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Nature Immunology

Nature Immunology

IF: 27.6
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A second-generation M1-polarized CAR macrophage with antitumor efficacy

Published:27 November 2023 DOI: PMID: 38012418
Anhua Lei, Hua Yu, Shan Lu, Hengxing Lu, Xizhong Ding, Tianyu Tan, Hailing Zhang, Mengmeng Zhu, Lin Tian, Xudong Wang, Siyu Su, Dixuan Xue, Shaolong Zhang, Wei Zhao, Yuge Chen, Wanrun Xie, Li Zhang, Yuqing Zhu, Jing Zhao, Wenhong Jiang, George Church, Francis Ka-Ming Chan, Zhihua Gao, Jin Zhang

Abstract

Chimeric antigen receptor (CAR) T cell therapies have successfully treated hematological malignancies. Macrophages have also gained attention as an immunotherapy owing to their immunomodulatory capacity and ability to infiltrate solid tumors and phagocytize tumor cells. The first-generation CD3ζ-based CAR-macrophages could phagocytose tumor cells in an antigen-dependent manner. Here we engineered induced pluripotent stem cell-derived macrophages (iMACs) with toll-like receptor 4 intracellular toll/IL-1R (TIR) domain-containing CARs resulting in a markedly enhanced antitumor effect over first-generation CAR-macrophages. Moreover, the design of a tandem CD3ζ-TIR dual signaling CAR endows iMACs with both target engulfment capacity and antigen-dependent M1 polarization and M2 resistance in a nuclear factor kappa B (NF-κB)-dependent manner, as well as the capacity to modulate the tumor microenvironment. We also outline a mechanism of tumor cell elimination by CAR-induced efferocytosis against tumor cell apoptotic bodies. Taken together, we provide a second-generation CAR-iMAC with an ability for orthogonal phagocytosis and polarization and superior antitumor functions in treating solid tumors relative to first-generation CAR-macrophages. Induced pluripotent stem cell (iPSC)-derived macrophages (iMACs) are being used to make chimeric antigen receptor (CAR) macrophages for immunotherapy. Here the authors design a second-generation macrophage-specific CAR by integrating CD3ζ and toll/IL-1R (TIR) domains resulting in an M1-polarized CAR-iMAC with increased antitumor functions.

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