The Journal of Membrane Biology

, Volume 17, Issue 1, pp 293–312 | Cite as

Routes of nonelectrolyte permeation across epithelial membranes

  • Ernest M. Wright
  • Richard J. Pietras


Radioactive tracer techniques were used to study the permeability of three epithelial membranes, the toad urinary bladder, frog choroid plexus, and rabbit gallbladder, to 16 nonelectrolytes. The general patterns of nonelectrolyte permeation were similar for all three membranes, and similar to those in other biological membranes. The permeability of lipophilic solutes was roughly proportional to their bulk phase oil/water partition coefficients, but the slope was greater in the toad bladder than in the gallbladder and plexus. Branched nonelectrolytes were less permeable than their straight-chain isomers in both the urinary bladder and gallbladder, but not in the choroid plexus. Small polar solutes permeated more rapidly than expected, and in the urinary bladder and gallbladder the permeation of urea and acetamide, but not water was inhibited by phloretin. This agent also increased 1,7-heptanediol permeability in the urinary bladder but in the gallbladder there was a marked inhibition. In all three epithelia a separate pathway exists for the permeation of large polar solutes, but quantitatively this is least important in the toad bladder. It is concluded that variations in passive nonelectrolyte permeation across epithelia are due to (i) variations in the composition and configuration of membrane lipids, (ii) the presence or absence of pathways for small solutes, and (iii) the absence of presence of pathways for larger polar solutes. We also conclude that there are at least two effects of phloretin on the permeation of nonelectrolytes across biological membranes, and that there are variations in each effect from one membrane to another.


Partition Coefficient Membrane Lipid Urinary Bladder Biological Membrane Acetamide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bindslev, N., Tormey, J. McD., Pietras, R. J., Wright, E. M. 1974. Electrically and osmotically induced changes in permeability and structure of toad urinary bladder.Biochim. Biophys. Acta 332 286Google Scholar
  2. Cass, A., Andersen, O. S., Katz, I., Finkelstein, A. 1973. Phloretin's action on cation and anion permeability of modified lipid bilayers.Biophys. Soc. Abstr. 13:108aGoogle Scholar
  3. Castel, M., Sahar, A., Erlij, D. 1972. Extracellular route for passive permeation in choroid plexus epithelium.Israel J. Med. Sci. 8:1768Google Scholar
  4. Collander, R. 1954. The permeability ofNitella cells to nonelectrolytes.Physiol. Pl. 7:420Google Scholar
  5. Collander, R. 1959. Das Permeationsvermögen des Pentaerythrits verglichen mit dem des Erythrits.Physiol. Pl. 12:139Google Scholar
  6. Demel, R. A., Bruckdorfer, K. R., Van Deenen, L. L. M. 1972. The effect of sterol structure on the permeability of liposomes to glucose, glycerol and Rb+.Biochim. Biophys. Acta 255:321PubMedGoogle Scholar
  7. Diamond, J. M., Katz, Y. J. 1974. Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water.J. Membrane Biol. 17:121Google Scholar
  8. Diamond, J. M., Wright, E. M. 1969a. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Annu. Rev. Physiol. 31:581PubMedGoogle Scholar
  9. Diamond, J. M., Wright, E. M. 1969b. Molecular forces governing non-electrolyte permeation through cell membranes.Proc. Roy. Soc. (London) B 172:273Google Scholar
  10. Dick, D. A. T. 1970. Water movement in cells.In: Membranes and Ion Transport. E. E. Bittar, editor. Vol. 3, p. 211. John Wiley & Sons, LondonGoogle Scholar
  11. Dix, J. A., Diamond, J. M., Kivelson, D. 1974. Translational diffusion coefficient and partition coefficient of a spin-labeled solute in lecithin bilayer membrane.Proc. Nat. Acad. Sci. 71:474PubMedGoogle Scholar
  12. Frömter, E. 1972. The route of passive ion movement through the epithelium ofNecturus gallbladder.J. Membrane Biol. 8:259Google Scholar
  13. Frömter, E., Diamond, J. 1972. Route of passive ion permeation in epithelia.Nature 235:9PubMedGoogle Scholar
  14. Galey, W. R., Owen, J. D., Solomon, A. K. 1973. Temperature dependence of non-electrolyte permeation across red cell membranes.J. Gen. Physiol. 61:727Google Scholar
  15. Hays, R. M. 1972. The movement of water across vasopressin-sensitive epithelia.In: Current Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. Vol. 3, p. 339. Academic Press Inc., New YorkGoogle Scholar
  16. Hingson, D. J., Diamond, J. M. 1972. Comparison of nonelectrolyte permeability patterns in several epithelia.J. Membrane Biol. 10:93Google Scholar
  17. Horowitz, S. B., Fenichel, I. R. 1964. Solute diffusional specificity in hydrogen bonding systems.J. Phys. Chem. 68:3378Google Scholar
  18. Hubbell, W. L., McConnell, H. M. 1971. Molecular motion in spin-labeled phospholipids and membranes.Amer. Chem. Soc. 93:314Google Scholar
  19. Kroes, J., Ostwald, R. 1971. Erythrocyte membranes — Effect of increased cholesterol content on permeability.Biochim. Biophys. Acta 249:647PubMedGoogle Scholar
  20. LaCelle, P., Passow, H. 1971. Permeability of the human red blood cell tomeso-erythritol.J. Membrane Biol. 4:270Google Scholar
  21. Leaf, A., Hays, R. M. 1962. Permeability of the isolated toad bladder to solutes and its modification by vasopressin.J. Gen. Physiol. 45:921PubMedGoogle Scholar
  22. Levine, S., Franki, N., Hays, R. M. 1973a. Effect of phloretin on water and solute movement in the toad bladder.J. Clin. Invest. 52:1435PubMedGoogle Scholar
  23. Levine, S., Franki, N., Hays, R. M.. 1973b. A saturable, vasopressin-sensitive carrier for urea and acetamide in the toad bladder epithelial cell.J. Clin. Invest. 52:2083PubMedGoogle Scholar
  24. Lieb, W. R., Stein, W. D. 1969. Biological membranes behave as non-porous polymeric sheets with respect to diffusion of non-electrolytes.Nature 224:240PubMedGoogle Scholar
  25. Macy, R. I., Karan, D. M., Farmer, R. E. L. 1972. Properties of water channels in human red cells.In: Passive Permeability of Cell Membranes. Biomembranes. F. Krenzer and J. F. G. Slegers, editors. Vol. 3, p. 331. Plenum Press, New YorkGoogle Scholar
  26. Moreno, J. H., Diamond, J. M. 1874a. Role of hydrogen bonding in organic cation discrimination by “tight” junctions of gall bladder epithelium.Nature (In press) Google Scholar
  27. Moreno, J. H., Diamond, J. M. 1974b. Cation permeation mechanisms and cation selectivity in “tight junctions” of gall bladder epithelium.In: Membranes — A Series of Advances. G. Eisenman, editor. Marcel Dekker, New York (In press)Google Scholar
  28. Naccache, P., Sha'afi, R. I. 1973. Patterns of nonelectrolyte permeability in human red blood cell membrane.J. Gen. Physiol. 62:714PubMedGoogle Scholar
  29. Owen, J. D., Solomon, A. K. 1972 Control of nonelectrolyte permeability in red cells.Biochim. Biophys. Acta 290:414PubMedGoogle Scholar
  30. Pietras, R. J., Wright, E. M. 1974. Non-electrolyte probes of membrane structure in ADH-treated toad urinary bladder.Nature 247:222PubMedGoogle Scholar
  31. Sha'afi, R. I., Gary-Bobo, C. M., Solomon, A. K. 1971. Permeability of red cell membrane to small hydrophilic and lipophilic solutes.J. Gen. Physiol. 58:238PubMedGoogle Scholar
  32. Smulders, A. P., Tormey, J. McD., Wright, E. M. 1972. The effect of osmotically induced water flows on the permeability and ultrastructure of the rabbit gallbladder.J. Membrane Biol. 7:164Google Scholar
  33. Smulders, A. P., Wright, E. M. 1971. The magnitude of nonelectrolyte selectivity in the gallbladder epithelium.J. Membrane Biol. 5:297Google Scholar
  34. Smyth, D. H., Wright, E. M. 1966. Streaming potentials in the rat small intestine.J. Physiol. 182:591PubMedGoogle Scholar
  35. Solomon, A. K., Gary-Bobo, C. M. 1972. Aqueous pores in lipid bilayers and red cell membranes.Biochim. Biophys. Acta 255:1019PubMedGoogle Scholar
  36. Van Os, C. H., Slegers, J. F. G. 1973. Path of osmotic water flow through rabbit gall bladder epithelium.Biochim. Biophys. Acta 291:1973Google Scholar
  37. Weinstein, R. S., McNutt, N. S. 1972. Current concepts — Cell junctions.New Engl. J. Med. 286:521PubMedGoogle Scholar
  38. Welch, K., Sadler, K. 1966. Permeability of the choroid plexus of the rabbit to several solutes.Amer. J. Physiol. 210:652PubMedGoogle Scholar
  39. Wilson, G., Rose, S. P., Fox, C. F. 1970. The effect of membrane lipid unsaturation on glycoside transport.Biochem. Biophys. Res. Commun. 38:617PubMedGoogle Scholar
  40. Wright, E. M. 1972a. Mechanisms of ion transport across the choroid plexus.J. Physiol. 226:545PubMedGoogle Scholar
  41. Wright, E. M. 1972b. Accumulation and transport of amino acids by the frog choroid plexus.Brain Res. 44:207PubMedGoogle Scholar
  42. Wright, E. M. 1974. Active transport of iodide and other anions across the choroid plexus.J. Physiol. (In press) Google Scholar
  43. Wright, E. M., Diamond, J. M. 1969a. An electrical method of measuring non-electrolyte permeability.Proc. Roy. Soc. (London) B. 172:203Google Scholar
  44. Wright, E. M., Diamond, J. M. 1969b. Patterns of non-electrolyte permeability.Proc. Roy. Soc. (London) B. 172:227Google Scholar
  45. Wright, E. M., Prather, J. W. 1970. The permeability of the frog choroid plexus to nonelectrolytes.J. Membrane Biol. 2:127Google Scholar
  46. Wright, E. M., Smulders, A. P., Tormey, J. McD. 1972. The role of the lateral intercellular spaces and solute polarization effects in the passive flow of water across the rabbit gallbladder.J. Membrane Biol. 7:198Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1974

Authors and Affiliations

  • Ernest M. Wright
    • 1
  • Richard J. Pietras
    • 1
  1. 1.Department of PhysiologyUniversity of California Medical CenterLos Angeles

Personalised recommendations