IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31799-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31799-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31799-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    4. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Charlotte M. François & Thomas Pihl & Marion Dunoyer de Segonzac & Chloé Hérault & Bruno Hudry, 2023. "Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Ali Vaziri-Gohar & Jonathan J. Hue & Ata Abbas & Hallie J. Graor & Omid Hajihassani & Mehrdad Zarei & George Titomihelakis & John Feczko & Moeez Rathore & Sylwia Chelstowska & Alexander W. Loftus & Ru, 2023. "Increased glucose availability sensitizes pancreatic cancer to chemotherapy," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Hayden T. Pacl & Krishna C. Chinta & Vineel P. Reddy & Sajid Nadeem & Ritesh R. Sevalkar & Kievershen Nargan & Kapongo Lumamba & Threnesan Naidoo & Joel N. Glasgow & Anupam Agarwal & Adrie J. C. Steyn, 2023. "NAD(H) homeostasis underlies host protection mediated by glycolytic myeloid cells in tuberculosis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Erika M. Palmieri & Ronald Holewinski & Christopher L. McGinity & Ciro L. Pierri & Nunziata Maio & Jonathan M. Weiss & Vincenzo Tragni & Katrina M. Miranda & Tracey A. Rouault & Thorkell Andresson & D, 2023. "Pyruvate dehydrogenase operates as an intramolecular nitroxyl generator during macrophage metabolic reprogramming," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    5. Kun-Xu Teng & Li-Ya Niu & Nan Xie & Qing-Zheng Yang, 2022. "Supramolecular photodynamic agents for simultaneous oxidation of NADH and generation of superoxide radical," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Xueman Chen & Rong Luo & Yunmei Zhang & Shuying Ye & Xin Zeng & Jiang Liu & Di Huang & Yujie Liu & Qiang Liu & Man-Li Luo & Erwei Song, 2022. "Long noncoding RNA DIO3OS induces glycolytic-dominant metabolic reprogramming to promote aromatase inhibitor resistance in breast cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Dorothy Koveal & Paul C. Rosen & Dylan J. Meyer & Carlos Manlio Díaz-García & Yongcheng Wang & Li-Heng Cai & Peter J. Chou & David A. Weitz & Gary Yellen, 2022. "A high-throughput multiparameter screen for accelerated development and optimization of soluble genetically encoded fluorescent biosensors," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Douglas Adamoski & Larissa M. dos Reis & Ana Carolina Paschoalini Mafra & Felipe Corrêa-da-Silva & Pedro Manoel Mendes de Moraes-Vieira & Ioana Berindan-Neagoe & George A. Calin & Sandra Martha Gomes , 2024. "HuR controls glutaminase RNA metabolism," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Juraj Adamik & Paul V. Munson & Deena M. Maurer & Felix J. Hartmann & Sean C. Bendall & Rafael J. Argüello & Lisa H. Butterfield, 2023. "Immuno-metabolic dendritic cell vaccine signatures associate with overall survival in vaccinated melanoma patients," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    10. Katia Monsorno & Kyllian Ginggen & Andranik Ivanov & An Buckinx & Arnaud L. Lalive & Anna Tchenio & Sam Benson & Marc Vendrell & Angelo D’Alessandro & Dieter Beule & Luc Pellerin & Manuel Mameli & Ros, 2023. "Loss of microglial MCT4 leads to defective synaptic pruning and anxiety-like behavior in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Qiang Feng & Zhida Liu & Xuexin Yu & Tongyi Huang & Jiahui Chen & Jian Wang & Jonathan Wilhelm & Suxin Li & Jiwon Song & Wei Li & Zhichen Sun & Baran D. Sumer & Bo Li & Yang-Xin Fu & Jinming Gao, 2022. "Lactate increases stemness of CD8 + T cells to augment anti-tumor immunity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    12. Yang Yang & Jinshu Huang & Wei Wei & Qin Zeng & Xipeng Li & Da Xing & Bo Zhou & Tao Zhang, 2022. "Switching the NIR upconversion of nanoparticles for the orthogonal activation of photoacoustic imaging and phototherapy," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    13. Juraj Adamik & Paul V. Munson & Felix J. Hartmann & Alexis J. Combes & Philippe Pierre & Matthew F. Krummel & Sean C. Bendall & Rafael J. Argüello & Lisa H. Butterfield, 2022. "Distinct metabolic states guide maturation of inflammatory and tolerogenic dendritic cells," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31799-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.