Activation of liver-X-receptor α but not liver-X-receptor β protects against myocardial ischemia/reperfusion injury

Circ Heart Fail. 2014 Nov;7(6):1032-41. doi: 10.1161/CIRCHEARTFAILURE.114.001260. Epub 2014 Oct 2.

Abstract

Background: Liver-X-receptors, LXRα (NR1H3) and LXRβ (NR1H2), encode 2 different but highly homologous isoforms of transcription factors belonging to the nuclear receptor superfamily. Whether LXRα and LXRβ subtypes have discrete roles in the regulation of cardiac physiology/pathology is unknown. We determine the role of each LXR subtype in myocardial ischemia/reperfusion (MI/R) injury.

Methods and results: Mice (wild type; those genetically depleted of LXRα, LXRβ, or both; and those overexpressing LXRα or LXRβ by in vivo intramyocardial adenoviral vector) were subjected to MI/R injury. Both LXRα and LXRβ were detected in wild-type mouse heart. LXRα, but not LXRβ, was significantly upregulated after MI/R. Dual activation of LXRα and LXRβ by natural and synthetic agonists reduced myocardial infarction and improved contractile function after MI/R. Mechanistically, LXR activation inhibited MI/R-induced oxidative stress and nitrative stress, attenuated endoplasmic reticulum stress and mitochondrial dysfunction, and reduced cardiomyocyte apoptosis in ischemic/reperfused myocardium. The aforementioned cardioprotective effects of LXR agonists were impaired in the setting of cardiac-specific gene silencing of LXRα, but not LXRβ subtype. Moreover, LXRα/β double-knockout and LXRα-knockout mice, but not LXRβ-knockout mice, increased MI/R injury, exacerbated MI/R-induced oxidative/nitrative stress, and aggravated endoplasmic reticulum stress and mitochondrial dysfunction. Furthermore, cardiac LXRα, not LXRβ, overexpression via adenoviral transfection suppressed MI/R injury.

Conclusions: Our study provides the first direct evidence that the LXRα, but not LXRβ, subtype is a novel endogenous cardiac protective receptor against MI/R injury. Drug development strategies specifically targeting LXRα may be beneficial in treating ischemic heart disease.

Keywords: apoptosis; myocardium; receptors, cytoplasmic and nuclear; reperfusion injury.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Benzoates / pharmacology
  • Benzylamines / pharmacology
  • Endoplasmic Reticulum / physiology
  • Gene Silencing
  • Liver X Receptors
  • Male
  • Mice
  • Mice, Knockout
  • Mitochondria, Liver / physiology
  • Myocardial Reperfusion Injury / metabolism
  • Myocardial Reperfusion Injury / physiopathology*
  • Myocardial Reperfusion Injury / prevention & control
  • Orphan Nuclear Receptors / agonists
  • Orphan Nuclear Receptors / physiology*
  • Oxidative Stress / physiology
  • Protein Isoforms
  • Up-Regulation

Substances

  • Benzoates
  • Benzylamines
  • GW 3965
  • Liver X Receptors
  • Nr1h2 protein, mouse
  • Nr1h3 protein, mouse
  • Orphan Nuclear Receptors
  • Protein Isoforms