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A homodimer interface without base pairs in an RNA mimic of red fluorescent protein.

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Warner KD, Sjekloća L, Song W, Filonov GS, Jaffrey SR, Ferré-D'Amaré AR
OpenAccess logo Nat Chem Biol 13 1195-1201 (2017)
Cited: 64 times
EuropePMC logo PMID: 28945234

Abstract

Corn, a 28-nucleotide RNA, increases yellow fluorescence of its cognate ligand 3,5-difluoro-4-hydroxybenzylidene-imidazolinone-2-oxime (DFHO) by >400-fold. Corn was selected in vitro to overcome limitations of other fluorogenic RNAs, particularly rapid photobleaching. We now report the Corn-DFHO co-crystal structure, discovering that the functional species is a quasisymmetric homodimer. Unusually, the dimer interface, in which six unpaired adenosines break overall two-fold symmetry, lacks any intermolecular base pairs. The homodimer encapsulates one DFHO at its interprotomer interface, sandwiching it with a G-quadruplex from each protomer. Corn and the green-fluorescent Spinach RNA are structurally unrelated. Their convergent use of G-quadruplexes underscores the usefulness of this motif for RNA-induced small-molecule fluorescence. The asymmetric dimer interface of Corn could provide a basis for the development of mutants that only fluoresce as heterodimers. Such variants would be analogous to Split GFP, and may be useful for analyzing RNA co-expression or association, or for designing self-assembling RNA nanostructures.

Reviews - 5bjo mentioned but not cited (4)

  1. The emerging structural complexity of G-quadruplex RNAs. Banco MT, Ferré-D'Amaré AR. RNA 27 390-402 (2021)
  2. RNA Structure and Cellular Applications of Fluorescent Light-Up Aptamers. Neubacher S, Hennig S. Angew Chem Int Ed Engl 58 1266-1279 (2019)
  3. Tracking RNA with light: selection, structure, and design of fluorescence turn-on RNA aptamers. Trachman RJ, Ferré-D'Amaré AR. Q Rev Biophys 52 e8 (2019)
  4. Structural Insights into RNA Dimerization: Motifs, Interfaces and Functions. Bou-Nader C, Zhang J. Molecules 25 E2881 (2020)

Articles - 5bjo mentioned but not cited (10)

  1. A homodimer interface without base pairs in an RNA mimic of red fluorescent protein. Warner KD, Sjekloća L, Song W, Filonov GS, Jaffrey SR, Ferré-D'Amaré AR. Nat Chem Biol 13 1195-1201 (2017)
  2. Exploring the RNA-Recognition Mechanism Using Supervised Molecular Dynamics (SuMD) Simulations: Toward a Rational Design for Ribonucleic-Targeting Molecules? Bissaro M, Sturlese M, Moro S. Front Chem 8 107 (2020)
  3. Recognition of small molecule-RNA binding sites using RNA sequence and structure. Su H, Peng Z, Yang J. Bioinformatics 37 36-42 (2021)
  4. Large Stokes shift fluorescence activation in an RNA aptamer by intermolecular proton transfer to guanine. Mieczkowski M, Steinmetzger C, Bessi I, Lenz AK, Schmiedel A, Holzapfel M, Lambert C, Pena V, Höbartner C. Nat Commun 12 3549 (2021)
  5. Base-intercalated and base-wedged stacking elements in 3D-structure of RNA and RNA-protein complexes. Baulin E, Metelev V, Bogdanov A. Nucleic Acids Res 48 8675-8685 (2020)
  6. Co-crystal structures of the fluorogenic aptamer Beetroot show that close homology may not predict similar RNA architecture. Passalacqua LFM, Starich MR, Link KA, Wu J, Knutson JR, Tjandra N, Jaffrey SR, Ferré-D'Amaré AR. Nat Commun 14 2969 (2023)
  7. Novel Design of RNA Aptamers as Cancer Inhibitors and Diagnosis Targeting the Tyrosine Kinase Domain of the NT-3 Growth Factor Receptor Using a Computational Sequence-Based Approach. Muhammad AM, Zari A, Alsubhi NH, Al-Zahrani MH, Alghamdi RA, Labib MM. Molecules 27 4518 (2022)
  8. RR3DD: an RNA global structure-based RNA three-dimensional structural classification database. Hong X, Zheng J, Xie J, Tong X, Liu X, Song Q, Liu S, Liu S. RNA Biol 18 738-746 (2021)
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  10. Thermal titration molecular dynamics (TTMD): shedding light on the stability of RNA-small molecule complexes. Dodaro A, Pavan M, Menin S, Salmaso V, Sturlese M, Moro S. Front Mol Biosci 10 1294543 (2023)


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  4. G-Quadruplex-Based Fluorescent Turn-On Ligands and Aptamers: From Development to Applications. Umar MI, Ji D, Chan CY, Kwok CK. Molecules 24 E2416 (2019)
  5. RNA-based fluorescent biosensors for live cell imaging of small molecules and RNAs. Su Y, Hammond MC. Curr Opin Biotechnol 63 157-166 (2020)
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  9. Bacterial metabolic heterogeneity: origins and applications in engineering and infectious disease. Evans TD, Zhang F. Curr Opin Biotechnol 64 183-189 (2020)
  10. Imaging Approaches for the Study of Metabolism in Real Time Using Genetically Encoded Reporters. Chandris P, Giannouli CC, Panayotou G. Front Cell Dev Biol 9 725114 (2021)
  11. Multidimensional futuristic approaches to address the pandemics beyond COVID-19. Kotwal SB, Orekondey N, Saradadevi GP, Priyadarshini N, Puppala NV, Bhushan M, Motamarry S, Kumar R, Mohannath G, Dey RJ. Heliyon 9 e17148 (2023)

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  4. Structure and functional reselection of the Mango-III fluorogenic RNA aptamer. Trachman RJ, Autour A, Jeng SCY, Abdolahzadeh A, Andreoni A, Cojocaru R, Garipov R, Dolgosheina EV, Knutson JR, Ryckelynck M, Unrau PJ, Ferré-D'Amaré AR. Nat Chem Biol 15 472-479 (2019)
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  6. Modulation of Fluorescent Protein Chromophores To Detect Protein Aggregation with Turn-On Fluorescence. Liu Y, Wolstenholme CH, Carter GC, Liu H, Hu H, Grainger LS, Miao K, Fares M, Hoelzel CA, Yennawar HP, Ning G, Du M, Bai L, Li X, Zhang X. J Am Chem Soc 140 7381-7384 (2018)
  7. Structural basis for activation of fluorogenic dyes by an RNA aptamer lacking a G-quadruplex motif. Shelke SA, Shao Y, Laski A, Koirala D, Weissman BP, Fuller JR, Tan X, Constantin TP, Waggoner AS, Bruchez MP, Armitage BA, Piccirilli JA. Nat Commun 9 4542 (2018)
  8. A Multicolor Large Stokes Shift Fluorogen-Activating RNA Aptamer with Cationic Chromophores. Steinmetzger C, Palanisamy N, Gore KR, Höbartner C. Chemistry 25 1931-1935 (2019)
  9. Selective recognition of c-MYC Pu22 G-quadruplex by a fluorescent probe. Zhai Q, Gao C, Ding J, Zhang Y, Islam B, Lan W, Hou H, Deng H, Li J, Hu Z, Mohamed HI, Xu S, Cao C, Haider SM, Wei D. Nucleic Acids Res 47 2190-2204 (2019)
  10. In Situ Genetically Cascaded Amplification for Imaging RNA Subcellular Locations. Ren K, Wu R, Karunanayake Mudiyanselage APKK, Yu Q, Zhao B, Xie Y, Bagheri Y, Tian Q, You M, You M. J Am Chem Soc 142 2968-2974 (2020)
  11. A Fluorogenic RNA-Based Sensor Activated by Metabolite-Induced RNA Dimerization. Kim H, Jaffrey SR. Cell Chem Biol 26 1725-1731.e6 (2019)
  12. Forced Intercalation (FIT)-Aptamers. Ebrahimi SB, Samanta D, Cheng HF, Nathan LI, Mirkin CA. J Am Chem Soc 141 13744-13748 (2019)
  13. Binding between G Quadruplexes at the Homodimer Interface of the Corn RNA Aptamer Strongly Activates Thioflavin T Fluorescence. Sjekloća L, Ferré-D'Amaré AR. Cell Chem Biol 26 1159-1168.e4 (2019)
  14. Structure-based investigation of fluorogenic Pepper aptamer. Huang K, Chen X, Li C, Song Q, Li H, Zhu L, Yang Y, Ren A. Nat Chem Biol 17 1289-1295 (2021)
  15. A protein-independent fluorescent RNA aptamer reporter system for plant genetic engineering. Bai J, Luo Y, Wang X, Li S, Luo M, Yin M, Zuo Y, Li G, Yao J, Yang H, Zhang M, Wei W, Wang M, Wang R, Fan C, Zhao Y. Nat Commun 11 3847 (2020)
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  17. Structure-Guided Engineering of the Homodimeric Mango-IV Fluorescence Turn-on Aptamer Yields an RNA FRET Pair. Trachman RJ, Cojocaru R, Wu D, Piszczek G, Ryckelynck M, Unrau PJ, Ferré-D'Amaré AR. Structure 28 776-785.e3 (2020)
  18. Supramolecular Fluorescence Resonance Energy Transfer in Nucleobase-Modified Fluorogenic RNA Aptamers. Steinmetzger C, Bäuerlein C, Höbartner C. Angew Chem Int Ed Engl 59 6760-6764 (2020)
  19. DNA G-Quadruplexes Activate Heme for Robust Catalysis of Carbene Transfer Reactions. Ibrahim H, Mulyk P, Sen D. ACS Omega 4 15280-15288 (2019)
  20. Highly specific, multiplexed isothermal pathogen detection with fluorescent aptamer readout. Aufdembrink LM, Khan P, Gaut NJ, Adamala KP, Engelhart AE. RNA 26 1283-1290 (2020)
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  22. Structure-fluorescence activation relationships of a large Stokes shift fluorogenic RNA aptamer. Steinmetzger C, Bessi I, Lenz AK, Höbartner C. Nucleic Acids Res 47 11538-11550 (2019)
  23. A SNAP-tag fluorogenic probe mimicking the chromophore of the red fluorescent protein Kaede. Jung KH, Fares M, Grainger LS, Wolstenholme CH, Hou A, Liu Y, Zhang X. Org Biomol Chem 17 1906-1915 (2019)
  24. Self-Assembly of Intracellular Multivalent RNA Complexes Using Dimeric Corn and Beetroot Aptamers. Wu J, Svensen N, Song W, Kim H, Zhang S, Li X, Jaffrey SR. J Am Chem Soc 144 5471-5477 (2022)
  25. Detection of SARS-CoV-2 RNA Using a DNA Aptamer Mimic of Green Fluorescent Protein. VarnBuhler BS, Moon J, Dey SK, Wu J, Jaffrey SR. ACS Chem Biol 17 840-853 (2022)
  26. Structural Basis for Fluorescence Activation by Pepper RNA. Rees HC, Gogacz W, Li NS, Koirala D, Piccirilli JA. ACS Chem Biol 17 1866-1875 (2022)
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  28. Co-crystal structure of the iMango-III fluorescent RNA aptamer using an X-ray free-electron laser. Trachman RJ, Stagno JR, Conrad C, Jones CP, Fischer P, Meents A, Wang YX, Ferré-D'Amaré AR. Acta Crystallogr F Struct Biol Commun 75 547-551 (2019)
  29. Photophysics of DFHBI bound to RNA aptamer Baby Spinach. Dao NT, Haselsberger R, Khuc MT, Phan AT, Voityuk AA, Michel-Beyerle ME. Sci Rep 11 7356 (2021)
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  34. A ribose modification of Spinach aptamer accelerates lead(ii) cation association in vitro. Savage JC, Shinde P, Bächinger HP, Davare MA, Shinde U. Chem Commun (Camb) 55 5882-5885 (2019)
  35. A universal orthogonal imaging platform for living-cell RNA detection using fluorogenic RNA aptamers. Yin P, Ge M, Xie S, Zhang L, Kuang S, Nie Z. Chem Sci 14 14131-14139 (2023)
  36. Double-stemmed and split structural variants of fluorescent RNA Mango aptamers. Herrera-Gutierrez J, Burden SJ, Kobernat SE, Shults NH, Smith M, Fologea D, Hayden EJ. RNA 29 1355-1364 (2023)
  37. Intracellular RNA and DNA tracking by uridine-rich internal loop tagging with fluorogenic bPNA. Liang Y, Willey S, Chung YC, Lo YM, Miao S, Rundell S, Tu LC, Bong D. Nat Commun 14 2987 (2023)
  38. Ligands with polyfluorophenyl moieties promote a local structural rearrangement in the Spinach2 and Broccoli aptamers that increases ligand affinities. Anisuzzaman S, Geraskin IM, Ilgu M, Bendickson L, Kraus GA, Nilsen-Hamilton M. RNA 28 865-877 (2022)
  39. Spinach-based RNA mimicking GFP in plant cells. Yu Z, Wang Y, Mei F, Yan H, Jin Z, Zhang P, Zhang X, Tör M, Jackson S, Shi N, Hong Y. Funct Integr Genomics 22 423-428 (2022)


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