N6 -Methyladenosine Reader Protein YT521-B Homology Domain-Containing 2 Suppresses Liver Steatosis by Regulation of mRNA Stability of Lipogenic Genes

Hepatology. 2021 Jan;73(1):91-103. doi: 10.1002/hep.31220. Epub 2020 Oct 25.

Abstract

Background and aims: Nonalcoholic fatty liver disease (NAFLD) is characterized by accumulation of excessive triglycerides (TGs) in hepatocytes. Obesity is a major risk factor for developing fatty liver, although the intracellular molecular basis remains largely unclear. N6 -methyladenosine (m6 A) RNA methylation is the most common internal modification in eukaryotic mRNA.

Approach and results: In the present study, by m6 A sequencing and RNA sequencing, we found that both m6 A enrichment and mRNA expression of lipogenic genes were significantly increased in leptin-receptor-deficient db/db mice. Importantly, our results showed that YT521-B homology domain-containing 2 (Ythdc2), an m6 A reader, was markedly down-regulated in livers of obese mice and NAFLD patients. Suppression of Ythdc2 in livers of lean mice led to TG accumulation, whereas ectopic overexpression of Ythdc2 in livers of obese mice improved liver steatosis and insulin resistance. Mechanistically, we found that Ythdc2 could bind to mRNA of lipogenic genes, including sterol regulatory element-binding protein 1c, fatty acid synthase, stearoyl-CoA desaturase 1, and acetyl-CoA carboxylase 1, to decrease their mRNA stability and inhibit gene expression.

Conclusions: Our findings describe an important role of the m6 A reader, Ythdc2, for regulation of hepatic lipogenesis and TG homeostasis, which might provide a potential target for treating obesity-related NAFLD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Fatty Acid Synthases / metabolism
  • Hep G2 Cells
  • Hepatocytes / metabolism
  • Humans
  • Lipogenesis / genetics*
  • Liver / embryology*
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Obese
  • Non-alcoholic Fatty Liver Disease / enzymology
  • Non-alcoholic Fatty Liver Disease / etiology*
  • Non-alcoholic Fatty Liver Disease / genetics
  • Non-alcoholic Fatty Liver Disease / pathology
  • Obesity / complications*
  • Obesity / enzymology
  • Obesity / genetics
  • Obesity / pathology
  • RNA Helicases / genetics
  • RNA Helicases / metabolism*
  • RNA Stability / genetics*
  • Sterol Regulatory Element Binding Protein 1 / metabolism
  • Triglycerides / metabolism

Substances

  • Sterol Regulatory Element Binding Protein 1
  • Triglycerides
  • Fatty Acid Synthases
  • RNA Helicases
  • YTHDC2 protein, human
  • Ythdc2 protein, mouse