Deficiency of Histone Methyltransferase SET Domain-Containing 2 in Liver Leads to Abnormal Lipid Metabolism and HCC

Hepatology. 2021 May;73(5):1797-1815. doi: 10.1002/hep.31594. Epub 2021 Mar 17.

Abstract

Background and aims: Trimethylation of Lys36 on histone 3 (H3K36me3) catalyzed by histone methyltransferase SET domain-containing 2 (SETD2) is one of the most conserved epigenetic marks from yeast to mammals. SETD2 is frequently mutated in multiple cancers and acts as a tumor suppressor.

Approach and results: Here, using a liver-specific Setd2 depletion model, we found that Setd2 deficiency is sufficient to trigger spontaneous HCC. Meanwhile, Setd2 depletion significantly increased tumor and tumor size of a diethylnitrosamine-induced HCC model. The mechanistic study showed that Setd2 suppresses HCC not only through modulating DNA damage response, but also by regulating lipid metabolism in the liver. Setd2 deficiency down-regulated H3K36me3 enrichment and expression of cholesterol efflux genes and caused lipid accumulation. High-fat diet enhanced lipid accumulation and promoted the development of HCC in Setd2-deficient mice. Chromatin immunoprecipitation sequencing analysis further revealed that Setd2 depletion induced c-Jun/activator protein 1 (AP-1) activation in the liver, which was trigged by accumulated lipid. c-Jun acts as an oncogene in HCC and functions through inhibiting p53 in Setd2-deficient cells.

Conclusions: We revealed the roles of Setd2 in HCC and the underlying mechanisms in regulating cholesterol homeostasis and c-Jun/AP-1 signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine Transaminase / blood
  • Animals
  • Aspartate Aminotransferases / blood
  • CRISPR-Associated Protein 9
  • CRISPR-Cas Systems
  • Carcinoma, Hepatocellular / etiology*
  • Carcinoma, Hepatocellular / metabolism
  • Cell Line, Tumor
  • Cholesterol / blood
  • Chromatin Immunoprecipitation
  • Gene Editing
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Hep G2 Cells
  • Histone-Lysine N-Methyltransferase / deficiency*
  • Histone-Lysine N-Methyltransferase / metabolism
  • Humans
  • Lipid Metabolism*
  • Liver / metabolism*
  • Liver Neoplasms / etiology*
  • Liver Neoplasms / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Triglycerides / blood

Substances

  • Triglycerides
  • Cholesterol
  • Histone-Lysine N-Methyltransferase
  • SETD2 protein, mouse
  • Aspartate Aminotransferases
  • Alanine Transaminase
  • CRISPR-Associated Protein 9