Skip to main content
Log in

Cells and intercellular contacts in glomeruli and tubules of the frog kidney

A freeze-fracture and thin-section study

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

Summary

By the use of thin sections and freeze-fracture replicas the glomerular and tubular structures of the kidney of the frog (Rana esculenta) were studied with special reference to intercellular junctions.

In the glomerulus the filtration barrier is of very variable thickness, and frequent tight and gap junctional contacts occur between podocyte processes.

Although structurally less elaborate, the proximal tubule resembles its mammalian counterpart. In the initial part the tight junctions are relatively shallow but become very broad in the mid and distal portions of the proximal tubule. The proximal tubular cells are extensively linked by gap junctions. In some animals the shapes of the cells in the proximal and distal portions of the proximal tubule were markedly different.

The distal tubule consists of two segments which differ mainly in the pattern of interdigitations and the structure of the zonulae occludentes. Similarities with the tight junctional morphology of the mammalian distal tubule are striking. In the first part of the distal tubule (diluting segment) a narrow band of parallel tight junctions is found closely resembling that found in the mammalian straight distal tubule; in the more distal part of the distal tubule, however, a broad band of anastomosing tight junctional strands exists, like the zonula occludens of the mammalian convoluted distal tubule.

The connecting tubule displays cellular dimorphism: its wall contains a mixture of light and dark (flask) cells. The luminal and basolateral membranes of the flask cells are covered with numerous rod-shaped particles. The tight junctions of the connecting tubule are broad and increase in depth and number of strands along its length; they are typical of a very tight epithelium.

In spite of several dissimilarities with phylogenetically younger kidneys our findings suggest that many structural principles of the mammalian kidney are also represented in the kidneys of amphibians. The structural-functional relationships are discussed.

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

  • Ausiello DA, Kreisberg JI, Roy C, Karnovsky MJ (1980) Contraction of cultured rat glomerular cells of apparent mesangial origin after stimulation with angiotensin II and arginine vasopressin. J Clin Invest 65:754–760

    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, 91–118

    Google Scholar 

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

    Google Scholar 

  • Boulpaep EL (1976) Recent advances in electrophysiology of the nephron. Ann Rev Physiol 38:20–36

    Google Scholar 

  • Brown D (1978) Freeze-fracture of Xenopus laevis kidney: Rod-shaped particles in the canalicular membrane of the collecting tubule flask cell. J Ultrastruct Res 63:35–40

    Google Scholar 

  • Brown D, Ilic V, Orci L (1978) Rod-shaped particles in the plasma membrane of the mitochondria-rich cell of amphibian epidermis. Anat Rec 192:269–276

    Google Scholar 

  • Claude Ph (1978) Morphological factors influencing transepithelial permeability: A model for the resistance of the zonula occludens. J Membr 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 

  • Dantzler WH (1980) Significance of comparative studies for renal physiology. Am J Physiol 238:F437-F444

    Google Scholar 

  • Dantzler WH, Braun EJ (1980) Comparative nephron function in reptiles, birds, and mammals. Am J Physiol 239:R197-R213

    Google Scholar 

  • Deeds DG, Sullivan LP, Fenton RA, Tucker JM, Cuppage FE (1977) Function and structure of perfused bullfrog kidney. Am J Physiol 233:F481-F490

    Google Scholar 

  • Deeds DG, Sullivan LP, Welling DJ (1978) Potassium reabsorption and secretion in the perfused bullfrog kidney. Am J Physiol 235:F26-F32

    Google Scholar 

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

    Google Scholar 

  • Forster J, Steels PS, Boulpaep EL (1980) Organic substrate effects on and heterogeneity of Necturus proximal tubule function. Kidney Int 17:479–490

    Google Scholar 

  • Fujimoto M, Kubota T, Kotera K (1977) Electrochemical profile of K and Cl ions across the proximal tubule of bullfrog kidneys. A study using double-barreled ion-sensitive microelectrodes. Contr Nephrol 6:114–123

    Google Scholar 

  • Gallardo R, Pang PKT, Sawyer WH (1980) Neural influences on bullfrog renal functions. Proc Soc Exp Biol Med 165:233–240

    Google Scholar 

  • Geyer G, Linss W (1964) Elektronenmikroskopische Untersuchung des Epithels im Verbindungsstück der Niere von Rana esculenta. Anat Anz 114:236–246

    Google Scholar 

  • Hoshi T, Suzuki Y, Itoi K (1981) Differences in functional properties between the early and the late segments of the distal tubule of amphibian (Triturus) kidney. Jap J Nephrol 23:889–896

    Google Scholar 

  • Humbert F, Pricam C, Perrelet A, Orci L (1975) Specific plasma membrane differentiations in the cells of the kidney collecting tubule. J Ultrastruct Res 52:13–20

    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 

  • Kubota T, Honda M, Kotera K, Fujimoto M (1980) The effect of diffusible ions on the peritubular membrane potential of proximal tubular cells in perfused bullfrog kidneys. Jap J Physiol 30:775–790

    Google Scholar 

  • Kühn K, Stolte H, Reale E (1975) The fine structure of the kidney of the hagfish (Myxine glutinosa L.). A thin section and freeze-fracture study. Cell Tissue Res 164:201–213

    Google Scholar 

  • Kühn KW, Luciano L, Stolte H, Reale E (1980) Cell junctions of the glomerular epithelium in a very early vertebrate (Myxine glutinosa). Contrib Nephrol 19:9–14

    Google Scholar 

  • Linss W, Geyer G (1964a) Elektronenmikroskopische Untersuchungen der interkapillären Zellen im Glomerulum von Rana esculenta. Anat Anz 114:225–235

    Google Scholar 

  • Linss W, Geyer G (1964b) Über die elektronenmikroskopische Struktur der Nierentubuli von Rana esculenta. Anat Anz 115:281–296

    Google Scholar 

  • Long WS (1973) Renal handling of urea in Rana catesbeiana. Am J Physiol 224:482–490

    Google Scholar 

  • Long S, Giebisch G (1979) Comparative physiology of renal tubular transport mechanisms. Yale J Biol Med 52:525–544

    Google Scholar 

  • Meseguer I, Agülleiro B, Liombart Bosch YA (1978a) Structure and ultrastructure of the frog's nephron (R. ridibunda). I. Renal corpuscle and ciliary body. Morph Normal Y Patol Sec A. 1:295–308

    Google Scholar 

  • Meseguer I, Agülleiro B, Liombart Bosch YA (1978b) Structure and ultrastructure of the frog's nephron (R. ridibunda). II. Proximal convoluted tubule, distal convoluted tubule and segment of connection. Morph Normal Y Patol Sec A. 2:41–60

    Google Scholar 

  • Mink D, Schiller A, Nobiling R, Taugner R (1982) Intercellular junctions in renal blood vessels and morphometry of endothelial fenestrations of renal cortical capillaries. In preparation

  • Minuth M, Schiller A, Taugner R (1981) The development of cell junctions during nephrogenesis. Anat Embryol 163:307–319

    Google Scholar 

  • Peek WD, McMillan DB (1979) Ultrastructure of the tubular nephron of the garter snake Thamnophis sirtalis. Am J Anat 154:103–127

    Google Scholar 

  • Peek WD, Shivers RR, McMillan DB (1977) Freeze-fracture analysis of junctional complexes in the nephron of the garter snake, Thamnophis sirtalis. Cell Tissue Res 179:441–451

    Google Scholar 

  • Persson B-E (1978) Dynamics and regulation of glomerular ultrafiltration in the Amphiuma kidney. Acta Universitatis Upsaliensis. Abstr of Uppsala Dissertations from the Faculty of Medicine 308

  • Pricam C, Humbert F, Perrelet A, Orci L (1974) Gap junctions in mesangial and lacis cells. J Cell Biol 63:349–354

    Google Scholar 

  • Renkin EM, Gilmore JP (1973) Glomerular filtration. In: Orloff J, Berliner RW (eds) Handbook of physiology, Sect 8: Renal Physiology. American Physiological Society, Washington DC, pp 185–248

    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 

  • Schaffner A, Rodewald R (1975) Glomerular filtration of ferritin in the bullfrog Rana catesbeiana. J Cell Biol 67:385a

    Google Scholar 

  • Schiller A (1981) Funktionelle Ultrastruktur der Interzellularverbindungen in der Niere. Habilitationsschrift, Universität Heidelberg

  • Schiller A, Taugner R (1982) Heterogeneity of tight junctions along the collecting duct in the renal medulla. A freeze-fracture study in rat and rabbit. Cell Tissue Res 223:603–614

    Google Scholar 

  • Schiller A, Tiedemann K (1981) The mature mesonephric nephron of the rabbit embryo. III. Freezefracture studies. Cell Tissue Res 221:431–442

    Google Scholar 

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

    Google Scholar 

  • Schiller A, Forssmann WG, Taugner R (1980b) The tight junctions of renal tubules in the cortex and outer medulla. A quantitative study of the kidneys of six species. Cell Tissue Res 212:395–413

    Google Scholar 

  • Stetson DL, Wade JB, Giebisch G (1980) Morphologic alterations in the rat medullary collecting duct following potassium depletion. Kidney Int 17:45–56

    Google Scholar 

  • Stoner LC (1977) Isolated, perfused amphibian renal tubules: the diluting segment. Am J Physiol 233:F438-F444

    Google Scholar 

  • Sullivan LP, Welling DJ, Deeds DG, Simone JN (1977) Kinetic analysis of potassium transport in bullfrog kidney. Am J Physiol 233:F464-F480

    Google Scholar 

  • Sullivan LP, Welling DJ, Rome LA (1981) Effects of sodium and chloride on potassium transport by the bullfrog kidney. Am J Physiol 240:F127-F137

    Google Scholar 

  • Taugner R, Schiller A, Kaissling B, Kriz W (1978a) Gap junctional coupling between the JGA and the glomerular tuft. Cell Tissue Res 186:279–285

    Google Scholar 

  • Taugner R, Sonnhof U, Richter DW, Schiller A (1978b) Mixed (chemical and electrical) synapses on frog spinal motoneurons. Cell Tissue Res 193:41–59

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taugner, R., Schiller, A. & Ntokalou-Knittel, S. Cells and intercellular contacts in glomeruli and tubules of the frog kidney. Cell Tissue Res. 226, 589–608 (1982). https://doi.org/10.1007/BF00214787

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214787

Key words

Navigation