Single mRNA Imaging with Fluorogenic RNA Aptamers and Small-molecule Fluorophores
Wei Chen
Institute of Cytology and Genetics, the Hengyang Key Laboratory of Cellular Stress Biology, Hengyang Medical School, University of South China, Hengyang, Hunan, 421001 China
Beijing Institutes of Life Science, State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Science, Beijing, 100101 China
These authors contributed equally to this work
Search for more papers by this authorProf. Dr. Xiaoying Zhao
College of Chemistry and Materials Engineering, Beijing Technology and Business University, Beijing, 100048 China
These authors contributed equally to this work
Search for more papers by this authorCorresponding Author
Prof. Dr. Nanyang Yang
Institute of Cytology and Genetics, the Hengyang Key Laboratory of Cellular Stress Biology, Hengyang Medical School, University of South China, Hengyang, Hunan, 421001 China
Search for more papers by this authorCorresponding Author
Prof. Dr. Xing Li
Beijing Institutes of Life Science, State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Science, Beijing, 100101 China
Search for more papers by this authorWei Chen
Institute of Cytology and Genetics, the Hengyang Key Laboratory of Cellular Stress Biology, Hengyang Medical School, University of South China, Hengyang, Hunan, 421001 China
Beijing Institutes of Life Science, State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Science, Beijing, 100101 China
These authors contributed equally to this work
Search for more papers by this authorProf. Dr. Xiaoying Zhao
College of Chemistry and Materials Engineering, Beijing Technology and Business University, Beijing, 100048 China
These authors contributed equally to this work
Search for more papers by this authorCorresponding Author
Prof. Dr. Nanyang Yang
Institute of Cytology and Genetics, the Hengyang Key Laboratory of Cellular Stress Biology, Hengyang Medical School, University of South China, Hengyang, Hunan, 421001 China
Search for more papers by this authorCorresponding Author
Prof. Dr. Xing Li
Beijing Institutes of Life Science, State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Science, Beijing, 100101 China
Search for more papers by this authorAbstract
Messenger RNA (mRNA) is the fundamental information transfer system in the cell. Tracking single mRNA from transcription to degradation with fluorescent probes provides spatiotemporal information in cells about how the genetic information is transferred from DNA to proteins. The traditional single mRNA imaging approach utilizes RNA hairpins (e.g. MS2) and tethered fluorescent protein as probes. As an exciting alternative, RNA aptamers: small-molecule fluorophores (SFs) systems have emerged as novel single mRNA imaging probes since 2019, exhibiting several advantages including fluorogenic ability and minimal perturbation. This review summarizes all five reported RNA aptamers: SFs systems for single mRNA imaging in living cells so far. It also discusses the challenges and provides prospects for single mRNA imaging applications. This review is expected to inspire researchers to develop RNA aptamers: SFs systems for studying gene expression at single-molecule resolution in cells.
Conflict of interest
The authors declare no conflict of interest.
References
- 1F. Crick, Nature 1970, 227, 561–563.
- 2S. H. Kim, M. Vieira, J. Y. Shim, H. Choi, H. Y. Park, RNA Biol. 2019, 16, 1108–1118.
- 3A. Raj, P. van den Bogaard, S. A. Rifkin, A. van Oudenaarden, S. Tyagi, Nat. Methods 2008, 5, 877–879.
- 4C. Wang, B. Han, R. Zhou, X. Zhuang, Cell 2016, 165, 990–1001.
- 5T. Morisaki, T. J. Stasevich, Cold Spring Harbor Perspect. Biol. 2018, 10, a032078.
- 6
- 6aE. Bertrand, P. Chartrand, M. Schaefer, S. M. Shenoy, R. H. Singer, R. M. Long, Mol. Cell 1998, 2, 437–445;
- 6bJ. A. Chao, Y. Patskovsky, S. C. Almo, R. H. Singer, Nat. Struct. Mol. Biol. 2008, 15, 103–105.
- 7E. Tutucci, N. M. Livingston, R. H. Singer, B. Wu, Annu. Rev. Biophys. 2018, 47, 85–106.
- 8D. M. Chudakov, M. V. Matz, S. Lukyanov, K. A. Lukyanov, Physiol. Rev. 2010, 90, 1103–1163.
- 9X. Chen, D. Zhang, N. Su, B. Bao, X. Xie, F. Zuo, L. Yang, H. Wang, L. Jiang, Q. Lin, M. Fang, N. Li, X. Hua, Z. Chen, C. Bao, J. Xu, W. Du, L. Zhang, Y. Zhao, L. Zhu, J. Loscalzo, Y. Yang, Nat. Biotechnol. 2019, 37, 1287–1293.
- 10E. Braselmann, A. J. Wierzba, J. T. Polaski, M. Chrominski, Z. E. Holmes, S. T. Hung, D. Batan, J. R. Wheeler, R. Parker, R. Jimenez, D. Gryko, R. T. Batey, A. E. Palmer, Nat. Chem. Biol. 2018, 14, 964–971.
- 11X. Li, H. Kim, J. L. Litke, J. Wu, S. R. Jaffrey, Angew. Chem. Int. Ed. 2020, 59, 4511–4518; Angew. Chem. 2020, 132, 4541–4548.
- 12J. S. Paige, K. Y. Wu, S. R. Jaffrey, Science 2011, 333, 642–646.
- 13G. S. Filonov, J. D. Moon, N. Svensen, S. R. Jaffrey, J. Am. Chem. Soc. 2014, 136, 16299–16308.
- 14W. Song, R. L. Strack, N. Svensen, S. R. Jaffrey, J. Am. Chem. Soc. 2014, 136, 1198–1201.
- 15R. A. Friesner, J. L. Banks, R. B. Murphy, T. A. Halgren, J. J. Klicic, D. T. Mainz, M. P. Repasky, E. H. Knoll, M. Shelley, J. K. Perry, D. E. Shaw, P. Francis, P. S. Shenkin, J. Med. Chem. 2004, 47, 1739–1749.
- 16A. D. Cawte, P. J. Unrau, D. S. Rueda, Nat. Commun. 2020, 11, 1283.
- 17E. V. Dolgosheina, S. C. Jeng, S. S. Panchapakesan, R. Cojocaru, P. S. Chen, P. D. Wilson, N. Hawkins, P. A. Wiggins, P. J. Unrau, ACS Chem. Biol. 2014, 9, 2412–2420.
- 18A. Autour, S. C. Y. Jeng, A. D. Cawte, A. Abdolahzadeh, A. Galli, S. S. S. Panchapakesan, D. Rueda, M. Ryckelynck, P. J. Unrau, Nat. Commun. 2018, 9, 656.
- 19E. Braselmann, T. J. Stasevich, K. Lyon, R. T. Batey, A. E. Palmer, Biorxiv 2019, https://doi.org/10.1101/701649.
10.1101/701649 Google Scholar
- 20A. Nahvi, J. E. Barrick, R. R. Breaker, Nucleic Acids Res. 2004, 32, 143–150.
- 21M. Tokunaga, N. Imamoto, K. Sakata-Sogawa, Nat. Methods 2008, 5, 159–161.
- 22M. Sunbul, J. Lackner, A. Martin, D. Englert, B. Hacene, F. Grun, K. Nienhaus, G. U. Nienhaus, A. Jaschke, Nat. Biotechnol. 2021, 39, 686–690.
- 23M. Sunbul, A. Jaschke, Nucleic Acids Res. 2018, 46, e110.
- 24B. Bühler, A. Benderoth, D. Englert, F. Grün, J. Schokolowski, A. Jäschke, M. Sunbul, bioRxiv 2021, https://doi.org/10.1101/2021.11.02.466936.
- 25D. M. Kolpashchikov, A. A. Spelkov, Angew. Chem. Int. Ed. 2021, 60, 4988–4999; Angew. Chem. 2021, 133, 5040–5051.
- 26Q. Wang, F. Xiao, H. Su, H. Liu, J. Xu, H. Tang, S. Qin, Z. Fang, Z. Lu, J. Wu, X. Weng, X. Zhou, Nucleic Acids Res. 2022, 50, e84.
- 27
- 27aM. R. Rink, M. A. P. Baptista, F. J. Flomm, T. Hennig, A. W. Whisnant, N. Wolf, J. Seibel, L. Dölken, J. B. Bosse, PLoS One 2021, 16, e0244166;
- 27bJ. U. Guo, D. P. Bartel, Science 2016, 353, aaf5371.
- 28B. Wu, J. Chen, R. H. Singer, Sci. Rep. 2014, 4, 3615.
- 29B. Wu, C. Eliscovich, Y. J. Yoon, R. H. Singer, Science 2016, 352, 1430–1435.
- 30E. Tutucci, M. Vera, R. H. Singer, Nat. Protoc. 2018, 13, 2268–2296.
- 31W. Tan, K. Wang, T. J. Drake, Curr. Opin. Chem. Biol. 2004, 8, 547–553.
- 32H. Wang, M. Nakamura, T. R. Abbott, D. Zhao, K. Luo, C. Yu, C. M. Nguyen, A. Lo, T. P. Daley, M. La Russa, Y. Liu, L. S. Qi, Science 2019, 365, 1301–1305.
- 33J. Wu, S. Zaccara, D. Khuperkar, H. Kim, M. E. Tanenbaum, S. R. Jaffrey, Nat. Methods 2019, 16, 862–865.
- 34W. Song, G. S. Filonov, H. Kim, M. Hirsch, X. Li, J. D. Moon, S. R. Jaffrey, Nat. Chem. Biol. 2017, 13, 1187–1194.
- 35J. Wu, N. Svensen, W. Song, H. Kim, S. Zhang, X. Li, S. R. Jaffrey, J. Am. Chem. Soc. 2022, 144, 5471–5477.
- 36X. Li, J. Wu, S. R. Jaffrey, Angew. Chem. Int. Ed. 2021, 60, 24153–24161; Angew. Chem. 2021, 133, 24355–24363.
- 37X. Li, L. Mo, J. L. Litke, S. K. Dey, S. R. Suter, S. R. Jaffrey, J. Am. Chem. Soc. 2020, 142, 14117–14124.
- 38
- 38aL. Truong, H. Kooshapur, S. K. Dey, X. Li, N. Tjandra, S. R. Jaffrey, A. R. Ferré-D'Amaré, Nat. Chem. Biol. 2022, 18, 191–198;
- 38bS. K. Dey, G. S. Filonov, A. O. Olarerin-George, B. T. Jackson, L. W. S. Finley, S. R. Jaffrey, Nat. Chem. Biol. 2022, 18, 180–190.
- 39C. Steinmetzger, N. Palanisamy, K. R. Gore, C. Hobartner, Chemistry 2019, 25, 1931–1935.
- 40D. Englert, E.-M. Burger, J. Lackner, M. Lampe, B. Bühler, F. Grün, J. Schokolowski, G. U. Nienhaus, A. Jäschke, M. Sunbul, bioRxiv 2022, https://doi.org/10.1101/2022.10.24.513449.
10.1101/2022.10.24.513449 Google Scholar
- 41
- 41aH. Sato, S. Das, R. H. Singer, M. Vera, Annu. Rev. Biochem. 2020, 89, 159–187;
- 41bE. Braselmann, C. Rathbun, E. M. Richards, A. E. Palmer, Cell Chem. Biol. 2020, 27, 891–903;
- 41cA. Schmidt, G. Gao, S. R. Little, A. P. Jalihal, N. G. Walter, Wiley Interdiscip. Rev. RNA 2020, 11, e1587;
- 41dR. J. Trachman, A. R. Ferre-D′Amare, Q. Rev. Biophys. 2019, 52, e8.
- 42
- 42aJ. S. Paige, T. Nguyen-Duc, W. Song, S. R. Jaffrey, Science 2012, 335, 1194–1194;
- 42bW. Song, R. L. Strack, S. R. Jaffrey, Nat. Methods 2013, 10, 873;
- 42cJ. D. Moon, J. Wu, S. K. Dey, J. L. Litke, X. Li, H. Kim, S. R. Jaffrey, Cell Chem. Biol. 2021, 28, 1569–1580.
- 42dQ. Yu, J. Shi, A. Mudiyanselage, R. Wu, B. Zhao, M. Zhou, M. You, Chem Commun (Camb) 2019, 55, 707–710.
- 43H. Ma, L.-C. Tu, A. Naseri, Y.-C. Chung, D. Grunwald, S. Zhang, T. Pederson, Nat. Methods 2018, 15, 928–931.
- 44G. S. Filonov, W. Song, S. R. Jaffrey, Biochemistry 2019, 58, 1560–1564.
- 45K. D. Warner, M. C. Chen, W. Song, R. L. Strack, A. Thorn, S. R. Jaffrey, A. R. Ferre-D′Amare, Nat. Struct. Mol. Biol. 2014, 21, 658–663.
- 46R. J. Trachman 3rd, A. Abdolahzadeh, A. Andreoni, R. Cojocaru, J. R. Knutson, M. Ryckelynck, P. J. Unrau, A. R. Ferre-D′Amare, Biochemistry 2018, 57, 3544–3548.
- 47J. E. Johnson Jr., F. E. Reyes, J. T. Polaski, R. T. Batey, Nature 2012, 492, 133–137.
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