Langvad, A. H.; Grossi, G.; Gothelf, K. V.; Andersen, E. S. Development of a Genetically Encodable FRET System Using Fluorescent RNA Aptamers. Nat. Commun. 2018, 9, 18. DOI: 10.1038/s41467-017-02435-x.
  • Debiais, M.; Lelievre, A.; Smietana, M.; Müller, S. Splitting Aptamers and Nucleic Acid Enzymes for the Development of Advanced biosensors. Nucleic Acids Res. 2020, 48, 3400–3422. DOI: 10.1093/nar/gkaa132.
  • Danilchanka, O.; Mekalanos, J. J. Cyclic Dinucleotides and the Innate Immune Response. Cell 2013, 154, 962–970. DOI: 10.1016/j.cell.2013.08.014.
  • Wright, T. A.; Jiang, L.; Park, J. J.; Anderson, W. A.; Chen, G.; Hallberg, Z. F.; Nan, B.; Hammond, M. C. Second Messengers and Divergent HD-GYP Phosphodiesterases Regulate 3',3'-cGAMP signaling. Mol. Microbiol. 2020, 113, 222–236. DOI: 10.1111/mmi.14412.
  • Barrett, S. P.; Salzman, J. Circular RNAs: analysis, Expression and Potential Functions. Development 2016, 143, 1838–1847. DOI: 10.1242/dev.128074.
  • Wesselhoeft, R. A.; Kowalski, P. S.; Anderson, D. G. Engineering Circular RNA for Potent and Stable Translation in Eukaryotic Cells. Nat. Commun. 2018, 9, 2629. DOI: 10.1038/s41467-018-05096-6.
  • Serganov, A.; Nudler, E. A Decade of Riboswitches. Cell 2013, 152, 17–24. DOI: 10.1016/j.cell.2012.12.024.
  • Winkler, W.; Nahvi, A.; Breaker, R. R. Thiamine Derivatives Bind Messenger RNAs Directly to Regulate Bacterial Gene Expression. Nature 2002, 419, 952–956. DOI: 10.1038/nature01145.
  • Takezawa, Y.; Shionoya, M. Metal-Mediated DNA Base Pairing: Alternatives to Hydrogen-Bonded Watson-Crick Base Pairs. Acc. Chem. Res. 2012, 45, 2066–2076. DOI: 10.1021/ar200313h.
  • Roszyk, L.; Kollenda, S.; Hennig, S. Using a Specific RNA-Protein Interaction to Quench the Fluorescent RNA Spinach. ACS Chem. Biol. 2017, 12, 2958–2964. DOI: 10.1021/acschembio.7b00332.

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