Interleukin 17 drives vascular inflammation, endothelial dysfunction, and arterial hypertension in psoriasis-like skin disease

Arterioscler Thromb Vasc Biol. 2014 Dec;34(12):2658-68. doi: 10.1161/ATVBAHA.114.304108. Epub 2014 Oct 23.

Abstract

Objective: Interleukin (IL)-17A is regarded as an important cytokine to drive psoriasis, an inflammatory skin disease marked by increased cardiovascular mortality. We aimed to test the hypothesis that overproduction of IL-17A in the skin leading to dermal inflammation may systemically cause vascular dysfunction in psoriasis-like skin disease.

Approach and results: Conditional overexpression of IL-17A in keratinocytes caused severe psoriasis-like skin inflammation in mice (K14-IL-17A(ind/+) mice), associated with increased reactive oxygen species formation and circulating CD11b(+) inflammatory leukocytes in blood, with endothelial dysfunction, increased systolic blood pressure, left ventricular hypertrophy, and reduced survival compared with controls. In K14-IL-17A(ind/+) mice, immunohistochemistry and flow cytometry revealed increased vascular production of the nitric oxide/superoxide reaction product peroxynitrite and infiltration of the vasculature with myeloperoxidase(+)CD11b(+)GR1(+)F4/80(-) cells accompanied by increased expression of the inducible nitric oxide synthase and the nicotinamide dinucleotide phosphate (NADPH) oxidase, nox2. Neutrophil depletion by anti-GR-1 antibody injections reduced oxidative stress in blood and vessels. Neutralization of tumor necrosis factor-α and IL-6 (both downstream of IL-17A) reduced skin lesions, attenuated oxidative stress in heart and blood, and partially improved endothelial dysfunction in K14-IL-17A(ind/+) mice.

Conclusions: Dermal overexpression of IL-17A induces systemic endothelial dysfunction, vascular oxidative stress, arterial hypertension, and increases mortality mainly driven by myeloperoxidase(+)CD11b(+)GR1(+)F4/80(-) inflammatory cells. Depletion of the GR-1(+) immune cells or neutralization of IL-17A downstream cytokines by biologicals attenuates the vascular phenotype in K14-IL-17A(ind/+) mice.

Keywords: animal model of human disease; immune system; inflammation; vascular dysfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Aorta / pathology
  • Cardiovascular Diseases / etiology
  • Case-Control Studies
  • Disease Models, Animal
  • Endothelium, Vascular / immunology
  • Endothelium, Vascular / physiopathology
  • Female
  • Humans
  • Hypertension / etiology
  • Hypertension / immunology
  • Hypertension / physiopathology
  • Interleukin-17 / genetics
  • Interleukin-17 / physiology*
  • Interleukin-6 / antagonists & inhibitors
  • Interleukin-6 / physiology
  • Keratinocytes / immunology
  • Keratinocytes / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Middle Aged
  • Myocytes, Cardiac / pathology
  • Neutrophils / pathology
  • Neutrophils / physiology
  • Nitric Oxide / metabolism
  • Psoriasis / complications
  • Psoriasis / etiology*
  • Psoriasis / physiopathology*
  • Reactive Oxygen Species / metabolism
  • Risk Factors
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / physiology
  • Up-Regulation
  • Vasculitis / etiology
  • Vasculitis / immunology
  • Vasculitis / physiopathology

Substances

  • IL17A protein, human
  • Il17a protein, mouse
  • Interleukin-17
  • Interleukin-6
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • Nitric Oxide