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Iron-mediated ferroptosis impairs CAR-T cell function and antitumor efficacy

  • Delin Kong,
  • Tingting Yang,
  • Mengyu Zhao,
  • Lin Yang,
  • Ruirui Jing,
  • Youqin Feng,
  • Shaohui Shi,
  • Zhouning Lin,
  • Shi Han,
  • Cong Wei,
  • Rongrong Chen,
  • Qiqi Zhang,
  • Jiazhen Cui,
  • Tianning Gu,
  • Xiujian Wang,
  • Xia Li,
  • Ye Meng,
  • Xiaolin Yuan,
  • Mingming Zhang,
  • Linghui Zhou,
  • Houli Zhao,
  • Ruimin Hong,
  • Simao Huang,
  • Mi Shao,
  • Xiaohui Si,
  • Yingli Han,
  • Shufen Wang,
  • Xiangjun Zeng,
  • Dawei Huo,
  • Meng Zhang,
  • Kejia Hu,
  • Zenan Cen,
  • Haiqiong Zheng,
  • Guoqing Wei,
  • Dongrui Wang,
  • Yongxian Hu,
  • Pengxu Qian,
  • He Huang

摘要

Long-term persistence of chimeric antigen receptor (CAR)-T cells is essential for durable therapeutic efficacy but the mechanisms underlying CAR-T cell dysfunction remain unclear. On the basis of integrated analyses of clinical samples from participants with multiple myeloma and acute lymphoblastic leukemia treated with CAR-T cells, we show that rapid expansion of CAR-T cells after infusion is followed by a ‘diminution’ phase characterized by ferroptosis-associated features and elevated serum iron levels. In preclinical cancer models in female mice and ex vivo culture systems, excess intracellular iron impaired CAR-T cell function. Mechanistically, iron promoted ferroptosis by increasing mitochondrial reactive oxygen species and lipid peroxidation, in part through acyl-CoA synthetase long-chain family member 4 (ACSL4)-associated lipid remodeling. Targeting ferroptosis, particularly through genetic ablation of ACSL4 in CAR-T cells, substantially enhanced antitumor efficacy. Together, these findings identify iron-driven ferroptosis as a determinant of CAR-T cell dysfunction and a targetable barrier to durable CAR-T efficacy.