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Effectual Labeling of Natural Killer Cells with Upconverting Nanoparticles by Electroporation for In Vivo Tracking and Biodistribution Assessment

  • Hye Sun Park
    Hye Sun Park
    Research Center for Bioconvergence Analysis, Korea Basic Science Institute, Cheongju 28119, Korea
    More by Hye Sun Park
  • Jongwoo Kim
    Jongwoo Kim
    Center for Convergent Research of Emerging Virus Infection, Korea Research Institute of Chemical Technology, Daejeon 34114, Korea
    Laboratory for Advanced Molecular Probing (LAMP), Korea Research Institute of Chemical Technology, Daejeon 34114, Korea
    More by Jongwoo Kim
  • Mi Young Cho
    Mi Young Cho
    Research Center for Bioconvergence Analysis, Korea Basic Science Institute, Cheongju 28119, Korea
    More by Mi Young Cho
  • Youn-Joo Cho
    Youn-Joo Cho
    Research Center for Bioconvergence Analysis, Korea Basic Science Institute, Cheongju 28119, Korea
    Graduate School of Analytical Science and Technology, Chungnam National University, Daejeon 34134, Korea
    More by Youn-Joo Cho
  • Yung Doug Suh
    Yung Doug Suh
    Laboratory for Advanced Molecular Probing (LAMP), Korea Research Institute of Chemical Technology, Daejeon 34114, Korea
    School of Chemical Engineering, Sungkyunkwan University, Suwon 16419, Korea
  • Sang Hwan Nam*
    Sang Hwan Nam
    Center for Convergent Research of Emerging Virus Infection, Korea Research Institute of Chemical Technology, Daejeon 34114, Korea
    Laboratory for Advanced Molecular Probing (LAMP), Korea Research Institute of Chemical Technology, Daejeon 34114, Korea
    *Email: [email protected]
  • , and 
  • Kwan Soo Hong*
    Kwan Soo Hong
    Research Center for Bioconvergence Analysis, Korea Basic Science Institute, Cheongju 28119, Korea
    Graduate School of Analytical Science and Technology, Chungnam National University, Daejeon 34134, Korea
    *Email: [email protected]
Cite this: ACS Appl. Mater. Interfaces 2020, 12, 44, 49362–49370
Publication Date (Web):October 13, 2020
https://doi.org/10.1021/acsami.0c12849
Copyright © 2020 American Chemical Society

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    Abstract

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    Natural killer (NK) cells, which are cytotoxic lymphocytes of the innate immune system and recognize cancer cells via various immune receptors, are promising agents in cell immunotherapy. To utilize NK cells as a therapeutic agent, their biodistribution and pharmacokinetics need to be evaluated following systemic administration. Therefore, in vivo imaging and tracking with efficient labeling and quantitative analysis of NK cells are required. However, the lack of the phagocytic capacity of NK cells makes it difficult to establish breakthroughs in cell labeling and subsequent in vivo studies. Herein, an effective labeling of upconverting nanoparticles (UCNPs) in NK cells is proposed using electroporation with high sensitivity and stability. The labeling performance of UCNPs functionalized with carboxy-polyethylene glycol (PEG) is better than with methoxy-PEG or with amine-PEG. The labeling efficiency becomes higher, but cell damage is greater as electric field increases; thus, there is an optimum electroporation condition for internalization of UCNPs into NK cells. The tracking and biodistribution imaging analyses of intravenously injected NK cells show that the labeled NK cells are initially distributed primarily in lungs and then spread to the liver and spleen. These advances will accelerate the application of NK cells as key components of immunotherapy against cancer.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.0c12849.

    • X-ray diffraction analysis of the as-synthesized UCNPs (Figure S1), FT-IR spectra of the as-synthesized UCNPs, lipid-PEG, and surface-modified UCNPs (Figure S2), cell viability of NK-92 cells after electroporation under cell culture media or electroporation buffer with or without carboxy-PEG-UCNPs (Figure S3); effect of the surface modification of UCNPs used in electroporation on labeling and viability of the NK-92 cells (Figure S4), in vitro microscope images of the NK-92 cells labeled with the carboxy-PEG-UCNPs using the electroporation condition OPT2 (Figure S5), in vitro microscope images taken at different focal distances of the NK-92 cells labeled with the carboxy-PEG-UCNPs using the electroporation condition OPT2 and OPT6 (Figures S6 and S7, respectively); comparison of secretion levels of TNF-α in the supernatants of the cultured NK-92 cells with or without electroporation and UCNPs analyzed after 24 h from the electroporation (Figure S8) (PDF)

    • Three-dimensional constructed image of the NK-92 cells labeled with the carboxy-PEG-UCNPs using electroporation condition OPT2 (Movie S1) (MP4)

    • Three-dimensional constructed image of the NK-92 cells labeled with the carboxy-PEG-UCNPs using the electroporation condition OPT6 (Movie S2) (MP4)

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    Cited By

    This article is cited by 9 publications.

    1. Saji Uthaman, Gabriel Cutshaw, Saman Ghazvini, Rizia Bardhan. Nanomaterials for Natural Killer Cell-Based Immunoimaging and Immunotherapies in Cancer. ACS Applied Materials & Interfaces 2023, 15 (44) , 50708-50720. https://doi.org/10.1021/acsami.2c08619
    2. Jongwoo Kim, Hye Sun Park, Yun Ahn, Youn-Joo Cho, Hyeon Ho Shin, Kwan Soo Hong, Sang Hwan Nam. Universal Emission Characteristics of Upconverting Nanoparticles Revealed by Single-Particle Spectroscopy. ACS Nano 2023, 17 (1) , 648-656. https://doi.org/10.1021/acsnano.2c09896
    3. Bingzhu Zheng, Jingyue Fan, Bing Chen, Xian Qin, Juan Wang, Feng Wang, Renren Deng, Xiaogang Liu. Rare-Earth Doping in Nanostructured Inorganic Materials. Chemical Reviews 2022, 122 (6) , 5519-5603. https://doi.org/10.1021/acs.chemrev.1c00644
    4. Ashok Kumar Jangid, Sungjun Kim, Kyobum Kim. Polymeric biomaterial-inspired cell surface modulation for the development of novel anticancer therapeutics. Biomaterials Research 2023, 27 (1) https://doi.org/10.1186/s40824-023-00404-8
    5. Mengsi Zhan, Yunqi Guo, Mingwu Shen, Xiangyang Shi. Nanomaterial‐Boosted Tumor Immunotherapy Through Natural Killer Cells. Advanced NanoBiomed Research 2022, 2 (12) https://doi.org/10.1002/anbr.202200096
    6. Yeongchang Goh, Jongwoo Kim, Hye Sun Park, Taeyoung Jung, Kwan Soo Hong, Sang Hwan Nam, Yung Doug Suh, Kang Taek Lee. Visualization of intercellular cargo transfer using upconverting nanoparticles. Nanoscale 2022, 14 (38) , 14008-14013. https://doi.org/10.1039/D2NR01999J
    7. Xianbin Ma, Meng‐Jie Zhang, Jingting Wang, Tian Zhang, Peng Xue, Yuejun Kang, Zhi‐Jun Sun, Zhigang Xu. Emerging Biomaterials Imaging Antitumor Immune Response. Advanced Materials 2022, 34 (42) https://doi.org/10.1002/adma.202204034
    8. Maria E. Nikolaeva, Andrey V. Nechaev, Elena V. Shmendel, Roman A. Akasov, Mikhail A. Maslov, Andrey F. Mironov. New Cysteine-Containing PEG-Glycerolipid Increases the Bloodstream Circulation Time of Upconverting Nanoparticles. Molecules 2022, 27 (9) , 2763. https://doi.org/10.3390/molecules27092763
    9. Tingrui Zhang, Zongguang Tai, Zhen Cui, Rongrong Chai, Quangang Zhu, Zhongjian Chen. Nano-engineered immune cells as “guided missiles” for cancer therapy. Journal of Controlled Release 2022, 341 , 60-79. https://doi.org/10.1016/j.jconrel.2021.11.016

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