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Photodecaging of a Mitochondria-Localized Iridium(III) Endoperoxide Complex for Two-Photon Photoactivated Therapy under Hypoxia

  • Shi Kuang
    Shi Kuang
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Shi Kuang
  • Fangmian Wei
    Fangmian Wei
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Fangmian Wei
  • Johannes Karges
    Johannes Karges
    Department of Chemistry and Biochemistry, University of California, 9500 Gilman Drive, La Jolla, San Diego, California 92093, United States
  • Libing Ke
    Libing Ke
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Libing Ke
  • Kai Xiong
    Kai Xiong
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Kai Xiong
  • Xinxing Liao
    Xinxing Liao
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Xinxing Liao
  • Gilles Gasser*
    Gilles Gasser
    Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
    *Email: [email protected]
  • Liangnian Ji
    Liangnian Ji
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    More by Liangnian Ji
  • , and 
  • Hui Chao*
    Hui Chao
    MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Guangdong Provincial Key Laboratory of Digestive Cancer Research, The Seventh Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510006, P. R. China
    MOE Key Laboratory of Theoretical Organic Chemistry and Functional Molecule, School of Chemistry and Chemical Engineering, Hunan University of Science and Technology, Xiangtan 400201, P. R. China
    *Email: [email protected]
    More by Hui Chao
Cite this: J. Am. Chem. Soc. 2022, 144, 9, 4091–4101
Publication Date (Web):February 16, 2022
https://doi.org/10.1021/jacs.1c13137
Copyright © 2022 American Chemical Society

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    Abstract

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    Despite the clinical success of photodynamic therapy (PDT), the application of this medical technique is intrinsically limited by the low oxygen concentrations found in cancer tumors, hampering the production of therapeutically necessary singlet oxygen (1O2). To overcome this limitation, we report on a novel mitochondria-localized iridium(III) endoperoxide prodrug (2-O-IrAn), which, upon two-photon irradiation in NIR, synergistically releases a highly cytotoxic iridium(III) complex (2-IrAn), singlet oxygen, and an alkoxy radical. 2-O-IrAn was found to be highly (photo-)toxic in hypoxic tumor cells and multicellular tumor spheroids (MCTS) in the nanomolar range. To provide cancer selectivity and improve the pharmacological properties of 2-O-IrAn, it was encapsulated into a biotin-functionalized polymer. The generated nanoparticles were found to nearly fully eradicate the tumor inside a mouse model within a single treatment. This study presents, to the best of our knowledge, the first example of an iridium(III)-based endoperoxide prodrug for synergistic photodynamic therapy/photoactivated chemotherapy, opening up new avenues for the treatment of hypoxic tumors.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.1c13137.

    • Details on reagents and instruments and experimental sections including the synthesis procedures of iridium(III) complexes and DSPE-PEG-Biotin@2-O-IrAn; ROS generation; cellular uptake and localization; phosphorescence lifetime imaging microscopy; and (photo-)cytotoxicity in vitro and in vivo, as well as some additional supporting data (PDF)

    • Within 10 min, the asymptotic maximum of the conversion was reached with an 84 times stronger luminescence for 2-O-IrAn and an 18 times stronger luminescence for 9-O-IrAn in comparison to their respective complexes (MP4)

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