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A hypoxia-activated and microenvironment-remodeling nanoplatform for multifunctional imaging and potentiated immunotherapy of cancer

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  • Jianwen Song

    (Nankai University)

  • He Wang

    (The First Affiliated Hospital of Soochow University)

  • Xue Meng

    (Nankai University)

  • Wen Li

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Ji Qi

    (Nankai University)

Abstract

Activatable theranostic systems combining precise diagnosis and robust immune activation have significant potential in cancer treatment. Herein, we develop a versatile nanoplatform integrating hypoxia-activatable molecular imaging with effective photoimmunotherapy for cancer treatment. Our molecular probe features turn-on near-infrared-II (NIR-II) fluorescence and photoacoustic signals in hypoxic tumor environments. It also induces hypoxia-triggered photodynamic and photothermal effects, promoting immunogenic cell death and activating the STING pathway, engaging both innate and adaptive immunity. The molecular probe is formulated with a vascular disrupting agent to amplify the hypoxia-responsive phototheranostic properties, on which M1-like macrophage membrane is camouflaged to shield against premature release while conferring cancer-targeting affinity. The activatable NIR-II fluorescence and photoacoustic imaging enable precise tumor delineation, while the enhanced phototherapy activates tumor-specific cytotoxic T cells, impeding both primary and distant tumor progression and providing protective immunity against rechallenge in 4T1 tumor-bearing female mice. This work advances activatable theranostic protocols for image-guided immunotherapy.

Suggested Citation

  • Jianwen Song & He Wang & Xue Meng & Wen Li & Ji Qi, 2024. "A hypoxia-activated and microenvironment-remodeling nanoplatform for multifunctional imaging and potentiated immunotherapy of cancer," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53906-x
    DOI: 10.1038/s41467-024-53906-x
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    1. Xiaotu Ma & Xiaolong Liang & Yao Li & Qingqing Feng & Keman Cheng & Nana Ma & Fei Zhu & Xinjing Guo & Yale Yue & Guangna Liu & Tianjiao Zhang & Jie Liang & Lei Ren & Xiao Zhao & Guangjun Nie, 2023. "Modular-designed engineered bacteria for precision tumor immunotherapy via spatiotemporal manipulation by magnetic field," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Yu-Chen Wang & Xi Wang & Jiaji Yu & Feiyang Ma & Zhe Li & Yang Zhou & Samuel Zeng & Xiaoya Ma & Yan-Ruide Li & Adam Neal & Jie Huang & Angela To & Nicole Clarke & Sanaz Memarzadeh & Matteo Pellegrini , 2021. "Targeting monoamine oxidase A-regulated tumor-associated macrophage polarization for cancer immunotherapy," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Xiaoying Kang & Yuan Zhang & Jianwen Song & Lu Wang & Wen Li & Ji Qi & Ben Zhong Tang, 2023. "A photo-triggered self-accelerated nanoplatform for multifunctional image-guided combination cancer immunotherapy," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Kaiyuan Wang & Yang Li & Xia Wang & Zhijun Zhang & Liping Cao & Xiaoyuan Fan & Bin Wan & Fengxiang Liu & Xuanbo Zhang & Zhonggui He & Yingtang Zhou & Dong Wang & Jin Sun & Xiaoyuan Chen, 2023. "Gas therapy potentiates aggregation-induced emission luminogen-based photoimmunotherapy of poorly immunogenic tumors through cGAS-STING pathway activation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Ying Huang & Geng Qin & TingTing Cui & Chuanqi Zhao & Jinsong Ren & Xiaogang Qu, 2023. "A bimetallic nanoplatform for STING activation and CRISPR/Cas mediated depletion of the methionine transporter in cancer cells restores anti-tumor immune responses," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Ji Qi & Chao Chen & Xiaoyan Zhang & Xianglong Hu & Shenglu Ji & Ryan T. K. Kwok & Jacky W. Y. Lam & Dan Ding & Ben Zhong Tang, 2018. "Light-driven transformable optical agent with adaptive functions for boosting cancer surgery outcomes," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    7. Yuming Zhang & Wenxuan Zhao & Yuncong Chen & Hao Yuan & Hongbao Fang & Shankun Yao & Changli Zhang & Hongxia Xu & Nan Li & Zhipeng Liu & Zijian Guo & Qingshun Zhao & Yong Liang & Weijiang He, 2021. "Rational construction of a reversible arylazo-based NIR probe for cycling hypoxia imaging in vivo," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    8. Luyan Wu & Yusuke Ishigaki & Wenhui Zeng & Takashi Harimoto & Baoli Yin & Yinghan Chen & Shiyi Liao & Yongchun Liu & Yidan Sun & Xiaobo Zhang & Ying Liu & Yong Liang & Pengfei Sun & Takanori Suzuki & , 2021. "Generation of hydroxyl radical-activatable ratiometric near-infrared bimodal probes for early monitoring of tumor response to therapy," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    9. Xiaotu Ma & Xiaolong Liang & Yao Li & Qingqing Feng & Keman Cheng & Nana Ma & Fei Zhu & Xinjing Guo & Yale Yue & Guangna Liu & Tianjiao Zhang & Jie Liang & Lei Ren & Xiao Zhao & Guangjun Nie, 2023. "Author Correction: Modular-designed engineered bacteria for precision tumor immunotherapy via spatiotemporal manipulation by magnetic field," Nature Communications, Nature, vol. 14(1), pages 1-1, December.
    10. Ning Wang & Chao Liu & Yingjie Li & Dongxue Huang & Xinyue Wu & Xiaorong Kou & Xiye Wang & Qinjie Wu & Changyang Gong, 2023. "A cooperative nano-CRISPR scaffold potentiates immunotherapy via activation of tumour-intrinsic pyroptosis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Lei Ge & Yikai Tang & Chongzhi Wang & Jian Chen & Hui Mao & Xiqun Jiang, 2024. "A light-activatable theranostic combination for ratiometric hypoxia imaging and oxygen-deprived drug activity enhancement," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Danyu Wang & Jingwen Liu & Jie Duan & Hua Yi & Junjie Liu & Haiwei Song & Zhenzhong Zhang & Jinjin Shi & Kaixiang Zhang, 2023. "Enrichment and sensing tumor cells by embedded immunomodulatory DNA hydrogel to inhibit postoperative tumor recurrence," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Chaoyu Wang & Ruoshi Zhang & Jia He & Lvshan Yu & Xinyan Li & Junxia Zhang & Sai Li & Conggang Zhang & Jonathan C. Kagan & Jeffrey M. Karp & Rui Kuai, 2023. "Ultrasound-responsive low-dose doxorubicin liposomes trigger mitochondrial DNA release and activate cGAS-STING-mediated antitumour immunity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Marta Łuksza & Nadeem Riaz & Vladimir Makarov & Vinod P. Balachandran & Matthew D. Hellmann & Alexander Solovyov & Naiyer A. Rizvi & Taha Merghoub & Arnold J. Levine & Timothy A. Chan & Jedd D. Wolcho, 2017. "A neoantigen fitness model predicts tumour response to checkpoint blockade immunotherapy," Nature, Nature, vol. 551(7681), pages 517-520, November.
    15. Hailey J. Knox & Jamila Hedhli & Tae Wook Kim & Kian Khalili & Lawrence W. Dobrucki & Jefferson Chan, 2017. "A bioreducible N-oxide-based probe for photoacoustic imaging of hypoxia," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    16. Yuling Xiao & Jiang Chen & Hui Zhou & Xiaodong Zeng & Zhiping Ruan & Zhangya Pu & Xingya Jiang & Aya Matsui & Lingling Zhu & Zohreh Amoozgar & Dean Shuailin Chen & Xiangfei Han & Dan G. Duda & Jinjun , 2022. "Combining p53 mRNA nanotherapy with immune checkpoint blockade reprograms the immune microenvironment for effective cancer therapy," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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