CCL2 conditionally determines CCL22-dependent Th2-accumulation during TGF-β-induced breast cancer progression

Immunobiology. 2018 Feb;223(2):151-161. doi: 10.1016/j.imbio.2017.10.031. Epub 2017 Oct 16.

Abstract

We investigated expressions of -CC chemokine ligand 2 (CCL2) and CCL5 in tumor samples from 147 breast cancer (BCa) patients and correlated with transforming growth factor-β (TGF-β) expression. We observed an inverse correlation of TGF-β expression with CCL2, CCL5 expression in early stages of BCa. On contrary, in late stages, CCL2, not CCL5, expression was found to be directly proportional with TGF-β expression. TGF-β stimulated MDA-MB-231 cells to express CCL2, however, downregulated both CCL2 and CCL5 in MCF-7. Interestingly, a significant swing of Th1-Th2 ratio towards Th2 is seen within the primary tumors expressing moderate/high-CCL2-low/negative-CCL5. We observed that CCL2-CCR2 interaction induces monocytes/macrophages to secrete Th2-attracting chemokine CCL22 in vitro. Therefore, CCL2 secreted from the tumor microenvironment may attract and interact with monocytes/macrophages, and favor Th2 accumulation by inducing CCL22 secretion. Study in 4T1-BALB/c BCa mouse model demonstrated significant (p<0.05) decrease in CCL2, CCL5 and CCL22 levels and reduction in lung metastatic nodule numbers upon administering TGF-β inhibitor. These findings collectively indicate that TGF-β regulates CCL2 and CCL5 expression in a stage-dependent manner during BCa progression, which in turn, determines Th1-Th2 balance within the tumor microenvironment.

Keywords: Breast cancer; CCL2; CCL22; CCL5; TGF-β; Th1-Th2 ratio.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / immunology*
  • Breast Neoplasms / pathology
  • Carcinogenesis
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism*
  • Chemokine CCL22 / metabolism
  • Chemokine CCL5 / genetics
  • Chemokine CCL5 / metabolism*
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Humans
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / secondary
  • MCF-7 Cells
  • Macrophages / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Th1-Th2 Balance
  • Th2 Cells / immunology*
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Chemokine CCL2
  • Chemokine CCL22
  • Chemokine CCL5
  • Transforming Growth Factor beta