Chimeric antigen receptor (CAR) T cell therapy, while highly efficacious for the treatment of certain haematological malignancies, remains ineffective in solid cancers. This can be attributed to various factors, including immunosuppression in the tumour microenvironment (TME). “Armouring” CAR T cells to express anti-tumour factors such as proinflammatory cytokines and chemokines is a promising strategy to address their limitations in the solid tumour setting and engage endogenous anti-tumour immunity, which we have demonstrated to be critical for the treatment of heterogeneous solid cancers1. However, conventional armouring approaches utilise a synthetic promoter to drive cytokine expression, which leads to unrestricted cytokine production and can cause severe clinical toxicities2. Recent advances in CRISPR/Cas9 gene editing for primary T lymphocytes have presented new avenues for the precise engineering of armoured CAR T cells3. We aimed to engineer CAR T cells to express anti-tumour factors under the transcriptional control of tumour-specific promoters, and hypothesised that this would enhance the safety and efficacy of armoured CAR T cells.
Through a screen of promoters that are selectively active in CAR T cells isolated form the tumour site but not peripheral sites such as the spleen, we have identified two lead candidates that enable potent and highly restricted cytokine production. A novel CRISPR/Cas9-mediated homology directed repair (CRISPR HDR) strategy was employed to knock in (KI) anti-cancer factors into these gene loci and was applied to syngeneic CAR T and OT-I murine models that enable clinically relevant assessment of efficacy and safety1, 3.
Integrating proinflammatory cytokines and chemokines downstream of these identified promoters led to antigen-specific induction of transgene expression and tumour-restricted expression in vivo resulting in significantly enhanced efficacy. Importantly, these factors did not exhibit elevated systemic expression, and provided a favourable safety profile to conventional armoured CAR T cell approaches.