Summary
In order to assess the contribution of transcellular water flow to isosmotic fluid transport acrossNecturus gallbladder epithelium, we have measured the water permeability of the epithelial cell membranes using a nuclear magnetic resonance method. Spin-lattice (T 1) relaxation of water protons in samples of gallbladder tissue where the extracellular fluid contained 10 to 20mm Mn2+ showed two exponential components. The fraction of the total water population responsible for the slower of the two was 24±2%. Both the size of the slow component, and the fact that it disappeared when the epithelial layer was removed from the tissue, suggest that it was due to water efflux from the epithelial cells. The rate constant of efflux was estimated to be 15.6±1.0 sec1 which would be consistent with a diffusive membrane water permeabilityP d of 1.6×103 cm sec1 and an osmotic permeabilityP os of between 0.3×104 and 1.4×104 cm sec1 osmolar1. Using these data and a modified version of the standing-gradient model, we have reassessed the adequacy of a fluid transport theory based purely on transcellular osmotic water flow. We find that the model accounts satisfactorily for near-isosmotic fluid transport by the unilateral gallbladder preparation, but a substantial serosal diffusion barrier has to be included in order to account for the transport of fluid against opposing osmotic gradients.
Similar content being viewed by others
References
Diamond, J.M. 1979. Osmotic water flow in leaky epithelia.J. Membrane Biol. 51:195–216
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. 50:2061–2083
Fabry, M.E., Eisenstadt, M. 1975. Water exchange between red cells and plasma. Measurement by nuclear magnetic relaxation.Biophys. J. 15:1101–1110
Fabry, M.E., Eisenstadt, M. 1978. Water exchange across red cell membranes: II. Measurement by nuclear magnetic resonanceT 1,T 2, andT 12 hybrid relaxation. The effects of osmolarity, cell volume, and medium.J. Membrane Biol. 42:375–398
Farrar, T.C., Becker, E.D. 1971. Pulse and Fourier Transform NMR. Academic, New York
Fettiplace, R., Haydon, D.A. 1980. Water permeability of lipid membranes.Physiol. Rev. 60:510–550
Hill, A.E. 1975. Solute-solvent coupling in epithelia: A critical examination of the standing-gradient osmotic flow theory.Proc. R. Soc. London B 190:99–114
Hill, A.E. 1979. Osmosis.Q. Rev. Biophys. 12:67–99
Hill, A.E. 1980. Salt-water coupling in leaky epithelia.J. Membrane Biol. 56:177–182
Hill, A.E., Hill, B.S. 1978. Sucrose fluxes and junctional water flow acrossNecturus gall bladder epithelium.Proc. R. Soc. London B 200:163–174
House, C.R. 1974. Water Transport in Cells and Tissues. Arnold, London
Mathur-De Vré, R. 1979. The NMR studies of water in biological systems.Prog. Biophys. Mol. Biol. 35:103–134
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. 49:1–20
Persson, B.-E., Spring, K.R. 1982. Gallbladder epithelial cell hydraulic water permeability and volume regulation.J. Gen. Physiol. 79:481–505
Rosenberg, P.A., Finkelstein, A. 1978. Water permeability of gramicidin A-treated lipid bilayer membranes.J. Gen. Physiol. 72:341–350
Sackin, H., Boulpaep, E.L. 1975. Models for coupling of salt and water transport. Proximal tubular reabsorption inNecturus kidney.J. Gen. Physiol. 66:671–733
Spring, K.R. 1983. Fluid transport by gallbladder epithelium.J. Exp. Biol. 106:181–194
Spring, K.R., Ericson, A.-C. 1982. Epithelial cell volume modulation and regulation.J. Membrane Biol. 69:167–176
Spring, K.R., Hope, A. 1979. Fluid transport and the dimensions of cells and interspaces of livingNecturus gallbladder.J. Gen. Physiol. 73:287–305
Suzuki, K., Kottra, G., Kampmann, L., Frömter, E. 1982. Square wave pulse analysis of cellular and paracellular conductance pathways inNecturus gallbladder epithelium.Pfluegers Arch. 394:302–312
Weinstein, A.M., Stephenson, J.L. 1981. Coupled water transport in standing gradient models of the lateral intercellular space.Biophys. J. 35:167–191
Whitlock, R.T., Wheeler, H.O. 1964. Coupled transport of solute and water across rabbit gallbladder epithelium.J. Clin. Invest. 43:2249–2265
Woessner, D.E. 1961. Nuclear transfer effects in nuclear magnetc resonance pulse experiments.J. Chem. Phys. 35:41–48
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Steward, M.C., Garson, M.J. Water permeability ofNecturus gallbladder epithelial cell membranes measured by nuclear magnetic resonance. J. Membrain Biol. 86, 203–210 (1985). https://doi.org/10.1007/BF01870599
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01870599