Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies

Abstract Background Despite the promising results of CAR-T cell therapy, still a significant proportion of patients experience treatment failure due to absence of response, progression or treatment-related toxicities. Our research aims to investigate how the CAR-T cell product characteristics and pa...

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Main Authors: Belén Sierro-Martínez, Beatriz Guijarro-Albaladejo, Ricardo Fernández-Cisnal, Alfonso Rodríguez-Gil, Paola Hernández-Díaz, María de la Rosa-Garrido, Inmaculada Carrasco-Brocal, Maribel Lara-Chica, Virginia Escamilla-Gómez, Raquel Muñoz-García, Ángela Bella, Francisco Jose García-Cózar, Jose Antonio Pérez-Simón, Estefanía García-Guerrero
Format: Article
Language:English
Published: BMC 2025-08-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-025-06899-0
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author Belén Sierro-Martínez
Beatriz Guijarro-Albaladejo
Ricardo Fernández-Cisnal
Alfonso Rodríguez-Gil
Paola Hernández-Díaz
María de la Rosa-Garrido
Inmaculada Carrasco-Brocal
Maribel Lara-Chica
Virginia Escamilla-Gómez
Raquel Muñoz-García
Ángela Bella
Francisco Jose García-Cózar
Jose Antonio Pérez-Simón
Estefanía García-Guerrero
author_facet Belén Sierro-Martínez
Beatriz Guijarro-Albaladejo
Ricardo Fernández-Cisnal
Alfonso Rodríguez-Gil
Paola Hernández-Díaz
María de la Rosa-Garrido
Inmaculada Carrasco-Brocal
Maribel Lara-Chica
Virginia Escamilla-Gómez
Raquel Muñoz-García
Ángela Bella
Francisco Jose García-Cózar
Jose Antonio Pérez-Simón
Estefanía García-Guerrero
author_sort Belén Sierro-Martínez
collection DOAJ
description Abstract Background Despite the promising results of CAR-T cell therapy, still a significant proportion of patients experience treatment failure due to absence of response, progression or treatment-related toxicities. Our research aims to investigate how the CAR-T cell product characteristics and particularly the percentage of CAR-negative cells present in the infusion product affects its efficacy and safety. Methods CAR-positive (CAR-pos) and CAR-negative (CAR-neg) cells were analyzed during in vitro expansion with IL-2 or IL-7/IL-15. FACS-sorted populations were assessed for cytotoxic effect and secretion of cytokines. Transcriptomic analyses were conducted for CAR-pos and CAR-neg populations. Results A significant reduction in the percentage of transduced (CAR-pos) T cells was observed throughout the in vitro cell culture, where CAR-neg T cells displayed greater expansion along the procedure compared to CAR-pos T cells, using either IL-2 or IL-7/IL-15. CAR-pos T cells exhibited increased expression of activation and exhaustion markers. Comparative analyses of CAR-pos and CAR-neg showed an increased cytotoxic effect in purified samples with 100% CAR-pos T cells compared to non-purified product. Quantification of cytokine levels revealed a significant decrease in IL-6 in purified compared to non-purified products. RNA sequencing analysis revealed significant differential gene expression profile between CAR-pos and CAR-neg cells, the prior exhibiting an upregulation of genes associated with immune checkpoint regulation, cytokine-cytokine receptor interaction and Th1/Th2 and Th17 cell differentiation pathways. Conclusion CAR-neg T cells exhibit a significantly greater expansion compared to CAR-pos T cells alongside CAR-T cell production. The percentage of CAR-neg cells influences the specific cytotoxicity of the product and on the cytokine pattern, which might influence both efficacy and toxicity and, therefore, the number of CAR-neg T cells within the infusion product must be considered in the clinical setting. Purification of CAR-pos T cells could potentially optimize product characteristics.
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spelling doaj-art-0c37a21d4dab4d9ea8e61753bbfb87722025-08-24T11:48:00ZengBMCJournal of Translational Medicine1479-58762025-08-0123111410.1186/s12967-025-06899-0Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapiesBelén Sierro-Martínez0Beatriz Guijarro-Albaladejo1Ricardo Fernández-Cisnal2Alfonso Rodríguez-Gil3Paola Hernández-Díaz4María de la Rosa-Garrido5Inmaculada Carrasco-Brocal6Maribel Lara-Chica7Virginia Escamilla-Gómez8Raquel Muñoz-García9Ángela Bella10Francisco Jose García-Cózar11Jose Antonio Pérez-Simón12Estefanía García-Guerrero13Instituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Investigación E Innovación Biomédica (INiBICA)Instituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Investigación E Innovación Biomédica (INiBICA)Instituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaInstituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de SevillaAbstract Background Despite the promising results of CAR-T cell therapy, still a significant proportion of patients experience treatment failure due to absence of response, progression or treatment-related toxicities. Our research aims to investigate how the CAR-T cell product characteristics and particularly the percentage of CAR-negative cells present in the infusion product affects its efficacy and safety. Methods CAR-positive (CAR-pos) and CAR-negative (CAR-neg) cells were analyzed during in vitro expansion with IL-2 or IL-7/IL-15. FACS-sorted populations were assessed for cytotoxic effect and secretion of cytokines. Transcriptomic analyses were conducted for CAR-pos and CAR-neg populations. Results A significant reduction in the percentage of transduced (CAR-pos) T cells was observed throughout the in vitro cell culture, where CAR-neg T cells displayed greater expansion along the procedure compared to CAR-pos T cells, using either IL-2 or IL-7/IL-15. CAR-pos T cells exhibited increased expression of activation and exhaustion markers. Comparative analyses of CAR-pos and CAR-neg showed an increased cytotoxic effect in purified samples with 100% CAR-pos T cells compared to non-purified product. Quantification of cytokine levels revealed a significant decrease in IL-6 in purified compared to non-purified products. RNA sequencing analysis revealed significant differential gene expression profile between CAR-pos and CAR-neg cells, the prior exhibiting an upregulation of genes associated with immune checkpoint regulation, cytokine-cytokine receptor interaction and Th1/Th2 and Th17 cell differentiation pathways. Conclusion CAR-neg T cells exhibit a significantly greater expansion compared to CAR-pos T cells alongside CAR-T cell production. The percentage of CAR-neg cells influences the specific cytotoxicity of the product and on the cytokine pattern, which might influence both efficacy and toxicity and, therefore, the number of CAR-neg T cells within the infusion product must be considered in the clinical setting. Purification of CAR-pos T cells could potentially optimize product characteristics.https://doi.org/10.1186/s12967-025-06899-0CAR-TFACS-sortingCAR-negativeRNA-seqICANSCRS
spellingShingle Belén Sierro-Martínez
Beatriz Guijarro-Albaladejo
Ricardo Fernández-Cisnal
Alfonso Rodríguez-Gil
Paola Hernández-Díaz
María de la Rosa-Garrido
Inmaculada Carrasco-Brocal
Maribel Lara-Chica
Virginia Escamilla-Gómez
Raquel Muñoz-García
Ángela Bella
Francisco Jose García-Cózar
Jose Antonio Pérez-Simón
Estefanía García-Guerrero
Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
Journal of Translational Medicine
CAR-T
FACS-sorting
CAR-negative
RNA-seq
ICANS
CRS
title Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
title_full Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
title_fullStr Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
title_full_unstemmed Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
title_short Unveiling the influence of CAR-negative T-cells: enhancing efficacy and ensuring safety in CAR-T therapies
title_sort unveiling the influence of car negative t cells enhancing efficacy and ensuring safety in car t therapies
topic CAR-T
FACS-sorting
CAR-negative
RNA-seq
ICANS
CRS
url https://doi.org/10.1186/s12967-025-06899-0
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