Cycling hypoxia promotes a pro-inflammatory phenotype in macrophages via JNK/p65 signaling pathway

Sci Rep. 2020 Jan 21;10(1):882. doi: 10.1038/s41598-020-57677-5.

Abstract

Cycling hypoxia (cyH), also called intermittent hypoxia, occurs in solid tumors and affects different cell types in the tumor microenvironment and in particular the tumor-associated macrophages (TAMs). As cyH and TAMs both favor tumor progression, we investigated whether cyH could drive the pro-tumoral phenotype of macrophages. Here, the effects of cyH on human THP-1 macrophages and murine bone marrow-derived macrophages (BMDM), either unpolarized M0, or polarized in M1 or M2 phenotype were studied. In M0 macrophages, cyH induced a pro-inflammatory phenotype characterized by an increase in TNFα and IL-8/MIP-2 secretion. CyH amplified the pro-inflammatory phenotype of M1 macrophages evidenced by an increased pro-inflammatory cytokine secretion and pro-inflammatory gene expression. Furthermore, cyH increased c-jun activation in human M0 macrophages and highly increased c-jun and NF-κB activation in M1 macrophages. C-jun and p65 are implicated in the effects of cyH on M0 and M1 macrophages since inhibition of their activation prevented the cyH pro-inflammatory effects. In conclusion, we demonstrated that cyH induces or amplifies a pro-inflammatory phenotype in M0 and M1 macrophages by activating JNK/p65 signaling pathway. These results highlight a specific role of cyH in the amplification of tumor-related inflammation by modulating the inflammatory phenotype of macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anthracenes / pharmacology
  • Cell Line
  • Cytokines / metabolism
  • Gene Expression Regulation
  • Humans
  • MAP Kinase Signaling System*
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology*
  • Male
  • Mice, Inbred C57BL
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism*
  • Nitriles / pharmacology
  • Proto-Oncogene Proteins c-jun / metabolism
  • STAT1 Transcription Factor / metabolism
  • Sulfones / pharmacology
  • Tumor Hypoxia*
  • Tumor Microenvironment
  • Urachal Cyst / metabolism
  • Urachal Cyst / pathology*

Substances

  • 3-(4-methylphenylsulfonyl)-2-propenenitrile
  • Anthracenes
  • Cytokines
  • NF-kappa B
  • Nitriles
  • Proto-Oncogene Proteins c-jun
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Sulfones
  • pyrazolanthrone

Supplementary concepts

  • Benign non-infected urachal cyst