Chronic skin inflammation accelerates macrophage cholesterol crystal formation and atherosclerosis

JCI Insight. 2018 Jan 11;3(1):e97179. doi: 10.1172/jci.insight.97179.

Abstract

Inflammation is critical to atherogenesis. Psoriasis is a chronic inflammatory skin disease that accelerates atherosclerosis in humans and provides a compelling model to understand potential pathways linking these diseases. A murine model capturing the vascular and metabolic diseases in psoriasis would accelerate our understanding and provide a platform to test emerging therapies. We aimed to characterize a new murine model of skin inflammation (Rac1V12) from a cardiovascular standpoint to identify novel atherosclerotic signaling pathways modulated in chronic skin inflammation. The RacV12 psoriasis mouse resembled the human disease state, including presence of systemic inflammation, dyslipidemia, and cardiometabolic dysfunction. Psoriasis macrophages had a proatherosclerotic phenotype with increased lipid uptake and foam cell formation, and also showed a 6-fold increase in cholesterol crystal formation. We generated a triple-genetic K14-RacV12-/+/Srb1-/-/ApoER61H/H mouse and confirmed psoriasis accelerates atherogenesis (~7-fold increase). Finally, we noted a 60% reduction in superoxide dismutase 2 (SOD2) expression in human psoriasis macrophages. When SOD2 activity was restored in macrophages, their proatherogenic phenotype reversed. We demonstrate that the K14-RacV12 murine model captures the cardiometabolic dysfunction and accelerates vascular disease observed in chronic inflammation and that skin inflammation induces a proatherosclerotic macrophage phenotype with impaired SOD2 function, which associated with accelerated atherogenesis.

Keywords: Atherosclerosis; Cardiology; Cardiovascular disease; Inflammation; Macrophages.

Publication types

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

MeSH terms

  • Adolescent
  • Animals
  • Atherosclerosis / genetics
  • Atherosclerosis / immunology*
  • Cardiovascular Diseases / immunology
  • Child
  • Cholesterol / metabolism*
  • Cytokines / metabolism
  • Disease Models, Animal
  • Dyslipidemias
  • Female
  • Foam Cells
  • Humans
  • Inflammation / immunology*
  • Keratinocytes / metabolism
  • Macrophages / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Multivariate Analysis
  • Neuropeptides / metabolism
  • Psoriasis / immunology*
  • Regression Analysis
  • Skin / immunology*
  • Superoxide Dismutase / metabolism
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Cytokines
  • Neuropeptides
  • Rac1 protein, mouse
  • Cholesterol
  • Superoxide Dismutase
  • superoxide dismutase 2
  • rac1 GTP-Binding Protein