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. 1984 Jun 1;83(6):875–899. doi: 10.1085/jgp.83.6.875

Effects of cyclic AMP on fluid absorption and ion transport across frog retinal pigment epithelium. Measurements in the open-circuit state

PMCID: PMC2215661  PMID: 6330281

Abstract

A modified version of a capacitance probe technique has been used to measure fluid transport across the isolated retinal pigment epithelium (RPE)-choroid of the bullfrog. The accuracy of this measurement is 0.5- 1.0 nl/min. Experiments carried out in the absence of external osmotic or hydrostatic gradients show that the RPE-choroid transports fluid from the retinal to the choroid side of the tissue at a rate of approximately 10 nl/min (4-6 microliters/cm2 X h). Net fluid absorption (Jv) was abolished within 10 min by the mitochondrial uncoupler 2,4- dinitrophenol. It was also inhibited (70%) by the removal of bicarbonate from the bulk solutions bathing the tissue. Ouabain caused a slow decrease in Jv (no effect at 10 min, 70% at 3 h), which indicates that RPE fluid transport is not directly coupled to the activity of the Na-K pump located at the apical membrane of this epithelium. In contrast to ouabain, cyclic AMP (cAMP) produced a quick decrease in Jv (84% within 5 min). Radioisotope experiments in the open circuit show that cAMP stimulated secretory fluxes of Na and Cl, which accounted for the observed cAMP-induced decrease in Jv. The direction of net fluid absorption, the magnitudes of the net ionic fluxes in the open circuit, and the dependence of Jv on external bicarbonate concentration strongly suggest that fluid absorption is generated primarily by the active absorption of bicarbonate.

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Selected References

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  1. Bach G., Berman E. R. Amino sugar-containing compounds of the retina. I. Isolation and identification. Biochim Biophys Acta. 1971 Dec 21;252(3):453–461. doi: 10.1016/0304-4165(71)90148-6. [DOI] [PubMed] [Google Scholar]
  2. Capovilla M., Cervetto L., Torre V. Effects of changing external potassium and chloride concentrations on the photoresponses of Bufo bufo rods. J Physiol. 1980 Oct;307:529–551. doi: 10.1113/jphysiol.1980.sp013452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cohen L. HCO3-Cl exchange transport in the adaptive response to alkalosis by turtle bladder. Am J Physiol. 1980 Aug;239(2):F167–F174. doi: 10.1152/ajprenal.1980.239.2.F167. [DOI] [PubMed] [Google Scholar]
  4. Feeney L. The interphotoreceptor space. II. Histochemistry of the matrix. Dev Biol. 1973 May;32(1):115–128. doi: 10.1016/0012-1606(73)90224-8. [DOI] [PubMed] [Google Scholar]
  5. Fisher R. S., Persson B. E., Spring K. R. Epithelial cell volume regulation: bicarbonate dependence. Science. 1981 Dec 18;214(4527):1357–1359. doi: 10.1126/science.7313695. [DOI] [PubMed] [Google Scholar]
  6. Frederiksen O., Rostgaard J. Absence of dilated lateral intercellular spaces in fluid-transporting frog gallbladder epithelium. Direct microscopy observations. J Cell Biol. 1974 Jun;61(3):830–834. doi: 10.1083/jcb.61.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Freeman R. D. Oxygen consumption by the component layers of the cornea. J Physiol. 1972 Aug;225(1):15–32. doi: 10.1113/jphysiol.1972.sp009927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gold G. H., Korenbrot J. I. Light-induced calcium release by intact retinal rods. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5557–5561. doi: 10.1073/pnas.77.9.5557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Linsenmeier R. A., Mines A. H., Steinberg R. H. Effects of hypoxia and hypercapnia on the light peak and electroretinogram of the cat. Invest Ophthalmol Vis Sci. 1983 Jan;24(1):37–46. [PubMed] [Google Scholar]
  10. Linsenmeier R. A., Steinberg R. H. Origin and sensitivity of the light peak in the intact cat eye. J Physiol. 1982 Oct;331:653–673. doi: 10.1113/jphysiol.1982.sp014396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Marmor M. F., Abdul-Rahim A. S., Cohen D. S. The effect of metabolic inhibitors on retinal adhesion and subretinal fluid resorption. Invest Ophthalmol Vis Sci. 1980 Aug;19(8):893–903. [PubMed] [Google Scholar]
  12. Miller S. S., Hughes B. A., Machen T. E. Fluid transport across retinal pigment epithelium is inhibited by cyclic AMP. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2111–2115. doi: 10.1073/pnas.79.6.2111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Miller S. S., Steinberg R. H. Active transport of ions across frog retinal pigment epithelium. Exp Eye Res. 1977 Sep;25(3):235–248. doi: 10.1016/0014-4835(77)90090-2. [DOI] [PubMed] [Google Scholar]
  14. Miller S. S., Steinberg R. H., Oakley B., 2nd The electrogenic sodium pump of the frog retinal pigment epithelium. J Membr Biol. 1978 Dec 29;44(3-4):259–279. doi: 10.1007/BF01944224. [DOI] [PubMed] [Google Scholar]
  15. Miller S. S., Steinberg R. H. Passive ionic properties of frog retinal pigment epithelium. J Membr Biol. 1977 Sep 15;36(4):337–372. doi: 10.1007/BF01868158. [DOI] [PubMed] [Google Scholar]
  16. Miller S. S., Steinberg R. H. Potassium modulation of taurine transport across the frog retinal pigment epithelium. J Gen Physiol. 1979 Aug;74(2):237–259. doi: 10.1085/jgp.74.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Miller S. S., Steinberg R. H. Potassium transport across the frog retinal pigment epithelium. J Membr Biol. 1982;67(3):199–209. doi: 10.1007/BF01868661. [DOI] [PubMed] [Google Scholar]
  18. Miller S., Farber D. Cyclic AMP modulation of ion transport across frog retinal pigment epithelium. Measurements in the short-circuit state. J Gen Physiol. 1984 Jun;83(6):853–874. doi: 10.1085/jgp.83.6.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Norby L. H., Bethencourt D., Schwartz J. H. Dual effect of carbonic anhydrase inhibitors on H+ transport by the turtle bladder. Am J Physiol. 1981 May;240(5):F400–F405. doi: 10.1152/ajprenal.1981.240.5.F400. [DOI] [PubMed] [Google Scholar]
  20. Oakley B., 2nd, Green D. G. Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol. 1976 Sep;39(5):1117–1133. doi: 10.1152/jn.1976.39.5.1117. [DOI] [PubMed] [Google Scholar]
  21. Oakley B., 2nd, Miller S. S., Steinberg R. H. Effect of intracellular potassium upon the electrogenic pump of frog retinal pigment epithelium. J Membr Biol. 1978 Dec 29;44(3-4):281–307. doi: 10.1007/BF01944225. [DOI] [PubMed] [Google Scholar]
  22. Oakley B., 2nd Potassium and the photoreceptor-dependent pigment epithelial hyperpolarization. J Gen Physiol. 1977 Oct;70(4):405–425. doi: 10.1085/jgp.70.4.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ostwald T. J., Steinberg R. H. Localization of frog retinal pigment epithelium Na+-K+ ATPase. Exp Eye Res. 1980 Sep;31(3):351–360. doi: 10.1016/s0014-4835(80)80043-1. [DOI] [PubMed] [Google Scholar]
  24. Reuss L., Bello-Reuss E., Grady T. P. Effects of ouabain on fluid transport and electrical properties of Necturus gallbladder. Evidence in favor of a neutral basolateral sodium transport mechanism. J Gen Physiol. 1979 Apr;73(4):385–402. doi: 10.1085/jgp.73.4.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Riley M. V., Winkler B. S., Benner J., Yates E. M. ATPase activities in retinal pigment epithelium and choroid. Exp Eye Res. 1978 Oct;27(4):445–455. doi: 10.1016/0014-4835(78)90023-4. [DOI] [PubMed] [Google Scholar]
  26. SIDMAN R. L. Histochemical studies on photoreceptor cells. Ann N Y Acad Sci. 1959 Nov 12;74(2):182–195. doi: 10.1111/j.1749-6632.1958.tb39543.x. [DOI] [PubMed] [Google Scholar]
  27. Smith P. A., Weight F. F., Lehne R. A. Potentiation of Ca2+-dependent K+ activation by theophylline is independent of cyclic nucleotide elevation. Nature. 1979 Aug 2;280(5721):400–402. doi: 10.1038/280400a0. [DOI] [PubMed] [Google Scholar]
  28. Steinberg R. H., Oakley B., 2nd, Niemeyer G. Light-evoked changes in [K+]0 in retina of intact cat eye. J Neurophysiol. 1980 Nov;44(5):897–921. doi: 10.1152/jn.1980.44.5.897. [DOI] [PubMed] [Google Scholar]
  29. Welsh M. J., Widdicombe J. H., Nadel J. A. Fluid transport across the canine tracheal epithelium. J Appl Physiol Respir Environ Exerc Physiol. 1980 Nov;49(5):905–909. doi: 10.1152/jappl.1980.49.5.905. [DOI] [PubMed] [Google Scholar]
  30. Wright E. M., Wiedner G., Rumrich G. Fluid secretion by the frog choroid plexus. Exp Eye Res. 1977;25 (Suppl):149–155. doi: 10.1016/s0014-4835(77)80013-4. [DOI] [PubMed] [Google Scholar]
  31. van Os C. H., Wiedner G., Wright E. M. Volume flows across gallbladder epithelium induced by small hydrostatic and osmotic gradients. J Membr Biol. 1979 Aug;49(1):1–20. doi: 10.1007/BF01871037. [DOI] [PubMed] [Google Scholar]

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