High endogenous CCL2 expression promotes the aggressive phenotype of human inflammatory breast cancer

Nat Commun. 2021 Nov 25;12(1):6889. doi: 10.1038/s41467-021-27108-8.

Abstract

Inflammatory Breast Cancer (IBC) is a highly aggressive malignancy with distinct clinical and histopathological features whose molecular basis is unresolved. Here we describe a human IBC cell line, A3250, that recapitulates key IBC features in a mouse xenograft model, including skin erythema, diffuse tumor growth, dermal lymphatic invasion, and extensive metastases. A3250 cells express very high levels of the CCL2 chemokine and induce tumors enriched in macrophages. CCL2 knockdown leads to a striking reduction in macrophage densities, tumor proliferation, skin erythema, and metastasis. These results establish IBC-derived CCL2 as a key factor driving macrophage expansion, and indirectly tumor growth, with transcriptomic analysis demonstrating the activation of multiple inflammatory pathways. Finally, primary human IBCs exhibit macrophage infiltration and an enriched macrophage RNA signature. Thus, this human IBC model provides insight into the distinctive biology of IBC, and highlights potential therapeutic approaches to this deadly disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / immunology
  • Chemokine CCL2 / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Inflammation
  • Inflammatory Breast Neoplasms / genetics
  • Inflammatory Breast Neoplasms / immunology
  • Inflammatory Breast Neoplasms / metabolism*
  • Inflammatory Breast Neoplasms / pathology*
  • Mice
  • Mice, SCID
  • Myeloid Cells / metabolism
  • Neoplasm Metastasis
  • Receptors, CCR2 / metabolism
  • Transplantation, Heterologous
  • Tumor Microenvironment / immunology
  • Tumor-Associated Macrophages / immunology
  • Tumor-Associated Macrophages / pathology

Substances

  • CCL2 protein, human
  • CCR2 protein, human
  • Chemokine CCL2
  • Receptors, CCR2