Fibrotic response to anti-CSF-1R therapy potentiates glioblastoma recurrence

Cancer Cell. 2024 Sep 9;42(9):1507-1527.e11. doi: 10.1016/j.ccell.2024.08.012.

Abstract

Glioblastoma recurrence is currently inevitable despite extensive standard-of-care treatment. In preclinical studies, an alternative strategy of targeting tumor-associated macrophages and microglia through CSF-1R inhibition was previously found to regress established tumors and significantly increase overall survival. However, recurrences developed in ∼50% of mice in long-term studies, which were consistently associated with fibrotic scars. This fibrotic response is observed following multiple anti-glioma therapies in different preclinical models herein and in patient recurrence samples. Multi-omics analyses of the post-treatment tumor microenvironment identified fibrotic areas as pro-tumor survival niches that encapsulated surviving glioma cells, promoted dormancy, and inhibited immune surveillance. The fibrotic treatment response was mediated by perivascular-derived fibroblast-like cells via activation by transforming growth factor β (TGF-β) signaling and neuroinflammation. Concordantly, combinatorial inhibition of these pathways inhibited treatment-associated fibrosis, and significantly improved survival in preclinical trials of anti-colony-stimulating factor-1 receptor (CSF-1R) therapy.

MeSH terms

  • Animals
  • Brain Neoplasms* / drug therapy
  • Brain Neoplasms* / pathology
  • Cell Line, Tumor
  • Fibrosis*
  • Glioblastoma* / drug therapy
  • Glioblastoma* / pathology
  • Humans
  • Mice
  • Neoplasm Recurrence, Local* / drug therapy
  • Neoplasm Recurrence, Local* / pathology
  • Receptor, Macrophage Colony-Stimulating Factor / antagonists & inhibitors
  • Receptor, Macrophage Colony-Stimulating Factor / metabolism
  • Signal Transduction / drug effects
  • Transforming Growth Factor beta / metabolism
  • Tumor Microenvironment* / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Receptor, Macrophage Colony-Stimulating Factor
  • CSF1R protein, human
  • Transforming Growth Factor beta