Frequency-Dependent Capacitance of the Apical Membrane of Frog Skin: Dielectric Relaxation Processes

Abstract

Impedance analysis of the isolated epithelium of frog skin (northern Rana pipiens) was carried out in the frequency range between 0.1 Hz and 5.5 kHz while Na + transport was abolished. Under these conditions, the impedance is determined almost completely by the dielectric properties of the apical membranes of the cells and the parallel shunt resistance. The modeling of the apical membrane impedance function required the inclusion of dielectric relaxation processes as originally described by Cole and Cole (1941. J. Chem. Phys. 9:341–351), where each process is characterized by a dielectric increment, relaxation frequency, and power law dependence. We found that the apical plasma membrane exhibited several populations of audio frequency dielectric relaxation processes centered at 30, 103, 2364, and 6604 Hz, with mean capacitive increments of 0.72, 1.00, 0.88, and 0.29 μF/cm 2, respectively, that gave rise to dc capacitances of 1.95 ± 0.06 μF/cm 2 in 49 tissues. Capacitance was uncorrelated with large ranges of parallel shunt resistance and was not changed appreciably within minutes by K + depolarization and hence a decrease in basolateral membrane resistance. A significant linear correlation existed between the dc capacitance and Na + transport rates measured as short-circuit currents ( C a dc = 0.028 I sc + 1.48; I sc between 4 and 35 μA/cm 2) before inhibition of transport by amiloride and substitution of all Na + with NMDG ( N-methyl- d-glucamine) in the apical solution. The existence of dominant audio frequency capacitive relaxation processes complicates and precludes unequivocal interpretation of changes of capacitance in terms of membrane area alone when capacitance is measured at audio frequencies.