Lim domain binding 2: a key driver of transendothelial migration of leukocytes and atherosclerosis

Arterioscler Thromb Vasc Biol. 2014 Sep;34(9):2068-77. doi: 10.1161/ATVBAHA.113.302709. Epub 2014 Jun 12.

Abstract

Objective: Using a multi-tissue, genome-wide gene expression approach, we recently identified a gene module linked to the extent of human atherosclerosis. This atherosclerosis module was enriched with inherited risk for coronary and carotid artery disease (CAD) and overlapped with genes in the transendothelial migration of leukocyte (TEML) pathway. Among the atherosclerosis module genes, the transcription cofactor Lim domain binding 2 (LDB2) was the most connected in a CAD vascular wall regulatory gene network. Here, we used human genomics and atherosclerosis-prone mice to evaluate the possible role of LDB2 in TEML and atherosclerosis.

Approach and results: mRNA profiles generated from blood macrophages in patients with CAD were used to infer transcription factor regulatory gene networks; Ldlr(-/-)Apob(100/100) mice were used to study the effects of Ldb2 deficiency on TEML activity and atherogenesis. LDB2 was the most connected gene in a transcription factor regulatory network inferred from TEML and atherosclerosis module genes in CAD macrophages. In Ldlr(-/-)Apob(100/100) mice, loss of Ldb2 increased atherosclerotic lesion size ≈2-fold and decreased plaque stability. The exacerbated atherosclerosis was caused by increased TEML activity, as demonstrated in air-pouch and retinal vasculature models in vivo, by ex vivo perfusion of primary leukocytes, and by leukocyte migration in vitro. In THP1 cells, migration was increased by overexpression and decreased by small interfering RNA inhibition of LDB2. A functional LDB2 variant (rs10939673) was associated with the risk and extent of CAD across several cohorts.

Conclusions: As a key driver of the TEML pathway in CAD macrophages, LDB2 is a novel candidate to target CAD by inhibiting the overall activity of TEML.

Keywords: atherosclerosis; coronary artery disease; gene regulatory networks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoprotein B-100 / genetics
  • Atherosclerosis / physiopathology*
  • Carotid Artery Diseases / genetics
  • Carotid Artery Diseases / pathology*
  • Cell Line, Tumor
  • Chemokine CCL2 / pharmacology
  • Chemotaxis, Leukocyte / physiology*
  • Coronary Artery Disease / genetics
  • Coronary Artery Disease / pathology*
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Genome-Wide Association Study
  • Humans
  • LIM Domain Proteins / deficiency
  • LIM Domain Proteins / genetics
  • LIM Domain Proteins / physiology*
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • RNA, Messenger / biosynthesis
  • Transcription Factors / deficiency
  • Transcription Factors / genetics
  • Transcription Factors / physiology*
  • Transendothelial and Transepithelial Migration / genetics
  • Transendothelial and Transepithelial Migration / physiology*

Substances

  • Apolipoprotein B-100
  • Chemokine CCL2
  • LDB2 protein, human
  • LIM Domain Proteins
  • Ldb2 protein, mouse
  • RNA, Messenger
  • Transcription Factors