IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49156-6.html
   My bibliography  Save this article

Hyperbaric oxygen enhances tumor penetration and accumulation of engineered bacteria for synergistic photothermal immunotherapy

Author

Listed:
  • Ke-Fei Xu

    (Southeast University)

  • Shun-Yu Wu

    (Southeast University)

  • Zihao Wang

    (Southeast University)

  • Yuxin Guo

    (Southeast University)

  • Ya-Xuan Zhu

    (Tongji University School of Medicine)

  • Chengcheng Li

    (Nanjing Forestry University)

  • Bai-Hui Shan

    (Southeast University)

  • Xinping Zhang

    (Southeast University)

  • Xiaoyang Liu

    (Southeast University)

  • Fu-Gen Wu

    (Southeast University)

Abstract

Bacteria-mediated cancer therapeutic strategies have attracted increasing interest due to their intrinsic tumor tropism. However, bacteria-based drugs face several challenges including the large size of bacteria and dense extracellular matrix, limiting their intratumoral delivery efficiency. In this study, we find that hyperbaric oxygen (HBO), a noninvasive therapeutic method, can effectively deplete the dense extracellular matrix and thus enhance the bacterial accumulation within tumors. Inspired by this finding, we modify Escherichia coli Nissle 1917 (EcN) with cypate molecules to yield EcN-cypate for photothermal therapy, which can subsequently induce immunogenic cell death (ICD). Importantly, HBO treatment significantly increases the intratumoral accumulation of EcN-cypate and facilitates the intratumoral infiltration of immune cells to realize desirable tumor eradication through photothermal therapy and ICD-induced immunotherapy. Our work provides a facile and noninvasive strategy to enhance the intratumoral delivery efficiency of natural/engineered bacteria, and may promote the clinical translation of bacteria-mediated synergistic cancer therapy.

Suggested Citation

  • Ke-Fei Xu & Shun-Yu Wu & Zihao Wang & Yuxin Guo & Ya-Xuan Zhu & Chengcheng Li & Bai-Hui Shan & Xinping Zhang & Xiaoyang Liu & Fu-Gen Wu, 2024. "Hyperbaric oxygen enhances tumor penetration and accumulation of engineered bacteria for synergistic photothermal immunotherapy," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49156-6
    DOI: 10.1038/s41467-024-49156-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49156-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49156-6?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. 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. Shibin Zhou, 2016. "Bacteria synchronized for drug delivery," Nature, Nature, vol. 536(7614), pages 33-34, August.
    3. Yuxin Guo & Shao-Zhe Wang & Xinping Zhang & Hao-Ran Jia & Ya-Xuan Zhu & Xiaodong Zhang & Ge Gao & Yao-Wen Jiang & Chengcheng Li & Xiaokai Chen & Shun-Yu Wu & Yi Liu & Fu-Gen Wu, 2022. "In situ generation of micrometer-sized tumor cell-derived vesicles as autologous cancer vaccines for boosting systemic immune responses," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    4. Rong Sun & Mingzhu Liu & Jianping Lu & Binbin Chu & Yunmin Yang & Bin Song & Houyu Wang & Yao He, 2022. "Bacteria loaded with glucose polymer and photosensitive ICG silicon-nanoparticles for glioblastoma photothermal immunotherapy," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Liping Huang & Yanan Li & Yunai Du & Yiyi Zhang & Xiuxia Wang & Yuan Ding & Xiangliang Yang & Fanling Meng & Jiasheng Tu & Liang Luo & Chunmeng Sun, 2019. "Mild photothermal therapy potentiates anti-PD-L1 treatment for immunologically cold tumors via an all-in-one and all-in-control strategy," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    6. Yuyan Jiang & Jiaguo Huang & Cheng Xu & Kanyi Pu, 2021. "Activatable polymer nanoagonist for second near-infrared photothermal immunotherapy of cancer," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    7. Huilong Luo & Yanmei Chen & Xiao Kuang & Xinyue Wang & Fengmin Yang & Zhenping Cao & Lu Wang & Sisi Lin & Feng Wu & Jinyao Liu, 2022. "Chemical reaction-mediated covalent localization of bacteria," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. 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.
    9. Wei Li & Jie Yang & Lihua Luo & Mengshi Jiang & Bing Qin & Hang Yin & Chunqi Zhu & Xiaoling Yuan & Junlei Zhang & Zhenyu Luo & Yongzhong Du & Qingpo Li & Yan Lou & Yunqing Qiu & Jian You, 2019. "Targeting photodynamic and photothermal therapy to the endoplasmic reticulum enhances immunogenic cancer cell death," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    Full references (including those not matched with items on IDEAS)

    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. Jingchao Li & Yu Luo & Ziling Zeng & Dong Cui & Jiaguo Huang & Chenjie Xu & Liping Li & Kanyi Pu & Ruiping Zhang, 2022. "Precision cancer sono-immunotherapy using deep-tissue activatable semiconducting polymer immunomodulatory nanoparticles," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Xin Li & Tuying Yong & Zhaohan Wei & Nana Bie & Xiaoqiong Zhang & Guiting Zhan & Jianye Li & Jiaqi Qin & Jingjing Yu & Bixiang Zhang & Lu Gan & Xiangliang Yang, 2022. "Reversing insufficient photothermal therapy-induced tumor relapse and metastasis by regulating cancer-associated fibroblasts," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Yiyi Zhang & Sidan Tian & Liping Huang & Yanan Li & Yuan Lu & Hongyu Li & Guiping Chen & Fanling Meng & Gang L. Liu & Xiangliang Yang & Jiasheng Tu & Chunmeng Sun & Liang Luo, 2022. "Reactive oxygen species-responsive and Raman-traceable hydrogel combining photodynamic and immune therapy for postsurgical cancer treatment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Chi Zhang & Jingsheng Huang & Ziling Zeng & Shasha He & Penghui Cheng & Jingchao Li & Kanyi Pu, 2022. "Catalytical nano-immunocomplexes for remote-controlled sono-metabolic checkpoint trimodal cancer therapy," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Xuan Wang & Yingqi Liu & Chencheng Xue & Yan Hu & Yuanyuan Zhao & Kaiyong Cai & Menghuan Li & Zhong Luo, 2022. "A protein-based cGAS-STING nanoagonist enhances T cell-mediated anti-tumor immune responses," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    6. Qian Zhang & Bin Song & Yanan Xu & Yunmin Yang & Jian Ji & Wenjun Cao & Jianping Lu & Jiali Ding & Haiting Cao & Binbin Chu & Jiaxu Hong & Houyu Wang & Yao He, 2023. "In vivo bioluminescence imaging of natural bacteria within deep tissues via ATP-binding cassette sugar transporter," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Minglun Liu & Yuncong Chen & Yan Guo & Hao Yuan & Tongxiao Cui & Shankun Yao & Suxing Jin & Huanhuan Fan & Chengjun Wang & Ran Xie & Weijiang He & Zijian Guo, 2022. "Golgi apparatus-targeted aggregation-induced emission luminogens for effective cancer photodynamic therapy," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Shanzhi Lyu & Yonglin He & Xinglei Tao & Yuge Yao & Xiangyi Huang & Yingchao Ma & Zhimin Peng & Yanjun Ding & Yapei Wang, 2022. "Subcutaneous power supply by NIR-II light," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Songlei Zhou & Yukun Huang & Yu Chen & Yipu Liu & Laozhi Xie & Yang You & Shiqiang Tong & Jianpei Xu & Gan Jiang & Qingxiang Song & Ni Mei & Fenfen Ma & Xiaoling Gao & Hongzhuan Chen & Jun Chen, 2023. "Reprogramming systemic and local immune function to empower immunotherapy against glioblastoma," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Imran Noorani & Jorge Rosa, 2023. "Breaking barriers for glioblastoma with a path to enhanced drug delivery," Nature Communications, Nature, vol. 14(1), pages 1-4, December.
    11. Jing Lin & Shihui Sun & Kui Zhao & Fei Gao & Renling Wang & Qi Li & Yanlong Zhou & Jing Zhang & Yue Li & Xinyue Wang & Le Du & Shuai Wang & Zi Li & Huijun Lu & Yungang Lan & Deguang Song & Wei Guo & Y, 2023. "Oncolytic Parapoxvirus induces Gasdermin E-mediated pyroptosis and activates antitumor immunity," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:15:y:2024:i:1:d:10.1038_s41467-024-49156-6. 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.