Skip to main content
SpringerLink
Log in

The tight junctions of renal tubules in the cortex and outer medulla

A quantitative study of the kidneys of six species

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Quantitative aspects of tight junction morphology were systematically studied in the cortical and outer medullary segments of the distal urinary tubules of rat, hamster, rabbit, cat, dog and the primitve primate Tupaia belangeri.

Only minor differences in junctional architecture were found between straight and convoluted portions of the distal tubule. In contrast, the collecting duct in cortex and outer medulla, in all species, exhibits the most elaborate tight junctions observed along the uriniferous tubule.

The present and previous findings from this laboratory indicate that increasing “tightness” of the junctional complexes is apparent along the course of the nephron in all species studied.

The proposed relationship between quantitative aspects of the zonula occludens and presently available values for transepithelial electrical resistance was re-examined for the renal tubules. It was found that for the mammalian kidney a satisfactory correlation exists between the tight junction morphology and presently known functional parameters. This relationship is the more evident the more additional dimensional characteristics of the intercellular clefts are taken into consideration.

It may therefore be concluded that, at least for the mammalian kidney, the assumption of differences in the molecular organization of the tight junctions is not needed to explain so far unresolved discrepancies between tubular morphology and function.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bargmann W (1978) Handbuch der mikroskopischen Anatomie des Menschen, VII/5, Niere und ableitende Harnwege. Springer Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Barry Ph H, Diamond JM, Wright EM (1971) The mechanism of cation permeation in rabbit gallbladder. Dilution potentials and biionic potentials. J Membrane Biol 4:358–394

    Google Scholar 

  • Bermudez L de, Windhager EE (1975) Osmotically induced changes in electrical resistance of distal tubules of rat kidney. Am J Physiol 229:1536–1546

    Google Scholar 

  • Berry CA, Boulpaep EL (1975) Nonelectrolyte permeability of the paracellular pathway in Necturus proximal tubule. Am J Physiol 228:581–595

    Google Scholar 

  • Bindslev N, Tormey J McD, Wright EM (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

    Google Scholar 

  • Boulpaep EL (1971) Electrophysiological properties of the proximal tubule: importance of cellular and intercellular transport pathways. In: Giebisch G (ed), Electrophysiology of epithelial cells. Symp Med Hoechst. Schattauer Verlag, Stuttgart, pp 91–118

    Google Scholar 

  • Boulpaep EL (1977) The role of tight junction in the control of electrolyte movements across Necturus proximal tubule. J Physiol 266:31 P

    Google Scholar 

  • Boulpaep EL, Seely JF (1971) Electrophysiology of proximal and distal tubules in the autoperfused dog kidney. Am J Physiol 221:1084–1096

    Google Scholar 

  • Bulger RE, Lorentz WB, Colindres RE, Gottschalk CW (1974) Morphologic changes in rat renal proximal tubules and their tight junctions with increased intraluminal pressure. Lab Invest 30:136–144

    Google Scholar 

  • Burg MB (1976) The renal handling of sodium chloride. In: Brenner BM, Rector FC (eds) The kidney, Saunders, Philadelphia London Toronto, Vol. I, pp 272–298

    Google Scholar 

  • Burg MB, Green N (1973) Function of the thick ascending limb of Henle's loop. Am J Physiol 224:659–668

    Google Scholar 

  • Burg M, Stoner L (1974) Sodium transport in the distal nephron. Fed Proc 33:31–36

    Google Scholar 

  • Burg MB, Isaacson L, Grantham J, Orloff J (1968) Electrical properties of the isolated perfused rabbit renal tubules. Am J Physiol 215:788–794

    Google Scholar 

  • Clarkson TW (1967) The transport of salt and water across isolated rat ileum. Evidence for at least two distinct pathways. J Gen Physiol 50:695–727

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Crayen M, Thoenes W (1975) Architektur und cytologische Charakterisierung des distalen Tubulus der Rattenniere. Fortschr Zool 23:279–288

    Google Scholar 

  • Deurs B van, Luft JH (1979) Effects of glutaraldehyde fixation on the structure of tight junctions. J Ultrastruct Res 68:160–172

    Google Scholar 

  • DiBona DR, Mills JW (1979) Distribution of Na+-pump sites in transporting epithelia. Fed Proc 38:134–143

    Google Scholar 

  • Dratwa M, Tisher CC, Sommer JR, Croker BP (1979) Intramembranous particle aggregation in toad urinary bladder after vasopressin stimulation. Lab Invest 40:46–54

    Google Scholar 

  • Erlij D, Martinez-Palomo A (1972) Opening of tight junctions in frog skin by hypertonic urea solutions. J Membrane Biol 9:229–240

    Google Scholar 

  • Erlij D, Martinez-Palomo A (1978) Role of tight junctions in epithelial function. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology. Springer Verlag, Berlin Heidelberg New York, Vol. III, chapt 2, pp 27–53

    Google Scholar 

  • Farquhar MG, Palade GE (1963) Functional complexes in various epithelia. J Cell Biol 17:375–412

    Google Scholar 

  • Forssmann WG, Ito S, Weihe E, Aoki A, Dym M, Fawcett DW (1977) An unproved perfusion fixation method for the testis. Anat Rec 188:307–314

    CAS  PubMed  Google Scholar 

  • Friend DS, Gilula NB (1972) Variations in tight and gap junctions in mammalian tissues. J Cell Biol 53:758–776

    Google Scholar 

  • Frömter E (1972) The route of passive ion movement through the epithelium of Necturus gallbladder. J Membrane Biol 8:259–301

    Google Scholar 

  • Frömter E, Müller CW, Wick T (1971) Permeability properties of the proximal tubular epithelium of the rat kidney studied with electrophysiological methods. In: Giebisch G (ed) Electrophysiology of epithelial cells. Symp Med Hoechst, Schattauer Verlag, Stuttgart, pp 119–148

    Google Scholar 

  • Harmanci MC, Wade JB, DiScala VA (1975) Altered structure of tight junctions in rat proximal tubules with volume expansion. Kidney Int 8:478

    Google Scholar 

  • Harmanci MC, Kachadorian WA, Valtin H, DiScala VA (1978) Antidiuretic hormone-induced intramembranous alterations in mammalian collecting ducts. Am J Physiol 235: F440-F443

    Google Scholar 

  • Hegel U, Frömter E, Wick T (1967) Der elektrische Wandwiderstand des proximalen Konvolutes der Rattenniere. Pflügers Arch 294:274–290

    Google Scholar 

  • Helman SJ, Grantham JJ, Burg MB (1971) Effect of vasopressin on electrical resistance of renal cortical collecting tubules. Am J Physiol 220:1825–1832

    Google Scholar 

  • Humbert F, Grandchamp A, Pricam C, Perrelet A, Orci L (1976) Morphological changes in tight junctions of Necturus maculosus proximal tubules undergoing saline diuresis. J Cell Biol 69:90–96

    Google Scholar 

  • Imai M (1977) Function of the thin ascending limb of Henle of rats and hamsters perfused in vitro. Am J Physiol 232:F 201-F 209

    Google Scholar 

  • Imai M, Kokko JP (1974) Sodium chloride, urea and water transport in the thin ascending limb of Henle: Generation of osmotic gradients by passive diffusion of solutes. J Clin Invest 53:393–402

    Google Scholar 

  • Kaissling B, Kriz W (1979) Structural analysis of the rabbit kidney. (Advances in anatomy, embryology and cell biology, Vol. 56). Springer Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Karnovsky MJ (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. J Cell Biol 51:ASCB abstracts, 146

    Google Scholar 

  • Kriz W, Schiller A, Kaissling B, Taugner R (1978) Comparative and functional aspects of thin loop limb ultrastructure. Abstr. Int. Symp: Correlation of renal ultrastructure and function. University of Aarhus, Aarhus

    Google Scholar 

  • Kühn K, Reale E (1975) Junctional complexes of the tubular cells in the human kidney as revealed with freeze-fracture. Cell Tissue Res 160:193–205

    Google Scholar 

  • Luft JH (1973) Embedding media — old and new. In: Koehler JK (ed) Advanced techniques in biological electron microscopy, Springer Verlag, Berlin Heidelberg New York, pp 1–34

    Google Scholar 

  • Machen TE, Erlij D, Wooding FBP (1972) Permeable junctional complexes. The movement of lanthanum across rabbit gallbladder and intestine. J Cell Biol 54:302–312

    Google Scholar 

  • Malnic G, Giebisch G (1972) Some electrical properties of distal tubular epithelium in the rat. Am J Physiol 223:797–808

    Google Scholar 

  • Martinez-Palomo A, Erlij D (1973) The distribution of lanthanum in tight junctions of the kidney tubule. Pflügers Arch 343:267–272

    Google Scholar 

  • Martinez-Palomo A, Erlij D (1975) Structure of tight junctions in epithelia with different permeability. Proc Natl Acad Sci USA 72:4487–4491

    Google Scholar 

  • Maunsbach AB (1973) Ultrastructure of the proximal tubule. In: Handbook of physiology (J Orloff and RW Berliner, eds), pp 31–79, Section 8: Renal Physiology, Washington, D C: Am Physiol Soc

    Google Scholar 

  • 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

    Google Scholar 

  • Moreno JH, Diamond JM (1974) Discrimination of monovalent inorganic cations by “tight” junctions of gallbladder epithelium. J Membrane Biol 15:277–318

    Google Scholar 

  • Oschman JL (1978) Morphology correlates of transport. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology. Springer Verlag, Berlin Heidelberg New York, Vol III, chapt 3, pp 67–93

    Google Scholar 

  • Pricam C, Humbert F, Perrelet A, Orci L (1974) A freeze-etch study of the tight junctions of the rat kidney tubules. Lab Invest 30:286–291

    Google Scholar 

  • Reuss L (1978) Transport in gallbladder. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology. Springer Verlag, Berlin Heidelberg New York, Vol III, chapt 17, pp 853–898

    Google Scholar 

  • Rocha AS, Kokko JP (1973) Sodium chloride and water transport in the medullary thick ascending limb of Henle. Evidence for active chloride transport. J Clin Invest 53:612–623

    Google Scholar 

  • Roesinger B, Schiller A, Taugner R (1978) A freeze-fracture study of tight junctions in the pars convoluta and pars recta of the renal proximal tubule. Cell Tissue Res 186:121–133

    Google Scholar 

  • Rogers AW (1973) Techniques of autoradiography. Chapt 8: The autoradiography of radioisotopes in diffusible state. Elsevier Scientific Publishing Company, Amsterdam London New York

    Google Scholar 

  • Schiller A, Taugner R (1979) Are there specialized junctions in the pars maculata of the distal tubule? Cell Tissue Res 200:337–344

    Google Scholar 

  • Schiller A, Taugner R (1980) Freeze-fracturing and deep-etching with the volatile cryoprotectant ethanol reveals true membrane surfaces of kidney structures. Cell Tissue Res 210:57–69

    Google Scholar 

  • Schiller A, Taugner R, Roesinger B (1978) Vergleichende Morphologie der Zonulae occludentes am Nierentubulus. Verh Anat Ges 72:229–234

    Google Scholar 

  • Schiller A, Taugner R, Kriz W (1980) The thin limbs of Henle's loop in the rabbit: a freeze-fracture study. Cell Tissue Res 207:249–265

    Google Scholar 

  • Schwartz MM, Karnovsky MJ, Venkatachalam MA (1979) Regional membrane specialization in the thin limbs of Henle's loops as seen by freeze-fracture electron microscopy. Kidney Int 16:577–589

    Google Scholar 

  • Staehelin LA (1973) Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci 13:763–786

    Google Scholar 

  • Stoner LC, Burg MB, Orloff J (1974) Ion transport in cortical collecting tubule; effect of amiloride. Am J Physiol 227:453–459

    Google Scholar 

  • Taugner R, Boll U, Zahn P, Forssmann WG (1976) Cell junctions in the epithelium of Bowman's capsule. Cell Tissue Res 172:431–446

    Google Scholar 

  • Thoenes W, Langer KK (1969) Relationship between cell structures of renal tubules and transport mechanisms. In: Thurau K, Jahrmärker H (eds) Renal Transport and Diuretics. Springer Verlag, Berlin, pp 37–65

    Google Scholar 

  • Tisher CC (1976) Anatomy of the kidney. In: Brenner BM, Rector FC (eds) The kidney. Saunders, Philadelphia London Toronto, pp 3–64

    Google Scholar 

  • Tisher CC, Yarger WE (1973) Lanthanum permeability of the tight junction (zonula occludens) in the renal tubule of the rat. Kidney Int 3:238–250

    Google Scholar 

  • Tisher CC, Bulger RE, Trump BF (1968) Human renal ultrastructure. III. The distal tubule in healthy individuals. Lab Invest 18:655–668

    Google Scholar 

  • Trump BF, Bulger RE (1968) Morphology of the kidney. In: Becker EL (ed) Structural basis of renal disease. Harper and Row, Publishers, Hoeber Medical Division, New York, pp 1–98

    Google Scholar 

  • Ullrich KJ, Frömter E, Murer H (1979) Prinzipien des epithelialen Transportes in Niere und Darm. Klin Wochenschr 57:977–991

    Google Scholar 

  • Ussing HH, Windhager EE (1964) Nature of shunt path and active transport path through frog skin epithelium. Acta Physiol Scand 61:484–504

    Google Scholar 

  • Wade JB, Karnovsky MJ (1974) Fracture faces of osmotically disrupted zonulae occludentes. J Cell Biol 62:344–350

    Google Scholar 

  • Welling LW, Welling DJ, Hill JJ (1978) Shape of cells and intercellular channels in rabbit thick ascending limb of Henle. Kidney Int 13:144–151

    Google Scholar 

  • Windhager EE, Boulpaep EL, Giebisch G (1967) Electrophysiological studies on single nephrons. Proc 3rd Int Congr Nephrol, Washington, DC, 1:35–47

    Google Scholar 

  • Wright FS (1971) Increasing magnitude of electrical potential along the renal distal tubule. Am J Physiol 220:624–638

    Google Scholar 

  • Wright EM, Diamond JM (1968) Effects of pH and polyvalent cations on the selective permeability of gallbladder epithelium to monovalent ions. Biochim Biophys Acta 163:57–74

    Google Scholar 

  • Wright EM, Barry PH, Diamond JM (1971) The mechanism of cation permeation in rabbit gallbladder. J Membrane Biol 4:331–357

    Google Scholar 

  • Wright EM, Smulders AP, Tormey J McD (1972) The role of the lateral intercellular spaces and solute polarization effects in the passive flow of water across the rabbit gallbladder. J Membrane Biol 7:198–219

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Physiology I and Anatomy III, University of Heidelberg, Heidelberg, Germany

    A. Schiller, W. G. Forssmann &  R. Taugner

Authors
  1. A. Schiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. G. Forssmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Taugner
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Parts of these findings were presented at the 72nd Meeting of the Anatomical Society, Aachen; April 1977 (see Verh. Anat. Ges. 72:229–234 [1978])

Supported by the Deutsche Forschungsgemeinschaft

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schiller, A., Forssmann, W.G. & Taugner, R. The tight junctions of renal tubules in the cortex and outer medulla. Cell Tissue Res. 212, 395–413 (1980). https://doi.org/10.1007/BF00236506

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00236506

Key words

Search

Navigation