Summary
Histological, ultrastructural, immunohistochemical, intravital microscopic and electrophysiological techniques have been applied to study experimental hydronephrosis in rats in order to assess its value as a preparation for the investigation of renal microcirculation and of the electrophysiological properties of the renin-containing juxtaglomerular (JG) cells of the afferent glomerular arteriole.
As hydronephrosis develops, the kidney parenchyma becomes progressively thinner owing to tubular atrophy. Twelve weeks after ureteral ligature, this process results in a transparent tissue sheet of about 150–200 μm in thickness. In this preparation, the renal arterial tree as well as the glomeruli can be easily visualized for intravital microscopic studies, e.g. the determination of kidney vessel diameters, or the identification of JG cells for penetration with an intracellular microelectrode. In contrast to the tubular atrophy, the vascular system is well preserved, and the JG cells and the sympathetic axon terminals are ultrastructurally intact. This is also true for the glomeruli, except for a certain confluence of the podocyte foot processes and a thickening of the basal laminae. Renin immunostaining and kidney renin content in the hydronephrotic organ correspond to those in control kidneys. In addition, there are no differences in the plasma renin levels of hydronephrotic and control rats.
Intravital microscopic observations reveal that the renal vascular tree reacts in a typical, concentration dependent manner to the vasoconstrictor agent angiotensin II, mainly at the level of the resistance vessels. Electrophysiological recordings from juxtaglomerular granulated cells show a high membrane potential (−60 mV), and spontaneous depolarizing junction potentials, owing to random transmitter release from the nerve terminals. Angiotensin II, an inhibitor of renin release, depolarizes JG cells reversibly.
Hence, we may infer that the hydronephrotic rat kidney is a suitable model for in vivo studies of the renal microcirculation as well as for in vitro investigations of the electrophysiological properties of the media cells of the afferent glomerular arteriole.
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References
Bolton TB (1979) Mechanisms of action of transmitters and other substances on smooth muscle. Physiol Rev 59:607–688
Bührle ChPh, Nobiling R, Mannek E, Schneider D, Hackenthal E, Taugner R (1984) The afferent glomerular arteriole: Immunocytochemical and electrophysiological investigations. J Cardiovasc Pharmacol 6:S383-S393
Bührle CP, Nobiling R, Taugner R (1985) Intracellular recordings from renin-positive cells of the afferent glomerular arteriole. Am J Physiol 249:F272-F281
Bührle CP, Scholz H, Hackenthal E, Nobiling R, Taugner R (1986a) Epithelioid cells: Membrane potential changes induced by substances influencing renin secretion. Mol Cell Endocrinol 45:37
Bührle CP, Scholz H, Nobiling R, Taugner R (1986b) Junctional transmission in renin-containing and smooth muscle cells of the afferent arteriole. Pflügers Arch 406:578–586
Cheung DW (1982) Spontaneous and evoked excitatory junction potentials in rat tail arteries. J Physiol (Lond) 328:449–459
Cohen LB, DeWeer P (1977) Structural and metabolic processes directly related to action potential propagation. In: Kandel ER (ed) Handbook of physiology Section 1: the nervous system, Vol 1: cellular biology of neurons, Part 1. Am Physiol Society, Bethesda, Maryland, pp 137–159
Davis JO, Blaine EH, Witty RT, Johnson JA, Shade RE, Braverman B (1972) The control of renin release in the non-filtering kidney. In: Assaykeen TA (ed) Control of renin secretion: advances in experimental & biology series, vol 17. Plenum Press, New York, pp 117–129
Endes P, Dévényi I, Gomba Sz (1962) Experimentelle Beeinflussung der granulierten Zellen des juxtaglomerulären Apparates durch Heminephrektomie und bilaterale Ureterligatur. Virchows Arch [Pathol Anat] 336:40–45
Forssmann WG, Ito S, Weihe E, Aoki A, Dym M, Fawcett DW (1977) An improved perfusion fixation method for the testis. Anat Rec 188:307–314
Hackenthal E, Schwertschlag U, Taugner R (1983) Cellular mechanisms of renin release. Clin Exp Hypertens A5(7, 8):975–993
Hall JE, Guyton AC, Jackson TE, Coleman TG, Lohmeier TE, Trippodo NC (1977) Control of glomerular filtration rate by renin-angiotensin system. Am J Physiol 233:F366–F372
Handa RK, Johns EJ (1985) Interaction of the renin-angiotensin system and the renal nerves in the regulation of rat kidney function. J Physiol (Lond) 369:311–321
Hinman F (1934) The pathogenesis of hydronephrosis. Surg Gynecol Obstet 58:356–376
Hinman F (1945a) Hydronephrosis. I. The structural changes. Surgery 17:816–835
Hinman F (1945b) Hydronephrosis. II. The functional changes. Surgery 17:836–845
Hinman F (1945c) Hydronephrosis. III. Hydronephrosis and hypertension. Surgery 17:845–849
Hirst GDS, Neild TO (1978) An analysis of excitatory junction potentials recorded from arterioles. J Physiol (Lond) 280:87–104
Holle G, Schneider HJ (1961) Über das Verhalten der Nierengefäße bei einseitiger experimenteller Hydronephrose. Virchows Arch [Pathol Anat] 334:475–488
Kajiwara M, Kitamura K, Kuriyama H (1981) Neuromuscular transmission and smooth muscle membrane properties in the guinea-pig ear artery. J Physiol 315:283–302
Kelemen JT, Endes P (1965) Die juxtaglomerulären granulierten Zellen bei einseitiger Hydronephrose der Ratte. Virchows Arch [Pathol Anat] 339:301–303
Mink D, Schiller A, Kriz W, Taugner R (1984) Interendothelial junctions in kidney vessels. Cell Tissue Res 236:567–576
Navar LG, Rosivall L (1984) Contribution of the renin-angiotensin system to the control of intrarenal hemodynamics. Kidney Int 25:857–868
Rao NR, Heptinstall RH (1968) Experimental hydronephrosis: A microangiographic study. Invest Urol 6:183–204
Steinhausen M, Snoei H, Parekh N, Baker R, Johnson PC (1983) Hydronephrosis: A new method to visualize vas afferens, efferens, and glomerular network. Kidney Int 23:794–806
Sternberger LA (1979) Immunocytochemistry. 2nd ed, John Wiley, New York
Takata Y (1980) Regional differences in electrical and mechanical properties of guinea-pig mesenteric vessels. Jpn J Physiol 30:709–728
Taugner Ch, Poulsen K, Hackenthal E, Taugner R (1979) Immunocytochemical localization of renin in mouse kidney. Histochemistry 62:19–27
Taugner R, Bührle ChPh, Ganten D, Hackenthal E, Hardegg Ch, Hardegg G, Nobiling R (1983) Immunohistochemistry of the renin-angiotensin-system in the kidney. Clin Exper Hypertens-Theory Practice A5(7, 8):1163–1177
Taugner R, Bührle CP, Hackenthal E, Mannek E, Nobiling R (1984a) Morphology of the juxtaglomerular apparatus and secretory mechanisms. Contr Nephrol 43:76–101
Taugner R, Bührle ChPh, Nobiling R (1984b) Ultrastructural changes associated with renin secretion from the juxtaglomerular apparatus of mice. Cell Tissue Res 237:459–472
Taugner R, Kirchheim H, Forssmann WG (1984c) Myoendothelial contacts in glomerular arterioles and in renal interlobular arteries of rat, mouse andTupaia belangeri. Cell Tissue Res 235:319–325
Taugner R, Mannek E, Nobiling R, Bührle CP, Hackenthal E, Ganten D, Inagami T, Schröder H (1984d) Coexistence of renin and angiotensin II in epitheloid cell secretory granules of rat kidney. Histochemistry 81:39–45
Wyker AT, Ritter RC, Marion DN, Gillenwater JY (1981) Mechanical factors and tissue stresses in chronic hydronephrosis. Invest Urol 18:430–436
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This work was supported by the Deutsche Forschungsgemeinschaft within the Sonderforschungsbereich 90 ‘Cardiovaskuläres System’ and within the Forschergruppe Niere/ Heidelberg
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Nobiling, R., Bührle, C.P., Hackenthal, E. et al. Ultrastructure, renin status, contractile and electrophysiological properties of the afferent glomerular arteriole in the rat hydronephrotic kidney. Vichows Archiv A Pathol Anat 410, 31–42 (1986). https://doi.org/10.1007/BF00710903
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DOI: https://doi.org/10.1007/BF00710903