Gal-3 (Galectin-3) and KCa3.1 Mediate Heterogeneous Cell Coupling and Myocardial Fibrogenesis Driven by βAR (β-Adrenoceptor) Activation

Hypertension. 2020 Feb;75(2):393-404. doi: 10.1161/HYPERTENSIONAHA.119.13696. Epub 2019 Dec 16.

Abstract

Heart failure is associated with sympatho-βAR (β-adrenoceptor) activation and cardiac fibrosis. Gal-3 (galectin-3) and KCa3.1 channels that are upregulated in diverse cells of diseased heart are implicated in mediating myocardial inflammation and fibrosis. It remains unclear whether Gal-3 interacts with KCa3.1 leading to cardiac fibrosis in the setting of βAR activation. We tested the effect of KCa3.1 blocker TRAM-34 on cardiac fibrosis and inflammation in cardiac-restricted β2-TG (β2AR overexpressed transgenic) mice and determined KCa3.1 expression in β2-TG×Gal-3-/- mouse hearts. Mechanisms of KCa3.1 in mediating Gal-3 induced fibroblast activation were studied ex vivo. Expression of Gal-3 and KCa3.1 was elevated in β2-TG hearts. Gal-3 gene deletion in β2-TG mice decreased KCa3.1 expression in inflammatory cells but not in fibroblasts. Treatment of β2-TG mice with TRAM-34 for 1 or 2 months significantly ameliorated cardiac inflammation and fibrosis and reduced Gal-3 level. In cultured fibroblasts, Gal-3 upregulated KCa3.1 expression and channel currents with enhanced membrane potential and Ca2+ entry through TRPV4 (transient receptor potential V4) and TRPC6 (transient receptor potential C6) channels leading to fibroblast activation. In conclusion, βAR stimulation promotes Gal-3 production that upregulates KCa3.1 channels in noncardiomyocyte cells and activates KCa3.1 channels in fibroblasts leading to hyperpolarization of membrane potential and Ca2+ entry via TRP channels. Gal-3-KCa3.1 signaling mobilizes diverse cells facilitating regional inflammation and fibroblast activation and hence myocardial fibrosis.

Keywords: fibroblast; fibrosis; galectin-3; heart failure; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cardiomyopathies / genetics*
  • Cardiomyopathies / metabolism
  • Cardiomyopathies / pathology
  • Cells, Cultured
  • Fibrosis / genetics
  • Fibrosis / metabolism
  • Fibrosis / pathology
  • Galectin 3 / biosynthesis
  • Galectin 3 / genetics*
  • Gene Expression Regulation*
  • Immunohistochemistry
  • Intermediate-Conductance Calcium-Activated Potassium Channels / biosynthesis
  • Intermediate-Conductance Calcium-Activated Potassium Channels / genetics*
  • Male
  • Mice
  • Mice, Transgenic
  • RNA / genetics*
  • RNA Splicing
  • Receptors, Adrenergic, beta-2 / biosynthesis
  • Receptors, Adrenergic, beta-2 / genetics*
  • Signal Transduction

Substances

  • Galectin 3
  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Kcnn4 protein, mouse
  • Lgals3 protein, mouse
  • Receptors, Adrenergic, beta-2
  • RNA