Extracellular sodium dependence of the conduction velocity-calcium relationship: evidence of ephaptic self-attenuation

Am J Physiol Heart Circ Physiol. 2016 May 1;310(9):H1129-39. doi: 10.1152/ajpheart.00857.2015. Epub 2016 Mar 4.

Abstract

Our laboratory previously demonstrated that perfusate sodium and potassium concentrations can modulate cardiac conduction velocity (CV) consistent with theoretical predictions of ephaptic coupling (EpC). EpC depends on the ionic currents and intercellular separation in sodium channel rich intercalated disk microdomains like the perinexus. We suggested that perinexal width (WP) correlates with changes in extracellular calcium ([Ca(2+)]o). Here, we test the hypothesis that increasing [Ca(2+)]o reduces WP and increases CV. Mathematical models of EpC also predict that reducing WP can reduce sodium driving force and CV by self-attenuation. Therefore, we further hypothesized that reducing WP and extracellular sodium ([Na(+)]o) will reduce CV consistent with ephaptic self-attenuation. Transmission electron microscopy revealed that increasing [Ca(2+)]o (1 to 3.4 mM) significantly decreased WP Optically mapping wild-type (WT) (100% Cx43) mouse hearts demonstrated that increasing [Ca(2+)]o increases transverse CV during normonatremia (147.3 mM), but slows transverse CV during hyponatremia (120 mM). Additionally, CV in heterozygous (∼50% Cx43) hearts was more sensitive to changes in [Ca(2+)]o relative to WT during normonatremia. During hyponatremia, CV slowed in both WT and heterozygous hearts to the same extent. Importantly, neither [Ca(2+)]o nor [Na(+)]o altered Cx43 expression or phosphorylation determined by Western blotting, or gap junctional resistance determined by electrical impedance spectroscopy. Narrowing WP, by increasing [Ca(2+)]o, increases CV consistent with enhanced EpC between myocytes. Interestingly, during hyponatremia, reducing WP slowed CV, consistent with theoretical predictions of ephaptic self-attenuation. This study suggests that serum ion concentrations may be an important determinant of cardiac disease expression.

Keywords: calcium; conduction; ephaptic coupling; ion concentration; sodium.

Publication types

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

MeSH terms

  • Action Potentials*
  • Animals
  • Calcium / metabolism*
  • Calcium Signaling*
  • Cell Communication*
  • Computer Simulation
  • Connexin 43 / deficiency
  • Connexin 43 / genetics
  • Dielectric Spectroscopy
  • Electric Impedance
  • Gap Junctions / metabolism
  • Genotype
  • Hyponatremia / blood
  • Hyponatremia / physiopathology
  • Isolated Heart Preparation
  • Kinetics
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron, Transmission
  • Models, Cardiovascular*
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / ultrastructure
  • Phenotype
  • Sodium / metabolism*
  • Voltage-Sensitive Dye Imaging

Substances

  • Connexin 43
  • GJA1 protein, mouse
  • Sodium
  • Calcium