Monitoring melanoma patients on treatment reveals a distinct macrophage population driving targeted therapy resistance

Cell Rep Med. 2024 Jul 16;5(7):101611. doi: 10.1016/j.xcrm.2024.101611. Epub 2024 Jun 27.

Abstract

Resistance to targeted therapy remains a major clinical challenge in melanoma. To uncover resistance mechanisms, we perform single-cell RNA sequencing on fine-needle aspirates from resistant and responding tumors of patients undergoing BRAFi/MEKi treatment. Among the genes most prominently expressed in resistant tumors is POSTN, predicted to signal to a macrophage population associated with targeted therapy resistance (TTR). Accordingly, tumors from patients with fast disease progression after therapy exhibit high POSTN expression levels and high numbers of TTR macrophages. POSTN polarizes human macrophages toward a TTR phenotype and promotes resistance to targeted therapy in a melanoma mouse model, which is associated with a phenotype change in intratumoral macrophages. Finally, polarized TTR macrophages directly protect human melanoma cells from MEKi-induced killing via CD44 receptor expression on melanoma cells. Thus, interfering with the protective activity of TTR macrophages may offer a strategy to overcome resistance to targeted therapy in melanoma.

Keywords: CD44 pathway; Periostin; immune landscape; melanoma; resistance; single-cell transcriptome analysis; targeted therapy; tumor microenvironment; tumor-associated macrophages.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm* / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Humans
  • Hyaluronan Receptors / genetics
  • Hyaluronan Receptors / metabolism
  • Macrophages* / drug effects
  • Macrophages* / metabolism
  • Melanoma* / drug therapy
  • Melanoma* / genetics
  • Melanoma* / metabolism
  • Melanoma* / pathology
  • Mice
  • Molecular Targeted Therapy
  • Protein Kinase Inhibitors / pharmacology

Substances

  • Protein Kinase Inhibitors
  • Hyaluronan Receptors