Targeting hypoxia downstream signaling protein, CAIX, for CAR T-cell therapy against glioblastoma

Neuro Oncol. 2019 Nov 4;21(11):1436-1446. doi: 10.1093/neuonc/noz117.

Abstract

Background: Glioblastoma survival remains unchanged despite continuing therapeutic innovation. Herein, we aim to (i) develop chimeric antigen receptor (CAR) T cells with a specificity to a unique antigen, carbonic anhydrase IX (CAIX), which is expressed in the hypoxic microenvironment characteristic of glioblastoma, and (ii) demonstrate its efficacy with limited off-target effects.

Methods: First we demonstrated expression of CAIX in patient-derived glioblastoma samples and available databases. CAR T cells were generated against CAIX and efficacy was assessed in 4 glioblastoma cell lines and 2 glioblastoma stem cell lines. Cytotoxicity of anti-CAIX CAR T cells was assessed via interferon gamma, tumor necrosis factor alpha, and interleukin-2 levels when co-cultured with tumor cells. Finally, we assessed efficacy of direct intratumoral injection of the anti-CAIX CAR T cells on an in vivo xenograft mouse model using the U251 luciferase cell line. Tumor infiltrating lymphocyte analyses were performed.

Results: We confirm that CAIX is highly expressed in glioblastoma from patients. We demonstrate that CAIX is a suitable target for CAR T-cell therapy using anti-CAIX CAR T cells against glioblastoma in vitro and in vivo. In our mouse model, a 20% cure rate was observed without detectable systemic effects.

Conclusions: By establishing the specificity of CAIX under hypoxic conditions in glioblastoma and highlighting its efficacy as a target for CAR T-cell therapy, our data suggest that anti-CAIX CAR T may be a promising strategy to treat glioblastoma. Direct intratumoral injection increases anti-CAIX CAR T-cell potency while limiting its off-target effects.

Keywords: carbonic anhydrase IX; chimeric antigen receptor; glioblastoma; immunotherapy.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Antigens, Neoplasm / immunology
  • Antigens, Neoplasm / metabolism
  • Apoptosis
  • Biomarkers, Tumor / metabolism*
  • Carbonic Anhydrase IX / antagonists & inhibitors*
  • Carbonic Anhydrase IX / immunology
  • Carbonic Anhydrase IX / metabolism
  • Cell Proliferation
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma / immunology
  • Glioblastoma / metabolism
  • Glioblastoma / pathology
  • Glioblastoma / therapy*
  • Humans
  • Immunotherapy, Adoptive / methods*
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Prognosis
  • Signal Transduction
  • Tumor Cells, Cultured
  • Tumor Microenvironment / immunology*
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, Neoplasm
  • Biomarkers, Tumor
  • CA9 protein, human
  • Carbonic Anhydrase IX