Biophys J, November 2001, p. 2442-2457, Vol. 81, No. 5

The Influence of Plasma Membrane Electrostatic Properties on the Stability of Cell Ionic Composition

Stéphane Genet,^* Robert Costalat,^* and Jacques Burger

 ^*Institut National de la Santé et de la Recherche Médicale U. 483, Université Pierre et Marie Curie, 75252 Paris Cedex 05, France; and  Laboratoire d'Ingéniérie des Systèmes Automatisés, Université d'Angers, 49000 Angers Cedex, France

An electro-osmotic model is developed to examine the influence of plasma membrane superficial charges on the regulation of cell ionic composition. Assuming membrane osmotic equilibrium, the ion distribution predicted by Gouy-Chapman-Grahame (GCG) theory is introduced into ion transport equations, which include a kinetic model of the Na/K-ATPase based on the stimulation of this ion pump by internal Na⁺ ions. The algebro-differential equation system describing dynamics of the cell model has a unique resting state, stable with respect to finite-sized perturbations of various types. Negative charges on the membrane are found to greatly enhance relaxation toward steady state following these perturbations. We show that this heightened stability stems from electrostatic interactions at the inner membrane side that shift resting state coordinates along the sigmoidal activation curve of the sodium pump, thereby increasing the pump sensitivity to internal Na⁺ fluctuations. The accuracy of electrostatic potential description with GCG theory is proved using an alternate formalism, based on irreversible thermodynamics, which shows that pressure contribution to ion potential energy is negligible in electrostatic double layers formed at the surfaces of biological membranes. We discuss implications of the results regarding a reliable operation of ionic process coupled to the transmembrane electrochemical gradient of Na⁺ ions.

Biophys J, November 2001, p. 2442-2457, Vol. 81, No. 5
© 2001 by the Biophysical Society   0006-3495/01/11/2442/16  $2.00