T Cell-Derived IL-17A Induces Vascular Dysfunction via Perivascular Fibrosis Formation and Dysregulation of ·NO/cGMP Signaling

Oxid Med Cell Longev. 2019 Jul 18:2019:6721531. doi: 10.1155/2019/6721531. eCollection 2019.

Abstract

Aims: The neutrophil recruiting cytokine Interleukin-17A (IL-17A) is a key component in vascular dysfunction and arterial hypertension. Moreover, IL-17A has a central role for the vascular infiltration of myeloid cells into the arterial wall in Angiotensin II-induced vascular inflammation. The intention of our study was to analyze the impact of T cell-derived IL-17A on hypertension, vascular function, and inflammation.

Methods and results: Chronic IL-17A overexpression in T cells (CD4-IL-17Aind/+ mice) resulted in elevated reactive oxygen species in the peripheral blood and a significant vascular dysfunction compared to control mice. The vascular dysfunction seen in the CD4-IL-17Aind/+ mice was only accompanied by a modest and nonsignificant accumulation of inflammatory cells within the vessel wall. Therefore, infiltrating myeloid cells did not serve as an explanation of the vascular dysfunction seen in a chronic IL-17A-driven mouse model. In addition to vascular dysfunction, CD4-IL-17Aind/+ mice displayed vascular fibrosis with highly proliferative fibroblasts. This fibroblast proliferation was induced by exposure to IL-17A as confirmed by in vitro experiments with primary murine fibroblastic cells. We also found that the ·NO/cGMP pathway was downregulated in the vasculature of the CD4-IL-17Aind/+ mice, while levels of protein tyrosine kinase 2 (PYK2), an oxidative stress-triggered process associated with T cell activation, were upregulated in the perivascular fat tissue (PVAT).

Conclusions: Our data demonstrate that T cell-derived IL-17A elicits vascular dysfunction by mediating proliferation of fibroblasts and subsequent vascular fibrosis associated with PYK2 upregulation.

MeSH terms

  • Animals
  • Aorta / metabolism
  • Aorta / pathology
  • Cell Proliferation
  • Cyclic GMP / metabolism*
  • Down-Regulation
  • Endothelium, Vascular / physiopathology*
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Fibrosis
  • Focal Adhesion Kinase 2 / metabolism
  • Interleukin-17 / genetics
  • Interleukin-17 / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nitric Oxide / metabolism*
  • Protein Subunits / metabolism
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Soluble Guanylyl Cyclase / metabolism
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • Up-Regulation

Substances

  • Interleukin-17
  • Protein Subunits
  • Reactive Oxygen Species
  • Nitric Oxide
  • Focal Adhesion Kinase 2
  • Soluble Guanylyl Cyclase
  • Cyclic GMP