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Engineered biomimetic nanoparticles achieve targeted delivery and efficient metabolism-based synergistic therapy against glioblastoma

Author

Listed:
  • Guihong Lu

    (The First Affiliated Hospital of Shenzhen University, Shenzhen Second People’s Hospital
    Chinese Academy of Sciences)

  • Xiaojun Wang

    (Chinese Academy of Sciences)

  • Feng Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Shuang Wang

    (Chinese Academy of Sciences)

  • Jiawei Zhao

    (Chinese Academy of Sciences)

  • Jinyi Wang

    (The First Affiliated Hospital of Shenzhen University, Shenzhen Second People’s Hospital)

  • Jing Liu

    (The First Affiliated Hospital of Shenzhen University, Shenzhen Second People’s Hospital)

  • Chengliang Lyu

    (Chinese Academy of Sciences)

  • Peng Ye

    (Chinese Academy of Sciences)

  • Hui Tan

    (The First Affiliated Hospital of Shenzhen University, Shenzhen Second People’s Hospital
    Shenzhen Children’s Hospital)

  • Weiping Li

    (The First Affiliated Hospital of Shenzhen University, Shenzhen Second People’s Hospital)

  • Guanghui Ma

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wei Wei

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

Glioblastoma multiforme (GBM) is an aggressive brain cancer with a poor prognosis and few treatment options. Here, building on the observation of elevated lactate (LA) in resected GBM, we develop biomimetic therapeutic nanoparticles (NPs) that deliver agents for LA metabolism-based synergistic therapy. Because our self-assembling NPs are encapsulated in membranes derived from glioma cells, they readily penetrate the blood-brain barrier and target GBM through homotypic recognition. After reaching the tumors, lactate oxidase in the NPs converts LA into pyruvic acid (PA) and hydrogen peroxide (H2O2). The PA inhibits cancer cell growth by blocking histones expression and inducing cell-cycle arrest. In parallel, the H2O2 reacts with the delivered bis[2,4,5-trichloro-6-(pentyloxycarbonyl)phenyl] oxalate to release energy, which is used by the co-delivered photosensitizer chlorin e6 for the generation of cytotoxic singlet oxygen to kill glioma cells. Such a synergism ensures strong therapeutic effects against both glioma cell-line derived and patient-derived xenograft models.

Suggested Citation

  • Guihong Lu & Xiaojun Wang & Feng Li & Shuang Wang & Jiawei Zhao & Jinyi Wang & Jing Liu & Chengliang Lyu & Peng Ye & Hui Tan & Weiping Li & Guanghui Ma & Wei Wei, 2022. "Engineered biomimetic nanoparticles achieve targeted delivery and efficient metabolism-based synergistic therapy against glioblastoma," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31799-y
    DOI: 10.1038/s41467-022-31799-y
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    References listed on IDEAS

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    1. Erika M. Palmieri & Marieli Gonzalez-Cotto & Walter A. Baseler & Luke C. Davies & Bart Ghesquière & Nunziata Maio & Christopher M. Rice & Tracey A. Rouault & Teresa Cassel & Richard M. Higashi & Andre, 2020. "Nitric oxide orchestrates metabolic rewiring in M1 macrophages by targeting aconitase 2 and pyruvate dehydrogenase," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    2. Jialin Li & Bo Diao & Sheng Guo & Xiaoyong Huang & Chengying Yang & Zeqing Feng & Weiming Yan & Qin Ning & Lixin Zheng & Yongwen Chen & Yuzhang Wu, 2017. "VSIG4 inhibits proinflammatory macrophage activation by reprogramming mitochondrial pyruvate metabolism," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. Zhengze Yu & Ping Zhou & Wei Pan & Na Li & Bo Tang, 2018. "A biomimetic nanoreactor for synergistic chemiexcited photodynamic therapy and starvation therapy against tumor metastasis," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    4. Cyril Corbet & Estelle Bastien & Nihed Draoui & Bastien Doix & Lionel Mignion & Bénédicte F. Jordan & Arnaud Marchand & Jean-Christophe Vanherck & Patrick Chaltin & Olivier Schakman & Holger M. Becker, 2018. "Interruption of lactate uptake by inhibiting mitochondrial pyruvate transport unravels direct antitumor and radiosensitizing effects," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    5. Sheng Hui & Jonathan M. Ghergurovich & Raphael J. Morscher & Cholsoon Jang & Xin Teng & Wenyun Lu & Lourdes A. Esparza & Tannishtha Reya & Le Zhan & Jessie Yanxiang Guo & Eileen White & Joshua D. Rabi, 2017. "Glucose feeds the TCA cycle via circulating lactate," Nature, Nature, vol. 551(7678), pages 115-118, November.
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    Cited by:

    1. Yan Zou & Yajing Sun & Yibin Wang & Dongya Zhang & Huiqing Yang & Xin Wang & Meng Zheng & Bingyang Shi, 2023. "Cancer cell-mitochondria hybrid membrane coated Gboxin loaded nanomedicines for glioblastoma treatment," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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