Dual targeting macrophages and microglia is a therapeutic vulnerability in models of PTEN-deficient glioblastoma

J Clin Invest. 2024 Oct 1;134(22):e178628. doi: 10.1172/JCI178628.

Abstract

Tumor-associated macrophages and microglia (TAMs) are critical for tumor progression and therapy resistance in glioblastoma (GBM), a type of incurable brain cancer. We previously identified lysyl oxidase (LOX) and olfactomedin like-3 (OLFML3) as essential macrophage and microglia chemokines, respectively, in GBM. Here, single-cell transcriptomics and multiplex sequential immunofluorescence followed by functional studies demonstrate that macrophages negatively correlate with microglia in the GBM tumor microenvironment. LOX inhibition in PTEN-deficient GBM cells upregulates OLFML3 expression via the NF-κB-PATZ1 signaling pathway, inducing a compensatory increase of microglia infiltration. Dual targeting macrophages and microglia via inhibition of LOX and the CLOCK-OLFML3 axis generates potent antitumor effects and offers a complete tumor regression in more than 60% of animals when combined with anti-PD1 therapy in PTEN-deficient GBM mouse models. Thus, our findings provide a translational triple therapeutic strategy for this lethal disease.

Keywords: Brain cancer; Cancer immunotherapy; Macrophages; Oncology.

MeSH terms

  • Animals
  • Brain Neoplasms* / drug therapy
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Cell Line, Tumor
  • Glioblastoma* / genetics
  • Glioblastoma* / immunology
  • Glioblastoma* / pathology
  • Humans
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Microglia* / metabolism
  • Microglia* / pathology
  • Neoplasm Proteins / deficiency
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / immunology
  • Neoplasm Proteins / metabolism
  • PTEN Phosphohydrolase* / deficiency
  • PTEN Phosphohydrolase* / genetics
  • PTEN Phosphohydrolase* / metabolism
  • Protein-Lysine 6-Oxidase* / genetics
  • Protein-Lysine 6-Oxidase* / metabolism
  • Signal Transduction
  • Tumor Microenvironment / immunology

Substances

  • PTEN Phosphohydrolase
  • PTEN protein, human
  • Pten protein, mouse
  • Protein-Lysine 6-Oxidase
  • LOX protein, human
  • Neoplasm Proteins