Changes in I K, ACh single-channel activity with atrial tachycardia remodelling in canine atrial cardiomyocytes

Cardiovasc Res. 2008 Jan;77(1):35-43. doi: 10.1093/cvr/cvm051. Epub 2007 Oct 26.

Abstract

Aims: Although atrial tachycardia (AT) remodelling promotes agonist-independent, constitutively active, acetylcholine-regulated K+-current (I K,ACh) that increases susceptibility to atrial fibrillation (AF), the underlying changes in I K,Ach channel function are unknown. This study aimed to establish how AT remodelling affects I K,ACh single-channel function.

Methods and results: I K,ACh single-channel activity was studied via cell-attached patch-clamp in isolated left atrial cardiomyocytes of control and AT (7 days, 400 min(-1)) dogs. Atrial tachycardia prolonged the mean duration of induced AF from 44 +/- 22 to 413 +/- 167 s, and reduced atrial effective refractory period at a 360 ms cycle length from 126 +/- 3 to 74 +/- 5 ms (n = 9/group, P < 0.001). In the absence of cholinergic stimulation, single-channel openings with typical I K,ACh conductance and rectification properties were sparse under control conditions. Atrial tachycardia induced prominent agonist-independent I K,ACh activity because of increased opening frequency (fo) and open probability (Po: approximately seven- and 10-fold, respectively, vs. control), but did not alter open time-constant, single-channel conductance, and membrane density. With maximum I K,ACh activation (10 micromol/L carbachol), channel Po was enhanced much more in control cells ( approximately 42-fold) than in AT-remodelled myocytes (approximately five-fold). The selective Kir3 current blocker tertiapin-Q (100 nmol/L) reduced fo and Po at -100 mV by 48 and 51%, respectively (P < 0.05 for each), without altering other channel properties, confirming the identity of I K,ACh. Atrial tachycardia had no significant effect on mRNA or protein expression of either of the subunits (Kir3.1, Kir3.4) underlying I K,ACh.

Conclusion: Atrial tachycardia increases agonist-independent constitutive I K,ACh single-channel activity by enhancing spontaneous channel opening, providing a molecular basis for AT effects on macroscopic I K,ACh observed in previous studies, as well as associated refractoriness abbreviation and tertiapin-suppressible AF promotion. These results suggest an important role for constitutive I K,Ach channel opening in AT remodelling and support its interest as a potential target for AF therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology*
  • Animals
  • Atrial Fibrillation / etiology
  • Bee Venoms / pharmacology
  • Carbachol / pharmacology
  • Dogs
  • Female
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / analysis
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / physiology
  • Heart Atria
  • Male
  • Myocytes, Cardiac / metabolism*
  • Potassium Channels, Inwardly Rectifying / drug effects
  • Potassium Channels, Inwardly Rectifying / physiology*
  • Tachycardia / complications
  • Tachycardia / metabolism*

Substances

  • Bee Venoms
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • tertiapin
  • Carbachol
  • Acetylcholine