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Cell softness renders cytotoxic T lymphocytes and T leukemic cells resistant to perforin-mediated killing

Author

Listed:
  • Yabo Zhou

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Dianheng Wang

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Li Zhou

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Nannan Zhou

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Zhenfeng Wang

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Jie Chen

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Ruiyang Pang

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Haixia Fu

    (Peking University Institute of Hematology)

  • Qiusha Huang

    (Peking University Institute of Hematology)

  • Fang Dong

    (Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Hui Cheng

    (Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Huafeng Zhang

    (School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology)

  • Ke Tang

    (Tongji Medical College, Huazhong University of Science and Technology)

  • Jingwei Ma

    (School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology)

  • Jiadi Lv

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College)

  • Tao Cheng

    (Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Roland Fiskesund

    (Karolinska University Hospital
    Karolinska Institutet)

  • Xiaohui Zhang

    (Peking University Institute of Hematology)

  • Bo Huang

    (Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College
    Tongji Medical College, Huazhong University of Science and Technology)

Abstract

Mechanical force contributes to perforin pore formation at immune synapses, thus facilitating the cytotoxic T lymphocytes (CTL)-mediated killing of tumor cells in a unidirectional fashion. How such mechanical cues affect CTL evasion of perforin-mediated autolysis remains unclear. Here we show that activated CTLs use their softness to evade perforin-mediated autolysis, which, however, is shared by T leukemic cells to evade CTL killing. Downregulation of filamin A is identified to induce softness via ZAP70-mediated YAP Y357 phosphorylation and activation. Despite the requirements of YAP in both cell types for softness induction, CTLs are more resistant to YAP inhibitors than malignant T cells, potentially due to the higher expression of the drug-resistant transporter, MDR1, in CTLs. As a result, moderate inhibition of YAP stiffens malignant T cells but spares CTLs, thus allowing CTLs to cytolyze malignant cells without autolysis. Our findings thus hint a mechanical force-based immunotherapeutic strategy against T cell leukemia.

Suggested Citation

  • Yabo Zhou & Dianheng Wang & Li Zhou & Nannan Zhou & Zhenfeng Wang & Jie Chen & Ruiyang Pang & Haixia Fu & Qiusha Huang & Fang Dong & Hui Cheng & Huafeng Zhang & Ke Tang & Jingwei Ma & Jiadi Lv & Tao C, 2024. "Cell softness renders cytotoxic T lymphocytes and T leukemic cells resistant to perforin-mediated killing," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45750-w
    DOI: 10.1038/s41467-024-45750-w
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    References listed on IDEAS

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    1. Jesse A. Rudd-Schmidt & Adrian W. Hodel & Tahereh Noori & Jamie A. Lopez & Hyun-Jung Cho & Sandra Verschoor & Annette Ciccone & Joseph A. Trapani & Bart W. Hoogenboom & Ilia Voskoboinik, 2019. "Lipid order and charge protect killer T cells from accidental death," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Daqian Xu & Zheng Wang & Yan Xia & Fei Shao & Weiya Xia & Yongkun Wei & Xinjian Li & Xu Qian & Jong-Ho Lee & Linyong Du & Yanhua Zheng & Guishuai Lv & Jia-shiun Leu & Hongyang Wang & Dongming Xing & T, 2020. "The gluconeogenic enzyme PCK1 phosphorylates INSIG1/2 for lipogenesis," Nature, Nature, vol. 580(7804), pages 530-535, April.
    3. Angelos Papaspyropoulos & Leanne Bradley & Asmita Thapa & Chuen Yan Leung & Konstantinos Toskas & Delia Koennig & Dafni-Eleftheria Pefani & Cinzia Raso & Claudia Grou & Garth Hamilton & Nikola Vlahov , 2018. "RASSF1A uncouples Wnt from Hippo signalling and promotes YAP mediated differentiation via p73," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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