Abstract
Measurements of transepithelial electrical impedance of continuously short-circuited A6 epithelia were made at audio frequencies (0.244 Hz to 10.45 kHz) to investigate the time course and extent to which prostaglandin E(2) (PGE(2)) modulates Cl(-) transport and apical membrane capacitance in this cell-cultured model epithelium. Apical and basolateral membrane resistances were determined by nonlinear curve-fitting of the impedance vectors at relatively low frequencies (<50 Hz) to equations (Păunescu, T. G., and S. I. Helman. 2001. Biophys. J. 81:838--851) where depressed Nyquist impedance semicircles were characteristic of the membrane impedances under control Na(+)-transporting and amiloride-inhibited conditions. In all tissues (control, amiloride-blocked, and amiloride-blocked and furosemide-pretreated), PGE(2) caused relatively small (< approximately 3 microA/cm(2)) and rapid (<60 s) maximal increase of chloride current due to activation of a rather large increase of apical membrane conductance that preceded significant activation of Na(+) transport through amiloride-sensitive epithelial Na(+) channels (ENaCs). Apical membrane capacitance was frequency-dependent with a Cole-Cole dielectric dispersion whose relaxation frequency was near 150 Hz. Analysis of the time-dependent changes of the complex frequency-dependent equivalent capacitance of the cells at frequencies >1.5 kHz revealed that the mean 9.8% increase of capacitance caused by PGE(2) was not correlated in time with activation of chloride conductance, but rather correlated with activation of apical membrane Na(+) transport.
Full Text
The Full Text of this article is available as a PDF (196.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Atia F., Zeiske W., van Driessche W. Secretory apical Cl- channels in A6 cells: possible control by cell Ca2+ and cAMP. Pflugers Arch. 1999 Aug;438(3):344–353. doi: 10.1007/s004240050919. [DOI] [PubMed] [Google Scholar]
- Awayda M. S., Van Driessche W., Helman S. I. Frequency-dependent capacitance of the apical membrane of frog skin: dielectric relaxation processes. Biophys J. 1999 Jan;76(1 Pt 1):219–232. doi: 10.1016/S0006-3495(99)77191-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baxendale-Cox L. M., Duncan R. L., Liu X., Baldwin K., Els W. J., Helman S. I. Steroid hormone-dependent expression of blocker-sensitive ENaCs in apical membranes of A6 epithelia. Am J Physiol. 1997 Nov;273(5 Pt 1):C1650–C1656. doi: 10.1152/ajpcell.1997.273.5.C1650. [DOI] [PubMed] [Google Scholar]
- Brazy P. C., Gunn R. B. Furosemide inhibition of chloride transport in human red blood cells. J Gen Physiol. 1976 Dec;68(6):583–599. doi: 10.1085/jgp.68.6.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butterworth M. B., Helman S. I., Els W. J. cAMP-sensitive endocytic trafficking in A6 epithelia. Am J Physiol Cell Physiol. 2001 Apr;280(4):C752–C762. doi: 10.1152/ajpcell.2001.280.4.C752. [DOI] [PubMed] [Google Scholar]
- Chalfant M. L., Coupaye-Gerard B., Kleyman T. R. Distinct regulation of Na+ reabsorption and Cl- secretion by arginine vasopressin in the amphibian cell line A6. Am J Physiol. 1993 Jun;264(6 Pt 1):C1480–C1488. doi: 10.1152/ajpcell.1993.264.6.C1480. [DOI] [PubMed] [Google Scholar]
- Els W. J., Helman S. I. Dual role of prostaglandins (PGE2) in regulation of channel density and open probability of epithelial Na+ channels in frog skin (R. pipiens). J Membr Biol. 1997 Jan 1;155(1):75–87. doi: 10.1007/s002329900159. [DOI] [PubMed] [Google Scholar]
- Els W. J., Helman S. I. Vasopressin, theophylline, PGE2, and indomethacin on active Na transport in frog skin: studies with microelectrodes. Am J Physiol. 1981 Sep;241(3):F279–F288. doi: 10.1152/ajprenal.1981.241.3.F279. [DOI] [PubMed] [Google Scholar]
- Fan P. Y., Haas M., Middleton J. P. Identification of a regulated Na/K/Cl cotransport system in a distal nephron cell line. Biochim Biophys Acta. 1992 Oct 19;1111(1):75–80. doi: 10.1016/0005-2736(92)90276-r. [DOI] [PubMed] [Google Scholar]
- Hall W. J., O'Donoghue J. P., O'Regan M. G., Penny W. J. Endogenous prostaglandins, adenosine 3':5'-monophosphate and sodium transport across isolated frog skin. J Physiol. 1976 Jul;258(3):731–753. doi: 10.1113/jphysiol.1976.sp011443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Helman S. I., Baxendale L. M. Blocker-related changes of channel density. Analysis of a three-state model for apical Na channels of frog skin. J Gen Physiol. 1990 Apr;95(4):647–678. doi: 10.1085/jgp.95.4.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Helman S. I., Liu X., Baldwin K., Blazer-Yost B. L., Els W. J. Time-dependent stimulation by aldosterone of blocker-sensitive ENaCs in A6 epithelia. Am J Physiol. 1998 Apr;274(4 Pt 1):C947–C957. doi: 10.1152/ajpcell.1998.274.4.C947. [DOI] [PubMed] [Google Scholar]
- Helman S. I., Liu X. Substrate-dependent expression of Na+ transport and shunt conductance in A6 epithelia. Am J Physiol. 1997 Aug;273(2 Pt 1):C434–C441. doi: 10.1152/ajpcell.1997.273.2.C434. [DOI] [PubMed] [Google Scholar]
- 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]
- Keeler R., Wong N. L. Evidence that prostaglandin E2 stimulates chloride secretion in cultured A6 renal epithelial cells. Am J Physiol. 1986 Mar;250(3 Pt 2):F511–F515. doi: 10.1152/ajprenal.1986.250.3.F511. [DOI] [PubMed] [Google Scholar]
- Koeppen B. M., Beyenbach K. W., Dantzler W. H., Helman S. I. Electrical characteristics of snake distal tubules: studies of I-V relationships. Am J Physiol. 1980 Nov;239(5):F402–F411. doi: 10.1152/ajprenal.1980.239.5.F402. [DOI] [PubMed] [Google Scholar]
- Kokko K. E., Matsumoto P. S., Ling B. N., Eaton D. C. Effects of prostaglandin E2 on amiloride-blockable Na+ channels in a distal nephron cell line (A6). Am J Physiol. 1994 Nov;267(5 Pt 1):C1414–C1425. doi: 10.1152/ajpcell.1994.267.5.C1414. [DOI] [PubMed] [Google Scholar]
- Kokko K. E., Matsumoto P. S., Zhang Z. R., Ling B. N., Eaton D. C. Prostaglandin E2 increases 7-pS Cl- channel density in the apical membrane of A6 distal nephron cells. Am J Physiol. 1997 Aug;273(2 Pt 1):C548–C557. doi: 10.1152/ajpcell.1997.273.2.C548. [DOI] [PubMed] [Google Scholar]
- Lambert A., Lowe A. G. Chloride-bicarbonate exchange in human red cells measured using a stopped flow apparatus. J Physiol. 1980 Sep;306:431–443. doi: 10.1113/jphysiol.1980.sp013405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macchia D. D., Helman S. I. Transepithelial current-voltage relationships of toad urinary bladder and colon. Estimates of ENaA and shunt resistance. Biophys J. 1979 Sep;27(3):371–392. doi: 10.1016/S0006-3495(79)85224-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marunaka Y., Eaton D. C. Effects of vasopressin and cAMP on single amiloride-blockable Na channels. Am J Physiol. 1991 May;260(5 Pt 1):C1071–C1084. doi: 10.1152/ajpcell.1991.260.5.C1071. [DOI] [PubMed] [Google Scholar]
- Matsumoto P. S., Mo L., Wills N. K. Osmotic regulation of Na+ transport across A6 epithelium: interactions with prostaglandin E2 and cyclic AMP. J Membr Biol. 1997 Nov 1;160(1):27–38. doi: 10.1007/s002329900292. [DOI] [PubMed] [Google Scholar]
- Niisato N., Marunaka Y. Regulation of Cl- transport by IBMX in renal A6 epithelium. Pflugers Arch. 1997 Jul;434(3):227–233. doi: 10.1007/s004240050389. [DOI] [PubMed] [Google Scholar]
- Noland T. D., Carter C. E., Jacobson H. R., Breyer M. D. PGE2 regulates cAMP production in cultured rabbit CCD cells: evidence for dual inhibitory mechanisms. Am J Physiol. 1992 Dec;263(6 Pt 1):C1208–C1215. doi: 10.1152/ajpcell.1992.263.6.C1208. [DOI] [PubMed] [Google Scholar]
- Perkins F. M., Handler J. S. Transport properties of toad kidney epithelia in culture. Am J Physiol. 1981 Sep;241(3):C154–C159. doi: 10.1152/ajpcell.1981.241.3.C154. [DOI] [PubMed] [Google Scholar]
- Păunescu T. G., Blazer-Yost B. L., Vlahos C. J., Helman S. I. LY-294002-inhibitable PI 3-kinase and regulation of baseline rates of Na(+) transport in A6 epithelia. Am J Physiol Cell Physiol. 2000 Jul;279(1):C236–C247. doi: 10.1152/ajpcell.2000.279.1.C236. [DOI] [PubMed] [Google Scholar]
- Păunescu T. G., Helman S. I. cAmp activation of apical membrane Cl(-) channels: theoretical considerations for impedance analysis. Biophys J. 2001 Aug;81(2):838–851. doi: 10.1016/S0006-3495(01)75745-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schlondorff D., Satriano J. A. Interactions of vasopressin, cAMP, and prostaglandins in toad urinary bladder. Am J Physiol. 1985 Mar;248(3 Pt 2):F454–F458. doi: 10.1152/ajprenal.1985.248.3.F454. [DOI] [PubMed] [Google Scholar]
- Sonnenburg W. K., Smith W. L. Regulation of cyclic AMP metabolism in rabbit cortical collecting tubule cells by prostaglandins. J Biol Chem. 1988 May 5;263(13):6155–6160. [PubMed] [Google Scholar]
- Stoddard J. S., Jakobsson E., Helman S. I. Basolateral membrane chloride transport in isolated epithelia of frog skin. Am J Physiol. 1985 Sep;249(3 Pt 1):C318–C329. doi: 10.1152/ajpcell.1985.249.3.C318. [DOI] [PubMed] [Google Scholar]
- Yanase M., Handler J. S. Adenosine 3',5'-cyclic monophosphate stimulates chloride secretion in A6 epithelia. Am J Physiol. 1986 Nov;251(5 Pt 1):C810–C814. doi: 10.1152/ajpcell.1986.251.5.C810. [DOI] [PubMed] [Google Scholar]
- Zeiske W., Atia F., Van Driessche W. Apical Cl- channels in A6 cells. J Membr Biol. 1998 Dec 1;166(3):169–178. doi: 10.1007/s002329900458. [DOI] [PubMed] [Google Scholar]
