Aim: Autologous CD19-specific CAR (CAR19) T-cells have shown remarkable efficacy against B-cell malignancies, but manufacture of individualised products is expensive, delays patient treatment and is unfeasible in patients with insufficient healthy T-cells. We sought to evaluate TCR suppression by short hairpin RNA (shRNA) in low-cost piggyBac-generated CAR T-cells, in order to generate a ready-made allogeneic product devoid of alloreactivity.
Methods: PiggyBac transposon plasmids were generated for expression of CAR19-28z alone, or additionally with shRNA against either TCRα-chain or TCRβ-chain (shRNA designed by Takara Bio Inc). T-cells isolated by immunomagnetic separation were electroporated with piggyBac transposon and transposase plasmids (n=3 donors per construct), and expanded over 22 days via CD19 stimulation with IL-15 support. TCRneg cells were enriched by immunomagnetic CD3 depletion in CAR T-cell cultures that had been transfected with shRNA, to create a final product. Final products were further cultured to ensure stability of TCR suppression.
Results: CAR T-cell final products had expanded over 100-fold. Overall, the proportion of T cells with the desired TCRnegCAR+ phenotype varied significantly (5% for CAR19-28z alone, 41% with additional TCRα-chain shRNA and 70% with additional TCRβ-chain shRNA). CAR expression on T-cells was robust with CAR19-28z alone or with additional TCRβ-chain shRNA (96% and 98%, respectively), but was significantly lower with additional TCRα-chain shRNA (56%). The proportion of CAR T-cells that were TCRneg was significantly greater with additional TCRα-chain and TCRβ-chain shRNA (74% and 71%, respectively) compared to CAR19-28z alone (5%). TCR silencing was stable over a further 42 days with TCRβ-chain shRNA, but not TCRα-chain shRNA (CAR T-cells lacking TCR: 71% vs 1%, respectively).
Conclusion: CAR19 T-cells with stably suppressed TCR were successfully generated by introducing genes for both CAR and shRNA against TCRβ-chain into T-cells via single-step genetic modification with the piggyBac transposase system. This platform could form the foundation for a bank of inexpensive allogeneic TCRneg CAR T-cells with low GVHD potential, suitable for rapid treatment of many partially HLA-matched recipients.