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Tracking RNA with light: selection, structure, and design of fluorescence turn-on RNA aptamers

Published online by Cambridge University Press:  19 August 2019

Robert J. Trachman III Open the ORCID record for Robert J. Trachman III [Opens in a new window]  and
Adrian R. Ferré-D'Amaré
Robert J. Trachman III
Affiliation:
Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, 50 South Drive MSC 8012, Bethesda, MD 20892-8012, USA
Adrian R. Ferré-D'Amaré*
Affiliation:
Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, 50 South Drive MSC 8012, Bethesda, MD 20892-8012, USA
*
Author for correspondence: A. R. Ferré-D'Amaré, E-mail: [email protected]
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Abstract

Fluorescence turn-on aptamers, in vitro evolved RNA molecules that bind conditional fluorophores and activate their fluorescence, have emerged as RNA counterparts of the fluorescent proteins. Turn-on aptamers have been selected to bind diverse fluorophores, and they achieve varying degrees of specificity and affinity. These RNA–fluorophore complexes, many of which exceed the brightness of green fluorescent protein and their variants, can be used as tags for visualizing RNA localization and transport in live cells. Structure determination of several fluorescent RNAs revealed that they have diverse, unrelated overall architectures. As most of these RNAs activate the fluorescence of their ligands by restraining their photoexcited states into a planar conformation, their fluorophore binding sites have in common a planar arrangement of several nucleobases, most commonly a G-quartet. Nonetheless, each turn-on aptamer has developed idiosyncratic structural solutions to achieve specificity and efficient fluorescence turn-on. The combined structural diversity of fluorophores and turn-on RNA aptamers has already produced combinations that cover the visual spectrum. Further molecular evolution and structure-guided engineering is likely to produce fluorescent tags custom-tailored to specific applications.

Keywords

Molecular engineeringRNA structureSELEXX-ray crystallography
Type
Major Review
Information
Quarterly Reviews of Biophysics , Volume 52 , 2019 , e8
Copyright
Copyright © Cambridge University Press 2019 

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References

Alam, KK, Tawiah, KD, Lichte, MF, Porciani, D and Burke, DH (2017) A fluorescent split aptamer for visualizing RNA-RNA assembly in vivo. ACS Synthetic Biology 6, 1710–1721.Google Scholar
Alam, KK, Jung, JK, Verosloff, MS, Clauer, PR, Lee, JW, Capdevila, DA, Pastén, PA, Giedroc, DP, Collins, JJ and Lucks, JB (2019) Rapid, low-cost detection of water contaminants using regulated in vitro transcription. bioRxiv, 619296. https://doi.org/10.1101/619296.Google Scholar
Armitage, BA (2011) Imaging of RNA in live cells. Current Opinion in Chemical Biology 15, 806–812.Google Scholar
Arora, A, Sunbul, M and Jäschke, A (2015) Dual-colour imaging of RNAs using quencher- and fluorophore-binding aptamers. Nucleic Acids Research 43, e144.Google Scholar
Autour, A, Westhof, E and Ryckelynck, M (2016) Ispinach: a fluorogenic RNA aptamer optimized for in vitro applications. Nucleic Acids Research 44, 2491–2500.Google Scholar
Autour, A, C Y Jeng, S, D Cawte, A, Abdolahzadeh, A, Galli, A, Panchapakesan, SSS, Rueda, D, Ryckelynck, M and Unrau, PJ (2018) Fluorogenic RNA Mango aptamers for imaging small non-coding RNAs in mammalian cells. Nature Communications 9, 656.Google Scholar
Babendure, JR, Adams, SR and Tsien, RY (2003) Aptamers switch on fluorescence of triphenylmethane dyes. Journal of the American Chemical Society 125, 14716–14717.Google Scholar
Baptista, M and Indig, G (1998) Effect of BSA binding on photophysical and photochemical properties of triarylmethane dyes. Journal of Physical Chemistry B 102, 4678–4688.Google Scholar
Baugh, C, Grate, D and Wilson, C (2000) 2·8 angstrom crystal structure of the malachite green aptamer. Journal of Molecular Biology 301, 117–128.Google Scholar
Bertrand, E, Chartrand, P, Schaefer, M, Shenoy, SM, Singer, RH and Long, RM (1998) Localization of ASH1 mRNA particles in living yeast. Molecular Cell 2, 437–445.Google Scholar
Bevis, BJ and Glick, BS (2002) Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nature Biotechnology 20, 83–87.Google Scholar
Brackett, DM and Dieckmann, T (2006) Aptamer to ribozyme: the intrinsic catalytic potential of a small RNA. Chembiochem 7, 839–843.Google Scholar
Braselmann, E, Wierzba, AJ, Polaski, JT, Chromiński, M, Holmes, ZE, Hung, ST, Batan, D, Wheeler, JR, Parker, R, Jimenez, R, Gryko, D, Batey, RT and Palmer, AE (2018) A multicolor riboswitch-based platform for imaging of RNA in live mammalian cells. Nature Chemical Biology 14, 964–971.Google Scholar
Chandler, M, Lyalina, T, Halman, J, Rackley, L, Lee, L, Dang, D, Ke, W, Sajja, S, Woods, S, Acharya, S, Baumgarten, E, Christopher, J, Elshalia, E, Hrebien, G, Kublank, K, Saleh, S, Stallings, B, Tafere, M, Striplin, C and Afonin, KA (2018) Broccoli fluorets: split aptamers as a user-friendly fluorescent toolkit for dynamic RNA nanotechnology. Molecules 23.Google Scholar
Chao, JA, Patskovsky, Y, Almo, SC and Singer, RH (2008) Structural basis for the coevolution of a viral RNA-protein complex. Nature Structural & Molecular Biology 15, 103–105.Google Scholar
Chapman, HN (2019) X-ray free-electron lasers for the structure and dynamics of macromolecules. Annual Review of Biochemistry 88, 35–58.Google Scholar
Constantin, TP, Silva, GL, Robertson, KL, Hamilton, TP, Fague, K, Waggoner, AS and Armitage, BA (2008) Synthesis of new fluorogenic cyanine dyes and incorporation into RNA fluoromodules. Organic Letters 10, 1561–1564.Google Scholar
Day, RN and Davidson, MW (2014) The Fluorescent Protein Revolution. Boca Raton, Florida, USA: CRC Press.Google Scholar
Dolgosheina, EV and Unrau, PJ (2016) Fluorophore-binding RNA aptamers and their applications. Wiley Interdisciplinary Reviews-Rna 7, 843–851.Google Scholar
Dolgosheina, EV, Jeng, SC, Panchapakesan, SS, Cojocaru, R, Chen, PS, Wilson, PD, Hawkins, N, Wiggins, PA and Unrau, PJ (2014) RNA mango aptamer-fluorophore: a bright, high-affinity complex for RNA labeling and tracking. ACS Chemical Biology 9, 2412–2420.Google Scholar
Draper, DE (2004) A guide to ions and RNA structure. Rna-a Publication of the Rna Society 10, 335–343.Google Scholar
Edwards, TE, Klein, DJ and Ferré-D'Amaré, AR (2007) Riboswitches: small-molecule recognition by gene regulatory RNAs. Current Opinion in Structural Biology 17, 273–279.Google Scholar
Ellington, AD and Szostak, JW (1990) In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818–822.Google Scholar
Fernandez-Millan, P, Autour, A, Ennifar, E, Westhof, E and Ryckelynck, M (2017) Crystal structure and fluorescence properties of the iSpinach aptamer in complex with DFHBI. RNA 23, 1788–1795.Google Scholar
Filonov, GS, Moon, JD, Svensen, N and Jaffrey, SR (2014) Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. Journal of the American Chemical Society 136, 16299–16308.Google Scholar
Flinders, J, DeFina, SC, Brackett, DM, Baugh, C, Wilson, C and Dieckmann, T (2004) Recognition of planar and nonplanar ligands in the malachite green-RNA aptamer complex. Chembiochem 5, 62–72.Google Scholar
Fuenzalida-Werner, JP, Janowski, R, Mishra, K, Weidenfeld, I, Niessing, D, Ntziachristos, V and Stiel, AC (2018) Crystal structure of a biliverdin-bound phycobiliprotein: interdependence of oligomerization and chromophorylation. Journal of Structural Biology 204, 519–522.Google Scholar
Garcia, JF and Parker, R (2015) MS2 coat proteins bound to yeast mRNAs block 5′ to 3′ degradation and trap mRNA decay products: implications for the localization of mRNAs by MS2-MCP system. RNA 21, 1393–1395.Google Scholar
Garcia, JF and Parker, R (2016) Ubiquitous accumulation of 3′ mRNA decay fragments in Saccharomyces cerevisiae mRNAs with chromosomally integrated MS2 arrays. RNA 22, 657–659.Google Scholar
Gotrik, M, Sekhon, G, Saurabh, S, Nakamoto, M, Eisenstein, M and Soh, HT (2018) Direct selection of fluorescence-enhancing RNA aptamers. Journal of the American Chemical Society 140, 3583–3591.Google Scholar
Grate, D and Wilson, C (1999) Laser-mediated, site-specific inactivation of RNA transcripts. Proceedings of the National Academy of Sciences of the USA 96, 6131–6136.Google Scholar
Grate, D and Wilson, C (2001) Inducible regulation of the S. cerevisiae cell cycle mediated by an RNA aptamer-ligand complex. Bioorganic & Medicinal Chemistry 9, 2565–2570.Google Scholar
Grimm, JB, Muthusamy, AK, Liang, Y, Brown, TA, Lemon, WC, Patel, R, Lu, R, Macklin, JJ, Keller, PJ, Ji, N and Lavis, LD (2017) A general method to fine-tune fluorophores for live-cell and in vivo imaging. Nature Methods 14, 987–994.Google Scholar
Guan, AJ, Zhang, XF, Sun, X, Li, Q, Xiang, JF, Wang, LX, Lan, L, Yang, FM, Xu, SJ, Guo, XM and Tang, YL (2018) Ethyl-substitutive thioflavin T as a highly-specific fluorescence probe for detecting G-quadruplex structure. Scientific Reports 8, 2666.Google Scholar
Han, KY, Leslie, BJ, Fei, JY, Zhang, JC and Ha, T (2013) Understanding the photophysics of the Spinach-DFHBI RNA aptamer-fluorogen complex to improve live-cell RNA imaging. Journal of the American Chemical Society 135, 19033–19038.Google Scholar
Hangauer, MJ, Vaughn, IW and McManus, MT (2013) Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genetics 9, e1003569.Google Scholar
Heim, R, Prasher, DC and Tsien, RY (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proceedings of the National Academy of Sciences of the USA 91, 12501–12504.Google Scholar
Holeman, LA, Robinson, SL, Szostak, JW and Wilson, C (1998) Isolation and characterization of fluorophore-binding RNA aptamers. Folding & Design 3, 423–431.Google Scholar
Huang, H, Suslov, NB, Li, NS, Shelke, SA, Evans, ME, Koldobskaya, Y, Rice, PA and Piccirilli, JA (2014) A G-quadruplex-containing RNA activates fluorescence in a GFP-like fluorophore. Nature Chemical Biology 10, 686–U128.Google Scholar
Jarikote, DV, Krebs, N, Tannert, S, Röder, B and Seitz, O (2007) Exploring base-pair-specific optical properties of the DNA stain thiazole orange. Chemistry 13, 300–310.Google Scholar
Jay, DG and Keshishian, H (1990) Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. Nature 348, 548–550.Google Scholar
Jeng, SCY, Chan, HHY, Booy, EP, McKenna, SA and Unrau, PJ (2016) Fluorophore ligand binding and complex stabilization of the RNA Mango and RNA Spinach aptamers. RNA 22, 1884–1892.Google Scholar
Jepsen, MDE, Sparvath, SM, Nielsen, TB, Langvad, AH, Grossi, G, Gothelf, KV and Andersen, ES (2018) Development of a genetically encodable FRET system using fluorescent RNA aptamers. Nature Communications 9, 18.Google Scholar
Johansson, HE, Dertinger, D, LeCuyer, KA, Behlen, LS, Greef, CH and Uhlenbeck, OC (1998) A thermodynamic analysis of the sequence-specific binding of RNA by bacteriophage MS2 coat protein. Proceedings of the National Academy of Sciences of the USA 95, 9244–9249.Google Scholar
Jones, CP and Ferré-D'Amaré, AR (2015) RNA quaternary structure and global symmetry. Trends in Biochemical Sciences 40, 211–220.Google Scholar
Kellenberger, CA, Chen, C, Whiteley, AT, Portnoy, DA and Hammond, MC (2015) RNA-based fluorescent biosensors for live cell imaging of second messenger cyclic di-AMP. Journal of the American Chemical Society 137, 6432–6435.Google Scholar
Klymchenko, AS (2017) Solvatochromic and fluorogenic dyes as environment-sensitive probes: design and biological applications. Accounts of Chemical Research 50, 366–375.Google Scholar
Koirala, D, Shelke, SA, Dupont, M, Ruiz, S, DasGupta, S, Bailey, LJ, Benner, SA and Piccirilli, JA (2018) Affinity maturation of a portable Fab-RNA module for chaperone-assisted RNA crystallography. Nucleic Acids Research 46, 2624–2635.Google Scholar
Lavis, LD (2017 a) Chemistry is dead. Long live chemistry!. Biochemistry 56, 5165–5170.Google Scholar
Lavis, LD (2017 b) Teaching old dyes new tricks: biological probes built from fluoresceins and rhodamines. Annual Review of Biochemistry 86, 825–843.Google Scholar
Lavis, LD and Raines, RT (2008) Bright ideas for chemical biology. ACS Chemical Biology 3, 142–155.Google Scholar
Li, N, Larson, T, Nguyen, HH, Sokolov, KV and Ellington, AD (2010) Directed evolution of gold nanoparticle delivery to cells. Chemical Communications 46, 392–394.Google Scholar
Misra, VK and Draper, DE (2002) The linkage between magnesium binding and RNA folding. Journal of Molecular Biology 317, 507–521.Google Scholar
Mohanty, J, Barooah, N, Dhamodharan, V, Harikrishna, S, Pradeepkumar, PI and Bhasikuttan, AC (2013) Thioflavin T as an efficient inducer and selective fluorescent sensor for the human telomeric G-quadruplex DNA. Journal of the American Chemical Society 135, 367–376.Google Scholar
Monici, M (2005) Cell and tissue autofluorescence research and diagnostic applications. Biotechnology Annual Review 11, 227–256.Google Scholar
Nelles, DA, Fang, MY, O'Connell, MR, Xu, JL, Markmiller, SJ, Doudna, JA and Yeo, GW (2016) Programmable RNA tracking in live cells with CRISPR/Cas9. Cell 165, 488–496.Google Scholar
Nguyen, DH, DeFina, SC, Fink, WH and Dieckmann, T (2002) Binding to an RNA aptamer changes the charge distribution and conformation of malachite green. Journal of the American Chemical Society 124, 15081–15084.Google Scholar
Ni, CZ, Syed, R, Kodandapani, R, Wickersham, J, Peabody, DS and Ely, KR (1995) Crystal structure of the MS2 coat protein dimer: implications for RNA binding and virus assembly. Structure 3, 255–263.Google Scholar
Niwa, H, Inouye, S, Hirano, T, Matsuno, T, Kojima, S, Kubota, M, Ohashi, M and Tsuji, FI (1996) Chemical nature of the light emitter of the Aequorea green fluorescent protein. Proceedings of the National Academy of Sciences of the USA 93, 13617–13622.Google Scholar
Nygren, J, Svanvik, N and Kubista, M (1998) The interactions between the fluorescent dye thiazole orange and DNA. Biopolymers 46, 39–51.Google Scholar
Ouellet, J (2016) RNA fluorescence with light-up aptamers. Frontiers in Chemistry 4, 12.Google Scholar
Paige, JS, Wu, KY and Jaffrey, SR (2011) RNA mimics of green fluorescent protein. Science 333, 642–646.Google Scholar
Paige, JS, Nguyen-Duc, T, Song, WJ and Jaffrey, SR (2012) Fluorescence imaging of cellular metabolites with RNA. Science 335, 1194–1194.Google Scholar
Pertea, M (2012) The human transcriptome: an unfinished story. Genes 3, 344–360.Google Scholar
Peselis, A and Serganov, A (2014) Themes and variations in riboswitch structure and function. Biochimica et Biophysica Acta 1839, 908–918.Google Scholar
Phan, AT, Kuryavyi, V, Darnell, JC, Serganov, A, Majumdar, A, Ilin, S, Raslin, T, Polonskaia, A, Chen, C, Clain, D, Darnell, RB and Patel, DJ (2011) Structure-function studies of FMRP RGG peptide recognition of an RNA duplex-quadruplex junction. Nature Structural & Molecular Biology 18, 796–804.Google Scholar
Piatkevich, KD, Hulit, J, Subach, OM, Wu, B, Abdulla, A, Segall, JE and Verkhusha, VV (2010 a) Monomeric red fluorescent proteins with a large Stokes shift. Proceedings of the National Academy of Sciences of the USA 107, 5369–5374.Google Scholar
Piatkevich, KD, Malashkevich, VN, Almo, SC and Verkhusha, VV (2010 b) Engineering ESPT pathways based on structural analysis of LSSmKate red fluorescent proteins with large Stokes shift. Journal of the American Chemical Society 132, 10762–10770.Google Scholar
Pleij, CW, Rietveld, K and Bosch, L (1985) A new principle of RNA folding based on pseudoknotting. Nucleic Acids Research 13, 1717–1731.Google Scholar
Renaud de la Faverie, A, Guédin, A, Bedrat, A, Yatsunyk, LA and Mergny, JL (2014) Thioflavin T as a fluorescence light-up probe for G4 formation. Nucleic Acids Research 42, e65.Google Scholar
Robertson, DL and Joyce, GF (1990) Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 344, 467–468.Google Scholar
Rodriguez, EA, Tran, GN, Gross, LA, Crisp, JL, Shu, XK, Lin, JY and Tsien, RY (2016) A far-red fluorescent protein evolved from a cyanobacterial phycobiliprotein. Nature Methods 13, 763–769.Google Scholar
Rodriguez, EA, Campbell, RE, Lin, JY, Lin, MZ, Miyawaki, A, Palmer, AE, Shu, XK, Zhang, J and Tsien, RY (2017) The growing and glowing toolbox of fluorescent and photoactive proteins. Trends in Biochemical Sciences 42, 111–129.Google Scholar
Rogers, TA, Andrews, GE, Jaeger, L and Grabow, WW (2015) Fluorescent monitoring of RNA assembly and processing using the split-spinach aptamer. ACS Synthetic Biology 4, 162–166.Google Scholar
Royant, A and Noirclerc-Savoye, M (2011) Stabilizing role of glutamic acid 222 in the structure of enhanced green fluorescent protein. Journal of Structural Biology 174, 385–390.Google Scholar
Shank, NI, Zanotti, KJ, Lanni, F, Berget, PB and Armitage, BA (2009) Enhanced photostability of genetically encodable fluoromodules based on fluorogenic cyanine dyes and a promiscuous protein partner. Journal of the American Chemical Society 131, 12960–9.Google Scholar
Shank, NI, Pham, HH, Waggoner, AS and Armitage, BA (2013) Twisted cyanines: a non-planar fluorogenic dye with superior photostability and its use in a protein-based fluoromodule. Journal of the American Chemical Society 135, 242–251.Google Scholar
Shcherbakova, DM, Hink, MA, Joosen, L, Gadella, TW and Verkhusha, VV (2012) An orange fluorescent protein with a large Stokes shift for single-excitation multicolor FCCS and FRET imaging. Journal of the American Chemical Society 134, 7913–7923.Google Scholar
Shelke, SA, Shao, Y, Laski, A, Koirala, D, Weissman, BP, Fuller, JR, Tan, X, Constantin, TP, Waggoner, AS, Bruchez, MP, Armitage, BA and Piccirilli, JA (2018) Structural basis for activation of fluorogenic dyes by an RNA aptamer lacking a G-quadruplex motif. Nature Communications 9, 4542.Google Scholar
Sjekloća, L and Ferré-D'Amaré, AR (2019) Binding between G Quadruplexes at the Homodimer Interface of the Corn RNA Aptamer Strongly Activates Thioflavin T Fluorescence. Cell Chem Biol pii: S2451-9456, 30143–30146.Google Scholar
Song, WJ, Strack, RL, Svensen, N and Jaffrey, SR (2014) Plug-and-play fluorophores extend the spectral properties of spinach. Journal of the American Chemical Society 136, 1198–1201.Google Scholar
Song, W, Filonov, GS, Kim, H, Hirsch, M, Li, X, Moon, JD and Jaffrey, SR (2017) Imaging RNA polymerase III transcription using a photostable RNA-fluorophore complex. Nature Chemical Biology 13, 1187–1194.Google Scholar
Sparano, BA and Koide, K (2005) A strategy for the development of small-molecule-based sensors that strongly fluoresce when bound to a specific RNA. Journal of the American Chemical Society 127, 14954–5.Google Scholar
Sparano, BA and Koide, K (2007) Fluorescent sensors for specific RNA: a general paradigm using chemistry and combinatorial biology. Journal of the American Chemical Society 129, 4785–4794.Google Scholar
Steinmetzger, C, Palanisamy, N, Gore, KR and Höbartner, C (2019) A multicolor large stokes shift fluorogen-activating RNA aptamer with cationic chromophores. Chemistry 25, 1931–1935.Google Scholar
Strack, RL, Disney, MD and Jaffrey, SR (2013) A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA. Nature Methods 10, 1219.Google Scholar
Subach, F, Subach, O, Gundorov, I, Morozova, K, Piatkevich, K, Cuervo, A and Verkhusha, V (2009) Monomeric fluorescent timers that change color from blue to red report on cellular trafficking. Nature Chemical Biology 5, 118–126.Google Scholar
Sunbul, M and Jäschke, A (2013) Contact-mediated quenching for RNA imaging in bacteria with a fluorophore-binding aptamer. Angewandte Chemie (International ed. in English) 52, 13401–4.Google Scholar
Szostak, JW (2003) Functional information: molecular messages. Nature 423, 689.Google Scholar
Tan, X, Constantin, TP, Sloane, KL, Waggoner, AS, Bruchez, MP and Armitage, BA (2017) Fluoromodules consisting of a promiscuous RNA aptamer and Red or blue fluorogenic cyanine dyes: selection, characterization, and bioimaging. Journal of the American Chemical Society 139, 9001–9009.Google Scholar
Trachman, RJ, Demeshkina, NA, Lau, MWL, Panchapakesan, SSS, Jeng, SCY, Unrau, PJ and Ferré-D'Amaré, AR (2017 a) Structural basis for high-affinity fluorophore binding and activation by RNA Mango. Nature Chemical Biology 13, 807–813.Google Scholar
Trachman, RJ, Truong, L and Ferre-D'Amare, AR (2017 b) Structural principles of fluorescent RNA aptamers. Trends in Pharmacological Sciences 38, 928–939.Google Scholar
Trachman, RJ, Abdolahzadeh, A, Andreoni, A, Cojocaru, R, Knutson, JR, Ryckelynck, M, Unrau, PJ and Ferré-D'Amaré, AR (2018) Crystal structures of the mango-II RNA aptamer reveal heterogeneous fluorophore binding and guide engineering of variants with improved selectivity and brightness. Biochemistry 57, 3544–3548.Google Scholar
Trachman, RJ III, Autour, AJ, Sunny, CY, Abdolahzadeh, A, Andreoni, A, Cojocaru, R, Garipov, R, Dolgosheina, EV, Knutson, JR, Ryckelynck, M, Unrau, PJ and Ferré-D'Amaré, AR (2019) Structure and functional reselection of the Mango-III fluorogenic RNA aptamer. Nature Chemical Biology 15(5), 472–479.Google Scholar
Troung, LA and Ferré-D'Amaré, AR (2019) From fluorescent proteins to fluorogenic RNAs: tools for imaging cellular macromolecules. Protein Science 28(8), 1374–1386.Google Scholar
Tucker, WO, Shum, KT and Tanner, JA (2012) G-quadruplex DNA aptamers and their ligands: structure, function and application. Current Pharmaceutical Design 18, 2014–2026.Google Scholar
Tuerk, C and Gold, L (1990) Systematic evolution of ligands by exponential enrichment – RNA ligands to bacteriophage-T4 DNA-polymerase. Science 249, 505–510.Google Scholar
Turaev, AV, Tsvetkov, VB, Tankevich, MV, Smirnov, IP, Aralov, AV, Pozmogova, GE and Varizhuk, AM (2019) Benzothiazole-based cyanines as fluorescent ‘light-up’ probes for duplex and quadruplex DNA. Biochimie 162, 216–228.Google Scholar
Valencia-Burton, M, McCullough, RM, Cantor, CR and Broude, NE (2007) RNA visualization in live bacterial cells using fluorescent protein complementation. Nature Methods 4, 421–427.Google Scholar
Vasilyev, N, Polonskaia, A, Darnell, JC, Darnell, RB, Patel, DJ and Serganov, A (2015) Crystal structure reveals specific recognition of a G-quadruplex RNA by a β-turn in the RGG motif of FMRP. Proceedings of the National Academy of Sciences of the USA 112, E5391–E5400.Google Scholar
Wakeman, CA, Winkler, WC and Dann, CE (2007) Structural features of metabolite-sensing riboswitches. Trends in Biochemical Sciences 32, 415–424.Google Scholar
Wang, PC, Querard, J, Maurin, S, Nath, SS, Le Saux, T, Gautier, A and Jullien, L (2013) Photochemical properties of Spinach and its use in selective imaging. Chemical Science 4, 2865–2873.Google Scholar
Ward, WW and Bokman, SH (1982) Reversible denaturation of aquoria green-fluorescent protein: physical separation and characterization of the renatured protein. Biochemistry 21, 4535–4540.Google Scholar
Warner, KD, Chen, MC, Song, WJ, Strack, RL, Thorn, A, Jaffrey, SR and Ferre-D'Amare, AR (2014) Structural basis for activity of highly efficient RNA mimics of green fluorescent protein. Nature Structural & Molecular Biology 21, 658–663.Google Scholar
Warner, KD, Sjekloca, L, Song, W, Filonov, GS, Jaffrey, SR and Ferré-D'Amaré, AR (2017) A homodimer interface without base pairs in an RNA mimic of red fluorescent protein. Nat Chem Biol 13, 1195–1201.Google Scholar
Wu, B, Chen, J and Singer, RH (2014) Background free imaging of single mRNAs in live cells using split fluorescent proteins. Scientific Reports 4, 3615.Google Scholar
Xu, S, Li, Q, Xiang, J, Yang, Q, Sun, H, Guan, A, Wang, L, Liu, Y, Yu, L, Shi, Y, Chen, H and Tang, Y (2016) Thioflavin T as an efficient fluorescence sensor for selective recognition of RNA G-quadruplexes. Scientific Reports 6, 24793.Google Scholar
You, MX and Jaffrey, SR (2015) Structure and mechanism of RNA mimics of green fluorescent protein. In Dill, KA (ed.), Annual Review of Biophysics. Palo Alto: Annual Reviews, pp. 187–206.Google Scholar
Yu, D, Gustafson, WC, Han, C, Lafaye, C, Noirclerc-Savoye, M, Ge, WP, Thayer, DA, Huang, H, Kornberg, TB, Royant, A, Jan, LY, Jan, YN, Weiss, WA and Shu, XK (2014) An improved monomeric infrared fluorescent protein for neuronal and tumour brain imaging. Nature Communications 5, 7.Google Scholar