Nitric oxide inhibits Kv4.3 and human cardiac transient outward potassium current (Ito1)

Cardiovasc Res. 2008 Dec 1;80(3):375-84. doi: 10.1093/cvr/cvn205. Epub 2008 Aug 4.

Abstract

Aims: Chronic atrial fibrillation (CAF) is characterized by a shortening of the plateau phase of the action potentials (AP) and a decrease in the bioavailability of nitric oxide (NO). In this study, we analysed the effects of NO on Kv4.3 (I(Kv4.3)) and on human transient outward K(+) (I(to1)) currents as well as the signalling pathways responsible for them. We also analysed the expression of NO synthase 3 (NOS3) in patients with CAF.

Methods and results: I(Kv4.3) and I(to1) currents were recorded in Chinese hamster ovary cells and in human atrial and mouse ventricular dissociated myocytes using the whole-cell patch clamp. The expression of NOS3 was analysed by western blotting. AP were recorded using conventional microelectrode techniques in mouse atrial preparations. NO and NO donors inhibited I(Kv4.3) and human I(to1) in a concentration- and voltage-dependent manner (IC(50) for NO: 375.0 +/- 48 nM) as a consequence of the activation of adenylate cyclase and the subsequent activation of the cAMP-dependent protein kinase and the serine-threonine phosphatase 2A. The density of the I(to1) recorded in ventricular myocytes from wild-type (WT) and NOS3-deficient mice (NOS3(-/-)) was not significantly different. Furthermore, the duration of atrial AP repolarization in WT and NOS3(-/-) mice was not different. The increase in NO levels to 200 nM prolonged the plateau phase of the mouse atrial AP and lengthened the AP duration measured at 20 and 50% of repolarization of the human atrial CAF-remodelled AP as determined using a mathematical model. However, the expression of NOS3 was not modified in left atrial appendages from CAF patients.

Conclusion: Our results suggested that the increase in the atrial NO bioavailability could partially restore the duration of the plateau phase of CAF-remodelled AP by inhibiting the I(to1) as a result of the activation of non-canonical enzymatic pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Aged
  • Animals
  • Atrial Fibrillation / metabolism
  • Atrial Fibrillation / physiopathology
  • CHO Cells
  • Cells, Cultured
  • Chronic Disease
  • Cricetinae
  • Cricetulus
  • Female
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Theoretical
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type III / genetics
  • Nitric Oxide Synthase Type III / metabolism
  • Patch-Clamp Techniques
  • Shal Potassium Channels / antagonists & inhibitors*
  • Shal Potassium Channels / metabolism
  • Signal Transduction / physiology*

Substances

  • Shal Potassium Channels
  • Nitric Oxide
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse