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Remote Control of Neural Stem Cell Fate Using NIR-Responsive Photoswitching Upconversion Nanoparticle Constructs

  • Yixiao Zhang
    Yixiao Zhang
    Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
    More by Yixiao Zhang
  • Lisa M. Wiesholler
    Lisa M. Wiesholler
    Institute of Analytical Chemistry, Chemo- and Biosensors, University of Regensburg, 93040 Regensburg, Germany
  • Hudifah Rabie
    Hudifah Rabie
    Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
  • Pengfei Jiang
    Pengfei Jiang
    Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
  • Jinping Lai
    Jinping Lai
    Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
    More by Jinping Lai
  • Thomas Hirsch
    Thomas Hirsch
    Institute of Analytical Chemistry, Chemo- and Biosensors, University of Regensburg, 93040 Regensburg, Germany
  • , and 
  • Ki-Bum Lee*
    Ki-Bum Lee
    Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
    *Email: [email protected]. Tel: +1-732-445-2081. Fax: +1-732-445-5312.
    More by Ki-Bum Lee
Cite this: ACS Appl. Mater. Interfaces 2020, 12, 36, 40031–40041
Publication Date (Web):August 11, 2020
https://doi.org/10.1021/acsami.0c10145
Copyright © 2020 American Chemical Society

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    Abstract

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    Light-mediated remote control of stem cell fate, such as proliferation, differentiation, and migration, can bring a significant impact on stem cell biology and regenerative medicine. Current UV/vis-mediated control approaches are limited in terms of nonspecific absorption, poor tissue penetration, and phototoxicity. Upconversion nanoparticle (UCNP)-based near-infrared (NIR)-mediated control systems have gained increasing attention for vast applications with minimal nonspecific absorption, good penetration depth, and minimal phototoxicity from NIR excitations. Specifically, 808 nm NIR-responsive upconversion nanomaterials have shown clear advantages for biomedical applications owing to diminished heating effects and better tissue penetration. Herein, a novel 808 nm NIR-mediated control method for stem cell differentiation has been developed using multishell UCNPs, which are optimized for upconverting 808 nm NIR light to UV emission. The locally generated UV emissions further toggle photoswitching polymer capping ligands to achieve spatiotemporally controlled small-molecule release. More specifically, with 808 nm NIR excitation, stem cell differentiation factors can be released to guide neural stem cell (NSC) differentiation in a highly controlled manner. Given the challenges in stem cell behavior control, the developed 808 nm NIR-responsive UCNP-based approach to control stem cell differentiation can represent a new tool for studying single-molecule roles in stem cell and developmental biology.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.0c10145.

    • NIR penetration depth and heating effect, TEM characterization of core–shell UCNPs, luminescence decay of synthesized core–shell UCNPs, TEM characterizations of core–shell UCNP with varied Nd3+ and Yb3+ concentrations, luminescent spectra of synthesized UCNPs, lattice characterizations and particle distribution analysis of the core–shell structures, composition analysis of the UCNPs synthesized through ICP-OES, photoswitching monomer characterization, FTIR characterization of polymer-functionalized UCNPs, hiPSC-NSCs cellular uptake, cytotoxicity characterizations, proliferation characterizations through microscopy and immunofluorescence staining, hiPSC-NSCs stemness characterizations through immunofluorescence staining, releasing profile under dark conditions, spatial small-molecule release analysis, NIR-based tissue phantom penetration characterization, heating effect comparison, and primer sequences for quantitative PCR (PDF)

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    Cited By

    This article is cited by 13 publications.

    1. Zakaria Ziani, Saioa Cobo, Frédérique Loiseau, Damien Jouvenot, Elise Lognon, Martial Boggio-Pasqua, Guy Royal. All Visible Light Photoswitch Based on the Dimethyldihydropyrene Unit Operating in Aqueous Solutions with High Quantum Yields. JACS Au 2023, 3 (1) , 131-142. https://doi.org/10.1021/jacsau.2c00552
    2. Karan Malhotra, David Hrovat, Balmiki Kumar, Grace Qu, Justin Van Houten, Reda Ahmed, Paul A. E. Piunno, Patrick T. Gunning, Ulrich J. Krull. Lanthanide-Doped Upconversion Nanoparticles: Exploring A Treasure Trove of NIR-Mediated Emerging Applications. ACS Applied Materials & Interfaces 2023, 15 (2) , 2499-2528. https://doi.org/10.1021/acsami.2c12370
    3. Marija Matulionyte, Artiom Skripka, Alma Ramos-Guerra, Antonio Benayas, Fiorenzo Vetrone. The Coming of Age of Neodymium: Redefining Its Role in Rare Earth Doped Nanoparticles. Chemical Reviews 2023, 123 (1) , 515-554. https://doi.org/10.1021/acs.chemrev.2c00419
    4. Brandon Conklin, Brian M. Conley, Yannan Hou, Meizi Chen, Ki-Bum Lee. Advanced theragnostics for the central nervous system (CNS) and neurological disorders using functional inorganic nanomaterials. Advanced Drug Delivery Reviews 2023, 192 , 114636. https://doi.org/10.1016/j.addr.2022.114636
    5. Yongxin Zhan, Zekun Zhou, Miao Chen, Xu Gong. Photothermal Treatment of Polydopamine Nanoparticles@Hyaluronic Acid Methacryloyl Hydrogel Against Peripheral Nerve Adhesion in a Rat Model of Sciatic Nerve. International Journal of Nanomedicine 2023, Volume 18 , 2777-2793. https://doi.org/10.2147/IJN.S410092
    6. Evan M. Mettenbrink, Wen Yang, Stefan Wilhelm. Bioimaging with Upconversion Nanoparticles. Advanced Photonics Research 2022, 3 (12) https://doi.org/10.1002/adpr.202200098
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    8. G. Lesly Jimenez, Binita Shrestha, Tyron Porter, Bartlomiej Starzyk, Magdalena Lesniak, Marta Kuwik, Marcin Kochanowicz, Magdalena Szumera, R. Lisiecki, D. Dorosz. Highly efficient green up-conversion emission from fluoroindate glass nanoparticles functionalized with a biocompatible polymer. RSC Advances 2022, 12 (31) , 20074-20079. https://doi.org/10.1039/D2RA03171J
    9. Jaber Keyvan Rad, Zahra Balzade, Ali Reza Mahdavian. Spiropyran-based advanced photoswitchable materials: A fascinating pathway to the future stimuli-responsive devices. Journal of Photochemistry and Photobiology C: Photochemistry Reviews 2022, 51 , 100487. https://doi.org/10.1016/j.jphotochemrev.2022.100487
    10. Jinzhu Huang, Xiaoyuan Zhang, Kun Fu, Gang Wei, Zhiqiang Su. Stimulus-responsive nanomaterials under physical regulation for biomedical applications. Journal of Materials Chemistry B 2021, 9 (47) , 9642-9657. https://doi.org/10.1039/D1TB02130C
    11. Sang Ah Yi, Yixiao Zhang, Christopher Rathnam, Thanapat Pongkulapa, Ki‐Bum Lee. Bioengineering Approaches for the Advanced Organoid Research. Advanced Materials 2021, 33 (45) https://doi.org/10.1002/adma.202007949
    12. Xiaoling Qi, Yingdong Han, Shujing Liu, Haofeng Hu, Zhenzhou Cheng, Tiegen Liu. NaYF 4 :Yb/Tm@SiO 2 -Dox/Cur-CS/OSA nanoparticles with pH and photon responses. Nanotechnology 2021, 32 (25) , 255703. https://doi.org/10.1088/1361-6528/abecba
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