Cancer cell CCL5 mediates bone marrow independent angiogenesis in breast cancer

Oncotarget. 2016 Dec 20;7(51):85437-85449. doi: 10.18632/oncotarget.13387.

Abstract

It has recently been suggested that the chemokine receptor (CCR5) is required for bone marrow (BM) derived endothelial progenitor cell (EPC) mediated angiogenesis. Here we show that suppression of either cancer cell produced CCL5, or host CCR5 leads to distinctive vascular and tumor growth defects in breast cancer. Surprisingly, CCR5 restoration in the BM alone was not sufficient to rescue the wild type phenotype, suggesting that impaired tumor growth associated with inhibiting CCL5/CCR5 is not due to defects in EPC biology. Instead, to promote angiogenesis cancer cell CCL5 may signal directly to endothelium in the tumor-stroma. In support of this hypothesis, we have also shown: (i) that endothelial cell CCR5 levels increases in response to tumor-conditioned media; (ii) that the amount of CCR5+ tumor vasculature correlates with invasive grade; and (iii) that inhibition of CCL5/CCR5 signaling impairs endothelial cell migration, associated with a decrease in activation of mTOR/AKT pathway members. Finally, we show that treatment with CCR5 antagonist results in less vasculature, impaired tumor growth, reduced metastases and improved survival. Taken as a whole, this work demonstrates that directly inhibiting CCR5 expressing vasculature constitutes a novel strategy for inhibiting angiogenesis and blocking metastatic progression in breast cancer.

Keywords: CCL5; CCR5; angiogenesis; breast cancer; shRNAi.

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Breast Neoplasms / blood supply
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • CCR5 Receptor Antagonists / pharmacology
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Chemokine CCL5 / genetics
  • Chemokine CCL5 / metabolism*
  • Culture Media, Conditioned / metabolism
  • Cyclohexanes / pharmacology
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Female
  • Humans
  • Maraviroc
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasm Grading
  • Neoplasm Invasiveness
  • Neovascularization, Pathologic*
  • Paracrine Communication
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, CCR5 / genetics
  • Receptors, CCR5 / metabolism
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism
  • Time Factors
  • Triazoles / pharmacology
  • Tumor Burden
  • Tumor Microenvironment

Substances

  • Angiogenesis Inhibitors
  • CCL5 protein, human
  • CCR5 Receptor Antagonists
  • CCR5 protein, human
  • CCR5 protein, mouse
  • Ccl5 protein, mouse
  • Chemokine CCL5
  • Culture Media, Conditioned
  • Cyclohexanes
  • Receptors, CCR5
  • Triazoles
  • MTOR protein, human
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Maraviroc