Skip to main content
Log in

Tight junction regulation during impaired ion transport in blind loops of rat jejunum

  • Published:
Research in Experimental Medicine

Summary

Epithelial cell tight junction structure in self-filling blind loops of rat jejunum, a model for blind loop syndrome in humans, was analyzed morphometrically along the crypt-villus axis. In control jejunum, the number of strands and junctional depth, including meshwork depth, decreased from crypt to villus tip. In the blind loop, aberrant strands appeared below the meshwork, particularly in crypt cells. Consequently, total junctional depth was greater than in controls. Furthermore, strand number and junctional meshwork depth were increased in blind loops at the villus tip. It is that site along the crypt-villus axis which showed the most shallow junction in control jejunum. This structural change is paralleled by a three-fold increase in epithelial resistance as previously measured by alternating current impedance analysis. Relative Na over Cl permeability (PNa:Cl) was obtained from dilution potential measurements. PNa:Cl was 1.50∶1 in control jejunum and 1.35∶1 in the blind loop (n.s.). Considering the cation selectivity of the tight junction, the increase in epithelial resistance in blind loops cannot be attributed to a collapse of the lateral intercellular space but is due to changes in tight junctional permeability resulting from structural alteration. The blind loop syndrome represents a further example of diminished epithelial ion transport and concomitant decrease in tight junction permeability, thus supporting the general concept of regulation of the tight junction in response to active transport activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bentzel CJ, Fromm M, Palant CE, Hegel U (1987) Protamine alters structure and conductance of Necturus gallbladder tight junctions without major effect on the apical membrane. J Membrane Biol 95:9–20

    Article  CAS  Google Scholar 

  2. Bentzel CJ, Hainau B, Ho S, Hui SW, Edelman A, Anagnostopoulos T, Benedetti EL (1980) Cytoplasmic regulation of tight-junction permeability: effect of plant cytokinins. Am J Physiol 239:C75-C89

    PubMed  CAS  Google Scholar 

  3. Bentzel CJ, Martinez M, Hainau B, Fromm M, Hegel U (1982) Morphological and physiological factors determining transjunctional fluxes. In: Bradley SE, Purcell EF (eds) The paracellular pathway. Josiah Macy Jr Foundation, New York, pp 275–286

    Google Scholar 

  4. Boulpaep EL (1972) Permeability changes of the proximal tubule of Necturus during saline loading. Am J Physiol 222:517–531

    PubMed  CAS  Google Scholar 

  5. Claude P (1978) Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludens. J Membrane Biol 39:219–232

    Article  CAS  Google Scholar 

  6. Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from tight and leaky epithelia. J Cell Biol 58:390–400

    Article  PubMed  CAS  Google Scholar 

  7. Duffey ME, Hainau B, Ho S, Bentzel CJ (1981) Regulation of epithelial tight junction permeability by cyclic AMP. Nature 294:451–453

    Article  PubMed  CAS  Google Scholar 

  8. Fromm M, Palant CE, Bentzel CJ, Hegel U (1985) Protamine reversibly decreases paracellular cation permeability in Necturus gallbladder. J Membrane Biol 87:141–150

    Article  CAS  Google Scholar 

  9. Fromm M, Schulzke JD, Hegel U (1985) Epithelial and subepithelial contributions to transmural electrical resistance of intact rat jejunum, in vitro. Pflügers Arch 405:400–402

    Article  PubMed  CAS  Google Scholar 

  10. Gracey M, Papadimitriou J, Bower G (1974) Ultrastructural changes in the small intestines of rats with self-filling blind loops. Gastroenterology 67:646–651

    PubMed  CAS  Google Scholar 

  11. Kottra G, Frömter E (1984) Rapid determination of intraepithelial resistance barriers by alternating current spectroscopy. II. Test of model circuits and quantification of results. Pflügers Arch 402:421–432

    Article  PubMed  CAS  Google Scholar 

  12. Krasny EJ, DiBona AI, Frizzell RA (1982) Regulation of paracellular permselectivity in flounder intestine. Bull Mount Des Isl Biol Lab 22:83–85

    Google Scholar 

  13. Lewy JE, Windhager EE (1968) Peritubular control of proximal tubular fluid reabsorption in the rat kidney. Am J Physiol 214:943–954

    PubMed  CAS  Google Scholar 

  14. Luciano L, Reale E, Rechkemmer G, Engelhardt W v. (1984) Structure of zonulae occludentes and the permeability of the epithelium to short-chain fatty acids in the proximal and the distal colon of guinea pig. J Membrane Biol 82:145–156

    Article  CAS  Google Scholar 

  15. Madara JL (1987) Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am J Physiol 253:C171–175

    PubMed  CAS  Google Scholar 

  16. Madara JL (1983) Increases in guinea pig small intestinal transepithelial resistance induced by osmotic loads are accompanied by rapid alterations in absorptive-cell tight-junction structure. J Cell Biol 97:125–136

    Article  PubMed  CAS  Google Scholar 

  17. Madara JL, 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 and junctional charge selectivity. J Cell Biol 102:2125–2136

    Article  PubMed  CAS  Google Scholar 

  18. Madara JL, Pappenheimer JR (1987) Structural basis for physiological regulation of paracellular pathways in intestinal epithelia. J Membrane Biol 100:149–164

    Article  CAS  Google Scholar 

  19. Madara JL, Trier JS, Neutra MR (1980) Structural changes in the plasma membrane accompanying differentiation of epithelial cells in human and monkey small intestine. Gastroenterology 78:963–975

    PubMed  CAS  Google Scholar 

  20. Madara JL, Trier JS (1982) Structure and permeability of goblet cell tight junctions in rat small intestine. J Membrane Biol 66:145–157

    Article  CAS  Google Scholar 

  21. Marcial MA, Carlson SL, Madara JL (1984) Partitioning of paracellular conductance along the ileal crypt-villus-axis: a hypothesis based on structural analysis with detailed consideration of tight junction structure-function relationships. J Membrane Biol 80:59–70

    Article  CAS  Google Scholar 

  22. Martinez-Palomo A, Meza I, Beaty G, Cereijido M (1980) Experimental modulation of occluding junctions in a transporting epithelium. J Cell Biol 87:736–745

    Article  PubMed  CAS  Google Scholar 

  23. Maunsbach AB, Boulpaep EL (1980) Hydrostatic pressure changes related to paracellular shunt ultrastructure in proximal tubule. Kidney Int 17:732–748

    Article  PubMed  CAS  Google Scholar 

  24. Menge H, Köhn R, Dietermann KH, Lorenz-Mayer H, Riecken EO, Robinson JWL (1975) Structural and morphological alterations in the intestines of rats with an experimental blind loop syndrome. Res Exp Med 166:67–78

    Article  Google Scholar 

  25. Menge H, Murer H (1983) Funktionelle Charakterisierung der Bürstensaummembranen selbstfüllender Blindschlingen des Rattenjejunums. Z Gastroenterol 21:381–382

    Google Scholar 

  26. Møllgård K, Malinowska DH, Saunders NR (1976) Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus. Nature 264:293–294

    Article  Google Scholar 

  27. Palant CE, Duffey ME, Mookerjee BK, Ho S, Bentzel CJ (1983) Regulation of tight junction permeability and structure in Necturus gallbladder. Am J Physiol 245:C203-C212

    PubMed  CAS  Google Scholar 

  28. Robinson RA, Stokes RH (1959) Electrolyte solutions, 2nd edn. Academic, London

    Google Scholar 

  29. Schultz SG (1977) The role of paracellular pathways in isotonic fluid transport. Yale J Biol Med 50:99–113

    PubMed  CAS  Google Scholar 

  30. Schulzke JD, Fromm M, Hegel U (1986) Epithelial and subepithelial resistance of rat large intestine: segmental differences, effect of stripping, time course, and action of aldosterone. Pflügers Arch 407:632–637

    Article  PubMed  CAS  Google Scholar 

  31. Schulzke JD, Fromm M, Menge H, Riecken EO (1987) Impaired intestinal sodium and chloride transport in the blind loop syndrome of the rat. Gastroenterology 92:693–698

    PubMed  CAS  Google Scholar 

  32. Schulzke JD, Fromm M, Menge H, Riecken EO (1985) Der gestörte Elektrolyttransport im experimentellen Blindsacksyndrom. Schweiz Med Wochenschr 115:1032

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schulzke, J.D., Fromm, M., Zeitz, M. et al. Tight junction regulation during impaired ion transport in blind loops of rat jejunum. Res. Exp. Med. 190, 59–68 (1990). https://doi.org/10.1007/PL00020007

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/PL00020007

Key words

Navigation