KCa3.1 Channels Promote Cardiac Fibrosis Through Mediating Inflammation and Differentiation of Monocytes Into Myofibroblasts in Angiotensin II -Treated Rats

J Am Heart Assoc. 2019 Jan 8;8(1):e010418. doi: 10.1161/JAHA.118.010418.

Abstract

Background Cardiac fibrosis is a core pathological process associated with heart failure. The recruitment and differentiation of primitive fibroblast precursor cells of bone marrow origin play a critical role in pathological interstitial cardiac fibrosis. The KCa3.1 channels are expressed in both ventricular fibroblasts and circulating mononuclear cells in rats and are upregulated by angiotensin II . We hypothesized that KCa3.1 channels mediate the inflammatory microenvironment in the heart, promoting the infiltrated bone marrow-derived circulating mononuclear cells to differentiate into myofibroblasts, leading to myocardial fibrosis. Methods and Results We established a cardiac fibrosis model in rats by infusing angiotensin II to evaluate the impact of the specific KCa3.1 channel blocker TRAM -34 on cardiac fibrosis. At the same time, mouse CD 4+ T cells and rat circulating mononuclear cells were separated to investigate the underlying mechanism of the TRAM -34 anti-cardiac fibrosis effect. TRAM -34 significantly attenuated cardiac fibrosis and the inflammatory reaction and reduced the number of fibroblast precursor cells and myofibroblasts. Inhibition of KCa3.1 channels suppressed angiotensin II -stimulated expression and secretion of interleukin-4 and interleukin-13 in CD 4+ T cells and interleukin-4- or interleukin-13-induced differentiation of monocytes into fibrocytes. Conclusions KCa3.1 channels facilitate myocardial inflammation and the differentiation of bone marrow-derived monocytes into myofibroblasts in cardiac fibrosis caused by angiotensin II infusion.

Keywords: K‐channel; angiotensin II; cardiac remodeling; differentiation; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / toxicity
  • Animals
  • Blotting, Western
  • Cardiomyopathies / genetics*
  • Cardiomyopathies / metabolism
  • Cardiomyopathies / pathology
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Fibrosis / genetics
  • Fibrosis / metabolism
  • Fibrosis / pathology
  • Gene Expression Regulation*
  • Heart Ventricles / metabolism
  • Heart Ventricles / pathology
  • Immunohistochemistry
  • Inflammation / genetics*
  • Inflammation / metabolism
  • Inflammation / pathology
  • Intermediate-Conductance Calcium-Activated Potassium Channels / biosynthesis
  • Intermediate-Conductance Calcium-Activated Potassium Channels / genetics*
  • Male
  • Monocytes / metabolism
  • Monocytes / pathology*
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Myofibroblasts / metabolism
  • Myofibroblasts / pathology
  • RNA / genetics
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Kcnn4 protein, rat
  • Angiotensin II
  • RNA