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Near-infrared light-activatable upconversion nanoparticle/curcumin hybrid nanodrug: a potent strategy to induce the differentiation and elimination of glioma stem cells

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Abstract

Glioma stem cells (GSCs) are major contributors to the recurrence and drug resistance of glioblastoma (GBM) and are therefore a key target for GBM treatment. However, due to the therapeutic resistance of GSCs, innovative and efficient clinical treatment tools to eliminate GSCs are urgently needed. Photodynamic therapy (PDT) is a new strategy for killing GSCs because of its high safety and sensitive targeting ability. However, the existing photosensitizers applied to kill GSCs generally lack long-wavelength excitation light with effective tissue penetration, which prevents their effective application in vivo. Hence, a novel near-infrared light (NIR)-activated photosensitive drug was developed from upconversion nanoparticles (UCNPs), Pluronic F127 (F127) and curcumin (Cur) to form UCNPs-F127@Cur. This hybrid nanodrug significantly promoted the apoptosis of GSCs, increased the production of intracellular reactive oxygen species, inhibited the expression of pluripotency-related genes in GSCs, and inhibited the growth of transplanted GSCs into tumors in vivo under 980 nm excitation light. However, UCNPs-F127@Cur did not exert the above anti-GSC effects without excitation by 980 nm light. Transcriptome sequencing analysis revealed that PDT with UCNPs-F127@Cur could cause cell cycle arrest and induce the differentiation of GSCs by suppressing the Wnt-β-catenin and Jak-Stat signaling pathways. In conclusion, we constructed a novel NIR-activated, targeted GSC-killing hybrid nanodrug and elucidated its molecular mechanism, thereby providing a new strategy for the treatment of GBM.

Graphical abstract

UCNPs-F127@Cur activated by NIR light with good tissue penetration were constructed and shown to effectively eliminate GSCs by inducing cell apoptosis, arresting cell cycle progression and the self-renewal of GSCs both in vivo and in vitro.

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Data availability

The data that support the findings of this study are available upon request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

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Funding

This work was financially supported by the National Natural Science Foundation of China (Grant No. 32071401), the Shanghai Natural Science Foundation (Grant No. 20ZR1461600) and the China Postdoctoral Science Foundation (2021M692442).

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  1. Guoxin Jing and Youyuan Li contributed equally to this work.

Authors and Affiliations

  1. Research Center for Translational Medicine at East Hospital, School of Life Science and Technology, Tongji University, Shanghai, 200092, People’s Republic of China

    Guoxin Jing, Youyuan Li, Feiyue Sun, Qiang Liu, Hong Wang, Jintong Niu & Shilong Wang

  2. School of Physics Science and Engineering, Tongji University, Shanghai, 200092, People’s Republic of China

    Ai Du & Jialu Lu

  3. Department of Respiratory Disease, Baoshan District Hospital of Integrated Traditional Chinese and Western Medicine, Shanghai, 201900, PR China

    Yechang Qian

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  1. Guoxin Jing
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Contributions

Guoxin Jing was responsible for the investigation, methodology, data curation, and writing of the original draft. Youyuan Li, Feiyue Sun and Qiang Liu were responsible for nanoparticle synthesis, characterization, cell culture and animal model construction. Hong Wang, Jintong Niu and Jialu Lu performed the characterization and the image and data analyses. Ai Du provided methodology and project administration. Shilong Wang and Yechang Qian performed the conceptualization, supervision, and project administration of this work. All the authors reviewed the manuscript.

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Jing, G., Li, Y., Sun, F. et al. Near-infrared light-activatable upconversion nanoparticle/curcumin hybrid nanodrug: a potent strategy to induce the differentiation and elimination of glioma stem cells. Adv Compos Hybrid Mater 7, 82 (2024). https://doi.org/10.1007/s42114-024-00886-7

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