PGC-1β suppresses saturated fatty acid-induced macrophage inflammation by inhibiting TAK1 activation

IUBMB Life. 2016 Feb;68(2):145-55. doi: 10.1002/iub.1470. Epub 2016 Jan 9.

Abstract

Inflammation of infiltrated macrophages in adipose tissue is a key contributor to the initiation of adipose insulin resistance. These macrophages are exposed to high local concentrations of free fatty acids (FFAs) and can be proinflammatory activated by saturated fatty acids (SFAs). However, the regulatory mechanisms on SFA-induced macrophage inflammation are still elusive. Peroxisome proliferator-activated receptor γ coactivator-1β (PGC-1β) is a member of the PGC-1 family of transcriptional coactivators and has been reported to play a key role in SFAs metabolism and in the regulation of inflammatory signaling. However, it remains unclear whether PGC-1β is involved in SFA-induced macrophage inflammation. In this study, we found that PGC-1β expression was significantly decreased in response to palmitic acid (PA) in macrophages in a dose dependent manner. PGC-1β inhibited PA induced TNFα, MCP-1, and IL-1β mRNA and protein expressions. Furthermore, PGC-1β significantly antagonized PA induced macrophage nuclear factor-κB (NF-κB) p65 and JUN N-terminal kinase activation. Mechanistically, we revealed that TGF-β-activated kinase 1 (TAK1) and its adaptor protein TAK1 binding protein 1 (TAB1) played a dominant role in the regulatory effects of PGC-1β. We confirmed that PGC-1β inhibited downstream inflammatory signals via binding with TAB1 and thus preventing TAB1/TAK1 binding and TAK1 activation. Finally, we showed that PGC-1β overexpression in PA treated macrophages improved adipocytes PI3K-Akt insulin signaling in a paracrine fashion. Collectively, our results uncovered a novel mechanism on how macrophage inflammation induced by SFAs was regulated and suggest a potential target in the treatment of obesity induced insulin resistance.

Keywords: NF-κB; TAK1 binding protein 1; TGF-β-activated kinase 1; inflammation; peroxisome proliferator-activated receptor γ coactivator-1β; saturated fatty acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / biosynthesis
  • Adaptor Proteins, Signal Transducing / genetics*
  • Adipose Tissue / drug effects
  • Adipose Tissue / metabolism*
  • Animals
  • Chemokine CCL2 / biosynthesis
  • Gene Expression Regulation
  • Humans
  • Inflammation / chemically induced
  • Inflammation / genetics*
  • Inflammation / pathology
  • Insulin Resistance / genetics
  • Interleukin-1beta / biosynthesis
  • MAP Kinase Kinase Kinases / biosynthesis
  • MAP Kinase Kinase Kinases / genetics*
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Palmitic Acid / toxicity
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics*
  • Transcriptional Activation / genetics
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Adaptor Proteins, Signal Transducing
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Interleukin-1beta
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, mouse
  • Tab1 protein, mouse
  • Transcription Factors
  • Tumor Necrosis Factor-alpha
  • Palmitic Acid
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7