Compensatory CSF2-driven macrophage activation promotes adaptive resistance to CSF1R inhibition in breast-to-brain metastasis

Nat Cancer. 2021 Oct;2(10):1086-1101. doi: 10.1038/s43018-021-00254-0. Epub 2021 Oct 18.

Abstract

Tumor microenvironment-targeted therapies are emerging as promising treatment options for different cancer types. Tumor-associated macrophages and microglia (TAMs) represent an abundant nonmalignant cell type in brain metastases and have been proposed to modulate metastatic colonization and outgrowth. Here we demonstrate that targeting TAMs at distinct stages of the metastatic cascade using an inhibitor of colony-stimulating factor 1 receptor (CSF1R), BLZ945, in murine breast-to-brain metastasis models leads to antitumor responses in prevention and intervention preclinical trials. However, in established brain metastases, compensatory CSF2Rb-STAT5-mediated pro-inflammatory TAM activation blunted the ultimate efficacy of CSF1R inhibition by inducing neuroinflammation gene signatures in association with wound repair responses that fostered tumor recurrence. Consequently, blockade of CSF1R combined with inhibition of STAT5 signaling via AC4-130 led to sustained tumor control, a normalization of microglial activation states and amelioration of neuronal damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Neoplasms* / secondary
  • Genes, fms
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Macrophage Activation
  • Melanoma
  • Melanoma, Cutaneous Malignant
  • Mice
  • Receptors, Colony-Stimulating Factor / metabolism
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor* / genetics
  • STAT5 Transcription Factor / genetics
  • Skin Neoplasms
  • Tumor Microenvironment

Substances

  • Csf1r protein, mouse
  • Receptors, Colony-Stimulating Factor
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor
  • STAT5 Transcription Factor
  • Granulocyte-Macrophage Colony-Stimulating Factor