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A Mirror Image Fluorogenic Aptamer Sensor for Live-Cell Imaging of MicroRNAs

Cite this: ACS Sens. 2019, 4, 3, 566–570
Publication Date (Web):March 7, 2019
https://doi.org/10.1021/acssensors.9b00252
Copyright © 2019 American Chemical Society
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Development of biocompatible tools for intracellular imaging of RNA expression remains a central challenge. Herein, we report the use of heterochiral strand-displacement to sequence-specifically interface endogenous d-miRNAs with an l-RNA version of the fluorogenic aptamer Mango III, thereby generating a novel class of biocompatible miRNA sensors. Fluorescence activation of the sensor is achieved through the displacement of an achiral blocking strand from the l-Mango aptamer by the d-RNA target. In contrast to d-Mango, we show that the l-Mango sensor retains full functionality in serum, enabling a light-up fluorescence response to the target. Importantly, we employ a self-delivering version of the l-Mango sensor to image the expression of microRNA-155 in living cells, representing the first time l-oligonucleotides have been interfaced with a living system. Overall, this work provides a new paradigm for the development of biocompatible hybridization-based sensors for live-cell imaging of RNAs and greatly expands the utility of fluorogenic aptamers for cellular applications.

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Cited By

This article is cited by 29 publications.

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  2. Cole Emanuelson, Anirban Bardhan, Alexander Deiters. DNA Computing: NOT Logic Gates See the Light. ACS Synthetic Biology 2021, 10 (7) , 1682-1689. https://doi.org/10.1021/acssynbio.1c00062
  3. Wenrui Zhong, Jonathan T. Sczepanski. Direct Comparison of d-DNA and l-DNA Strand-Displacement Reactions in Living Mammalian Cells. ACS Synthetic Biology 2021, 10 (1) , 209-212. https://doi.org/10.1021/acssynbio.0c00527
  4. Tracy L. Mallette, Milan N. Stojanovic, Darko Stefanovic, Matthew R. Lakin. Robust Heterochiral Strand Displacement Using Leakless Translators. ACS Synthetic Biology 2020, 9 (7) , 1907-1910. https://doi.org/10.1021/acssynbio.0c00131
  5. Brian E. Young, Jonathan T. Sczepanski. Heterochiral DNA Strand-Displacement Based on Chimeric d/l-Oligonucleotides. ACS Synthetic Biology 2019, 8 (12) , 2756-2759. https://doi.org/10.1021/acssynbio.9b00335
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  11. Adam M. Kabza, Nandini Kundu, Wenrui Zhong, Jonathan T. Sczepanski. Integration of chemically modified nucleotides with DNA strand displacement reactions for applications in living systems. WIREs Nanomedicine and Nanobiotechnology 2022, 14 (2) https://doi.org/10.1002/wnan.1743
  12. Md. Mahbubur Rahman, Nasrin Siraj Lopa, Jae‐Joon Lee. Advances in electrochemical aptasensing for cardiac biomarkers. Bulletin of the Korean Chemical Society 2022, 43 (1) , 51-68. https://doi.org/10.1002/bkcs.12434
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  14. Danyang Ji, Kaixin Lyu, Haizhou Zhao, Chun Kit Kwok. Circular L-RNA aptamer promotes target recognition and controls gene activity. Nucleic Acids Research 2021, 49 (13) , 7280-7291. https://doi.org/10.1093/nar/gkab593
  15. Nandini Kundu, Brian E Young, Jonathan T Sczepanski. Kinetics of heterochiral strand displacement from PNA–DNA heteroduplexes. Nucleic Acids Research 2021, 3 https://doi.org/10.1093/nar/gkab499
  16. Zike Huang, Liping Qiu, Tao Zhang, Weihong Tan. Integrating DNA Nanotechnology with Aptamers for Biological and Biomedical Applications. Matter 2021, 4 (2) , 461-489. https://doi.org/10.1016/j.matt.2020.11.002
  17. Erika Schaudy, Mark M. Somoza, Jory Lietard. l ‐DNA Duplex Formation as a Bioorthogonal Information Channel in Nucleic Acid‐Based Surface Patterning. Chemistry – A European Journal 2020, 26 (63) , 14310-14314. https://doi.org/10.1002/chem.202001871
  18. Alessandro Bertucci, Alessandro Porchetta, Erica Del Grosso, Tania Patiño, Andrea Idili, Francesco Ricci. Protein‐Controlled Actuation of Dynamic Nucleic Acid Networks by Using Synthetic DNA Translators**. Angewandte Chemie 2020, 132 (46) , 20758-20762. https://doi.org/10.1002/ange.202008553
  19. Alessandro Bertucci, Alessandro Porchetta, Erica Del Grosso, Tania Patiño, Andrea Idili, Francesco Ricci. Protein‐Controlled Actuation of Dynamic Nucleic Acid Networks by Using Synthetic DNA Translators**. Angewandte Chemie International Edition 2020, 59 (46) , 20577-20581. https://doi.org/10.1002/anie.202008553
  20. Mubarak I Umar, Chun Kit Kwok. Specific suppression of D-RNA G-quadruplex–protein interaction with an L-RNA aptamer. Nucleic Acids Research 2020, 48 (18) , 10125-10141. https://doi.org/10.1093/nar/gkaa759
  21. Arnaud Gautier, Alison G. Tebo. Sensing cellular biochemistry with fluorescent chemical–genetic hybrids. Current Opinion in Chemical Biology 2020, 57 , 58-64. https://doi.org/10.1016/j.cbpa.2020.04.005
  22. Fanny Broch, Arnaud Gautier. Illuminating Cellular Biochemistry: Fluorogenic Chemogenetic Biosensors for Biological Imaging. ChemPlusChem 2020, 85 (7) , 1487-1497. https://doi.org/10.1002/cplu.202000413
  23. Adam M. Kabza, Jonathan T. Sczepanski. l-DNA-Based Catalytic Hairpin Assembly Circuit. Molecules 2020, 25 (4) , 947. https://doi.org/10.3390/molecules25040947
  24. Shanni Hong, Xiaoting Zhang, Ryan J. Lake, Gregory T. Pawel, Zijian Guo, Renjun Pei, Yi Lu. A photo-regulated aptamer sensor for spatiotemporally controlled monitoring of ATP in the mitochondria of living cells. Chemical Science 2020, 11 (3) , 713-720. https://doi.org/10.1039/C9SC04773E
  25. Michael Ryckelynck. Development and Applications of Fluorogen/Light-Up RNA Aptamer Pairs for RNA Detection and More. 2020, 73-102. https://doi.org/10.1007/978-1-0716-0712-1_5
  26. Baozhang Guan, Xingwang Zhang. <p>Aptamers as Versatile Ligands for Biomedical and Pharmaceutical Applications</p>. International Journal of Nanomedicine 2020, Volume 15 , 1059-1071. https://doi.org/10.2147/IJN.S237544
  27. Tiphaine Péresse, Arnaud Gautier. Next-Generation Fluorogen-Based Reporters and Biosensors for Advanced Bioimaging. International Journal of Molecular Sciences 2019, 20 (24) , 6142. https://doi.org/10.3390/ijms20246142
  28. Mohammed Dwidar, Yohei Yokobayashi. Development of a histamine aptasensor for food safety monitoring. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-52876-1
  29. , Adam M. Kabza, Brian E. Young, Nandini Kundu, Jonathan T. Sczepanski. Heterochiral nucleic acid circuits. Emerging Topics in Life Sciences 2019, 3 (5) , 501-506. https://doi.org/10.1042/ETLS20190102

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