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. 1996 Nov 15;497(Pt 1):3–17. doi: 10.1113/jphysiol.1996.sp021745

Cotransport of H+, lactate and H2O by membrane proteins in retinal pigment epithelium of bullfrog.

T Zeuthen 1, S Hamann 1, M la Cour 1
PMCID: PMC1160908  PMID: 8951707

Abstract

1. The interaction between H+, lactate and H2O fluxes in the retinal membrane of the pigment epithelium from bullfrog Rana catesbiana was studied by means of ion-selective micro-electrodes. 2. Changes in intracellular pH and cell volume were recorded in response to abrupt changes in retinal solution concentration and/or osmolarity. 3. Two parallel pathways for water transport were identified across the retinal membrane, an osmotic one with a hydraulic water permeability of 3.2 x 10(-4) cm s-1 (osmol l-1)-1 and one which depended on the presence of lactate. 4. Addition of sodium lactate to the retinal solution caused cell shrinkages that were small compared with those produced by mannitol. The reflection coefficient for sodium lactate was 0.25. 5. Isosmotic replacement of Cl- with lactate caused an influx of water. Simultaneous acidification of the retinal solution from pH 7.4 to 6.4 enhanced the effect. The influx of water could proceed against osmotic gradients elicited by mannitol. 6. The interdependence of the fluxes of H+, lactate and H2O can be described as cotransport: the fluxes had a fixed ratio of about 109 mmol of lactic acid per litre of water, the flux of one species was able to energize the flux of the other two, and the fluxes exhibited saturation for increasing driving forces. 7. The Gibbs equation gives an accurate quantitative description of these coupled fluxes.

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Selected References

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  1. Adorante J. S., Miller S. S. Potassium-dependent volume regulation in retinal pigment epithelium is mediated by Na,K,Cl cotransport. J Gen Physiol. 1990 Dec;96(6):1153–1176. doi: 10.1085/jgp.96.6.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Dornonville de la Cour M. Ion transport in the retinal pigment epithelium. A study with double barrelled ion-selective microelectrodes. Acta Ophthalmol Suppl. 1993;(209):1–32. [PubMed] [Google Scholar]
  3. Fischbarg J., Kuang K. Y., Vera J. C., Arant S., Silverstein S. C., Loike J., Rosen O. M. Glucose transporters serve as water channels. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3244–3247. doi: 10.1073/pnas.87.8.3244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Frambach D. A., Weiter J. J., Adler A. J. A photogrammetric method to measure fluid movement across isolated frog retinal pigment epithelium. Biophys J. 1985 Apr;47(4):547–552. doi: 10.1016/S0006-3495(85)83949-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Heath H., Kang S. S., Philippou D. Glucose, glucose-6-phosphate, lactate and pyruvate content of the retina, blood and liver of streptozotocin-diabetic rats fed sucrose- or starch-rich diets. Diabetologia. 1975 Feb;11(1):57–62. doi: 10.1007/BF00422819. [DOI] [PubMed] [Google Scholar]
  6. Hughes B. A., Adorante J. S., Miller S. S., Lin H. Apical electrogenic NaHCO3 cotransport. A mechanism for HCO3 absorption across the retinal pigment epithelium. J Gen Physiol. 1989 Jul;94(1):125–150. doi: 10.1085/jgp.94.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hughes B. A., Miller S. S., Machen T. E. Effects of cyclic AMP on fluid absorption and ion transport across frog retinal pigment epithelium. Measurements in the open-circuit state. J Gen Physiol. 1984 Jun;83(6):875–899. doi: 10.1085/jgp.83.6.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. KEDEM O., KATCHALSKY A. A physical interpretation of the phenomenological coefficients of membrane permeability. J Gen Physiol. 1961 Sep;45:143–179. doi: 10.1085/jgp.45.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kenyon E., Yu K., La Cour M., Miller S. S. Lactate transport mechanisms at apical and basolateral membranes of bovine retinal pigment epithelium. Am J Physiol. 1994 Dec;267(6 Pt 1):C1561–C1573. doi: 10.1152/ajpcell.1994.267.6.C1561. [DOI] [PubMed] [Google Scholar]
  10. La Cour M., Zeuthen T. Osmotic properties of the frog retinal pigment epithelium. Exp Eye Res. 1993 May;56(5):521–530. doi: 10.1006/exer.1993.1066. [DOI] [PubMed] [Google Scholar]
  11. Lin H., Miller S. S. pHi regulation in frog retinal pigment epithelium: two apical membrane mechanisms. Am J Physiol. 1991 Jul;261(1 Pt 1):C132–C142. doi: 10.1152/ajpcell.1991.261.1.C132. [DOI] [PubMed] [Google Scholar]
  12. Lin H., la Cour M., Andersen M. V., Miller S. S. Proton-lactate cotransport in the apical membrane of frog retinal pigment epithelium. Exp Eye Res. 1994 Dec;59(6):679–688. doi: 10.1006/exer.1994.1153. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Poole R. C., Halestrap A. P. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol. 1993 Apr;264(4 Pt 1):C761–C782. doi: 10.1152/ajpcell.1993.264.4.C761. [DOI] [PubMed] [Google Scholar]
  16. Reuss L. Changes in cell volume measured with an electrophysiologic technique. Proc Natl Acad Sci U S A. 1985 Sep;82(17):6014–6018. doi: 10.1073/pnas.82.17.6014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Roos A., Boron W. F. Intracellular pH. Physiol Rev. 1981 Apr;61(2):296–434. doi: 10.1152/physrev.1981.61.2.296. [DOI] [PubMed] [Google Scholar]
  18. Steinberg R. H. Scanning electron microscopy of the bullfrog's retina and pigment epithelium. Z Zellforsch Mikrosk Anat. 1973 Oct 26;143(4):451–463. doi: 10.1007/BF00306765. [DOI] [PubMed] [Google Scholar]
  19. Zeuthen T. Cotransport of K+, Cl- and H2O by membrane proteins from choroid plexus epithelium of Necturus maculosus. J Physiol. 1994 Jul 15;478(Pt 2):203–219. doi: 10.1113/jphysiol.1994.sp020243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Zeuthen T. Molecular mechanisms for passive and active transport of water. Int Rev Cytol. 1995;160:99–161. doi: 10.1016/s0074-7696(08)61554-5. [DOI] [PubMed] [Google Scholar]
  21. Zeuthen T. Relations between intracellular ion activities and extracellular osmolarity in Necturus gallbladder epithelium. J Membr Biol. 1982;66(2):109–121. doi: 10.1007/BF01868487. [DOI] [PubMed] [Google Scholar]
  22. Zeuthen T. Secondary active transport of water across ventricular cell membrane of choroid plexus epithelium of Necturus maculosus. J Physiol. 1991 Dec;444:153–173. doi: 10.1113/jphysiol.1991.sp018871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zeuthen T., Stein W. D. Cotransport of salt and water in membrane proteins: membrane proteins as osmotic engines. J Membr Biol. 1994 Feb;137(3):179–195. doi: 10.1007/BF00232587. [DOI] [PubMed] [Google Scholar]
  24. Zeuthen T. Water permeability of ventricular cell membrane in choroid plexus epithelium from Necturus maculosus. J Physiol. 1991 Dec;444:133–151. doi: 10.1113/jphysiol.1991.sp018870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. la Cour M. Kinetic properties and Na+ dependence of rheogenic Na(+)-HCO3- co-transport in frog retinal pigment epithelium. J Physiol. 1991 Aug;439:59–72. doi: 10.1113/jphysiol.1991.sp018656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. la Cour M., Lin H., Kenyon E., Miller S. S. Lactate transport in freshly isolated human fetal retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1994 Feb;35(2):434–442. [PubMed] [Google Scholar]
  27. la Cour M., Lund-Andersen H., Zeuthen T. Potassium transport of the frog retinal pigment epithelium: autoregulation of potassium activity in the subretinal space. J Physiol. 1986 Jun;375:461–479. doi: 10.1113/jphysiol.1986.sp016128. [DOI] [PMC free article] [PubMed] [Google Scholar]

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