Loss of Id3 increases VCAM-1 expression, macrophage accumulation, and atherogenesis in Ldlr-/- mice

Arterioscler Thromb Vasc Biol. 2012 Dec;32(12):2855-61. doi: 10.1161/ATVBAHA.112.300352. Epub 2012 Oct 4.

Abstract

Objective: Inhibitor of differention-3 (Id3) promotes B cells homing to the aorta and atheroprotection in Apoe(-/-) mice. We sought to determine the impact of loss of Id3 in the Ldlr((-/-)) mouse model of diet-induced atherosclerosis and identify novel Id3 targets in the vessel wall.

Methods and results: Ex vivo optical imaging confirmed that Id3((-/-)) Ldlr((-/-)) mice have significantly fewer aortic B cells than Id3((+/+)) Ldlr(-/-) mice. After 8 and 16 weeks of Western diet, Id3((-/-)) Ldlr((-/-)) mice developed significantly more atherosclerosis than Id3((+/+)) Ldlr((-/-)) mice, with Id3(+/-) Ldlr(-/-) mice demonstrating an intermediate phenotype. There were no differences in serum lipid levels between genotypes. Immunostaining demonstrated that aortas from Id3((-/-)) Ldlr((-/-)) mice had greater intimal macrophage density and C-C chemokine ligand 20 and vascular cell adhesion molecule 1 (VCAM-1) expression compared with Id3((+/+)) Ldlr(-/-) mice. Real-time polymerase chain reaction demonstrated increased VCAM-1 mRNA levels in the aortas of Id3(-/-) Ldlr(-/-) mice. Primary vascular smooth muscle cells from Id3((-/-)) mice expressed greater amounts of VCAM-1 protein compared with control. Gain and loss of function studies in primary vascular smooth muscle cells identified a role for Id3 in repressing VCAM-1 promoter activation. Chromatin immunoprecipitation demonstrated interaction of E12 with the VCAM-1 promoter, which is inhibited by Id3.

Conclusions: Id3 is an atheroprotective transcription regulator with targets in both B cells and vessel wall cells leading to reduced macrophage accumulation and reduced atherosclerosis formation.

Publication types

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

MeSH terms

  • Animals
  • Aorta / metabolism
  • Aorta / pathology
  • Atherosclerosis / epidemiology
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Atherosclerosis / physiopathology*
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • Cell Movement / physiology*
  • Cell Proliferation*
  • Chemokine CCL20 / metabolism
  • Disease Models, Animal
  • Inhibitor of Differentiation Proteins / deficiency*
  • Inhibitor of Differentiation Proteins / genetics
  • Inhibitor of Differentiation Proteins / metabolism
  • Macrophages / metabolism
  • Macrophages / pathology*
  • Mice
  • Mice, Knockout
  • Prevalence
  • Receptors, LDL / deficiency*
  • Receptors, LDL / genetics
  • Receptors, LDL / metabolism
  • Risk Factors
  • Vascular Cell Adhesion Molecule-1 / metabolism*

Substances

  • CCL20 protein, mouse
  • Chemokine CCL20
  • Inhibitor of Differentiation Proteins
  • Receptors, LDL
  • Vascular Cell Adhesion Molecule-1
  • Idb3 protein, mouse