Characterization of a hyperpolarization-activated time-dependent potassium current in canine cardiomyocytes from pulmonary vein myocardial sleeves and left atrium

J Physiol. 2004 Jun 1;557(Pt 2):583-97. doi: 10.1113/jphysiol.2004.061119. Epub 2004 Mar 12.

Abstract

Cardiomyocytes from the pulmonary vein sleeves (PVs) are known to play an important role in atrial fibrillation. PVs have been shown to exhibit time-dependent hyperpolarization-induced inward currents of uncertain nature. We observed a time-dependent K(+) current upon hyperpolarization of PV and left atrial (LA) cardiomyocytes (I(KH)) and characterized its biophysical and pharmacological properties. The activation time constant was weakly voltage dependent, ranging from 386 +/- 14 to 427 +/- 37 ms between -120 and -90 mV, and the half-activation voltage averaged -93 +/- 4 mV. I(KH) was larger in PV than LA cells (e.g. at -120 mV: -2.8 +/- 0.3 versus-1.9 +/- 0.2 pA pF(-1), respectively, P < 0.01). The reversal potential was approximately -84 mV with 5.4 mm[K(+)](o) and changed by 55.7 +/- 2.4 mV per decade [K(+)](o) change. I(KH) was exquisitely Ba(2+) sensitive, with a 50% inhibitory concentration (IC(50)) of 2.0 +/- 0.3 microm (versus 76.0 +/- 17.9 microm for instantaneous inward-rectifier current, P < 0.01), and showed similar Cs(+) sensitivity to instantaneous current. I(KH) was potently blocked by tertiapin-Q, a selective Kir3-subunit channel blocker (IC(50) 10.0 +/- 2.1 nm), was unaffected by atropine and was significantly increased by isoproterenol (isoprenaline), carbachol and the non-hydrolysable guanosine triphosphate analogue GTPgammaS. I(KH) activation by carbachol required GTP in the pipette and was prevented by pertussis toxin pretreatment. Tertiapin-Q delayed repolarization in atropine-exposed multicellular atrial preparations studied with standard microelectrodes (action potential duration pre- versus post-tertiapin-Q: 190.4 +/- 4.3 versus 234.2 +/- 9.9 ms, PV; 202.6 +/- 2.6 versus 242.7 +/- 6.2 ms, LA; 2 Hz, P < 0.05 each). Seven-day atrial tachypacing significantly increased I(KH) (e.g. at -120 mV in PV: from -2.8 +/- 0.3 to -4.5 +/- 0.5 pA pF(-1), P < 0.01). We conclude that I(KH) is a time-dependent, hyperpolarization-activated K(+) current that likely involves Kir3 subunits and appears to play a significant role in atrial physiology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • Atropine / pharmacology
  • Barium / pharmacology
  • Bee Venoms / pharmacology
  • Cardiotonic Agents / pharmacology
  • Cesium / pharmacology
  • Dogs
  • Electric Conductivity
  • Female
  • Fluorescent Antibody Technique
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • GTP-Binding Proteins / metabolism
  • Heart Atria
  • Isoproterenol / pharmacology
  • Male
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology*
  • Patch-Clamp Techniques
  • Physical Conditioning, Animal
  • Potassium Channels, Inwardly Rectifying / antagonists & inhibitors
  • Potassium Channels, Inwardly Rectifying / chemistry
  • Potassium Channels, Inwardly Rectifying / physiology*
  • Pulmonary Veins
  • Tachycardia, Ectopic Atrial / physiopathology
  • Time Factors

Substances

  • Bee Venoms
  • Cardiotonic Agents
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • Cesium
  • Barium
  • tertiapin
  • Atropine
  • GTP-Binding Proteins
  • Isoproterenol