Targeting CEA in metastatic triple negative breast cancer with image-guided radiation followed by Fab-mediated chimeric antigen receptor (CAR) T-cell therapy

Front Immunol. 2024 Dec 20:15:1499471. doi: 10.3389/fimmu.2024.1499471. eCollection 2024.

Abstract

Introduction: Although CAR-T cell therapy has limited efficacy against solid tumors, it has been hypothesized that prior treatment with Image-Guided Radiation Therapy (IGRT) would increase CAR-T cell tumor infiltration, leading to improved antigen specific expansion of CAR-T cells.

Methods: To test this hypothesis in a metastatic triple negative breast cancer (TNBC) model, we engineered two anti-CEA single-chain Fab (scFab) CAR-T cells with signaling domains from CD28zeta and 4-1BBzeta, and tested them in vitro and in vivo.

Results: The anti-CEA scFab CAR-T cells generated from three different human donors demonstrated robust in vitro expression, expansion, and lysis of only CEA-positive TNBC cells, with the CD28z-CAR-T cells showing the highest cytotoxicity. IFN-γ and granzyme B release assays revealed significantly higher IFN-γ production at a 4:1 effector-to-target (E:T) ratio in CD28z-CAR-T cells compared to 4-1BBz-CAR-T cells. Treatment of CEA-positive TNBC MDA-MB231 xenografts in the mammary fat pads of NSG mice, that produced spontaneous lung metastases over time, resulted in significant tumor growth reduction compared to either therapy alone (p<0.01). Immunohistochemical (IHC) analysis revealed that only combined IGRT and CAR-T therapy resulted in the elimination of lung metastases.

Discussion: These findings demonstrate that the combination of IGRT and anti-CEA scFab CAR-T therapy induces a strong antitumor response, effectively targeting both the primary tumor and distant metastatic lesions in the lungs, thus demonstrating that IGRT enhances CAR-T cell infiltration, persistence, and overall efficacy within both primary and metastatic lesions.

Keywords: carcinoembryonic antigen; cell immunotherapy; chimeric antigen receptor T cells; image-guided radiation therapy; triple-negative breast cancer.

MeSH terms

  • Animals
  • Carcinoembryonic Antigen* / genetics
  • Carcinoembryonic Antigen* / immunology
  • Cell Line, Tumor
  • Female
  • Humans
  • Immunoglobulin Fab Fragments / genetics
  • Immunoglobulin Fab Fragments / immunology
  • Immunotherapy, Adoptive* / methods
  • Mice
  • Radiotherapy, Image-Guided* / methods
  • Receptors, Chimeric Antigen* / genetics
  • Receptors, Chimeric Antigen* / immunology
  • Receptors, Chimeric Antigen* / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Triple Negative Breast Neoplasms* / immunology
  • Triple Negative Breast Neoplasms* / pathology
  • Triple Negative Breast Neoplasms* / therapy
  • Xenograft Model Antitumor Assays*

Substances

  • Receptors, Chimeric Antigen
  • Carcinoembryonic Antigen
  • Immunoglobulin Fab Fragments

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported in part by Cancer Grant National Cancer Institute P30 CA033572.