R. H. Amin, K. G. Haworth, H. F. Moffett, J. C. Chen, L. Park, J. K. Yokoyama, A. L. Wang, L. J. Tait, M. M. Steele, J. T. Crowl, T. M. Davenport, J. DeSautelle, J. L. Hammer, W. M. Obenza, V. R. Montoya, R. L. Kirkpatrick, T. Tan, K. M. Shirley, B. Hammerson, R. A. Langan, D. S. Clausen, P. J. Sample, B. D. Weitzner, S. Yuan, M. J. Lajoie, S. E. Boyken, A. E. Foster
The eradication of solid tumors by chimeric antigen receptor (CAR) T cells requires dynamic therapies capable of outlasting an immune suppressive tumor microenvironment (TME). However, biological barriers--including rapid exhaustion, poor expansion, and loss of stem-like memory--quickly neutralize these therapies. Because single-technology interventions often introduce unacceptable tradeoffs between efficacy and safety, durable remission demands a paradigm where multiple engineered solutions work in concert. To holistically address these mechanisms, we rationally designed a single-vector transgene that intrinsically drives CAR T functional persistence. The platform integrates four synergistic technologies: a high-avidity mesothelin (MSLN)-targeting CAR optimized to resist shed decoy antigens, a T-cell activation-responsive promoter (OUTLAST OP1) resisting exhaustion, a CD8-targeted designed IL-2 cytokine (OUTSMART dIL-2) driving intratumoral CAR-T expansion, and an EGFRopt safety switch. In lung and ovarian cancer models, this rational integration was required to drive antigen-dependent T cell expansion and eradicate established tumors at extremely low CAR T doses. Furthermore, engineered cells established a self-renewing pool of stem-like memory T cells capable of rejecting tumor rechallenge months later. Ultimately, this work demonstrates that intrinsic T cell dysfunction and extrinsic tumor-derived barriers can be simultaneously overcome by integrating synergistic technologies.