Inhibition of macrophage histone demethylase JMJD3 protects against abdominal aortic aneurysms

J Exp Med. 2021 Jun 7;218(6):e20201839. doi: 10.1084/jem.20201839.

Abstract

Abdominal aortic aneurysms (AAAs) are a life-threatening disease for which there is a lack of effective therapy preventing aortic rupture. During AAA formation, pathological vascular remodeling is driven by macrophage infiltration, and the mechanisms regulating macrophage-mediated inflammation remain undefined. Recent evidence suggests that an epigenetic enzyme, JMJD3, plays a critical role in establishing macrophage phenotype. Using single-cell RNA sequencing of human AAA tissues, we identified increased JMJD3 in aortic monocyte/macrophages resulting in up-regulation of an inflammatory immune response. Mechanistically, we report that interferon-β regulates Jmjd3 expression via JAK/STAT and that JMJD3 induces NF-κB-mediated inflammatory gene transcription in infiltrating aortic macrophages. In vivo targeted inhibition of JMJD3 with myeloid-specific genetic depletion (JMJD3f/fLyz2Cre+) or pharmacological inhibition in the elastase or angiotensin II-induced AAA model preserved the repressive H3K27me3 on inflammatory gene promoters and markedly reduced AAA expansion and attenuated macrophage-mediated inflammation. Together, our findings suggest that cell-specific pharmacologic therapy targeting JMJD3 may be an effective intervention for AAA expansion.

Publication types

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

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • Aortic Aneurysm, Abdominal / metabolism*
  • Disease Models, Animal
  • Histone Demethylases / metabolism*
  • Inflammation / metabolism
  • Inflammation Mediators / metabolism
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism
  • Up-Regulation / drug effects
  • Up-Regulation / physiology

Substances

  • Inflammation Mediators
  • NF-kappa B
  • Angiotensin II
  • Histone Demethylases
  • Jumonji Domain-Containing Histone Demethylases
  • Kdm6b protein, mouse