CAR-T cells targeting solid cancers have had limited success, reasons for this include poor long-term persistence in vivo. To address this issue, we used naïve T cells to generate second-generation CAR-T cells recognizing the tumor antigen Lewis Y (LeY), termed ‘early’ CAR-T cells. To do this, purified naïve T cells were activated by CD3/CD28 soluble tetrameric antibody complex, retrovirally transduced (LeY scFv-CD3z-CD28 CAR) and expanded in IL-7/IL-15. The early-CAR-T cells comprised stem cell memory-like (CD95+, CD62L+, CD45RA+) and central memory phenotype (CD95+, CD62L+, CD45RA-) T cells with increased expression of ICOS, Ki67, TCF1 and CD27. The early LeY CAR-T cell function was tested in vitro for cytotoxicity (Cr-release and degranulation), proliferation, and cytokine secretion by CBA, either de novo or following chronic stimulation for 1 month. The early-CAR-T cells showed potent antigen-specific cytotoxicity, and secreted significantly higher levels of cytokines (IFN-γ, TNF-α and IL-2) and increased proliferation compared to conventional CAR-T cells. Importantly, after long-term chronic stimulation, early-CAR-T cells had significantly higher proliferative capacity compared to conventional CAR-T cells, and CD4+ CAR-T cells were critical for effective early CD8+ CAR-T cell proliferation capacity in vitro. Early CAR-T cells had significantly better in vivo tumour control (NSG-OVCAR3) compared to conventional CAR-T cells, this was associated with increased persistence of circulating CAR-T cells. Finally, early LeY-CAR-T cells combined with anti-PD-1 therapy completely regressed OVCAR3 tumours in the NSG mice. This was associated with a significantly increased percentage of circulating stem-cell memory like CAR-T cells in vivo.
In conclusion, our early CAR-T cells have better in vitro function and potent anti-tumor efficacy in vivo. Importantly, early-LeY-CAR-T cells combined with anti-PD1-treatment completely cleared LeY+ solid tumors in vivo. Finally, our early CAR-T cell production protocol is directly translatable for improving CAR-T cell efficacy in clinical trials for patients with solid tumours.