Angiotensin II upregulates Kv1.5 expression through ROS-dependent transforming growth factor-beta1 and extracellular signal-regulated kinase 1/2 signalings in neonatal rat atrial myocytes

Biochem Biophys Res Commun. 2014 Nov 21;454(3):410-6. doi: 10.1016/j.bbrc.2014.10.088. Epub 2014 Oct 24.

Abstract

Kv1.5 potassium channel represents a promising target for atrial fibrillation (AF) therapy. During AF, the renin-angiotensin system is markedly activated. Recent evidence indicates that angiotensin II (Ang II) can upregulate Kv1.5 channel, but the mechanism remains unknown. In this study, we report that Ang II-mediated transforming growth factor-beta1 (TGF-β1)/Smad2/3 and extracellular signal-regulated kinase (ERK) 1/2 signalings are involved in atrial Kv1.5 expression. In neonatal rat atrial myocytes, quantitative PCR and Western blotting revealed that Ang II upregulated TGF-β1, synapse-associated protein 97 (SAP97) and Kv1.5 expression in a time- and concentration-dependent manner. The Ang II-induced upregulation of Kv1.5, SAP97 and phosphorylated Smad2/3 (P-Smad2/3) were reversed by the Ang II type 1 (AT1) receptor antagonist losartan, an anti-TGF-β1 antibody and the ERK 1/2 inhibitor PD98059 but not by the AT2 receptor antagonist PD123319. mRNA knockdown of either Smad2 or Smad3 blocked Ang II-induced expression of Kv1.5 and SAP97. These data suggest that AT1 receptor/TGF-β1/P-Smad2/3 and ERK 1/2 signalings are involved in Ang II-induced Kv1.5 and SAP97 expression. Flow cytometry and Western blotting revealed that losartan and the anti-TGF-β1 antibody diminished Ang II-induced reactive oxygen species (ROS) generation and that the antioxidants diphenyleneiodonium and N-acetyl cysteine inhibited Ang II-induced expression of P-Smad2/3, phosphorylated ERK (P-ERK) 1/2, Kv1.5, SAP97, suggesting that ROS participate in Kv1.5 and SAP97 regulation by modulating Ang II-induced P-Smad2/3 and P-ERK 1/2 expression. In conclusion, we demonstrate that ROS-dependent Ang II/AT1 receptor/TGF-β1/P-Smad2/3 and Ang II/ERK 1/2 signalings are involved in atrial Kv1.5 and SAP97 expression. Antioxidants would be beneficial for AF treatment through inhibiting atrial Kv1.5 expression.

Keywords: Angiotensin II; Antioxidant; ERK 1/2; Kv1.5; ROS; TGF-β(1).

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Angiotensin II / metabolism*
  • Animals
  • Cells, Cultured
  • Heart Atria / cytology
  • Heart Atria / metabolism
  • Kv1.5 Potassium Channel / genetics*
  • MAP Kinase Signaling System*
  • Membrane Proteins / genetics
  • Myocytes, Cardiac / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Receptor, Angiotensin, Type 1 / metabolism
  • Signal Transduction
  • Smad2 Protein / genetics
  • Smad3 Protein / genetics
  • Transforming Growth Factor beta1 / metabolism*
  • Up-Regulation*

Substances

  • Adaptor Proteins, Signal Transducing
  • Dlg1 protein, rat
  • Kv1.5 Potassium Channel
  • Membrane Proteins
  • Reactive Oxygen Species
  • Receptor, Angiotensin, Type 1
  • Smad2 Protein
  • Smad2 protein, rat
  • Smad3 Protein
  • Smad3 protein, rat
  • Transforming Growth Factor beta1
  • Angiotensin II