Summary
Isolated intestinal segments from rats or hamsters were recirculated with balanced salt solutions containing fluorocarbon emulsion to provide 6 vpc oxygen. The lumen contained an axial Ag−AgCl electrode, and the serosal surface was surrounded by a cylindrical shell of Ag−AgCl. Transmural impedances were measured at frequencies from 0.01–30 kHz before and after removal of the mucosal epithelium. The resistance of intercellular junctions,R J , the distributed resistance of the lateral spaces,R L , and the distributed membrane capacitance,C M , were computed from the relations between frequency and impedance. Activation of Na-coupled solute transport by addition of glucose, 3-0-methyl glucose, alanine or leucine caused two- to threefold decreases of transepithelial impedance. Typical changes induced by glucose in hamster small intestine wereR J 30→13 Ω,R L 23→10 Ω, andC M 8→20 μF (per cm length of segment). Half maximal response occurred at a glucose concentration of 2–3mm. The area per unit path length of the junctions (Ap/Δx=specific resistance ÷R J ) in glucose activated epithelium was 3.7 cm in hamster midgut and 6.8 cm in rat. These values are close to the 4.3 cm estimated independently from coefficients of solvent drag and hydrodynamic conductance in glucose-activated rat intestine in vivo. The transepithelial impedance response to Na-coupled solute transport was reversibly dependent upon oxygen tension.
It is proposed that activation of Na-coupled solute transport triggers contraction of circumferential actomyosin fibers in the terminal web of the microvillar cytoskeletal system, thereby pulling apart junctions and allowing paracellular absorption of nutrients by solvent drag as described in the previous accompanying paper. Anatomical evidence in support of this hypothesis is presented in the following second accompanying paper.
Similar content being viewed by others
References
Adibi, S.A. 1970. Leucine absorption rate and net movements of sodium and water in human jejunum.J. Appl. Physiol. 18:753–757
Albus, H., Heukelom, J.S. van 1976. The electrophysiological characterization of glucose absorption by the goldfish intestine as compared to mammalian intestines.Comp. Biochem. Physiol. 54A:113–119
Asano, T. 1963. Metabolic disturbances and short-circuit current across intestinal wall of rat.Am. J. Physiol. 207:425–422
Baker, R.D., Watson, S., Long, J.L., Wall, M.J. 1969. Effects of eversion on transmural electrical properties of rat jejunum.Biochim. Biophys. Acta 173:192–197
Barry, R.J.C., Smyth, D.H., Wright, E.M. 1965. Short circuit current and solute transfer by the rat jejunum.J. Physiol. (London) 181:410–431
Bindslev, N., Tormey, J. McD., Wright, E.M. 1974. The effects of electrical and osmotic gradients on lateral intercellular spaces and membrane conductance in a low resistance epithelium.J. Membrane Biol. 19:357–380
Boulpaep, E.L. 1972. Permeability changes of the proximal tubule ofNecturus during saline loading.Am. J. Physiol. 22:517–531
Cereijido, M., Meza, I., Martinez-Palomo, A. 1981. Occluding junctions in cultured epithelial monolayers.Am. J. Physiol. 240:C96-C102
Clarkson, T.W. 1967. The transport of salt and water across isolated rat ileum.J. Gen. Physiol. 50:695–727
Claude, P. 1978. Morphological factors influencing transepithelial permeability: A model for the resistance of the zonnulae occludens.J. Membrane Biol. 39:219–232
Clausen, C., Lewis, S.A., Diamond, J.M. 1979. Impedance analysis of a tight epithelium using a distributed resistance model.Biophys. J. 26:291–318
Cole, K.S. 1968. Membranes, Ions and Impulses. Chs. 1 and 10. University of California Press, Berkley
Crane, R.K. 1968. Absorption of sugars.In: APS Handbook of Physiology. Alimentary Canal III: Intestinal Absorption. pp. 1323–1351. C.F. Code, editor. Williams & Wilkins, Washington, D.C.
Crone, C. 1986. Modulation of solute permeability in microvascular endothelium.Fed. Proc. 45:77–83
Diamond, J.M., Machen, T.E. 1983. Impedance analysis in epithelia and the problem of gastric acid secretion.J. Membrane Biol. 72:17–41
Dorando, F.C., Crane, R.K. 1984. Studies of the kinetics of Na+ gradient-coupled glucose transport as found in brushborder membrane vesicles from rabbit jejunum.Biochim. Biophys. Acta 772:273–287
Feldman, D.S., Rabinovitch, S., Feldman, E.B. 1975. Surfactants and bioelectric properties of rat jejunum.Am. J. Dig. Dis. 20:866–870
Field, M., Fromm, D., McColl, I. 1971. Ion transport in rabbit ileal mucosa: I. Na and Cl fluxes and short circuit current.Am. J. Physiol. 220:1388–1396
Fisher, R.B. 1955. The absorption of water and of some small molecules from the isolated intestine of the rat.J. Physiol. (London) 130:655–664
Fisher, R.B., Parsons, D.S. 1957. Surface area of rat intestinal mucosa.J. Anat. 84:272–282
Frizzell, R.A., Schultz, S.G. 1972. Ionic conductance of extracellular shunt pathway in rabbit ileum.J. Gen. Physiol. 59:318–346
Fromm, M.M., Schulzke, J.D., Hegel, U.H. 1985. Epithelial and subepithelial contributions to transmural electrical resistance of intact rat jejeunum, in vitro.Pfluegers Arch. 405:400–402
Fromter, E. 1972. The route of passive ion movement through the epithelium ofNecturus gallbladder.J. Membrane Biol. 8:259–301
Geyer, R.P., Monroe, R.C., Taylor, K. 1969. Survival of rats having red cells totally replaced with emulsified fluorocarbon.Fed. Proc. 27:384
Hess, P., Lansman, J.B., Tsien, R.W. 1984. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists.Nature (London) 311:538–544
Hildmann, B., Schmidt, A., Murer, H. 1982. Ca2+ transport across basal-lateral plasma membranes from rat small intestinal epithelial cells.J. Membrane Biol. 65: 55–62
Hull, B.E., Staehelin, L.A. 1979. The terminal web. A reevaluation of its structure and function.J. Cell Biol. 81:67–82
Keller, T.C.S., Conzelman, K.A., Chasan, R. 1985. Role of myosin in terminal web contraction in isolated intestinal epithelial brush borders.J. Cell Biol. 100:1647–1655
Keller, T.C.S., Mooseker, M.S. 1982. Ca++-calmodulin dependent phosphorylation of myosin and its role in brush border contraction in vitro.J. Cell Biol. 95:943–959
Lesse, H.J., Mansford, K.R.L. 1971. The effects of insulin and insulin deficiency on the transport and metabolism of glucose by the small intestine.J. Physiol. (London) 212:819–836
Levine, R.R., McNary, W.W., Kornguth, P.J., Leblanc, R. 1970. Histological re-evaluation of everted gut technique for studying intestinal absorption.Eur. J. Pharmacol. 9:211–219
Madara, J.L. 1982. Cup cells: Structure and distribution of a unique class of epithelial cells in guinea pigs, rabbit and monkey small intestine.Gastroenterology 83:981–994
Madara, J.L. 1987. Intestinal absorptive cell tight junctions are linked by cytoskeleton.Am. J. Physiol. 253:C171-C175
Madara, J.L., Barenberg, D., Carlson, S. 1986. Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: Further evidence that the cytoskeleton may influence paracellular permeability.J. Cell Biol. 97:2125–2135
Madara, J.L., Pappenheimer, J.R. 1987. The structural basis for physiological regulation of paracellular pathways in intestinal epithelia.J. Membrane Biol. 100:149–164
Mooseker, M.S. 1985. Organization, chemistry and assembly of the cytoskeletal apparatus of the intestinal brush border.Annu. Rev. Cell Biol. 1:209–241
Munck, G.G. 1972. Effects of sugar and amino-acid transport on transepithelial fluxes of sodium and chloride of short circuited rat jejunum.J. Physiol. (London) 223:699–717
Munck, B.G., Schultz, S.G. 1974. Properties of the passive conductance pathway across in vitro rat jejunum.J. Membrane Biol. 16:163–174
Okada, Y., Irimajiri, A., Inouye, A. 1977. Electrical properties and active solute transport in rat small intestine: II. Conductive properties of transepithelial routes.J. Membrane Biol. 31:221–232
Olesen, P., Crone, C. 1983. Electrical resistance of muscle capillary endothelium.Biophys. J. 42:31–41
Pappenheimer, J.R. 1953. Passage of molecules through capillary walls.Physiol. Rev. 33:387–423
Pappenheimer, J.R., Reiss, K.Z. 1987. Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine of the rat.J. Membrane Biol. 100:123–136
Rodewald, R., Karnovsky, M.J. 1976. Contraction of isolated brush borders from the intestinal epithelium.J. Cell Biol. 70:541–554
Schmidt-Nielsen, B., Davis, L.E. 1968. Fluid transport and tubular intercellular spaces in reptilian kidneys.Science 159:1105–1108
Schultz, S.G., Zalusky, R. 1964. Ion transport in isolated rabbit ileum: I. Short circuit current and Na fluxes.J. Gen. Physiol. 47:567–584
Smulders, A.P., Tormey, J.M.D., Wright, E.M. 1972. The effect of osmotically induced water flows on the permeability and ultrastructure of the rabbit gallbladder.J. Membrane Biol. 7:164–197
Smyth, D.H., Taylor, C.B. 1957. Transfer of water and solutes by an in vitro intestinal preparation.J. Physiol. (London) 136:632–648
Tormey, J. McD., Diamond, J.M. 1967. The ultrastructural route of fluid transport in rabbit gall bladder.J. Gen. Physiol. 50:2031–2060
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pappenheimer, J.R. Physiological regulation of transepithelial impedance in the intestinal mucosa of rats and hamsters. J. Membrain Biol. 100, 137–148 (1987). https://doi.org/10.1007/BF02209146
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02209146