TRIF-dependent Toll-like receptor signaling suppresses Scd1 transcription in hepatocytes and prevents diet-induced hepatic steatosis

Sci Signal. 2017 Aug 8;10(491):eaal3336. doi: 10.1126/scisignal.aal3336.

Abstract

Nonalcoholic fatty liver disease (NAFLD) includes a spectrum of diseases that ranges in severity from hepatic steatosis to steatohepatitis, the latter of which is a major predisposing factor for liver cirrhosis and cancer. Toll-like receptor (TLR) signaling, which is critical for innate immunity, is generally believed to aggravate disease progression by inducing inflammation. Unexpectedly, we found that deficiency in TIR domain-containing adaptor-inducing interferon-β (TRIF), a cytosolic adaptor that transduces some TLR signals, worsened hepatic steatosis induced by a high-fat diet (HFD) and that such exacerbation was independent of myeloid cells. The aggravated steatosis in Trif-/- mice was due to the increased hepatocyte transcription of the gene encoding stearoyl-coenzyme A (CoA) desaturase 1 (SCD1), the rate-limiting enzyme for lipogenesis. Activation of the TRIF pathway by polyinosinic:polycytidylic acid [poly(I:C)] suppressed the increase in SCD1 abundance induced by palmitic acid or an HFD and subsequently prevented lipid accumulation in hepatocytes. Interferon regulatory factor 3 (IRF3), a transcriptional regulator downstream of TRIF, acted as a transcriptional suppressor by directly binding to the Scd1 promoter. These results suggest an unconventional metabolic function for TLR/TRIF signaling that should be taken into consideration when seeking to pharmacologically inhibit this pathway.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics
  • Adaptor Proteins, Vesicular Transport / metabolism*
  • Animals
  • Diet, High-Fat / adverse effects
  • Fatty Liver / genetics*
  • Fatty Liver / metabolism
  • HEK293 Cells
  • Hepatocytes / metabolism*
  • Humans
  • Inflammation / metabolism
  • Interferon Regulatory Factor-3 / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Palmitic Acid / metabolism
  • Poly C / metabolism
  • Primary Cell Culture
  • Stearoyl-CoA Desaturase / genetics*
  • Toll-Like Receptors / metabolism*

Substances

  • Adaptor Proteins, Vesicular Transport
  • Interferon Regulatory Factor-3
  • Irf3 protein, mouse
  • TICAM-1 protein, mouse
  • Toll-Like Receptors
  • Palmitic Acid
  • Poly C
  • Scd1 protein, mouse
  • Stearoyl-CoA Desaturase