Histone Methyltransferase SET1 Mediates Angiotensin II-Induced Endothelin-1 Transcription and Cardiac Hypertrophy in Mice

Arterioscler Thromb Vasc Biol. 2015 May;35(5):1207-17. doi: 10.1161/ATVBAHA.115.305230. Epub 2015 Mar 26.

Abstract

Objective: Endothelin-1 is a potent vasoconstrictor derived from vascular endothelium. Elevated endothelin-1 levels are observed in a host of cardiovascular pathologies including cardiomyopathy. The epigenetic mechanism responsible for endothelin-1 induction in these pathological processes remains elusive.

Approach and results: We report here that induction of endothelin-1 expression in endothelial cells by angiotensin II (Ang II) was accompanied by the accumulation of histone H3K4 trimethylation, a preeminent histone modification for transcriptional activation, on the endothelin-1 promoter. In the meantime, Ang II stimulated the expression and the occupancy of Suv, Ez, and Trithorax domain 1 (SET1), a mammalian histone H3K4 trimethyltransferase, on the endothelin-1 promoter, both in vitro and in vivo. SET1 was recruited to the endothelin-1 promoter by activating protein 1 (c-Jun/c-Fos) and synergized with activating protein 1 to activate endothelin-1 transcription in response to Ang II treatment. Knockdown of SET1 in endothelial cells blocked Ang II-induced endothelin-1 synthesis and abrogated hypertrophy of cultured cardiomyocyte. Finally, endothelial-specific depletion of SET1 in mice attenuated Ang II-induced pathological hypertrophy and cardiac fibrosis.

Conclusions: Our data suggest that SET1 epigenetically activates endothelin-1 transcription in endothelial cells, thereby contributing to Ang II-induced cardiac hypertrophy. As such, screening of small-molecule compound that inhibits SET1 activity will likely offer a new therapeutic solution to the treatment of cardiomyopathy.

Keywords: cardiomegaly; endothelial cells; endothelin-1; epigenenomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology*
  • Animals
  • Cardiomegaly / metabolism
  • Cardiomegaly / pathology*
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells
  • Endothelin-1 / drug effects
  • Endothelin-1 / genetics*
  • Epigenomics
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase / metabolism*
  • Mice
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism

Substances

  • Endothelin-1
  • Angiotensin II
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase