CCR5+T-bet+FoxP3+ Effector CD4 T Cells Drive Atherosclerosis

Circ Res. 2016 May 13;118(10):1540-52. doi: 10.1161/CIRCRESAHA.116.308648. Epub 2016 Mar 28.

Abstract

Rationale: CD4 T cells are involved in the pathogenesis of atherosclerosis, but atherosclerosis-specific CD4 T cells have not been described. Moreover, the chemokine(s) that regulates T-cell trafficking to the atherosclerotic lesions is also unknown.

Objective: In Apoe(-/-) mice with mature atherosclerotic lesions (5 months of high fat diet), we find that most aortic T cells express CCR5 and interferon-γ with a unique combination of cell surface markers (CD4(+)CD25(-)CD44(hi)CD62L(lo)) and transcription factors (FoxP3(+)T-bet(+)). We call these cells CCR5Teff. We investigated the role of CCR5 in regulating T-cell homing to the atherosclerotic aorta and the functionality of the CCR5Teff cells.

Methods and results: CCR5Teff cells are exclusively found in the aorta and para-aortic lymph nodes of Apoe(-/-) mice. They do not suppress T-cell proliferation in vitro and are less potent than regulatory T cells at inhibiting cytokine secretion. Blocking or knocking out CCR5 or its ligand CCL5 significantly blocks T-cell homing to atherosclerotic aortas. Transcriptomic analysis shows that CCR5Teff cells are more similar to effector T cells than to regulatory T cells. They secrete interferon-γ, interleukin-2, interleukin-10, and tumor necrosis factor. Adoptive transfer of these CCR5Teff cells significantly increases atherosclerosis.

Conclusions: CCR5 is specifically needed for CD4 T-cell homing to the atherosclerotic plaques. CCR5(+)CD4 T cells express an unusual combination of transcription factors, FoxP3 and T-bet. Although CCR5Teff express FoxP3, we showed that they are not regulatory and adoptive transfer of these cells exacerbates atherosclerosis.

Keywords: CCR5 protein, mouse; Ccl5 protein, mouse; Treg cells; atherosclerosis; chemokines; inflammation; vascular diseases.

Publication types

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

MeSH terms

  • Animals
  • Aorta / metabolism
  • Aorta / pathology
  • Apolipoproteins E / genetics
  • Apolipoproteins E / metabolism
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • CD4-Positive T-Lymphocytes / metabolism*
  • CD4-Positive T-Lymphocytes / physiology
  • Cell Proliferation
  • Cells, Cultured
  • Endothelial Cells / metabolism*
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism*
  • Hyaluronan Receptors / genetics
  • Hyaluronan Receptors / metabolism
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Interleukins / metabolism
  • L-Selectin / genetics
  • L-Selectin / metabolism
  • Mice
  • Receptors, CCR5 / genetics
  • Receptors, CCR5 / metabolism*
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism*

Substances

  • Apolipoproteins E
  • CCR5 protein, mouse
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Hyaluronan Receptors
  • Interleukin-2 Receptor alpha Subunit
  • Interleukins
  • Receptors, CCR5
  • T-Box Domain Proteins
  • T-box transcription factor TBX21
  • L-Selectin
  • Interferon-gamma