Induction of murine macrophage M2 polarization by cigarette smoke extract via the JAK2/STAT3 pathway

PLoS One. 2014 Sep 8;9(9):e107063. doi: 10.1371/journal.pone.0107063. eCollection 2014.

Abstract

Cigarette smoking is a major pathogenic factor in lung cancer. Macrophages play an important role in host defense and adaptive immunity. These cells display diverse phenotypes for performing different functions. M2 type macrophages usually exhibit immunosuppressive and tumor-promoting characteristics. Although macrophage polarization toward the M2 phenotype has been observed in the lungs of cigarette smokers, the molecular basis of the process remains unclear. In this study, we evaluated the possible mechanisms for the polarization of mouse macrophages that are induced by cigarette smoking (CS) or cigarette smoke extract (CSE). The results showed that exposure to CSE suppressed the production of reactive oxygen species (ROS) and nitric oxide (NO) and down-regulated the phagocytic ability of Ana-1 cells. The CD163 expressions on the surface of macrophages from different sources were significantly increased in in vivo and in vitro studies. The M1 macrophage cytokines TNF-α, IL-12p40 and enzyme iNOS decreased in the culture supernatant, and their mRNA levels decreased depending on the time and concentration of CSE. In contrast, the M2 phenotype macrophage cytokines IL-10, IL-6, TGF-β1 and TGF-β2 were up-regulated. Moreover, phosphorylation of JAK2 and STAT3 was observed after the Ana-1 cells were treated with CSE. In addition, pretreating the Ana-1 cells with the STAT3 phosphorylation inhibitor WP1066 inhibited the CSE-induced CD163 expression, increased the mRNA level of IL-10 and significantly decreased the mRNA level of IL-12. In conclusion, we demonstrated that the M2 polarization of macrophages induced by CS could be mediated through JAK2/STAT3 pathway activation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Cytokines / genetics
  • Cytokines / metabolism
  • Flow Cytometry
  • Janus Kinase 2 / genetics
  • Janus Kinase 2 / metabolism*
  • Macrophages, Alveolar / cytology
  • Macrophages, Alveolar / drug effects*
  • Macrophages, Alveolar / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Nicotiana / chemistry*
  • Phosphorylation / drug effects
  • Plant Extracts / pharmacology*
  • RNA, Messenger / genetics
  • Reactive Oxygen Species / metabolism
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects

Substances

  • Cytokines
  • Plant Extracts
  • RNA, Messenger
  • Reactive Oxygen Species
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Jak2 protein, mouse
  • Janus Kinase 2

Grants and funding

This study was financed by the National Nature Science Foundation of China (No. 81273121) and by State Key Laboratory of Pharmaceutical Biotechnology (KF-GN-201301). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.