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Ultrastructural changes associated with renin secretion from the juxtaglomerular apparatus of mice

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Summary

Thin sections and freeze-fracture replicas were used to investigate the ultrastructural changes associated with renin secretion from the juxtaglomerular part of the afferent arteriole of male mice. Adrenalectomized animals in which renin secretion was stimulated by furosemide application and bleeding were also studied. Exocytosis of mature electron-dense granules was found in all experimental groups. Before extrusion, the region of granule facing the cell membrane changed, with vesicular and/or stacked membrane-like profiles and a small local protrusion of the granule membrane appearance of. Concomitantly, punctuate sites of fusion between the cell and granule membranes were observed. Later, unaltered amorphous, and altered membrane-like granule content was released from omega-shaped cavities into the extracellular space. In stimulated animals the alteration and extrusion of several closely apposed granules was reminiscent of compound exocytosis. Coated pits were frequently seen, suggesting specific retrieval of the former granule membrane. The collapsing silhouette of a depleted granule very rarely took the form of a saccule whose narrow membrane-bounded neck was continuous with the extracellular space.

Observed were two additional events by which active and inactive renin may be released. Small electron-lucent vacuoles of undetermined origin fused with the cell membrane and, in stimulated kidneys, some epithelioid cell processes disintegrated. However, the interpretation of the related ultrastructural phenomena was uncertain.

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References

  • Amherdt M, Baggiolini M, Perrelet A, Orci L (1978) Freeze-fracture of membrane fusions in phagocytosing polymorphonuclear leukocytes. Lab Invest 39:398–404

    Google Scholar 

  • Atlas SA, Sealey JE, Hesson TE, Kaplan AP, Ménard J, Corvol P, Laragh JH (1982) Biochemical similarity of partially purified inactive renins from human plasma and kidney. Hypertension 4 (Suppl II):86–95

    Google Scholar 

  • Aunis D, Hesketh JE, Devilliers G (1979) Freeze-fracture study of the chromaffin cell during exocytosis: Evidence for connections between the plasma membrane and secretory granules and for movements of plasma membrane-associated particles. Cell Tissue Res 197:433–441

    Google Scholar 

  • Barajas L (1966) The development and ultrastructure of the juxtaglomerular cell granule. J Ultrastruct Res 15:400–413

    Google Scholar 

  • Barajas L, Latta H (1967) Structure of the juxtaglomerular apparatus. Circ Res 20–21 Suppl II:15–28

    Google Scholar 

  • Bohle A, Christensen J, Meyer DS, Laberke HG, Strauch M (1982) Juxtaglomerular apparatus of the human kidney: Correlation between structure and function. Kidney Int 22, Suppl 12, S18–23

    Google Scholar 

  • Brown MS, Anderson RGW, Goldstein JL (1983) Recycling receptors: The round-trip itinerary of migrant membrane proteins. Cell 32:663–667

    Google Scholar 

  • Cain H, Kraus B (1969) Struktur und Funktion des juxtaglomerulären Apparates der Niere unter geordneten Bedingungen. Dtsch Med Wochenschr 94:2173–2180

    Google Scholar 

  • Cain H, Kraus B (1970) Der juxtaglomeruläre Apparat der Niere bei verschiedenen pathologischen Prozessen. Dtsch Med Wochenschr 95:282–288

    Google Scholar 

  • Cain H, Kraus B (1971) Funktions- und Formwandel der Gefäß-wandzellen des juxtaglomerulären Apparates der Niere beim Kaninchen. Virchows Arch [Cell Pathol] 7:160–173

    Google Scholar 

  • Chi EY, Lagunoff D, Koehler JK (1976) Freeze-fracture study of mast cell secretion. Proc Natl Acad Sci USA 73:2823–2827

    Google Scholar 

  • Cohen FS, Zimmerberg J, Finkelstein A (1980) Fusion of phospho-lipid vesicles with planar phospholipid bilayer membranes. II. Incorporation of a vesicular membrane marker into the planar membrane. J Gen Physiol 75:251–270

    Google Scholar 

  • Douglas WW (1981) Aspects of the calcium hypothesis of stimulus-secretion coupling: Electrical activity in adenohypophyseal cells, and membrane retrieval after exocytosis. In: Hand AR, Oliver C (eds) Methods in cell biology, Vol 23. Academic Press, New York, London, Paris, San Diego, San Francisco, São Paulo, Sydney, Tokyo, Toronto, pp 483–501

    Google Scholar 

  • Farquhar MG (1981) Membrane recycling in secretory cells: Implications for traffic of products and specialized membranes within the Golgi complex. In: Hand AR, Oliver C (eds) Methods in cell biology, Vol 23. Academic Press, New York, London, Paris, San Diego, San Francisco, São Paulo, Sydney, Tokyo, Toronto, pp 399–427

    Google Scholar 

  • Fisher ER (1966) Lysosomal nature of Juxtaglomerular granules. Science 152:1752–1753

    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

    CAS  PubMed  Google Scholar 

  • Gomba Sz, Soltesz MB (1969) Histochemistry of lysosomal enzymes in Juxtaglomerular cells. Experientia 25:513

    Google Scholar 

  • Gomba Sz, Soltesz MB, Szokoly V (1967) Studies on the histochemistry of phosphatase enzymes in the juxtaglomerular complex. Histochemie 8:264–274

    Google Scholar 

  • Gorgas K (1978) Struktur und Innervation des juxtaglomerulären Apparates der Ratte. Springer, Berlin, Heidelberg, New York

    Google Scholar 

  • Hasty DL, Hay ED (1978) Freeze-fracture studies of the developing cell surface. II. Particle-free membrane blisters on glutaraldehyde-fixed corneal fibroblasts are artefacts. J Cell Biol 78:756–768

    Google Scholar 

  • Hoffstein S, Weismann G (1978) Microfilaments and microtubules in calcium ionophore-induced secretion of lysosomal enzymes from human polymorphonuclear leukocytes. J Cell Biol 78:769–781

    Google Scholar 

  • Ishimura K, Egawa K, Fujita H (1980) Freeze-fracture images of exocytosis and endocytosis in anterior pituitary cells of rabbits and mice. Cell Tissue Res 206:233–241

    Google Scholar 

  • Iwayama T (1971) Nexuses between areas of the surface membrane of the same arterial smooth muscle cell. J Cell Biol 49:521–525

    Google Scholar 

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

    Google Scholar 

  • Katz SA, Malvin RL (1982) Secretion of newly synthesized renin. Endocrinology 111:201–207

    Google Scholar 

  • Leckie BJ (1981) Inactive renin: an attempt at a perspective. Clin Sci 60:119–130

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Morris SJ, Costello MJ, Robertson JD, Südhof TC, Odenwald F, Haynes DH (1983) The chromaffin granule as a model for membrane fusion: implications for exocytosis. J Auton Nerv Syst 7:19–33

    Google Scholar 

  • Orci L, Gabbay KH, Malaisse WJ (1972) Pancreatic beta-cell web: Its possible role in insulin secretion. Science 175:1128–1130

    Google Scholar 

  • Orci L, Perrelet A, Friend DS (1977) Freeze-fracture of membrane fusions during exocytosis in pancreatic B-cells. J Cell Biol 75:23–30

    Google Scholar 

  • Ornberg RL, Reese TS (1981a) Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes. J Cell Biol 90:40–54

    Google Scholar 

  • Ornberg RL, Reese TS (1981b) Comparison of compound with plasmalemmal exocytosis in Limulus amebocytes. In: Hand AR, Oliver C (eds) Methods in cell biology, Vol 23. Academic Press, New York London Paris San Diego San Francisco São Paulo Sydney Tokyo Toronto, pp 301–311

    Google Scholar 

  • Peter S (1976) Ultrastructural studies on the secretory process in the epitheloid cells of the Juxtaglomerular apparatus. Cell Tissue Res 168:45–53

    Google Scholar 

  • Poulsen K (1980) Pre-prorenin synthesis, storage form of renin, and renin binding proteins in plasma: A review. In: Gross F, Vogel G (eds) Enzymatic release of vasoactive peptides. Raven Press, New York, pp 1–6

    Google Scholar 

  • Poulsen K, Jacobsen J (1983) The biochemistry of aggression-provoked renin. Clin Exp Hypertens [A] 5(7 & 8):969–973

    Google Scholar 

  • Poulsen K, Vuust J, Bravo R, Lund T (1981) Pre-prorenin and prorenin from mouse kidney and submaxillary gland identified by translation of messenger RNA in cell-free systems and in frog oocytes. In: Sambhi MP (ed) Heterogeneity of renin and renin-substrate. Elsevier North Holland, Inc, New York Amsterdam Oxford, pp 27–32

    Google Scholar 

  • Rouiller C, Orci L (1971) The structure of the juxtaglomerular complex. In: Rouiller C, Muller AF (eds) The kidney. Morphology, biochemistry, physiology, Vol IV. Academic Press, New York London, pp 1–80

    Google Scholar 

  • Ruyter JHC (1964) Studies on an improved lead phosphate technique for the demonstration of nonspecific acid phosphatase in non-deparaffinized organ and tissue sections. Histochemie 3:521–537

    Google Scholar 

  • Ryan GB, Alcorn D, Coghlan JP, Hill PA, Jacobs R (1982) Ultra-structural morphology of granule release from juxtaglomerular myoepithelioid and peripolar cells. Kidney Int 22, Suppl 12:S 3–8

    Google Scholar 

  • Steinman RM, Mellman IS, Muller WA, Cohn ZA (1983) Endocytosis and the recycling of plasma membrane. J Cell Biol 96:1–27

    Google Scholar 

  • Stolinski C, Breathnach AS, Bellairs R (1978) Effect of fixation on cell membrane of early embryonic material as observed on freeze-fracture replicas. J Microsc 112:Pt 3, 293–299

    Google Scholar 

  • Tanaka Y, De Camilli P, Meldolesi J (1980) Membrane interactions between secretion granules and plasmalemma in three exocrine glands. J Cell Biol 84:438–453

    Google Scholar 

  • Taugner R, Hackenthal E (1981) Angiotensin II in epitheloid (renin containing) cells of rat kidney. Histochemistry 72:499–509

    Google Scholar 

  • Taugner R, Forssmann W-G, Billich H, Boll U, Ganten D, Seller H (1978) Innervation of the juxtaglomerular apparatus and the effect of renal nerve stimulation. In: Coupland RE, Forssmann W-G (eds) Peripheral neuroendocrine interaction. Springer, Berlin Heidelberg New York, pp 153–163

    Google Scholar 

  • Taugner Ch, Poulsen K, Hackenthal E, Taugner R (1979) Immunocytochemical localization of renin in mouse kidney. Histochemistry 62:19–27

    Google Scholar 

  • Taugner R, Hackenthal E, Rix E, Nobiling R, Poulsen K (1982) Immunocytochemistry of the renin-angiotensin system: Renin, angiotensinogen, angiotensin I, angiotensin II, and converting enzyme in the kidneys of mice, rats, and tree shrews. Kidney Int 22:Suppl 12, 33–43

    Google Scholar 

  • Winterhager E, Kühnel W (1983) Membrane specializations of the cells of the Harderian gland of the rabbit with particular reference to the mechanism of exocytosis. Cell Tissue Res 231:623–636

    Google Scholar 

  • Zaki FG, Keim GR, Takii Y, Inagami T (1982) Hyperplasia of juxtaglomerular cells and renin localization in kidneys of normotensive animals given captopril. Electron microscopic and immunohistochemical studies. Ann Clin Lab Sci 12:200–215

    Google Scholar 

  • Zavagli G, Aleotti A, Farinelli A (1983) Human renin granules: Ultrastructural aspects. Nephron 33:29–33

    Google Scholar 

  • Zimmerberg J, Cohen FS, Finkelstein A (1980) Fusion of phospho-lipid vesicle with planar phospholipid bilayer membranes. I. Discharge of vesicular content across the planar membrane. J Gen Physiol 75:241–250

    Google Scholar 

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Authors and Affiliations

  1. Institute of Physiology I, University of Heidelberg, Heidelberg, Federal Republic of Germany

    R. Taugner, Ch.Ph. Bührle & R. Nobiling

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  1. R. Taugner
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  2. Ch.Ph. Bührle
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  3. R. Nobiling
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These studies were supported by the German Research Foundation within the SFB 90 “Cardiovasculäres System”

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Taugner, R., Bührle, C. & Nobiling, R. Ultrastructural changes associated with renin secretion from the juxtaglomerular apparatus of mice. Cell Tissue Res. 237, 459–472 (1984). https://doi.org/10.1007/BF00228430

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