Skip to main content
Log in

An ultrastructural study of the juxtaglomerular apparatus in the toad, Bufo bufo

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

Summary

The fine structure of the juxtaglomerular apparatus in the toad, Bufo bufo was investigated.—It is suggested that the granules in the media cells of the afferent arteriole are formed from the Golgi apparatus. Many granules have a content of lamellar material. The media cells do not show the ultrastructural features of active secretory cells. In the media cells, the myofilaments are situated near the vascular lumen. The other cell organelles, including the granules, are preferentially located at the opposite pole of the cell in the neighbourhood of the macula densa cells and the adventitial nerve fibres. In these regions the media cells show many pinocytotic vesicles. The nerve fibres innervating the juxtaglomerular cells are non-myelinated and their varicosities contain dense core vesicles. The basement membranes of media cells and adjacent macula densa cells occasionally fuse, which may indicate a functional relationship between these cells.

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

  • Barajas, L.: The innervation of the juxtaglomerular apparatus. An electron microscopic study of the innervation of the glomerular arterioles. Lab. Invest. 13, 916–929 (1964)

    Google Scholar 

  • Barajas, L.: The ultrastructure of the juxtaglomerular apparatus as disclosed by three-dimensional reconstructions from serial sections. J. Ultrastruct. Res. 33, 116–147 (1970)

    Google Scholar 

  • Barajas, L., Latta, H.: A three-dimensional study of the juxtaglomerular apparatus in the rat. Light and electron microscopic observations. Lab. Invest. 12, 257–269 (1963a)

    Google Scholar 

  • Barajas, L., Latta, H.: The juxtaglomerular apparatus in adrenalectomized rats. Light and electron microscopic observations. Lab. Invest. 12, 1046–1059 (1963b)

    Google Scholar 

  • Barajas, L., Latta, H.: Structure of the juxtaglomerular apparatus. Circulat. Res. 21, Suppl. II, 15–28 (1967)

    Google Scholar 

  • Barajas, L., Müller, J.: The innervation of the juxtaglomerular apparatus and surrounding tubules: A quantitative analysis by serial section electron microscopy. J. Ultrastruct. Res. 43, 107–132 (1973)

    Google Scholar 

  • Bellocci, M., Picardi, R., Martino, C. de: The juxtaglomerular apparatus in the mesonephros of newt (Trittirus cristatus). A morphologic study. Z. Zellforsch. 114, 203–219 (1971)

    Google Scholar 

  • Bertini, P., Santolaya, R.: A novel type of granules observed in toad endothelial cells and their relationship with blood pressure active factors. Experientia (Basel) 26, 522–523 (1970)

    Google Scholar 

  • Biava, C. G., West, M.: Fine structure of normal human juxtaglomerular cells. II. Specific and nonspecific cytoplasmic granules. Amer. J. Path. 49, 955–979 (1966)

    Google Scholar 

  • Bohle, A.: Elektronenmikroskopische Untersuchungen über die Struktur des Gefäßpols der Niere. Verh. dtsch. Ges. Path. 43, 219–225 (1959)

    Google Scholar 

  • Bucher, O., Reale, E.: Zur elektronenmikroskopischen Untersuchung der juxtaglomerulären Spezialeinrichtungen der Niere. I. Problemstellung und erste Beobachtungen. Z. Zellforsch. 54, 167–181 (1961)

    Google Scholar 

  • Bucher, O., Reale, E.: Zur elektronenmikroskopischen Untersuchung der juxtaglomerulären Spezialeinrichtungen der Niere. III. Die epitheloiden Zellen der Arteriola afferens. Z. Zellforsch. 56, 344–358 (1962)

    Google Scholar 

  • Bucher, O., Reale, E.: Weitere elektronenmikroskopische Befunde an den juxtaglomerulären epitheloiden Zellen. Verh. anat. Ges. 59, 194–200 (1964)

    Google Scholar 

  • Bucher, O., Zimmermann, E.: A propos de la macula densa du rein. Acta anat. (Basel) 42, 352–371 (1960)

    Google Scholar 

  • Capelli, J. P., Wesson, L. G., Aponte, G. E.: A phylogenetic study of the renin-angiotensin system. Amer. J. Physiol. 218, 1171–1178 (1970)

    Google Scholar 

  • Chandra, S., Hubbard, J. C., Skelton, F. R., Bernardis, L. L., Kamura, S.: Genesis of juxtaglomerular cell granules. A physiologic, light and electron microscopic study concerning experimental renal hypertension. Lab. Invest. 14, 1834–1847 (1965)

    Google Scholar 

  • Connell, G. M., Kaley, G.: Evidence for the presence of “renin” in kidneys of marine fish and amphibia. Biol. Bull. 127, 366–367 (1964)

    Google Scholar 

  • Dalton, A. J.: Structural details of some of the epithelial cell types in the kidney of the mouse as revealed by the electron microscope. J. nat. Cancer Inst. 11, 1163–1185 (1951)

    Google Scholar 

  • Dongen, W. J. van, Heijden, C. A. van der: The demonstration of renal juxtaglomerular granules and the evaluation of the index of granulation in the toad. Bufo bufo. Z. Zellforsch. 94, 40–45 (1969)

    Google Scholar 

  • Edwards, J. G.: The vascular pole of the glomerulus in the kidney of vertebrates. Anat. Rec. 76, 381–389 (1940)

    Google Scholar 

  • Falck, B., Hillarp, N.-Å., Thieme, G., Torp, A.: Fluorescence of catecholamines and related compounds condensed with formaldehyde. J. Histochem. Cytochem. 10, 348–354 (1962)

    Google Scholar 

  • Fisher, E. R.: Lysosomal nature of juxtaglomerular granules. Science 152, 1752–1753 (1966)

    Google Scholar 

  • Gomba, S., Bostelmann, W., Szokoly, V., Soltész, M. B.: Histochemische Untersuchung der adrenergen Innervation des juxtaglomerulären Apparates. Acta biol. med. germ. 22, 387–392 (1969)

    Google Scholar 

  • Gomba, S., Soltész, B. M., Szokoly, V.: Studies on the histochemistry of phosphatase enzymes in the juxtaglomerular complex. Histochemie 8, 264–274 (1967)

    Google Scholar 

  • Grill, G., Granger, P., Thurau, K.: The renin angiotensin system of amphibians. I. Determination of the renin content of amphibian kidneys. Pflügers Arch. 331, 1–12 (1972)

    Google Scholar 

  • Hartroft, P. M.: A preliminary study of the electron microscopy of renal juxtaglomerular cells; correlation with light microscopy. Anat. Rec. 124, 458 (1956)

    Google Scholar 

  • Hartroft, P. M.: “Juxtaglomerular” (JG) cells of the american bullfrog as seen by light and electron microscopy. Fed. Proc. 25, 238 (1966)

    Google Scholar 

  • Hartroft, P. M., Newmark, L. N.: Electron microscopy of renal juxtaglomerular cells. Anat. Rec. 139, 185–199 (1961)

    Google Scholar 

  • Krishnamurthy, V. G., Bern, H. A.: Correlative histologic study of the corpuscles of Stannius and the juxtaglomerular cells of teleost fishes. Gen. comp. Endocr. 13, 313–335 (1969)

    Google Scholar 

  • Lamers, A.P.M., Dongen, W. J. van: The morphology of the juxtaglomerular apparatus in Bufo bufo. Some light- and electronmicroscopic observations. Gen. comp. Endocr. 18, 602 (1972)

    Google Scholar 

  • Lamers, A.P.M., Dongen, W. J. van, Kemenade, J. A.M. van: The morphology of the juxtaglomerular apparatus in the toad, Bufo bufo. A light microscopic study. Z. Zellforsch. 138, 545–555 (1973)

    Google Scholar 

  • Lamers, A.P.M., Dongen, W. J. van, Kemenade, J. A.M. van, Speijers, G.J.A.: A macula densa-like structure in the kidney of the toad, Bufo bufo. Gen. comp. Endocr. 22, 355 (1974)

    Google Scholar 

  • Latta, H., Maunsbach, A. B.: The juxtaglomerular apparatus as studied electron microscopically. J. Ultrastruct. Res. 6, 547–561 (1962)

    Google Scholar 

  • Lee, J., Hurley, S., Hopper, J.: JGA granular cells (mouse): ultrastructural histochemistry and morphology in granules. Fed. Proc. 24, 434 (1965)

    Google Scholar 

  • Lee, J. C., Hurley, S., Hopper, J.: Secretory activity of the juxtaglomerular granular cells of the mouse. Morphologic and enzyme histochemical observations. Lab. Invest. 15, 1459–1476 (1966)

    Google Scholar 

  • Ljungqvist, A.: Sympathetic innervation of the juxtaglomerular cells of the kidney. Proc. 4th Int. Congr. Nephrol., Stockholm 2, 14–18 (1970)

    Google Scholar 

  • Ljungqvist, A., Ungerstedt, U.: Sympathetic innervation of the juxtaglomerular cells of the kidney in rats with renal hypertension. Acta path. microbiol. scand. 80, 38–46 (1972)

    Google Scholar 

  • Mandalenakis, N., Cantin, M., Dumont, A.: L'appareil juxtaglomérulaire du rein endocrinien. Étude histologique et ultrastructurale. Path. et Biol. 18, 233–240 (1970)

    Google Scholar 

  • McManus, J. F. A.: Apparent reversal of position of the Golgi element in the renal tubule. Nature (Lond.) 152, 417 (1943)

    Google Scholar 

  • Nolly, H., Fasciolo, J. C.: The renin-angiotensin system in Bufo arenarum and Bufo paracnemis. Comp. Biochem. Physiol. 39A, 823–831 (1971)

    Google Scholar 

  • Oberling, Ch., Hatt, P. Y.: Étude de l'appareil juxtaglomérulaire du rat au microscope électronique. Ann. Anat. path. 5, 441–460 (1960)

    Google Scholar 

  • Phelps, P. C., Luft, J. H.: Electron microscopical study of relaxation and constriction in frog arterioles. Amer. J. Anat. 125, 399–428 (1969)

    Google Scholar 

  • Reale, E., Marinozzi, V., Bucher, O.: A propos de l'ultrastructure de l'appareil juxtaglomérulaire du rein. V. Nouvelles observations sur les cellules épithélioïdes. Acta anat. (Basel) 52, 22–33 (1963)

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Rhodin, J. A. G.: Fine structure of vascular walls in mammals. With special reference to smooth muscle component. Physiol. Rev. 42, Suppl. 5, 48–87 (1962)

    Google Scholar 

  • Rouiller, C., Orci, L.: The structure of the juxtaglomerular complex. In: The kidney. Morphology, biochemistry, physiology, ed. by C. Rouiller and A. F. Muller, vol. IV, p. 1–80. London-New York: Academic Press 1971

    Google Scholar 

  • Skelton, F. R., Chandra, S., Hubbard, J. C., Bernardis, L. L.: Studies on the genesis of the juxtaglomerular cell granule. Circulat. Res. 21, Suppl. II, 29–46 (1967)

    Google Scholar 

  • Sokabe, H., Ogawa, M., Oguri, M., Nishimura, H.: Evolution of the juxtaglomerular apparatus in the vertebrate kidneys. Tex. Rep. Biol. Med. 27, 867–885 (1969)

    Google Scholar 

  • Stehbens, W. E.: Ultrastructure of vascular endothelium in the frog. Quart. J. exp. Physiol. 50, 375–384 (1965)

    Google Scholar 

  • Steinsiepe, K. F., Weibel, E. R.: Elektronenmikroskopische Untersuchungen an spezifischen Organellen von Endothelzellen des Frosches (Rana temporaria). Z. Zellforsch. 108, 105–126 (1970)

    Google Scholar 

  • Tsuda, N.: Ultrastructural study of secretory granules in the juxtaglomerular cells. Particularly on formation and extrusion. Acta med. Nagasaki. 13, 140–155 (1969)

    Google Scholar 

  • Tsuda, N., Nickerson, P. A., Molteni, A.: Ultrastructural study of developing juxtaglomerular cells in the rat. Lab. Invest. 25, 644–652 (1971)

    Google Scholar 

  • Wågermark, J., Ungerstedt, U., Ljungqvist, A.: Sympathetic innervation of the juxtaglomerular cells in the kidney. Circulat. Res. 22, 149–153 (1968)

    Google Scholar 

  • Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We express our great thanks to Dr. A. M. Stadhouders for enabling us to do this work in his Institute (Department of Electron Microscopy, University of Nijmegen) and for his critical reading of the manuscript, to Miss Thea Jansen for typing the text and Mr. A. J. Breebaart for preparing the electron micrographs. This investigation was supported by research grant 91-13 from the Netherlands Organization for the Advancement of Pure Research (Z.W.O.).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lamers, A.P.M., van Dongen, W.J. & van Kemenade, J.A.M. An ultrastructural study of the juxtaglomerular apparatus in the toad, Bufo bufo . Cell Tissue Res. 153, 449–464 (1974). https://doi.org/10.1007/BF00231540

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00231540

Key words

Navigation