Electroconformational coupling for ion transport in an oscillating electric field: Rectification versus active pumping

Abstract

To explain the activation of membrane ATPases by an oscillating electric field, an electroconformational coupling (ECC) model has previously been proposed [T.Y. Tsong and R.D. Astumian, Bioelectrochem. Bioenerg., 15 (1986) 457]. In this model, the ability of a membrane transport system to interact with an electric field is attributed solely to the ATPase: a concomitant charge displacement of the transporter during the ligand translocation step. To emphasize this point, the simulations of the electric field induced cation pumping by Na,K-ATPase have been done by assuming the transported ligand to be a neutral species. However, if the transported ligand is an ion, the effects of rectification must also be taken into account. Here we examine the properties of rectification and active pumping of the ECC model. Any electrically active membrane transport system may be classified into one of the following five categories (Table 1 below): (1) a transporter with gating charge and a neutral ligand, (2) a transporter without gating charge and charged ligand, (3) protein-ligand complexes without gating charge, i.e. the gating charge of the transporter being neutralized by the charge of the ligand, (4) a transporter and a protein-ligand complexes with gating charges of opposite signs, and (5) a transporter with a gating charge and a charged ligand of the same sign. Analysis indicates that in all these cases, there is an active transport and energy can be transduced from an oscillating field to a concentration gradient. In cases (1) and (5), energy can be transduced in both directions, with a theoretical maximum efficiency of 100%. In cases (2), (3), and (4), reverse energy transduction, i.e. conversion of chemical potential energy into electric energy, cannot be achieved. The maximum efficiency of direct energy transduction is 8.7% in cases (2) and (3) and 50% in case (4). The active transport in cases (2), (3) and (4) is mainly due to rectification. In all cases, the active flux depends strongly on the frequency of the field and on the concentration of the ligand, and it displays windows both on the frequency and the concentration axes. The maximum concentration gradient, ( A″/A′) max, which can be supported by this mechanism, i.e. the static head, has been calculated. When a four-state transporter is considered, the rate constants and the equilibrium constants can be determined by measuring the position of the windows, fluxes, and static head point by varying the experimental conditions.