Preclinical evaluation of antigen-sensitive B7-H3-targeting nanobody-based CAR-T cells in glioblastoma cautions for on-target, off-tumor toxicity.

in Journal for immunotherapy of cancer by Fien Meeus, Cyprine Neba Funeh, Robin Maximilian Awad, Katty Zeven, Dorien Autaers, Ann De Becker, Ivan Van Riet, Cleo Goyvaerts, Sandra Tuyaerts, Bart Neyns, Nick Devoogdt, Yannick De Vlaeminck, Karine Breckpot

TLDR

  • The study aimed to see if a type of special cells called CAR-T cells could help fight a type of brain tumor called glioblastoma. The CAR-T cells were designed to target a protein called B7-H3 that is found on glioblastoma cells but not on healthy brain tissue. The study found that the CAR-T cells were most effective at killing glioblastoma cells in a lab setting and showed promise in a mouse model of the disease. However, the study also found that the CAR-T cells could harm healthy tissue in the mouse, which could be a problem if used in humans. The study suggests that more research is needed to improve the specificity of the CAR-T cells and reduce their toxicity.

Abstract

Glioblastoma is the most common lethal primary brain tumor, urging evaluation of new treatment options. Chimeric antigen receptor (CAR)-T cells targeting B7 homolog 3 (B7-H3) are promising because of the overexpression of B7-H3 on glioblastoma cells but not on healthy brain tissue. Nanobody-based (nano)CARs are gaining increasing attention as promising alternatives to classical single-chain variable fragment-based (scFv)CARs, because of their single-domain nature and low immunogenicity. Still, B7-H3 nanoCAR-T cells have not been extensively studied in glioblastoma. B7-H3 nanoCAR- and scFvCAR-T cells were developed and evaluated in human glioblastoma models. NanoCAR-T cells targeting an irrelevant antigen served as control. T cell activation, cytokine secretion and killing capacity were evaluated in vitro using ELISA, live cell imaging and flow cytometry. Antigen-specific killing was assessed by generating B7-H3 knock-out cells using Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9-genome editing. The tumor tracing capacity of the B7-H3 nanobody was first evaluated in vivo using nuclear imaging. Then, the therapeutic potential of the nanoCAR-T cells was evaluated in a xenograft glioblastoma model. We showed that B7-H3 nanoCAR-T cells were most efficient in lysing B7-H3glioblastoma cells in vitro. Lack of glioblastoma killing by control nanoCAR-T cells and lack of B7-H3glioblastoma killing by B7-H3 nanoCAR-T cells showed antigen-specificity. We showed in vivo tumor targeting capacity of the B7-H3 nanobody-used for the nanoCAR design-in nuclear imaging experiments. Evaluation of the nanoCAR-T cells in vivo showed tumor control in mice treated with B7-H3 nanoCAR-T cells in contrast to progressive disease in mice treated with control nanoCAR-T cells. However, we observed limiting toxicity in mice treated with B7-H3 nanoCAR-T cells and showed that the B7-H3 nanoCAR-T cells are activated even by low levels of mouse B7-H3 expression. B7-H3 nanoCAR-T cells showed promise for glioblastoma therapy following in vitro characterization, but limiting in vivo toxicity was observed. Off-tumor recognition of healthy mouse tissue by the cross-reactive B7-H3 nanoCAR-T cells was identified as a potential cause for this toxicity, warranting caution when using highly sensitive nanoCAR-T cells, recognizing the low-level expression of B7-H3 on healthy tissue.

Overview

  • The study aims to evaluate the therapeutic potential of B7-H3 nanoCAR-T cells in glioblastoma therapy. The study developed and evaluated B7-H3 nanoCAR- and scFvCAR-T cells in human glioblastoma models. The study evaluated T cell activation, cytokine secretion, and killing capacity in vitro using ELISA, live cell imaging, and flow cytometry. The study assessed antigen-specific killing by generating B7-H3 knock-out cells using CRISPR/Cas9-genome editing. The study evaluated the tumor tracing capacity of the B7-H3 nanobody-used for the nanoCAR design in nuclear imaging experiments. The study evaluated the therapeutic potential of the nanoCAR-T cells in vivo in a xenograft glioblastoma model. The study showed that B7-H3 nanoCAR-T cells were most efficient in lysing B7-H3glioblastoma cells in vitro. The study showed in vivo tumor targeting capacity of the B7-H3 nanobody-used for the nanoCAR design in nuclear imaging experiments. The study showed tumor control in mice treated with B7-H3 nanoCAR-T cells in contrast to progressive disease in mice treated with control nanoCAR-T cells. However, the study observed limiting toxicity in mice treated with B7-H3 nanoCAR-T cells and showed that the B7-H3 nanoCAR-T cells are activated even by low levels of mouse B7-H3 expression. The study identified off-tumor recognition of healthy mouse tissue by the cross-reactive B7-H3 nanoCAR-T cells as a potential cause for this toxicity, warranting caution when using highly sensitive nanoCAR-T cells.

Comparative Analysis & Findings

  • The study compared the outcomes observed under different experimental conditions or interventions detailed in the study. The study identified that B7-H3 nanoCAR-T cells were most efficient in lysing B7-H3glioblastoma cells in vitro. The study showed in vivo tumor targeting capacity of the B7-H3 nanobody-used for the nanoCAR design in nuclear imaging experiments. The study showed tumor control in mice treated with B7-H3 nanoCAR-T cells in contrast to progressive disease in mice treated with control nanoCAR-T cells. However, the study observed limiting toxicity in mice treated with B7-H3 nanoCAR-T cells and showed that the B7-H3 nanoCAR-T cells are activated even by low levels of mouse B7-H3 expression. The study identified off-tumor recognition of healthy mouse tissue by the cross-reactive B7-H3 nanoCAR-T cells as a potential cause for this toxicity, warranting caution when using highly sensitive nanoCAR-T cells.

Implications and Future Directions

  • The study's findings suggest that B7-H3 nanoCAR-T cells have potential therapeutic value in glioblastoma therapy. However, the study identified limiting toxicity in mice treated with B7-H3 nanoCAR-T cells, which warrants caution when using highly sensitive nanoCAR-T cells. The study identified off-tumor recognition of healthy mouse tissue by the cross-reactive B7-H3 nanoCAR-T cells as a potential cause for this toxicity, which warrants further investigation. Future research could focus on developing nanoCAR-T cells with improved specificity for B7-H3glioblastoma cells and reduced toxicity. Future research could also investigate the use of nanoCAR-T cells in combination with other therapies, such as radiation or chemotherapy, to enhance their efficacy. Additionally, future research could investigate the use of nanoCAR-T cells in human glioblastoma models to further validate their therapeutic potential.