Integrative single-cell multi-omics of CD19-CARposand CARnegT cells suggest drivers of immunotherapy response in B-cell neoplasias

Author:

Guerrero-Murillo Mercedes,Rill-Hinarejos Aina,Trincado Juan L.,Bataller AlexORCID,Ortiz-Maldonado ValentínORCID,Benitez-Ribas Daniel,Español Marta,González Europa Azucena,Martinez-Cibrian Nuria,Marchese Doménica,Martín-Martín Lourdes,Garcia-Sancho Alejandro MartinORCID,Heyn Holger,Juan ManelORCID,Urbano-Ispizúa Álvaro,Delgado Julio,Orfao Alberto,Mereu Elisabetta,Bueno Clara,Menendez Pablo

Abstract

AbstractHow phenotypic, clonal, and functional heterogeneity of CAR-T-cells impact clinical outcomes remain understudied. Here, we integrated clonal kinetics with transcriptomic heterogeneity resolved by single-cell omics to explore cellular dynamics response of both non-transduced (CARneg) and transduced (CARpos)T-cells. CARnegand CARposT-cells were longitudinally interrogated in the manufactured infusion product (IP) andin-vivoat CAR-T cell expansion peak in five B-ALL patients treated with CD19CAR-T-cells (varni-cel). Significant differences were found in the cellular dynamics between CARposand CARnegT-cells in response to therapy. CARposT-cells in the IP exhibited a significant higher CD4:CD8 ratio than CARnegT-cells, and the CD4:CD8 CARposT-cell composition impacted therapy outcome as confirmed in a larger cohort of 24 varni-cel-treated B-ALL patients. Conversely, an inverted trend in the CD4:CD8 CARposT-cell ratio was consistently observed at the expansion peak, with clonally expanding CD8+effector memory and cytotoxic T-cells being the most abundant populations. Expanded cytotoxic CARposγδT cells emerged at the expansion peak, and the extent of theirin-vivoexpansion positively correlated with treatment efficacy, which was validated in a large cohort of B-ALL patients (n=18) treated with varni-cell and B-cell lymphoma patients (n=58) treated with either lisa-cel or axi-cel. Our data provide insights into the complexity and diversity of T-cell responses following CAR-T cell therapy and suggest drivers of immunotherapy response.

Publisher

Cold Spring Harbor Laboratory

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