Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis

J Clin Invest. 2013 Mar;123(3):1323-34. doi: 10.1172/JCI63891. Epub 2013 Feb 15.

Abstract

Atherosclerosis is a chronic inflammatory disease promoted by hyperlipidemia. Several studies support FOXP3-positive regulatory T cells (Tregs) as inhibitors of atherosclerosis; however, the mechanism underlying this protection remains elusive. To define the role of FOXP3-expressing Tregs in atherosclerosis, we used the DEREG mouse, which expresses the diphtheria toxin (DT) receptor under control of the Treg-specific Foxp3 promoter, allowing for specific ablation of FOXP3+ Tregs. Lethally irradiated, atherosclerosis-prone, low-density lipoprotein receptor-deficient (Ldlr(-/-)) mice received DEREG bone marrow and were injected with DT to eliminate FOXP3(+) Tregs. Depletion of Tregs caused a 2.1-fold increase in atherosclerosis without a concomitant increase in vascular inflammation. These mice also exhibited a 1.7-fold increase in plasma cholesterol and an atherogenic lipoprotein profile with increased levels of VLDL. Clearance of VLDL and chylomicron remnants was hampered, leading to accumulation of cholesterol-rich particles in the circulation. Functional and protein analyses complemented by gene expression array identified reduced protein expression of sortilin-1 in liver and increased plasma enzyme activity of lipoprotein lipase, hepatic lipase, and phospholipid transfer protein as mediators of the altered lipid phenotype. These results demonstrate that FOXP3(+) Tregs inhibit atherosclerosis by modulating lipoprotein metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta / pathology
  • Atherosclerosis / blood
  • Atherosclerosis / immunology*
  • Atherosclerosis / pathology
  • Cells, Cultured
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism*
  • Hypercholesterolemia / blood
  • Hypercholesterolemia / immunology*
  • Hypercholesterolemia / pathology
  • Lipase / metabolism
  • Lipid Metabolism / genetics
  • Lipids / blood
  • Lipoproteins, VLDL / biosynthesis
  • Liver / enzymology
  • Liver / metabolism
  • Lymphocyte Depletion
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Oligonucleotide Array Sequence Analysis
  • Phospholipid Transfer Proteins / blood
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • T-Lymphocytes, Regulatory / metabolism*
  • Transcriptome

Substances

  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Lipids
  • Lipoproteins, VLDL
  • Phospholipid Transfer Proteins
  • Receptors, LDL
  • phospholipid transfer protein, mouse
  • Lipase

Associated data

  • GEO/GSE36279
  • GEO/GSE39351