Loss of miR-141/200c ameliorates hepatic steatosis and inflammation by reprogramming multiple signaling pathways in NASH

JCI Insight. 2017 Nov 2;2(21):e96094. doi: 10.1172/jci.insight.96094.

Abstract

Accumulation of lipid droplets and inflammatory cell infiltration is the hallmark of nonalcoholic steatohepatitis (NASH). The roles of noncoding RNAs in NASH are less known. We aim to elucidate the function of miR-141/200c in diet-induced NASH. WT and miR-141/200c-/- mice were fed a methionine and choline deficient (MCD) diet for 2 weeks to assess markers of steatosis, liver injury, and inflammation. Hepatic miR-141 and miR-200c RNA levels were highly induced in human patients with NASH fatty liver and in WT MCD mice. miR-141/200c-/- MCD mice had reduced liver weights and triglyceride (TG) levels, which was associated with increased microsomal TG transfer protein (MTTP) and PPARα but reduced SREBP1c and FAS expression. Inflammation was attenuated and F4/80 macrophage activation was suppressed in miR-141/200c-/- mice, as evidenced by decreased serum aminotransferases and IL-6 and reduced hepatic proinflammatory, neutrophil, and profibrotic genes. Treatment with LPS in BM-derived macrophages isolated from miR-200c/141-/- mice polarized macrophages toward the M2 antiinflammatory state by increasing Arg1 and IL-10 levels while decreasing the M1 marker iNOS. In addition, elevated phosphorylated AMPK (p-AMPK), p-AKT, and p-GSK3β and diminished TLR4 and p-mTOR/p-4EBP1 proteins were observed. Lipidomics and metabolomics revealed alterations of TG and phosphatidylcholine (PC) lipid species by miR-141/200c deficiency. In summary, miR-141/200c deficiency diminished NASH-associated hepatic steatosis and inflammation by reprogramming lipid and inflammation signaling pathways.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Arginase / metabolism
  • Biomarkers
  • Cell Line
  • Diet
  • Fatty Acids / metabolism
  • Fatty Liver / metabolism*
  • Fatty Liver / pathology
  • Female
  • Gene Expression
  • Humans
  • Inflammation / metabolism*
  • Interleukin-6 / blood
  • Liver / injuries
  • Liver / metabolism
  • Liver / pathology
  • Macrophages / metabolism
  • Male
  • Metabolomics
  • Mice
  • Mice, Knockout
  • MicroRNAs / metabolism*
  • Neutrophils
  • Nitric Oxide Synthase Type II
  • Non-alcoholic Fatty Liver Disease / metabolism*
  • Non-alcoholic Fatty Liver Disease / pathology
  • PPAR alpha
  • Signal Transduction*
  • Sterol Regulatory Element Binding Protein 1
  • Toll-Like Receptor 4 / metabolism
  • Transaminases / blood
  • Triglycerides

Substances

  • Biomarkers
  • Fatty Acids
  • Interleukin-6
  • MIRN141 microRNA, human
  • MIRN200 microRNA, human
  • MicroRNAs
  • Mirn141 microRNA, mouse
  • Mirn200 microRNA, mouse
  • PPAR alpha
  • Sterol Regulatory Element Binding Protein 1
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Triglycerides
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Transaminases
  • Arg1 protein, mouse
  • Arginase