Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells

Circulation. 2006 May 16;113(19):2301-12. doi: 10.1161/CIRCULATIONAHA.105.605121. Epub 2006 May 8.

Abstract

Background: Studies to define the overall contribution of lymphocytes to lesion formation in atherosclerosis-susceptible mice have demonstrated relatively subtle effects; the use of lymphocyte-deficient mice, however, compromises both the effector and regulatory arms of the immune system. Here, we tested the hypothesis that deletion of CXCL10 (IP-10), a chemokine specific for effector T cells that has been localized within atherosclerotic lesions, would significantly inhibit atherogenesis.

Methods and results: Compound deficient Apoe(-/-)/Cxcl10(-/-) mice fed a Western-style diet for either 6 or 12 weeks demonstrated significant reductions in atherogenesis as compared with Apoe(-/-) controls, as assessed by both aortic en face and cross-sectional analyses. Immunohistochemical studies revealed a decrease in the accumulation of CD4+ T cells, whereas quantitative polymerase chain reaction analysis of lesion-rich aortic arches demonstrated a marked reduction in mRNA for CXCR3, the CXCL10 chemokine receptor. Although overall T-cell accumulation was diminished significantly, we found evidence to suggest that regulatory T-cell (Treg) numbers and activity were enhanced, as assessed by increased message for the Treg-specific marker Foxp3, as well as increases in immunostaining for the Treg-associated cytokines interleukin-10 and transforming growth factor-beta1. We also documented naturally occurring Treg cells in human atherosclerotic lesions.

Conclusions: We provide novel evidence for a functional role for the effector T-cell chemoattractant CXCL10 in atherosclerotic lesion formation by modulating the local balance of the effector and regulatory arms of the immune system.

Publication types

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

MeSH terms

  • Animals
  • Aorta / pathology
  • Apolipoproteins E / analysis
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / physiology
  • Atherosclerosis / pathology
  • Atherosclerosis / physiopathology*
  • CD4 Lymphocyte Count
  • CD4-Positive T-Lymphocytes / chemistry
  • CD4-Positive T-Lymphocytes / physiology
  • Chemokine CXCL10
  • Chemokines, CXC / analysis
  • Chemokines, CXC / deficiency
  • Chemokines, CXC / genetics
  • Chemokines, CXC / physiology*
  • Coronary Artery Disease / etiology
  • Coronary Artery Disease / pathology*
  • Coronary Artery Disease / physiopathology*
  • Coronary Vessels / pathology
  • Flow Cytometry
  • Forkhead Transcription Factors / analysis
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / physiology
  • Immunohistochemistry
  • Interleukin-10 / analysis
  • Interleukin-10 / genetics
  • Interleukin-10 / physiology
  • Mice
  • Mice, Mutant Strains
  • Polymerase Chain Reaction
  • RNA, Messenger / analysis
  • RNA, Messenger / genetics
  • Receptors, CXCR3
  • Receptors, Chemokine / analysis
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / physiology
  • Signal Transduction / physiology
  • T-Lymphocytes / chemistry
  • T-Lymphocytes / physiology*
  • Transforming Growth Factor beta / analysis
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / physiology
  • Transforming Growth Factor beta1

Substances

  • Apolipoproteins E
  • CXCR3 protein, human
  • Chemokine CXCL10
  • Chemokines, CXC
  • Cxcr3 protein, mouse
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • RNA, Messenger
  • Receptors, CXCR3
  • Receptors, Chemokine
  • TGFB1 protein, human
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Interleukin-10