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Temporal multi-modal single-cell analyses reveal dynamic interactions of CAR-T cells with glioblastoma and targeting of antigen-negative neoplastic cells

Zhang, D. Y.; Wang, X.; Sun, Y.; Cui, Q.; Nelson, E.; Zhang, Z.; Huang, B.; Giles, J.; Thokala, R.; Connolly, D. R.; Jacob, F.; Wherry, J.; Lucas, T.; Chen, I. H.; Shi, Y.; Binder, Z. A.; Brem, S.; Nasrallah, M.; Salinas, R.; O'Rourke, D. M.; Ming, G.-L.; Song, H.

2024-10-04 cancer biology
10.1101/2024.10.03.616537 bioRxiv
Show abstract

CAR-T therapy is a promising new immunotherapy for cancers, but its efficacy for solid tumors requires improvement. A detailed understanding of the interplay between solid tumors and CAR-T cells is critical. Here we report temporal, multi-modal, single-cell profiling of patient-derived glioblastoma organoids with CAR-T treatment. We found that all tumor cell types responded to CAR-T cell activation and contributed to an initially anti-tumor, but subsequently pro-tumor and immune-inhibitory microenvironment, accompanied by CAR-T cell exhaustion. Unexpectedly, CAR-T treatment attenuated glioma stem-like states of both antigen-positive and antigen-negative neoplastic cells and reduced their proliferation via diffusible factors, including IFN{gamma}. Analysis of samples from additional patients, including those in clinical trials, supported these findings. Our study reveals the dynamic interplay among different tumor cells and T cells in adaptive responses to immunotherapy and identifies previously unappreciated benefits of CAR-T therapy directly on antigen-negative neoplastic cells that may be leveraged to enhance therapeutic efficacy.

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