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. 1999 Jan;76(1 Pt 1):219–232. doi: 10.1016/S0006-3495(99)77191-2

Frequency-dependent capacitance of the apical membrane of frog skin: dielectric relaxation processes.

M S Awayda 1, W Van Driessche 1, S I Helman 1
PMCID: PMC1302513  PMID: 9876136

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. 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 microF/cm2, respectively, that gave rise to dc capacitances of 1.95 +/- 0.06 microF/cm2 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 (Cadc = 0.028 Isc + 1.48; Isc between 4 and 35 microA/cm2) 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.

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Selected References

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  1. Abramcheck F. J., Van Driessche W., Helman S. I. Autoregulation of apical membrane Na+ permeability of tight epithelia. Noise analysis with amiloride and CGS 4270. J Gen Physiol. 1985 Apr;85(4):555–582. doi: 10.1085/jgp.85.4.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almeida P. F., Vaz W. L., Thompson T. E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry. 1992 Jul 28;31(29):6739–6747. doi: 10.1021/bi00144a013. [DOI] [PubMed] [Google Scholar]
  3. Armstrong C. M. Currents associated with the ionic gating structures in nerve membrane. Ann N Y Acad Sci. 1975 Dec 30;264:265–277. doi: 10.1111/j.1749-6632.1975.tb31488.x. [DOI] [PubMed] [Google Scholar]
  4. Bao J. Z., Davis C. C., Schmukler R. E. Frequency domain impedance measurements of erythrocytes. Constant phase angle impedance characteristics and a phase transition. Biophys J. 1992 May;61(5):1427–1434. doi: 10.1016/S0006-3495(92)81948-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coster H. G., Smith J. R. The molecular organisation of bimolecular lipid membranes. A study of the low frequency Maxwell-Wagner impedance dispersion. Biochim Biophys Acta. 1974 Dec 10;373(2):151–164. doi: 10.1016/0005-2736(74)90142-4. [DOI] [PubMed] [Google Scholar]
  6. Fisher R. S., Erlij D., Helman S. I. Intracellular voltage of isolated epithelia of frog skin: apical and basolateral cell punctures. J Gen Physiol. 1980 Oct;76(4):447–453. doi: 10.1085/jgp.76.4.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Foster K. R., Schwan H. P. Dielectric properties of tissues and biological materials: a critical review. Crit Rev Biomed Eng. 1989;17(1):25–104. [PubMed] [Google Scholar]
  8. Fricke H., Morse S. THE ELECTRIC RESISTANCE AND CAPACITY OF BLOOD FOR FREQUENCIES BETWEEN 800 AND 4(1/2) MILLION CYCLES. J Gen Physiol. 1925 Nov 20;9(2):153–167. doi: 10.1085/jgp.9.2.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hanai T., Haydon D. A., Taylor J. The influence of lipid composition and of some adsorbed proteins on the capacitance of black hydrocarbon membranes. J Theor Biol. 1965 Nov;9(3):422–432. doi: 10.1016/0022-5193(65)90041-x. [DOI] [PubMed] [Google Scholar]
  10. Helman S. I., Fisher R. S. Microelectrode studies of the active Na transport pathway of frog skin. J Gen Physiol. 1977 May;69(5):571–604. doi: 10.1085/jgp.69.5.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Helman S. I., Thompson S. M. Interpretation and use of electrical equivalent circuits in studies of epithelial tissues. Am J Physiol. 1982 Dec;243(6):F519–F531. doi: 10.1152/ajprenal.1982.243.6.F519. [DOI] [PubMed] [Google Scholar]
  12. Jacobson K. Lateral diffusion in membranes. Cell Motil. 1983;3(5-6):367–373. doi: 10.1002/cm.970030504. [DOI] [PubMed] [Google Scholar]
  13. Kell D. B., Harris C. M. On the dielectrically observable consequences of the diffusional motions of lipids and proteins in membranes. 1. Theory and overview. Eur Biophys J. 1985;12(4):181–197. doi: 10.1007/BF00253845. [DOI] [PubMed] [Google Scholar]
  14. Mărgineanu D. G., Van Driessche W. Effects of millimolar concentrations of glutaraldehyde on the electrical properties of frog skin. J Physiol. 1990 Aug;427:567–581. doi: 10.1113/jphysiol.1990.sp018188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Tang J., Abramcheck F. J., Van Driessche W., Helman S. I. Electrophysiology and noise analysis of K+-depolarized epithelia of frog skin. Am J Physiol. 1985 Nov;249(5 Pt 1):C421–C429. doi: 10.1152/ajpcell.1985.249.5.C421. [DOI] [PubMed] [Google Scholar]
  16. Tocanne J. F., Dupou-Cézanne L., Lopez A., Tournier J. F. Lipid lateral diffusion and membrane organization. FEBS Lett. 1989 Oct 23;257(1):10–16. doi: 10.1016/0014-5793(89)81774-0. [DOI] [PubMed] [Google Scholar]
  17. Van Driessche W. Lidocaine blockage of basolateral potassium channels in the amphibian urinary bladder. J Physiol. 1986 Dec;381:575–593. doi: 10.1113/jphysiol.1986.sp016344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Watanabe M., Suzaki T., Irimajiri A. Dielectric behavior of the frog lens in the 100 Hz to 500 MHz range. Simulation with an allocated ellipsoidal-shells model. Biophys J. 1991 Jan;59(1):139–149. doi: 10.1016/S0006-3495(91)82206-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. White S. H., Thompson T. E. Capacitance, area, and thickness variations in thin lipid films. Biochim Biophys Acta. 1973 Sep 27;323(1):7–22. doi: 10.1016/0005-2736(73)90428-8. [DOI] [PubMed] [Google Scholar]
  20. van Meer G., Simons K. Lipid polarity and sorting in epithelial cells. J Cell Biochem. 1988 Jan;36(1):51–58. doi: 10.1002/jcb.240360106. [DOI] [PubMed] [Google Scholar]

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