Proton radiation boosts the efficacy of mesothelin-targeting chimeric antigen receptor T cell therapy in pancreatic cancer

Proc Natl Acad Sci U S A. 2024 Jul 30;121(31):e2403002121. doi: 10.1073/pnas.2403002121. Epub 2024 Jul 24.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) represents a challenge in oncology, with limited treatment options for advanced-stage patients. Chimeric antigen receptor T cell (CAR T) therapy targeting mesothelin (MSLN) shows promise, but challenges such as the hostile immunosuppressive tumor microenvironment (TME) hinder its efficacy. This study explores the synergistic potential of combining proton radiation therapy (RT) with MSLN-targeting CAR T therapy in a syngeneic PDAC model. Proton RT significantly increased MSLN expression in tumor cells and caused a significant increase in CAR T cell infiltration into tumors. The combination therapy reshaped the immunosuppressive TME, promoting antitumorigenic M1 polarized macrophages and reducing myeloid-derived suppressor cells (MDSC). In a flank PDAC model, the combination therapy demonstrated superior attenuation of tumor growth and improved survival compared to individual treatments alone. In an orthotopic PDAC model treated with image-guided proton RT, tumor growth was significantly reduced in the combination group compared to the RT treatment alone. Further, the combination therapy induced an abscopal effect in a dual-flank tumor model, with increased serum interferon-γ levels and enhanced proliferation of extratumoral CAR T cells. In conclusion, combining proton RT with MSLN-targeting CAR T therapy proves effective in modulating the TME, enhancing CAR T cell trafficking, and exerting systemic antitumor effects. Thus, this combinatorial approach could present a promising strategy for improving outcomes in unresectable PDAC.

Keywords: CAR T cells; pancreatic cancer; radiotherapy.

MeSH terms

  • Animals
  • Carcinoma, Pancreatic Ductal* / immunology
  • Carcinoma, Pancreatic Ductal* / pathology
  • Carcinoma, Pancreatic Ductal* / radiotherapy
  • Carcinoma, Pancreatic Ductal* / therapy
  • Cell Line, Tumor
  • Combined Modality Therapy
  • Female
  • GPI-Linked Proteins* / immunology
  • GPI-Linked Proteins* / metabolism
  • Humans
  • Immunotherapy, Adoptive* / methods
  • Mesothelin*
  • Mice
  • Pancreatic Neoplasms* / immunology
  • Pancreatic Neoplasms* / pathology
  • Pancreatic Neoplasms* / radiotherapy
  • Pancreatic Neoplasms* / therapy
  • Proton Therapy / methods
  • Receptors, Chimeric Antigen* / immunology
  • Receptors, Chimeric Antigen* / metabolism
  • T-Lymphocytes / immunology
  • Tumor Microenvironment* / immunology

Substances

  • Mesothelin
  • GPI-Linked Proteins
  • Receptors, Chimeric Antigen
  • Msln protein, mouse
  • MSLN protein, human