Breast Cancer-Derived Exosomes Alter Macrophage Polarization via gp130/STAT3 Signaling

Front Immunol. 2018 May 8:9:871. doi: 10.3389/fimmu.2018.00871. eCollection 2018.

Abstract

Tumor-derived exosomes are being recognized as essential mediators of intercellular communication between cancer and immune cells. It is well established that bone marrow-derived macrophages (BMDMs) take up tumor-derived exosomes. However, the functional impact of these exosomes on macrophage phenotypes is controversial and not well studied. Here, we show that breast cancer-derived exosomes alter the phenotype of macrophages through the interleukin-6 (IL-6) receptor beta (glycoprotein 130, gp130)-STAT3 signaling pathway. Addition of breast cancer-derived exosomes to macrophages results in the activation of the IL-6 response pathway, including phosphorylation of the key downstream transcription factor STAT3. Exosomal gp130, which is highly enriched in cancer exosomes, triggers the secretion of IL-6 from BMDMs. Moreover, the exposure of BMDMs to cancer-derived exosomes triggers changes from a conventional toward a polarized phenotype often observed in tumor-associated macrophages. All of these effects can be inhibited through the addition of a gp130 inhibitor to cancer-derived exosomes or by blocking BMDMs exosome uptake. Collectively, this work demonstrates that breast cancer-derived exosomes are capable of inducing IL-6 secretion and a pro-survival phenotype in macrophages, partially via gp130/STAT3 signaling.

Keywords: STAT3; breast cancer; cancer-derived exosomes; glycoprotein 130; interleukin-6; tumor-associated macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Coculture Techniques
  • Cytokine Receptor gp130 / antagonists & inhibitors
  • Cytokine Receptor gp130 / immunology
  • Cytokine Receptor gp130 / metabolism
  • Exosomes / drug effects
  • Exosomes / immunology*
  • Exosomes / metabolism
  • Female
  • Hydrazines / pharmacology
  • Interleukin-6 / immunology
  • Interleukin-6 / metabolism
  • Macrophage Activation / drug effects
  • Macrophage Activation / immunology
  • Macrophages / cytology
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Mammary Neoplasms, Experimental / immunology*
  • Mammary Neoplasms, Experimental / pathology
  • Mice
  • Mice, Inbred C57BL
  • Primary Cell Culture
  • Quinoxalines / pharmacology
  • STAT3 Transcription Factor / immunology
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / immunology*
  • Tumor Microenvironment / immunology*

Substances

  • Antineoplastic Agents
  • Hydrazines
  • Il6st protein, mouse
  • Interleukin-6
  • N'-(7-fluoroH-pyrrolo(1,2-a)quinoxalin-4-yl)pyrazine-2-carbohydrazide
  • Quinoxalines
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • interleukin-6, mouse
  • Cytokine Receptor gp130