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Near-Infrared Light-Activated DNA-Agonist Nanodevice for Nongenetically and Remotely Controlled Cellular Signaling and Behaviors in Live Animals

  • Miao Wang
    Miao Wang
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    More by Miao Wang
  • Fang He
    Fang He
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    More by Fang He
  • Hao Li
    Hao Li
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    More by Hao Li
  • Sihui Yang
    Sihui Yang
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    More by Sihui Yang
  • Jinghui Zhang
    Jinghui Zhang
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
  • Pradipta Ghosh
    Pradipta Ghosh
    Department of Medicine, Department of Cellular and Molecular Medicine, University of California at San Diego, La Jolla, California 92093-0651, United States
  • Hong-Hui Wang*
    Hong-Hui Wang
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    *(H.H.W.) E-mail: [email protected]. Tel: +86-731-88823821. Fax: +86-731-88821848.
  • , and 
  • Zhou Nie*
    Zhou Nie
    State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, College of Biology, Hunan Provincial Key Laboratory of Biomacromolecular Chemical Biology, Hunan University, Changsha, 410082, P.R. China
    *(Z.N.) E-mail: [email protected]. Tel.: +86-731-88821626. Fax: +86-731-88821848.
    More by Zhou Nie
Cite this: Nano Lett. 2019, 19, 4, 2603–2613
Publication Date (Web):March 25, 2019
https://doi.org/10.1021/acs.nanolett.9b00421
Copyright © 2019 American Chemical Society
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Abstract

Abstract Image

Optogenetics provides promising tools for the precise control of receptor-mediated cell behaviors in a spatiotemporal manner. Yet, most photoreceptors require extensive genetic manipulation and respond only to ultraviolet or visible light, which are suboptimal for in vivo applications because they do not penetrate thick tissues. Here we report a novel near-infrared light-activated DNA agonist (NIR-DA) nanodevice for nongenetic manipulation of cell signaling and phenotype in deep tissues. This nanodevice is prepared by conjugating a preinactivated DNA agonist onto the gold nanorods (AuNRs). Upon NIR light treatment, the DNA agonist is released through the localized surface plasmon resonance (LSPR)-based photothermal effect of AuNRs and becomes active. The active DNA agonist dimerizes the DNA-modified chimeric or native receptor tyrosine kinase (RTK) on cell surfaces and activates downstream signal transduction in live cells. Such NIR-DA activation of RTK signaling enables the control of cytoskeletal remodeling, cell polarization, and directional migration. Furthermore, we demonstrate that the NIR-DA system can be used in vivo to mediate RTK signaling and skeletal muscle satellite cell migration and myogenesis, which are critical cellular behaviors in the process of skeletal muscle regeneration. Thus, the NIR-DA system offers a powerful and versatile platform for exogenous modulation of deep tissues for purposes such as regenerative medicine.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nanolett.9b00421.

  • Experimental details and supplemental tables (Tables S1–S3) and figures (Figures S1–S36) (PDF)

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Cited By


This article is cited by 15 publications.

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  2. Huilin Dong, Lin Liu, Jieyu Wang, Jiahui Fan, Hong-Hui Wang, Zhou Nie. DNA-Based Reprogramming Strategy of Receptor-Mediated Cellular Behaviors: From Genetic Encoding to Nongenetic Engineering. ACS Applied Bio Materials 2020, 3 (5) , 2796-2804. https://doi.org/10.1021/acsabm.9b01223
  3. Tianhuan Peng, Xu Li, Kun Li, Zhou Nie, Weihong Tan. DNA-Modulated Plasmon Resonance: Methods and Optical Applications. ACS Applied Materials & Interfaces 2020, 12 (13) , 14741-14760. https://doi.org/10.1021/acsami.9b23608
  4. Jian Zhao, Yinghao Li, Mingming Yu, Zhanjun Gu, Lele Li, Yuliang Zhao. Time-Resolved Activation of pH Sensing and Imaging in Vivo by a Remotely Controllable DNA Nanomachine. Nano Letters 2020, 20 (2) , 874-880. https://doi.org/10.1021/acs.nanolett.9b03471
  5. Mirza Muhammad Faran Ashraf Baig, Qian-Wen Zhang, Muhammad Rizwan Younis, Xing-Hua Xia. A DNA Nanodevice Simultaneously Activating the EGFR and Integrin for Enhancing Cytoskeletal Activity and Cancer Cell Treatment. Nano Letters 2019, 19 (10) , 7503-7513. https://doi.org/10.1021/acs.nanolett.9b03325
  6. Fengrong Zhang, Qingyuan Wu, Huiyu Liu. NIR light‐triggered nanomaterials‐based prodrug activation towards cancer therapy. WIREs Nanomedicine and Nanobiotechnology 2020, 10 https://doi.org/10.1002/wnan.1643
  7. Ryosuke Ueki, Satoshi Uchida, Naoto Kanda, Naoki Yamada, Ayaka Ueki, Momoko Akiyama, Kazuko Toh, Horacio Cabral, Shinsuke Sando. A chemically unmodified agonistic DNA with growth factor functionality for in vivo therapeutic application. Science Advances 2020, 6 (14) , eaay2801. https://doi.org/10.1126/sciadv.aay2801
  8. Guangcun Chen, Yuheng Cao, Yanxing Tang, Xue Yang, Yongyang Liu, Dehua Huang, Yejun Zhang, Chunyan Li, Qiangbin Wang. Advanced Near‐Infrared Light for Monitoring and Modulating the Spatiotemporal Dynamics of Cell Functions in Living Systems. Advanced Science 2020, 7 (8) , 1903783. https://doi.org/10.1002/advs.201903783
  9. Jingying Li, Liping Wang, Jinmiao Tian, Zhilan Zhou, Juan Li, Huanghao Yang. Nongenetic engineering strategies for regulating receptor oligomerization in living cells. Chemical Society Reviews 2020, 49 (5) , 1545-1568. https://doi.org/10.1039/C9CS00473D
  10. Jiahui Fan, Hong‐Hui Wang, Shiyi Xie, Miao Wang, Zhou Nie. Engineering Cell‐Surface Receptors with DNA Nanotechnology for Cell Manipulation. ChemBioChem 2020, 21 (3) , 282-293. https://doi.org/10.1002/cbic.201900315
  11. Hao Ding, Weiliang Guo, Bin Su. Imaging Cell‐Matrix Adhesions and Collective Migration of Living Cells by Electrochemiluminescence Microscopy. Angewandte Chemie 2020, 132 (1) , 457-464. https://doi.org/10.1002/ange.201911190
  12. Hao Ding, Weiliang Guo, Bin Su. Imaging Cell-Matrix Adhesions and Collective Migration of Living Cells by Electrochemiluminescence Microscopy. Angewandte Chemie International Edition 2020, 59 (1) , 449-456. https://doi.org/10.1002/anie.201911190
  13. Qirong Xiong, Yun Lim, Di Li, Kanyi Pu, Li Liang, Hongwei Duan. Photoactive Nanocarriers for Controlled Delivery. Advanced Functional Materials 2020, 30 (2) , 1903896. https://doi.org/10.1002/adfm.201903896
  14. Meiran Zhang, Wei Zheng, Yan Liu, Ping Huang, Zhongliang Gong, Jiaojiao Wei, Yu Gao, Shanyong Zhou, Xingjun Li, Xueyuan Chen. A New Class of Blue‐LED‐Excitable NIR‐II Luminescent Nanoprobes Based on Lanthanide‐Doped CaS Nanoparticles. Angewandte Chemie 2019, 131 (28) , 9656-9660. https://doi.org/10.1002/ange.201905040
  15. Meiran Zhang, Wei Zheng, Yan Liu, Ping Huang, Zhongliang Gong, Jiaojiao Wei, Yu Gao, Shanyong Zhou, Xingjun Li, Xueyuan Chen. A New Class of Blue‐LED‐Excitable NIR‐II Luminescent Nanoprobes Based on Lanthanide‐Doped CaS Nanoparticles. Angewandte Chemie International Edition 2019, 58 (28) , 9556-9560. https://doi.org/10.1002/anie.201905040

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