IL-21- and CXCL9-engineered GPC3-specific CAR-T cells combined with PD-1 blockade enhance cytotoxic activities against hepatocellular carcinoma

Clin Exp Med. 2024 Aug 28;24(1):204. doi: 10.1007/s10238-024-01473-2.

Abstract

The application of CAR-T cells in solid tumors poses several challenges, including poor T cell homing ability, limited infiltration of T cells and an immunosuppressive tumor environment. In this study, we developed a novel approach to address these obstacles by designing GPC3-specific CAR-T cell that co-express IL-21 and CXCL9 (21 × 9 GPC3 CAR-T cells) and blocking the PD-1 expression on it. The proliferation, cell phenotype, cytokine secretion and cell migration of indicated CAR-T cells were evaluated in vitro. The cytotoxic activities of genetically engineered CAR-T cells were accessed in vitro and in vivo. Compared to conventional GPC3 CAR-T cells, the 21 × 9 GPC3 CAR-T cells demonstrated superior proliferation, cytokine secretion and chemotaxis capabilities in vitro. Furthermore, when combined with PD-1 blockade, the 21 × 9 GPC3 CAR-T cells exhibited enhanced proliferation, cytokine secretion and enrichment of effector T cells such as CTL, NKT and TEM cells. In xenograft tumor models, the PD-1 blocked 21 × 9 GPC3 CAR-T cells effectively suppressed HCC xenograft growth and increased T cell infiltration. Overall, our study successfully generated GPC3 CAR-T cells expressing both IL-21 and CXCL9, demonstrated that combining PD-1 blockade can further enhance CAR-T cell function by promoting proliferation, cytokine secretion, chemotaxis and antitumor activity. These findings present a hopeful and potentially effective strategy for GPC3-positive HCC patients.

Keywords: CAR-T; CXCL9; GPC3; HCC; IL-21; PD-1.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / drug therapy
  • Carcinoma, Hepatocellular* / immunology
  • Carcinoma, Hepatocellular* / pathology
  • Carcinoma, Hepatocellular* / therapy
  • Cell Line, Tumor
  • Cell Proliferation
  • Chemokine CXCL9* / genetics
  • Chemokine CXCL9* / metabolism
  • Glypicans* / antagonists & inhibitors
  • Glypicans* / genetics
  • Glypicans* / immunology
  • Glypicans* / metabolism
  • Humans
  • Immunotherapy, Adoptive* / methods
  • Interleukin-21
  • Interleukins* / genetics
  • Interleukins* / metabolism
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / pathology
  • Liver Neoplasms* / therapy
  • Mice
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Receptors, Chimeric Antigen* / immunology
  • Receptors, Chimeric Antigen* / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Glypicans
  • Interleukins
  • Interleukin-21
  • Programmed Cell Death 1 Receptor
  • GPC3 protein, human
  • Chemokine CXCL9
  • Receptors, Chimeric Antigen
  • CXCL9 protein, human
  • PDCD1 protein, human