IRF2BP2 Reduces Macrophage Inflammation and Susceptibility to Atherosclerosis

Circ Res. 2015 Sep 25;117(8):671-83. doi: 10.1161/CIRCRESAHA.114.305777. Epub 2015 Jul 20.

Abstract

Rationale: Inflammation impairs macrophage cholesterol clearance from vascular tissues and promotes atherosclerosis. Inflammatory macrophages suppress expression of the transcription cofactor interferon regulatory factor 2-binding protein 2 (IRF2BP2), and genetic variants near IRF2BP2 associate with ischemic heart disease progression in humans.

Objectives: To test whether IRF2BP2 in macrophages affects atherosclerosis in mice and humans.

Methods and results: We generated mice that delete IRF2BP2 in macrophages. IRF2BP2-deficient macrophages worsened atherosclerosis in irradiated low-density lipoprotein receptor null-recipient mice and in apolipoprotein E null mice. IRF2BP2-deficient macrophages were inflammatory and had impaired cholesterol efflux because of their inability to activate the cholesterol transporter ABCA1 in response to cholesterol loading. Their expression of the anti-inflammatory transcription factor Krüppel-like factor 2 was markedly reduced. Promoter studies revealed that IRF2BP2 is required for MEF2-dependent activation of Krüppel-like factor 2. Importantly, restoring Krüppel-like factor 2 in IRF2BP2-deficient macrophages attenuated M1 inflammatory and rescued M2 anti-inflammatory gene activation and improved the cholesterol efflux deficit by restoring ABCA1 activation in response to cholesterol loading. In a cohort of 1066 angiographic cases and 1011 controls, homozygous carriers of a deletion polymorphism (rs3045215) in the 3' untranslated region sequence of human IRF2BP2 mRNA had a higher risk of coronary artery disease (recessive model, odds ratio [95% confidence interval]=1.560 [1.179-2.065], P=1.73E-03) and had lower IRF2BP2 (and Krüppel-like factor 2) protein levels in peripheral blood mononuclear cells. The effect of this deletion polymorphism to suppress protein expression was confirmed in luciferase reporter studies.

Conclusion: Ablation of IRF2BP2 in macrophages worsens atherosclerosis in mice, and a deletion variant that lowers IRF2BP2 expression predisposes to coronary artery disease in humans.

Keywords: 3′ untranslated region; atherosclerosis; cholesterol; coronary artery disease; genetics; macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • ATP Binding Cassette Transporter 1 / metabolism
  • Aged
  • Aged, 80 and over
  • Animals
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / prevention & control*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Case-Control Studies
  • Cells, Cultured
  • Cholesterol / metabolism*
  • Coronary Artery Disease / diagnostic imaging
  • Coronary Artery Disease / genetics
  • Coronary Artery Disease / metabolism
  • Coronary Artery Disease / prevention & control*
  • DNA-Binding Proteins
  • Disease Models, Animal
  • Female
  • Genetic Predisposition to Disease
  • Homozygote
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism
  • Inflammation / prevention & control*
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • MEF2 Transcription Factors / metabolism
  • Macrophage Activation*
  • Macrophages / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Odds Ratio
  • Phenotype
  • Polymorphism, Genetic
  • Promoter Regions, Genetic
  • Protective Factors
  • Radiography
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • Risk Factors
  • Transcription Factors / deficiency
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transfection

Substances

  • 3' Untranslated Regions
  • ABCA1 protein, mouse
  • ATP Binding Cassette Transporter 1
  • Apolipoproteins E
  • Carrier Proteins
  • DNA-Binding Proteins
  • IRF2BP2 protein, human
  • IRF2BP2 protein, mouse
  • KLF2 protein, human
  • Klf2 protein, mouse
  • Kruppel-Like Transcription Factors
  • MEF2 Transcription Factors
  • Nuclear Proteins
  • Receptors, LDL
  • Transcription Factors
  • Cholesterol