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Osmotic water flow in leaky epithelia

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Summary

I review three currently unsolved and controversial problems in understanding solute-linked water transport in epithelia.

  1. 1.

    Values of osmotic water permeability (P osm) calculated from steady-state osmotic flow in response to a gradient of a probe molecule tend to be underestimates, because of three unstirred-layer (USL) effects. These are: dissipation of the probe's gradient by diffusion in USL's; reduction of the probe's gradient, due to the sweeping-away effect of water flow gencrated by the probe itself; and solute polarization (creation of an opposing gradient of an initially symmetrically distributed solute by the sweeping-away effect). These errors increase with probe permeability. USL thickness,P osm, and concentration ratio of symmetrically distributed solute to probe, and vary inversely as the fractional area available for water flow (e.g., lateral intercellular space width). The form of an osmotic transient, and the possibility of extracting a trueP osm value from the transient, depend on the relative values of three time constants: those for solute diffusion in USL's, for solute polarization by water flow in USL's and for measuring water flow. Sweeping-away effects cause major underestimates (by one or more orders of magnitude) in epithelialP osm determinations, as shown by apparent streaming potentials during osmotic flow and by transiently reversed flows after removal of the probe. TrueP osm values for leaky epithelia probably exceed 10−3 or 10−2 cm/sec·osm. The necessary conditions for resolving osmotic transients are set out.

  2. 2.

    I illustrate the difficulties in deciding what fraction of transepithelial water flow is via the cells, and what fraction via the junctions. There is no existing method for answering this question.

  3. 3.

    Controversies about the validity, or need for modification, of the standing-gradient theory are discussed.

Progress in this field requires new methods: to resolve osmotic transients; to separate transcellular and transjunctional water flows; and to measure solute concentrations in lateral intercellular spaces directly.

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References

  • Andreoli, T.F., Schafer, J.A. 1979. External solution driving forces for isotonic fluid absorption in proximal tubule.Fed. Proc. 38:154

    PubMed  Google Scholar 

  • Andreoli, T.E., Schafer, J.A., Troutman, S.L. 1978. Perfusion rate-dependence of transepithelial osmosis in isolated proximal convoluted tubules: Estimation of the hydraulic conductance.Kidney Int. 14:263

    PubMed  Google Scholar 

  • Barry, P.H., Hope, A.D. 1969. Electroosmosis in membranes: Effects of unstirred layers and transport numbers. II. Experimental.Biophys. J. 9:729

    PubMed  Google Scholar 

  • Boulpaep, E.L. 1978. Solute-coupled water transport in the kidney.In: Molecular Specialization and Symmetry in Membrane Function. A.K. Solomon and M. Karnovsky, editors. pp. 294–314. Harvard University Press, Cambridge

    Google Scholar 

  • Boulpaep, E.L., Sackin, H. 1977. Role of the paracellular pathway in isotonic fluid movement across the renal tubule.Yale J. Biol. Med. 50:115

    PubMed  Google Scholar 

  • Curran, P.F., McIntosh, J.R. 1962. A model system for biological water transport.Nature (London) 193:347

    Google Scholar 

  • Curran, P.F., Solomon, A.K. 1957. Ion and water fluxes in the ileum of rats.J. Gen. Physiol. 41:143

    PubMed  Google Scholar 

  • Dainty, J. 1963. Water relations in plant cells.Adv. Botan. Res. 1:279

    Google Scholar 

  • Dellasega, M., Grantham, J.J. 1973. Regulation of renal tubule cell volume in hypotonic media.Am. J. Physiol. 224:1299

    Google Scholar 

  • Diamond, J.M. 1964. The mechanism of isotonic water transport.J. Gen. Physiol. 48:15

    Google Scholar 

  • Diamond, J.M. 1966. Non-linear osmosis.J. Physiol. (London) 183:58

    Google Scholar 

  • Diamond, J.M. 1977. Twenty-first Bowditch Lecture. The epithelial junction: Bridge, gate, and fence.Physiologist 20:10

    PubMed  Google Scholar 

  • Diamond, J.M. 1978. Solute-linked water transport in epithelia.In: Membrane Transport Processes. J.M. Hoffman, editor. Vol. 1, pp. 257–276. Raven Press, New York

    Google Scholar 

  • Diamond, J.M., Bossert, W.H. 1967. Standing-gradient osmotic flow. A mechanism for coupling of water and solute transport in epithelia.J. Gen. Physiol. 50:2061

    PubMed  Google Scholar 

  • Diamond, J.M., Bossert, W.H. 1968. Functional consequences of ultrastructural geometry in “backwards” fluid-transporting epithelia.J. Cell Biol. 37:694

    PubMed  Google Scholar 

  • DiBona, D.R., Mills, J.W. 1979. Distribution of Na+ pump sites in transporting epithelia.Fed. Proc. 38:134

    PubMed  Google Scholar 

  • Fischbarg, J., Warshavsky, C.R., Lim, J.J. 1977. Pathways for hydraulically and osmotically-induced water flows across epithelia.Nature (London) 266:71

    Google Scholar 

  • Frömter, E., Diamond, J.M. 1972. Route of passive ion permeation in epithelia.Nature New Biol. 235:9

    PubMed  Google Scholar 

  • Frömter, E., Lüer, K. 1969. Determination of fixed-charge concentration in the epithelium of the convoluted tubule of the rat kindey. The effect of pH.Pfluegers. Arch. Gesamte Physiol. 307:R76

    Google Scholar 

  • Grandchamp, A., Boulpaep, E.L. 1974. Pressure control of sodium reabsorption and intercellular backflux across proximal kidney tubule.J. Clin. Invest. 54:69

    PubMed  Google Scholar 

  • Gupta, B.L., Hall, T.A. 1979. Quantitative electron probe X-ray microanalysis of electrolyte elements within epithelial tissue compartment.Fed. Proc. 38:144

    PubMed  Google Scholar 

  • Gupta, B.L., Hall, T.A., Naftalin, R.J. 1978. Microprobe measurement of Na, K and Cl concentration profiles in epithelial cells and intercellular spaces of rabbit ileum.Nature (London) 272:70

    Google Scholar 

  • Hays, R.M. 1972. The movement of water across vasopressin-sensitive epithelia.Curr. Top. Membr. Transp. 3:339

    Google Scholar 

  • Hill, A.E. 1975a. Solute-solvent coupling in epithelia. A critical examination of the standing-gradient osmotic flow theory.Proc. R. Soc. London B 190:99

    Google Scholar 

  • Hill, A.E. 1975b. Solute-solvent coupling in epithelia: An electro-osmotic theory of fluid transfer.Proc. R. Soc. London B 190:115

    Google Scholar 

  • Hill, A.E. 1975c. Solute-solvent coupling in epithelia: contribution of the junctional pathway to fluid production.Proc. R. Soc. London B 191:537

    Google Scholar 

  • Hill, A.E., Hill, B.S. 1978a. Sucrose fluxes and junctional water flow acrossNecturus gallbladder epithelium.Proc. R. Soc. London B 200:163

    Google Scholar 

  • Hill, B.S., Hill, A.E. 1978b. Fluid transfer byNecturus gallbladder epithelium as a function of osmolarity.Proc. R. Soc. London B 200:151

    Google Scholar 

  • House, C.R. 1974. Water Transport in Cells and Tissues. Edward Arnold, London

    Google Scholar 

  • Huss, R.E., Marsh, D.J. 1975. A model of NaCl and water flow through paracellular pathways and renal proximal tubules.J. Membrane Biol. 23:305

    Google Scholar 

  • Huss, R.E., Stephenson, J.L. 1979. A mathematical model of proximal tubule absorption.J. Membrane Biol. 47:377

    Google Scholar 

  • Lim, J.J., Fischbarg, J. 1976. Standing-gradient osmotic flow: Examination of its validity using an analytical method.Biochim. Biophys. Acta 443:339

    PubMed  Google Scholar 

  • Machen, T.E., Diamond, J.M. 1969. An estimate of the salt concentration in the lateral intercellular spaces of rabbit gall-bladder during maximal fluid transport.J. Membrane Biol. 1:194

    Google Scholar 

  • Moreno, J.H. 1975. Routes of nonelectrolyte permeability in gallbladder Effects of 2, 4,6-triaminopyrimidinium (TAP).J. Gen. Physiol. 66:117

    PubMed  Google Scholar 

  • Os, C.H. van, Slegers, J.F.G. 1973. Path of osmotic water flow through rabbit gallbladder epithelium.Biochim. Biophys. Acta 291:197

    PubMed  Google Scholar 

  • Os, C.H. van, Wiedner, G. 1977. Hydraulic conductivities of epithelial tissues: Osmosisvs. filtration.Proc. Int. Union Physiol. Sci. 13:778

    Google Scholar 

  • Os, C.H. van, Wiedner, G., Wright, E.M. 1979. Volume flows across gallbladder epithelium induced by small hydrostatic and osmotic gradients.J. Membrane Biol. 49:1

    Google Scholar 

  • Pedley, T.J., Fischbarg, J. 1978. The development of osmotic flow through an unstirred layer.J. Theor. Biol. 70:427

    PubMed  Google Scholar 

  • Sackin, H., Boulpaep, E.L. 1975. Models for coupling of salt and water transport. Proximal tubular reabsorption inNecturus kidney.J. Gen. Physiol. 66:671

    PubMed  Google Scholar 

  • Schafer, J.A., Patlak, C.S., Andreoli, T.E. 1974. Osmosis in cortical collecting tubules. A theoretical and experimental analysis of the osmotic transient phenomenon.J. Gen. Physiol. 64:201

    Google Scholar 

  • Schafer, J.A., Patlak, C.S., Andreoli, T.E. 1975. A component of fluid absorption linked to passive ion flows in the superficialpars recta.J. Gen. Physiol. 66:445

    PubMed  Google Scholar 

  • Schafer, J.A., Patlak, C.S., Troutman, S.L., Andreoli, T.E. 1978. Volume absorption in thepars recta. II. Hydraulic conductivity coefficient.Am. J. Physiol. 234:340

    Google Scholar 

  • Segel, L.A. 1970. Standing gradient flows driven by active solute transport.J. Theor. Biol. 29:223

    Google Scholar 

  • Smyth, D.H., Wright, E.M. 1966. Streaming potentials in the rat small intestine.J. Physiol. (London) 182:591

    Google Scholar 

  • Spring, K.R., Hope, A. 1978. Size and shape of the lateral intercellular spaces in a living epithelium.Science 200:54

    PubMed  Google Scholar 

  • Spring, K.R., Hope, A. 1979. Dimensions of cells and lateral intercellular spaces in livingNecturus gallbladder.Fed. Proc. 38:128

    PubMed  Google Scholar 

  • Tormey, J.M., Diamond, J.M. 1967. The ultrastructural route of fluid transport in rabbit gallbladder.J. Gen. Physiol. 50:2031

    PubMed  Google Scholar 

  • Wall, D.J., Oschman, J.L., Schmidt-Nielsen, B. 1970. Fluid transport: Concentration of the intercellular compartment.Science 167:1497

    PubMed  Google Scholar 

  • Wedner, H.J., Diamond, J.M. 1969. Contributions of unstirred-layer effects to apparent electrokinetic phenomena in the gall bladder.J. Membrane Biol. 1:92

    Google Scholar 

  • Weinbaum, S., Goldgraben, J.R. 1972. On the movement of water and solute in extracellular channels with filtration, osmosis, and active transport.J. Fluid Mech. 58:481

    Google Scholar 

  • Welling, D.J., Welling, L.W. 1979. Cell shape as an indicator of volume reabsorption in proximal nephron.Fed. Proc. 38:121

    PubMed  Google Scholar 

  • Whittembury, G. 1967. Sobre los mecanismos de absorción en el tubo proximal del riñón.Acta Cient. Venez. Supl. 3:71

    Google Scholar 

  • Whittembury, G., Oken, D.E., Windhager, E.E., Solomon, A.K. 1959. Single proximal tubules ofNecturus tubule. IV. Dependence of H2O movement on osmotic gradients.Am. J. Physiol. 197:1121

    PubMed  Google Scholar 

  • Whittembury, G., Sugino, N., Solomon, A.K. 1960. Effect of antidiuretic hormone and calcium on the equivalent pore radius of kidney slices fromNecturus.Nature (London) 187:699

    Google Scholar 

  • Wright, E.M., Prather, J.W. 1970. The permeability of the frog choroid plexus to nonelectrolytes.J. Membrane Biol. 2:127

    Google Scholar 

  • Wright, E.M., Smulders, A.P., Tormey, J.M. 1972. The role of the lateral intracellular spaces and solute polarization effects in the passive flow of water across the rabbit gallbladder.J. Membrane Biol. 7:198

    Google Scholar 

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  1. Physiology Department, UCLA Medical Center, 90024, Los Angeles, California

    Jared M. Diamond

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Diamond, J.M. Osmotic water flow in leaky epithelia. J. Membrain Biol. 51, 195–216 (1979). https://doi.org/10.1007/BF01869084

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