Fumagalli et al. developed a focused CRISPR-knockout library targeting loss-of-function of 50 relevant genes to screen low-affinity EGFR CAR-T cells in an orthotopic human lung adenocarcinoma (A549) model. In vivo screening identified ZC3H12A, SOCS1, PTPN2, and CDKN2A loss as top hits that enhanced CAR-T persistence and expansion, whereas MED12, PRDM1, or BATF loss impaired long-term efficacy. Targeted validation of ZC3H12A- and PTPN2-deficient CAR-T cells confirmed improved tumor control and survival. Gene-edited CAR-T cells showed versatility and tumor context specificity, and retained iCasp9 suicide switch activity.

Contributed by Shishir Pant

ABSTRACT: CAR-T cell therapies are revolutionizing the treatment of refractory or relapsed hematological malignancies, but many patients do not achieve durable responses, and these therapies remain ineffective against solid tumors. Therapeutic failure is closely associated with a poor persistence of CAR-T cells in patients, highlighting the need to identify strategies promoting in vivo expansion. Although numerous gene-editing strategies have been proposed, comparative studies to identify the most effective ones are still lacking. Here, using a focused CRISPR-knockout library targeting 50 selected gene candidates, we developed a competitive screening that revealed ZC3H12A, SOCS1, PTPN2, and CDKN2A as the most robust targets to improve persistence of EGFR CAR-T cells in human lung tumor-bearing mice. Surprisingly, disruption of other genes previously reported to improve CAR-T cell efficacy in other preclinical models-MED12, PRDM1, and BATF-had a detrimental effect in this context. These results suggest that some gene-editing strategies can yield beneficial, neutral, or even deleterious effects on CAR-T cell persistence, depending on specific conditions. Altogether, these findings highlight the importance of performing context-specific evaluations of genetic modifications to accelerate the clinical translation of the most promising editing strategies for optimizing CAR-T cell therapies.

Author Info: (1) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France; Thèse Financée par la Ligue Nationa le Contre le Cancer, Paris, France. Electronic address: fumatia97@gmail.com. (2) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (3) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (4) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (5) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France. (6) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France. (7) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France. (8) Technical University of Denmark, 2800 Kongens Lyngby, Denmark. (9) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France. (10) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (11) Pediatric Oncology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA. (12) Department of Onco-Haematology and Cell and Gene Therapy, Bambino Ges Children's Hospital, IRCCS, 00165 Rome, Italy. (13) Department of Onco-Haematology and Cell and Gene Therapy, Bambino Ges Children's Hospital, IRCCS, 00165 Rome, Italy. (14) Department of Onco-Haematology and Cell and Gene Therapy, Bambino Ges Children's Hospital, IRCCS, 00165 Rome, Italy; Department of Clinical Medicine and Surgery, Federico II University of Naples, 80131 Naples, Italy. (15) Department of Onco-Haematology and Cell and Gene Therapy, Bambino Ges Children's Hospital, IRCCS, 00165 Rome, Italy. (16) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (17) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. (18) Université Paris Cité, Institut Cochin, INSERM, CNRS, 75014 Paris, France; Equipe Labélisée Ligue Nationale Contre le Cancer, Paris, France. Electronic address: frederic.pendino@inserm.fr.