Principles of Water and Nonelectrolyte Transport across Membranes

  • James A. Schafer
  • Thomas E. Andreoli

Abstract

Classical deductions concerning the manner in which water and nonelectrolytes traverse biological membranes have their origin in the observations of Overton(1) and Collander and Bärlund.(2) Overton formulated the generalization that the rate of penetration of nonelectrolytes into plant cells was proportional to their oil-water partition coefficient. Collander and Barlund confirmed these observations but noted that, in certain instances, the cellular permeability of solutes was related primarily to molecular size rather than lipid solubility. These two dissimilar phenomena led to the hypothesis that natural membranes were mosaic structures containing lipids and pores, or molecular sieves. The degree to which molecular size, rather than lipid solubility, regulated the penetration of solutes into cells was dependent on the fractional membrane area occupied by pores and the characteristics of the individual pores.(3) Current theories concerning membrane pores depend, in the main, on this hypothesis.

Keywords

Entropy Sucrose Convection Urea Hydrocarbon 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Overton, E. 1902. Beitrage zur allgemeinen Muskel und Nerven Physiologie. Pfluegers Arch. 92: 115–280.CrossRefGoogle Scholar
  2. 2.
    Collander, R., and H. Bärlund. 1933. Permeabilitätsstudienen an Chara certatophylla. II. Die Permeabilität fur Nichtelectrolyte. Acta Bot. Fenn. 11: 1–114.Google Scholar
  3. 3.
    Höber, R. 1945. The Physical Chemistry of Cells and Tissues. McGraw-Hill ( Blakiston ), New York. pp. 229–242.Google Scholar
  4. 4.
    Einstein, A. 1956. Investigations on the Theory of the Brownian Movement. Dover, New York. pp. 76–89.Google Scholar
  5. 5.
    Jacobs, M. H. 1932. Diffusion processes. Ergeb. Biol. 12: 1–160.Google Scholar
  6. 6.
    Onsager, L. 1945. Theories and problems of liquid diffusion. Ann. N.Y. Acad. Sci. 46: 241–265.PubMedCrossRefGoogle Scholar
  7. 7.
    Hartley, G. S., and J. Crank. 1949. Some fundamental definitions and concepts in diffusion processes. Trans. Faraday Soc. 45:801– 818.Google Scholar
  8. 8.
    Spiegler, K. S. 1958. Transport processes in ionic membranes. Trans. Faraday Soc. 54: 1048–1428.CrossRefGoogle Scholar
  9. 9.
    Kedem, O., and A. Katchalsky. 1961. A physical interpretation of the phenomenological coefficients of membrane permeability. J. Gen. Physiol. 45: 143–179.PubMedCrossRefGoogle Scholar
  10. 10.
    Dainty, J., and B. Z. Ginzburg. 1963. Irreversible thermodynamics and frictional models of membrane processes, with particular reference to the cell membrane. J. Theor. Biol. 5:256– 265.PubMedCrossRefGoogle Scholar
  11. 11.
    Thau, G., R. Block, and O. Kedem. 1966. Water transport in porous and nonporous membranes. Desalination 1: 129–138.CrossRefGoogle Scholar
  12. 12.
    Robinson, R. A., and R. H. Stokes. 1959. Electrolyte Solutions. Butterworths, London, pp. 120–131.Google Scholar
  13. 13.
    Longsworth, L. G. 1955. Diffusion in liquids and the Stokes- Einstein relation. In: Electrochemistry in Biology and Medicine. T. Schedlovsky, ed. Wiley, New York. pp. 225–247.Google Scholar
  14. 14.
    Darling, B. T., and D. M. Dennison. 1940. The water vapor molecule. Phys. Rev. 57: 128–135.CrossRefGoogle Scholar
  15. 15.
    Bernal, J. D., and R. H. Fowler. 1933. A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions. J. Chem. Phys. 1: 515–521.CrossRefGoogle Scholar
  16. 16.
    Pople, J. A. 1951. Molecular association in liquids. II. A theory of the structure of water. Proc. R. Soc. London Ser. A 205: 163–178.CrossRefGoogle Scholar
  17. 17.
    Eisenberg, D., and W. Kauzmann. 1969. The Structure and Properties of Water. Oxford University Press, London, pp. 1–35.Google Scholar
  18. 18.
    Campbell, E., S. Gelernter, H. Heinen, and V. R. G. Moorti. 1967. Interpretation of the energy of hydrogen bonding: Permanent multipole contribution to the energy of ice as a function of the arrangement of hydrogens. J. Chem. Phys. 46: 2690–2707.CrossRefGoogle Scholar
  19. 19.
    Kavanau, J. L. 1964. Water and Solute-Water Interactions. Holden-Day, San Franciso. pp. 1–20.Google Scholar
  20. 20.
    Shibata, S., and L. S. Bartell. 1965. Electron-diffraction study of water and heavy water. J. Chem. Phys. 42: 1147–1151.CrossRefGoogle Scholar
  21. 21.
    Owston, P. G. 1958. Structure of ice-I, as determined by X-ray and neutron diffraction analysis. Adv. Phys. 7: 171–188.Google Scholar
  22. 22.
    Bjerrum, N. 1952. Structure and properties of ice. Science 115: 385–390.PubMedCrossRefGoogle Scholar
  23. 23.
    Morgan, J., and B. E. Warren. 1938. X-ray analysis of the structure of water. J. Chem. Phys. 6: 666–673.CrossRefGoogle Scholar
  24. 24.
    Kuhn, P. G. 1965. Tables of some physical and chemical properties of water. Symp. Soc. Exp. Biol. 19: 4–16.Google Scholar
  25. 25.
    Bernal, J. D. 1965. The structure of water and its biological implications. Symp. Soc. Exp. Biol. 19: 17–32.PubMedGoogle Scholar
  26. 26.
    Frank, H. S., and M. W. Evans. 1945. Free volume and entropy in condensed systems. III. Entropy in binary liquid mixtures: Partial molal entropy in dilute solutions; structure and thermodynamics in aqueous electrolytes. J. Chem. Phys. 13: 507–532.CrossRefGoogle Scholar
  27. 27.
    Nemethy, G., and H. A. Scheraga. 1962. Structure of water and hydrophobic bonding in proteins. I. A model for the thermodynamic properties of liquid water. J. Chem. Phys. 36:3382– 3400.Google Scholar
  28. 28.
    Frank, H. S., and W. Y. Wen. 1957. III. Ion-solvent interaction. Structural aspects of ion-solvent interactions in aqueous solutions: A suggested picture of water structure. Discuss. Faraday Soc. 24: 133–140.CrossRefGoogle Scholar
  29. 29.
    Diamond, J. M., and E. M. Wright. 1969. Biological membranes: The physical basis of ionic and nonelectrolyte selectivity. Annu. Rev. Physiol. 31: 581–646.PubMedCrossRefGoogle Scholar
  30. 30.
    Stein, W. D. 1967. The Movement of Molecules across Cell Membranes. Academic Press, New York. pp. 65–124.Google Scholar
  31. 31.
    Price, H. D., and T. E. Thompson. 1969. Properties of lipid bilayer membranes separating two aqueous phases: Temperature dependence of water permeability. J. Mol. Biol. 41: 453–457.CrossRefGoogle Scholar
  32. 32.
    de Grier, J., J. G. Mandersloot, J. V. Hupkes, R. N. McElhaney, and W. P. van Beer. 1971. On the mechanism of non-electrolyte permeation through lipid bilayers and through biomembranes. Biochim. Biophys. Acta 233: 610–618.CrossRefGoogle Scholar
  33. 33.
    Cohen, B. E. 1975. The permeability of liposomes to non- electrolytes. I. Activation energies for permeation. J. Membr. Biol. 20: 205–234.PubMedCrossRefGoogle Scholar
  34. 34.
    Redwood, W. R., and D. A. Haydon. 1969. Influence of temperature and membrane composition on the water permeability of lipid bilayers. J. Theor. Biol. 22: 1–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Graziani, Y., and A. Livne. 1972. Water permeability of lipid bilayer membranes: Sterol-lipid interaction. J. Membr. Biol. 7: 275–284.CrossRefGoogle Scholar
  36. 36.
    Engelman, D. M. 1970. X-ray diffraction studies of phase transitions in the membrane of Mycoplasma laidlawii. J. Mol. Biol. 47: 115–117.PubMedCrossRefGoogle Scholar
  37. 37.
    Phillips, M. C., R. M. Williams, and D. Chapman. 1969. On the nature of hydrocarbon chain motions in lipid liquid crystals. Chem. Phys. Lipids 3: 234–244.CrossRefGoogle Scholar
  38. 38.
    Hubbell, W. L., and H. M. McConnell. 1971. Molecular motion in spin-labeled phospholipids and membranes. J. Am. Chem. Soc. 93: 314–326.PubMedCrossRefGoogle Scholar
  39. 39.
    Sackmann, E., and H. Trauble. 1972. Studies of the crystalline- liquid crystalline phase transition of lipid model membranes. I. Use of spin labels and optical probes as indicators for the phase transition. J. Am. Chem. Soc. 94: 4482–4491.PubMedCrossRefGoogle Scholar
  40. 40.
    Kedem, O., and A. Katchalsky. 1958. Thermodynamic analysis of the permeability of biological membranes to nonelectrolytes. Biochim. Biophys. Acta 27: 229–246.PubMedCrossRefGoogle Scholar
  41. 41.
    Dampier, W. C. 1948. A History of Science. Cambridge University Press, London, pp. 249–251.Google Scholar
  42. 42.
    Starling, E. H. 1896. On the absorption of fluid from the connective tissue spaces. J. Physiol. ( London ) 19: 312–326.Google Scholar
  43. 43.
    Meschia, G., and I. Setnikar. 1958. Experimental study of osmosis through a collodion membrane. J. Gen. Physiol. 42:429– 444.PubMedCrossRefGoogle Scholar
  44. 44.
    Mauro, A. 1960. Some properties of ionic and nonionic semipermeable membranes. Circulation 21: 845–858.Google Scholar
  45. 45.
    Dainty, J. 1963. Water relations of plant cells. Adv. Bot. Res. 1: 279–326.CrossRefGoogle Scholar
  46. 46.
    Dainty, J. 1965. Osmotic flow. Symp. Soc. Exp. Biol. 19: 75–85.PubMedGoogle Scholar
  47. 47.
    Robbins, E., and A. Mauro. 1960. Experimental study of the independence of diffusion and hydrodynamic permeability coefficients in collodion membranes. J. Gen. Physiol. 43:523– 532.PubMedGoogle Scholar
  48. 48.
    Dick, D. A. T. 1966. Cell Water. Butterworths, London, pp. 17– 27.Google Scholar
  49. 49.
    Dennis, V. W., N. W. Stead, and T. E. Andreoli. 1970. Molecular aspects of polyene- and sterol-dependent pore formation in thin lipid membranes. J. Gen. Physiol. 55: 375–400.PubMedCrossRefGoogle Scholar
  50. 50.
    Hill, A. 1982. Osmosis: A bimodal theory with implications for symmetry. Proc. R. Soc. London Ser. B 215: 155–174.CrossRefGoogle Scholar
  51. 51.
    Staverman, A. J. 1951. The theory of measurement of osmotic pressure. Reel. Trav. Chim. Pays-Bas 70: 344–352.CrossRefGoogle Scholar
  52. 52.
    Andreoli, T. E., and J. A. Schäfer. 1976. Mass transport across cell membranes: The effects of antidiuretic hormone on water and solute flows in epithelia. Annu. Rev. Physiol. 39: 451–500.CrossRefGoogle Scholar
  53. 53.
    Koefoed-Johnsen, V., and H. H. Ussing. 1953. The contribution of diffusion and flow to the passage of D20 through living membranes: Effect of neurohypophysial hormone on isolated anuran skin. Acta Physiol. Scand. 28: 60–76.PubMedCrossRefGoogle Scholar
  54. 54.
    Pappenheimer, J. R., E. M. Renkin, and L. M. Borrero. 1951. Filtration, diffusion and molecular sieving through peripheral capillary membranes. Am. J. Physiol. 167: 13–46.PubMedGoogle Scholar
  55. 55.
    Pappenheimer, J. R. 1953. Passage of molecules through capillary walls. Physiol. Rev. 33: 387–423.PubMedGoogle Scholar
  56. 56.
    Andreoli, T. E., and S. L. Troutman. 1971. An analysis of unstirred layers in series with tight and porous lipid bilayer membranes. J. Gen. Physiol. 57: 464–478.PubMedCrossRefGoogle Scholar
  57. 57.
    Lea, E. J. A. 1963. Permeation through long narrow pores. J. Theor. Biol. 5: 102–107.PubMedCrossRefGoogle Scholar
  58. 58.
    Dick, D. A. T. 1966. Cell Water. Butterworths, London, pp. 102– 111.Google Scholar
  59. 59.
    Levitt, D. G. 1974. A new theory of transport for cell membrane pores. I. General theory and application to red cell. Biochim. Biophys. Acta 373: 115–131.PubMedCrossRefGoogle Scholar
  60. 60.
    Andersen, B., and H. H. Ussing. 1957. Solvent drag on non- electrolytes during osmotic flow through isolated toad skin and its response to antidiuretic hormone. Acta Physiol. Scand. 39:228– 239.PubMedCrossRefGoogle Scholar
  61. 61.
    Durbin, R. P., H. Frank, and A. K. Solomon. 1956. Water flow through frog gastric mucosa. J. Gen. Physiol. 39: 535–551.PubMedCrossRefGoogle Scholar
  62. 62.
    Renkin, E. M. 1955. Filtration, diffusion and molecular sieving through porous cellulose membranes. J. Gen. Physiol. 38:225– 243.Google Scholar
  63. 63.
    Solomon, A. K. 1968. Characterization of biological membranes by equivalent pores. J. Gen. Physiol. 51: 335s–364s.PubMedGoogle Scholar
  64. 64.
    Faxen, H. 1922. Die Bewegung einer starren Kugel längs der achse eines mit zäher Flüssigkeit gefüllten Rohres. Arch. Mat. Astron. Fys. 17: 27–43.Google Scholar
  65. 65.
    Ferry, J. D. 1937. Statistical evaluation of sieve constants in ultrafiltration. J. Gen. Physiol. 20: 95–104.CrossRefGoogle Scholar
  66. 66.
    Andreoli, T. E. 1973. On the anatomy of amphotericin B-cholesterol pores in lipid bilayer membranes. Kidney Int. 4: 337–345.PubMedCrossRefGoogle Scholar
  67. 67.
    Andreoli, T. E., V. W. Dennis, and A. M. Weigl. 1969. The effect of amphotericin B on the water and nonelectrolyte permeability of thin lipid membranes. J. Gen. Physiol. 53: 133–156.PubMedCrossRefGoogle Scholar
  68. 68.
    Andreoli, T. E., J. A. Schafer, and S. L. Troutman. 1971. Coupling of solute and solvent flows in porous lipid bilayer membranes. J. Gen. Physiol. 57: 479–493.PubMedCrossRefGoogle Scholar
  69. 69.
    Holz, R., and A. Finkelstein. 1970. The water and nonelectrolyte permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B. J. Gen. Physiol. 56:125– 145.CrossRefGoogle Scholar
  70. 70.
    Solomon, A. K., and C. M. Gary-Bobo. 1972. Aqueous pores in lipid bilayers and red cell membranes. Biochim. Biophys. Acta 255: 1019–1021.PubMedCrossRefGoogle Scholar
  71. 71.
    Al-Zahid, G., J. A. Schafer, S. L. Troutman, and T. E. Andreoli. 1977. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules: Evidence for parallel ADH- sensitive pathways for water and solute diffusion in luminal plasma membranes. J. Membr. Biol. 31: 103–129.PubMedCrossRefGoogle Scholar
  72. 72.
    Nernst, W. 1904. Theorie der Reactionsgeschwindigkeit in heterogenen Systemen. Z. Phys. Chem. 47: 52–55.Google Scholar
  73. 73.
    Teorell, T. 1936. A method of studying conditions within diffusion layers. J. Biol. Chem. 113: 735–748.Google Scholar
  74. 74.
    Cass, A., and A. Finkelstein. 1967. Water permeability of thin lipid membranes. J. Gen. Physiol. 50: 1765–1784.PubMedCrossRefGoogle Scholar
  75. 75.
    Ginzburg, B. Z., and A. Katchalsky. 1963. The frictional coefficient of the flows of nonelectrolytes through artificial membranes. J. Gen. Physiol. 47: 403–408.PubMedCrossRefGoogle Scholar
  76. 76.
    Dainty, J., and C. R. House. 1966. Unstirred layers in frog skin. J. Physiol. (London) 182: 66–78.Google Scholar
  77. 77.
    Dainty, J., and C. R. House. 1966. An examination of the evidence for membrane pores in frog skin. J. Physiol. ( London ) 185: 172–184.Google Scholar
  78. 78.
    Diamond, J. M. 1966. A rapid method for determining voltage- concentration relations across membranes. J. Physiol. ( London ) 183: 83–100.Google Scholar
  79. 79.
    Hays, R. M., and N. Franki. 1970. The role of water diffusion in the action of vasopressin. J. Membr. Biol. 2: 263–276.CrossRefGoogle Scholar
  80. 80.
    Sallee, V. L., and J. M. Dietschy. 1973. Determinants of intestinal mucosal uptake of short- and medium-chain fatty acids and alcohols. J. Lipid Res. 14: 475–484.PubMedGoogle Scholar
  81. 81.
    Wilson, F., and J. M. Dietschy. 1972. Characterization of bile acid absorption across the unstirred water layer and brush border of the rat jejunum. J. Clin. Invest. 51: 3015–3025.PubMedCrossRefGoogle Scholar
  82. 82.
    Wright, E. M., and J. W. Prather. 1970. The permeability of the frog choroid plexus to nonelectrolytes. J. Membr. Biol. 2:127– 149.CrossRefGoogle Scholar
  83. 83.
    Wright, E.M., A. P. Smulders, and J. M. Tormey. 1972. The role of the lateral intercellular spaces and solute polarization effects on the passive flow of water across the rabbit gallbladder. J. Membr. Biol. 7: 198–219.CrossRefGoogle Scholar
  84. 84.
    Schafer, J. A., C. S. Patlak, and T. E. Andreoli. 1974. Osmosis in cortical collecting tubules: A theoretical and experimental analysis of the osmotic transient phenomenon. J. Gen. Physiol. 64:201– 227.PubMedGoogle Scholar
  85. 85.
    Hanai, T., and D. A. Haydon. 1966. The permeability of bi- molecular lipid membranes. J. Theor. Biol. 11: 370–382.PubMedCrossRefGoogle Scholar
  86. 86.
    Green, K., and T. Otori. 1970. Direct measurements of membrane unstirred layers. J. Physiol. ( London ) 207: 93–102.Google Scholar
  87. 87.
    Colton, C. K. 1967. Artificial Kidney—Chronic Uremia Program, National Institute of Arthritis and Metabolic Disease, National Institutes of Health, Federal Clearinghouse Accession No. PB 182–281.Google Scholar
  88. 88.
    Farquhar, M. D., and G. E. Palade. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17: 375–412.PubMedCrossRefGoogle Scholar
  89. 89.
    Wright, E. M., and R. J. Pietras. 1974. Routes of nonelectrolyte permeation across epithelial membranes. J. Membr. Biol. 17:293– 312.PubMedGoogle Scholar
  90. 90.
    Everitt, C. T., W. R. Redwood, and D. A. Haydon. 1969. Problem of boundary layers in the exchange diffusion of water across bimolecular lipid membranes. J. Theor. Biol. 22: 20–32.PubMedCrossRefGoogle Scholar
  91. 91.
    Schafer, J. A., and T. E. Andreoli. 1972. Cellular constraints to diffusion: The flows in isolated mammalian collecting tubules. J. Clin. Invest. 51: 1264–1278.PubMedCrossRefGoogle Scholar
  92. 92.
    Hebert, S. C., and T. E. Andreoli. 1980. Interactions of temperature and ADH on transport processes in cortical collecting tubules. Am. J. Physiol. 238: F470–F480.PubMedGoogle Scholar
  93. 93.
    Schafer, J. A., and T. E. Andreoli. 1972. The effect of antidiuretic hormone on solute flows in isolated mammalian collecting tubules. J. Clin. Invest. 51: 1279–1286.PubMedCrossRefGoogle Scholar
  94. 94.
    Parisi, M., and Z. F. Piccini. 1973. The penetration of water into the epithelium of toad urinary bladder and its modification by oxytocin. J. Membr. Biol. 12: 227–246.PubMedCrossRefGoogle Scholar
  95. 95.
    Levine, S. D., M. Jacoby, and A. Finkelstein. 1984. The water permeability of toad bladder. I. Permeability of barriers in series with the luminal membrane. J. Gen. Physiol, 83: 529–541.PubMedCrossRefGoogle Scholar
  96. 96.
    Levine, S. D., M. Jacoby, and A. Finkelstein. 1984. The water permeability of toad bladder. II. The value of PfIPd(w) for the antidiuretic hormone-induced water-permeation pathway. J. Gen. Physiol. 83: 543–561.PubMedCrossRefGoogle Scholar
  97. 97.
    Hebert, S. C., J. A. Schafer, and T. E. Andreoli. 1981. The effects of antidiuretic hormone (ADH) on solute and water transport in mammalian nephron. J. Membr. Biol. 58: 1–19.PubMedCrossRefGoogle Scholar
  98. 98.
    Mackay, D., and P. Meares. 1959. The electrical conductivity and electro osmotic permeability of a cation exchange resin. Trans. Faraday Soc. 55: 1221–1229.CrossRefGoogle Scholar
  99. 99.
    Leaf, A., and R. M. Hays. 1962. Permeability of the isolated toad bladder to solutes and its modification by vasopressin. J. Gen. Physiol. 45: 921–932.PubMedCrossRefGoogle Scholar
  100. 100.
    Hays, R. M. 1972. The movement of water across vasopressin- sensitive epithelia. Curr. Top. Membr. Transp, Vol. 3, 339–366.CrossRefGoogle Scholar
  101. 101.
    Hays, R. M., and A. Leaf. 1962. Studies on the movement of water through the isolated toad bladder and its modification by vasopressin. J. Gen. Physiol. 45: 905–919.PubMedCrossRefGoogle Scholar
  102. 102.
    Wang, J. H., C. V. Robinson, and I. S. Edelman. 1953. Self- diffusion and structure of liquid water, III. Measurements of the self-diffusion of liquid water with H2, H3, and O18 as tracers. J. Am. Chem. Soc. 75: 466–476.CrossRefGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1986

Authors and Affiliations

  • James A. Schafer
    • 1
  • Thomas E. Andreoli
    • 2
  1. 1.Nephrology Research and Training Center, Departments of Physiology and Biophysics, and MedicineUniversity of AlabamaBirminghamUSA
  2. 2.Departments of Internal Medicine and PhysiologyUniversity of Texas Health Science CenterHoustonUSA

Personalised recommendations