Comparison of axicabtagene ciloleucel and tisagenlecleucel patient CAR-T cell products by single-cell RNA sequencing

Background Autologous CD19 chimeric antigen receptor (CAR) T-cell therapy leads to durable responses and improved survival in patients with relapsed or refractory large B-cell lymphoma (R/R LBCL). Among approved CAR T-cell products, axicabtagene ciloleucel (axi-cel; CD19/CD28) has greater real-world...

Full description

Saved in:
Bibliographic Details
Main Authors: Xuefeng Wang, Paulo C Rodriguez, Frederick L Locke, Xiaoqing Yu, Marco L Davila, Salvatore Corallo, Bijal Shah, Kayla Reid, Michael D Jain, Sean J Yoder, Chaomei Zhang, Reginald Atkins, Meghan A Menges, Ling Cen, Jerald D Noble, Turab J Mohammad, Christina A Bachmeier, Samira Naderinezhad, Lanmin Zhang, Julieta Abraham Miranda, Julio C Chavez, Rebecca S Hesterberg, Luis Cuadrado Delgado, Constanza Savid-Frontera, John L Cleveland
Format: Article
Language:English
Published: BMJ Publishing Group 2025-07-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/7/e011807.full
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:Background Autologous CD19 chimeric antigen receptor (CAR) T-cell therapy leads to durable responses and improved survival in patients with relapsed or refractory large B-cell lymphoma (R/R LBCL). Among approved CAR T-cell products, axicabtagene ciloleucel (axi-cel; CD19/CD28) has greater real-world efficacy and cytokine-associated toxicity than tisagenlecleucel (tisa-cel; CD19/4-1BB), for reasons that are poorly understood.Methods Here we report single-cell RNA sequencing (scRNA-seq) of 57 pre-infusion CAR T-cell products from axi-cel (n=39) and tisa-cel (n=18) patients treated as standard-of-care for R/R LBCL, and their biological associations with clinical outcomes. In vitro CAR manufacturing conditions mimicking those known for axi-cel and tisa-cel were performed using CD19/CD28z or CD19/4-1BBz constructs.Results ScRNA-seq revealed that axi-cel and tisa-cel are markedly different products. Axi-cel is comprised of more CD4 central memory, CD8 central memory, and CD8 effectors, whereas tisa-cel is comprised of more proliferative CD4 and CD8 cells. Across multiple T-cell subsets, axi-cel had greater expression of immune response pathways and protein synthesis and trafficking pathways versus tisa-cel. On comparison of infusion product CAR transgene-positive (CAR+) cells to CAR transgene-negative (CAR−) T cells, axi-cel CAR+ cells had vastly different gene expression than axi-cel CAR− cells. Unexpectedly, tisa-cel CAR+ cells were highly similar to tisa-cel CAR− cells. Under recapitulated CAR-T manufacturing conditions known to be used for axi-cel and tisa-cel, we found that CAR+ cells differed from CAR− cells early after manufacturing yet became more similar to CAR− cells after prolonged expansion. Prolonged time in expansion culture, as used during tisa-cel manufacturing, greatly decreased naïve and central memory T-cell subsets.Conclusions Following manufacture, axi-cel is less differentiated and has greater immune activation compared with tisa-cel, potentially accounting for its greater efficacy and toxicity in patients. Our data support the conclusion that tisa-cel is adversely affected by its manufacturing rather than by the CAR construct.
ISSN:2051-1426