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Photoinduced Synergism of Ferroptosis/Pyroptosis/Oncosis by an O2-Independent Photocatalyst for Enhanced Tumor Immunotherapy

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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Am. Chem. Soc. 2025, 147, 13, 11132-11144
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    Photoinduced Synergism of Ferroptosis/Pyroptosis/Oncosis by an O2-Independent Photocatalyst for Enhanced Tumor Immunotherapy
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    • Shankun Yao
      Shankun Yao
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
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    • Fengwu Xu
      Fengwu Xu
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      More by Fengwu Xu
    • Ying Wang
      Ying Wang
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      More by Ying Wang
    • Jizhen Shang
      Jizhen Shang
      Huzhou Key Laboratory of Medical and Environmental Applications Technologies, School of Life Sciences, Huzhou University, Huzhou, Zhejiang 313000 China
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    • Shumeng Li
      Shumeng Li
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      More by Shumeng Li
    • Xinyu Xu
      Xinyu Xu
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
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    • Zhipeng Liu
      Zhipeng Liu
      College of Materials Science and Engineering, Nanjing Forestry University, Nanjing 210037, China
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      Orcidhttps://orcid.org/0000-0002-5458-9362
    • Weijiang He
      Weijiang He
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      More by Weijiang He
      Orcidhttps://orcid.org/0000-0002-3157-5769
    • Zijian Guo*
      Zijian Guo
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      Nanchuang (Jiangsu) Institute of Chemistry and Health, Nanjing, Jiangsu 210000, China
      *Email: [email protected]
      More by Zijian Guo
      Orcidhttps://orcid.org/0000-0003-4986-9308
    • Yuncong Chen*
      Yuncong Chen
      State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering, Chemistry and Biomedicine Innovation Center (ChemBIC), ChemBioMed Interdisciplinary Research Center, Nanjing University, Nanjing 210023, China
      Department of Cardiothoracic Surgery, Nanjing Drum Tower Hospital, Medical School, Nanjing University, Nanjing 210008, China
      Nanchuang (Jiangsu) Institute of Chemistry and Health, Nanjing, Jiangsu 210000, China
      *Email: [email protected]
      More by Yuncong Chen
      Orcidhttps://orcid.org/0000-0002-8406-4866
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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2025, 147, 13, 11132–11144
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.4c17268
    Published March 20, 2025
    Copyright © 2025 American Chemical Society
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    Abstract

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    Due to O2 dependence, hypoxia-induced apoptosis resistance, and immunosuppressive microenvironment, the effect of traditional photodynamic therapy toward hypoxic solid tumors is severely limited. Herein, we report an O2-independent photocatalyst (EBSe) for tumor immunotherapy potentiation via synergism of near-infrared (NIR) light-induced ferroptosis/pyroptosis/oncosis. Simple Se and ethyl modifications on methylene blue (MB) endow EBSe with a remarkable phototoxicity enhancement (>2500 folds) and an excellent phototoxicity index (PI > 32,000) to 4T1 cells under hypoxia. EBSe exhibits self-adaptive photodynamic processes that generate enhanced type I/II ROS under normoxia and elevate carbon radical production under hypoxia. Interestingly, EBSe shows much higher cell uptake and undergoes photoinduced lysosomal-to-nucleus translocation, which activates ferroptosis, pyroptosis, and oncosis. The synergism of three nonapoptotic pathways potentiates antitumor immune responses in 4T1 tumor-bearing mice. This work offers a reliable strategy for developing powerful PSs to overcome the apoptosis resistance and immunosuppressive microenvironment of hypoxic tumors.

    Copyright © 2025 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.4c17268.

    • Contain synthesis procedure and characterization of key compounds and intermediate compounds, photophysical properties, details of in vivo experiments, and figures and tables (PDF)

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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2025, 147, 13, 11132–11144
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.4c17268
    Published March 20, 2025
    Copyright © 2025 American Chemical Society
    Request reuse permissions

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