Regional increase in extracellular potassium can be arrhythmogenic due to nonuniform muscle contraction in rat ventricular muscle

Am J Physiol Heart Circ Physiol. 2012 Jun 1;302(11):H2301-9. doi: 10.1152/ajpheart.01161.2011. Epub 2012 Mar 23.

Abstract

In the ischemic myocardium, extracellular potassium ([K(+)](o)) increases to ≥20 mmol/l. To determine how lethal arrhythmias occur during ischemia, we investigated whether the increased spatial pattern of [K(+)](o), i.e., a regional or a global increase, affects the incidence of arrhythmias. Force, sarcomere length, membrane potential, and nonuniform intracellular Ca(2+) ([Ca(2+)](i)) were measured in rat ventricular trabeculae. A "regional" or "global" increase in [K(+)](o) was produced by exposing a restricted region of muscle to a jet of 30 mmol/l KCl or by superfusing trabeculae with a solution containing 30 mmol/l KCl, respectively. The increase in [Ca(2+)](i) (Ca(CW)) during Ca(2+) waves was measured (24°C, 3.0 mmol/l [Ca(2+)](o)). A regional increase in [K(+)](o) caused nonuniform [Ca(2+)](i) and contraction. In the presence of isoproterenol, the regional increase in [K(+)](o) induced sustained arrhythmias in 10 of 14 trabeculae, whereas the global increase did not induce such arrhythmias. During sustained arrhythmias, Ca(2+) surged within the jet-exposed region. In the absence of isoproterenol, the regional increase in [K(+)](o) increased Ca(CW), whereas the global increase decreased it. This increase in Ca(CW) with the regional increase in [K(+)](o) was not suppressed by 100 μmol/l streptomycin, whereas it was suppressed by 1) a combination of 10 μmol/l cilnidipine and 3 μmol/l SEA0400; 2) 20 mmol/l 2,3-butanedione monoxime; and 3) 10 μmol/l blebbistatin. A regional but not a global increase in [K(+)](o) induces sustained arrhythmias, probably due to nonuniform excitation-contraction coupling. The same mechanism may underlie arrhythmias during ischemia.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arrhythmias, Cardiac / chemically induced*
  • Arrhythmias, Cardiac / physiopathology*
  • Calcium / metabolism
  • Cardiotonic Agents / pharmacology
  • Excitation Contraction Coupling / physiology
  • Heart Ventricles / drug effects
  • Heart Ventricles / metabolism
  • Heart Ventricles / physiopathology*
  • Isoproterenol / pharmacology
  • Membrane Potentials / physiology
  • Models, Animal
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology*
  • Myocardial Ischemia / metabolism
  • Myocardial Ischemia / physiopathology
  • Potassium / adverse effects*
  • Potassium / pharmacology
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Cardiotonic Agents
  • Isoproterenol
  • Potassium
  • Calcium