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Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation

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  • Wanzun Lin

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Li Chen

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Haojiong Zhang

    (Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy
    Shanghai Proton and Heavy Ion Center)

  • Xianxin Qiu

    (Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy
    Shanghai Proton and Heavy Ion Center)

  • Qingting Huang

    (Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy
    Shanghai Proton and Heavy Ion Center)

  • Fangzhu Wan

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Ziyu Le

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Shikai Geng

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Anlan Zhang

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Sufang Qiu

    (Fujian Cancer Hospital & Fujian Medical University Cancer Hospital)

  • Long Chen

    (Huashan Hospital, Fudan University)

  • Lin Kong

    (Fudan University Cancer Hospital
    Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy)

  • Jiade J. Lu

    (Shanghai Key Laboratory of Radiation Oncology (20dz2261000)
    Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy
    Shanghai Proton and Heavy Ion Center)

Abstract

The recently described role of RNA methylation in regulating immune cell infiltration into tumors has attracted interest, given its potential impact on immunotherapy response. YTHDF1 is a versatile and powerful m6A reader, but the understanding of its impact on immune evasion is limited. Here, we reveal that tumor-intrinsic YTHDF1 drives immune evasion and immune checkpoint inhibitor (ICI) resistance. Additionally, YTHDF1 deficiency converts cold tumors into responsive hot tumors, which improves ICI efficacy. Mechanistically, YTHDF1 deficiency inhibits the translation of lysosomal genes and limits lysosomal proteolysis of the major histocompatibility complex class I (MHC-I) and antigens, ultimately restoring tumor immune surveillance. In addition, we design a system for exosome-mediated CRISPR/Cas9 delivery to target YTHDF1 in vivo, resulting in YTHDF1 depletion and antitumor activity. Our findings elucidate the role of tumor-intrinsic YTHDF1 in driving immune evasion and its underlying mechanism.

Suggested Citation

  • Wanzun Lin & Li Chen & Haojiong Zhang & Xianxin Qiu & Qingting Huang & Fangzhu Wan & Ziyu Le & Shikai Geng & Anlan Zhang & Sufang Qiu & Long Chen & Lin Kong & Jiade J. Lu, 2023. "Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35710-7
    DOI: 10.1038/s41467-022-35710-7
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