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Innervation of the renal vasculature of the toad (Bufo marinus)

Cell and Tissue Research volume 231, pages 357–376 (1983)Cite this article

Summary

The innervation of the dorsal aorta and renal vasculature in the toad (Bufo marinus) has been studied with both fluorescence and ultrastructural histochemistry. The innervation consists primarily of a dense plexus of adrenergic nerves associated with all levels of the preglomerular vasculature. Non-adrenergic nerves are occasionally found in the renal artery, and even more rarely near the afferent arterioles. Many of the adrenergic nerve profiles in the dorsal aorta and renal vasculature are distinguished by high proportions of chromaffin-negative, large, filled vesicles. Close neuromuscular contacts are common in both the renal arteries and afferent arterioles. Possibly every smooth muscle cell in the afferent arterioles is multiply innervated. The glomerular capillaries and peritubular vessels are not innervated, and only 3–5% of efferent arterioles are accompanied by single adrenergic nerve fibres. Thus, nervous control of glomerular blood flow must be exerted primarily by adrenergic nerves acting on the preglomerular vasculature. The adrenergic innervation of the renal portal veins and efferent renal veins may play a role in regulating peritubular blood flow. In addition, glomerular and postglomerular control of renal blood flow could be achieved by circulating agents acting via contractile elements in the glomerular mesangial cells, and in the endothelial cells and pericytes of the efferent arterioles.

Some adrenergic nerve profiles near afferent arterioles are as close as 70 nm to distal tubule cells, indicating that tubular function may be directly controlled by adrenergic nerves.

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References

  • Adolph EF (1936) Epinephrine and urine formation in the frog. Am J Physiol 115:200–209

    Google Scholar 

  • Allan IJ, Newgreen DF (1977) Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Am J Anat 149:413–421

    Google Scholar 

  • Barajas L (1978) Innervation of the renal cortex. Fed Proc 37:1192–1201

    Google Scholar 

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

    Google Scholar 

  • Barajas L, Wang P (1975) Demonstration of acetylcholinesterase in the adrenergic nerves of the renal glomerular arterioles. J Ultrastruct Res 53:244–253

    Google Scholar 

  • Baumgarten MC, Holstein AF, Owman C (1970) Auerbach's plexus of mammals and man: electronmicroscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkeys, guinea-pigs and man. Z Zellforsch 106:376–397

    Google Scholar 

  • Becker CG (1972) Demonstration of actomyosin in mesangial cells of the renal glomerulus. Am J Pathol 66:97–110

    Google Scholar 

  • Becker CG, Murphy GE (1969) Demonstration of contractile protein in endothelium and cells of heart valves, endocardium, intima, arteriosclerotic plaques, and Aschoff bodies of rheumatic heart disease. Am J Pathol 55:1–37

    Google Scholar 

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

    Google Scholar 

  • Bennett HS, Wyrick AD, Lee SW, McNeil JH (1976) Science and art in preparing tissues embedded in plastic for light microscopy, with special reference to glycol methacrylate, glass knives and simple stains. Stain Technol 51:71–97

    Google Scholar 

  • Berger PJ, Gibbins IL, Hards DK, Crosby LJ (1982) The distribution and ultrastructure of sensory elements in the baroreceptor region of the truncus arteriosus of the lizard Trachydosaurus rugosus. Cell Tissue Res 226:389–406

    Google Scholar 

  • Bernik M (1969) Contractile activity of human glomeruli in culture. Nephron 6:1–10

    Google Scholar 

  • Bevan JA (1979) Some bases of differences in vascular response to sympathetic activity. Variation on a theme. Circ Res 45:161–171

    Google Scholar 

  • Bevan JA, Bevan RD, Duckles SP (1980) Adrenergic regulation of vascular smooth muscle. In: Bohr DF, Somlyo AP, Sparks HV (eds) Handbook of physiology, Section 2: The cardiovascular system, Vol II. Vascular smooth muscle. American Physiological Society, Bethesda, pp 515–566

    Google Scholar 

  • Bieter RN (1929) The effects of splanchnics upon glomerular blood flow in the frog's kidney. Am J Physiol 91: 436–460

    Google Scholar 

  • Campbell G, Haller CJ, Rogers DC (1978) Fine structural and cytochemical study of the innervation of smooth muscle in an amphibian (Bufo marinus) lung before and after denervation. Cell Tissue Res 194:419–432

    Google Scholar 

  • Coimbra A, Ribeiro-Silva A, Oswald W (1974) Fine structural and autoradiographic study of the innervation of the dog lateral saphenous vein. Blood Vessels 11:128–144

    Google Scholar 

  • Dieter E (1961) Die Wirkung von Adrenalin auf die Aktivität der Nierennerven beim Frosch. Pflügers Archiv 273:29–38

    Google Scholar 

  • Dieter E (1963) Die Wirkung des Depressorreflexes auf die Gefäße der Froschniere. Pflügers Archiv 276:368–377

    Google Scholar 

  • Elias H, Hossman A, Barth IB, Solmar A (1960) Blood flow in the renal glomerulus. J Urol 83:790–798

    Google Scholar 

  • Eränkö O, Klinge E, Sjöstrand NO (1976) Different types of synaptic vesicles in axons of the retractor penis muscle of the bull. Experientia 32:1335–1337

    Google Scholar 

  • Falck B (1962) Observations on the possibilities of the cellular localisation of monoamines by a fluorescence method. Acta Physiol Scand 56 Suppl 197:1–25

    Google Scholar 

  • Falck B, Häggendal J, Owman C (1963) The localisation of adrenaline in adrenergic nerves in the frog. Quart J Exp Physiol 48:253–257

    Google Scholar 

  • Forster RP (1943) The effect of epinephrine upon frog renal haemodynamics in the intact animal. Am J Physiol 140:221–225

    Google Scholar 

  • Fourman J (1970) The adrenergic innervation of the efferent arterioles and the vasa recta in the mammalian kidney. Experientia 26:293–294

    Google Scholar 

  • Furness JB, Costa M (1975) The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine. Histochemistry 41:335–352

    Google Scholar 

  • Gabbiani G, Badonnel M-C, Rona G (1975) Cytoplasmic contractile apparatus in aortic endothelial cells of hypertensive rats. Lab Invest 32:227–234

    Google Scholar 

  • Gibbins IL (1982) Lack of correlation between ultrastructural and pharmacological types of non-adrenergic autonomic nerves. Cell Tissue Res 221:551–581

    Google Scholar 

  • Gibbins IL, Haller CJ (1979) Ultrastructural identification of non-adrenergic, non-cholinergic nerves in the rat anococcygeus muscle. Cell Tissue Res 200:257–271

    Google Scholar 

  • Hammersen F (1976) Endothelial contractility — an undecided problem in vascular research. Beitr Pathol 157:327–348

    Google Scholar 

  • Hayman JM (1927) Estimations of afferent arteriole and glomerular capillary pressures in frog kidney. Am J Physiol 79:389–409

    Google Scholar 

  • Hökfelt T, Elfvin LG, Schultzberg M, Goldstein M, Luft R (1977) Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci USA 74:3587–3591

    Google Scholar 

  • Hunt SP, Emson PC, Gilbert R, Goldstein M, Kimmell JR (1981) Presence of avian pancreatic polypeptide-like immunoreactivity in catecholamine and methionine-enkephalin containing neurons within the central nervous system. Neurosci Lett 21:125–130

    Google Scholar 

  • Knight DS, Bazer GT, Feigen LP, Kadowitz PJ (1981) Intramedial renal arterial nerves. Blood Vessels 18:191–195

    Google Scholar 

  • Lauweryns JM, Baert J, DeLoecker W (1975) Intracytoplasmic filaments in pulmonary lymphatic endothelial cells. Fine structure and reaction after heavy meromyosin incubation. Cell Tissue Res 163:111–124

    Google Scholar 

  • Léránth CS, Williams TH, Jew JY, Arimura A (1980) Immunoelectronmicroscopic identification of somatostatin in cells and axons of sympathetic ganglia in the guinea-pig. Cell Tissue Res 212:83–89

    Google Scholar 

  • Lindvall O, Björklund A (1974) The glyoxylic acid fluorescence histochemical method: a detailed account of the methodology for the visualisation of central catecholamine neurons. Histochemistry 39:97–127

    Google Scholar 

  • Llewellyn-Smith IJ, Wilson AJ, Furness JB, Costa M, Rush RA (1981) Ultrastructural identification of noradrenergic axons and their distribution within the enteric plexuses of the guinea-pig small intestine. J Neurocytol 10:331–352

    Google Scholar 

  • Lorez HP, Kuhn H, Tranzer JP (1973) The adrenergic innervation of the renal artery of the rat. A fluorescence histochemical and electron microscopical study. Z Zellforsch 138:261–272

    Google Scholar 

  • Lundberg JM, Hökfelt T, Änggård A, Kimmel J, Goldstein M, Markey K (1980) Coexistence of an avian pancreatic polypeptide (APP)-immunoreactive substance and catecholamines in some peripheral and central neurons. Acta Physiol Scand 110:107–110

    Google Scholar 

  • Majno G, Shea SM, Leventhal M (1969) Endothelial contraction induced by histamine type mediators. J Cell Biol 42:647–672

    Google Scholar 

  • McKenna OC, Angelakos ET (1968) Acetylcholinesterase-containing nerve fibres in the canine kidney. Circ Res 23:645–651

    Google Scholar 

  • McLean J, Burnstock G (1966) Histochemical localisation of catecholamines in the urinary bladder of the toad (Bufo marinus). J Histochem Cytochem 14:538–548

    Google Scholar 

  • Morris JL (1983) Effects of renal nerve stimulation on vascular resistance in the toad kidney. Naunyn-Schmiedeberg's Archiv Pharmacol (in press)

  • Morris JL, Campbell G (1978) Renal vascular anatomy of the toad (Bufo marinus). Cell Tissue Res 189:501–514

    Google Scholar 

  • Morris JL, Clevers J (1980) Peripheral injection of 6-hydroxydopamine causes a weight increase in toads. Proc Aust Physiol Pharmacol Soc 11:75P

    Google Scholar 

  • Müller J, Barajas L (1972) Electron microscopic and histochemical evidence for a tubular innervation in the renal cortex of the monkey. J Ultrastruct Res 41:533–549

    Google Scholar 

  • Nicol JAC (1952) Autonomic nervous system in lower chordates. Biol Revs 27:1–49

    Google Scholar 

  • Owman C, Edvinsson L, Hardebo JE, Gröschel-Stewart U, Unsicker K, Walles B (1977) Immunohistochemical demonstration of actin and myosin in brain capillaries. Acta Physiol Scand (Suppl) 452:69–71

    Google Scholar 

  • Pak Poy RKF (1957) Electron microscopy of the amphibian renal glomerulus. Aust J Exp Biol 35:583–594

    Google Scholar 

  • Richards AN, Schmidt CF (1924) A description of the glomerular circulation in the frog's kidney and observations concerning the action of adrenaline and various other substances upon it. Am J Physiol 71:178–208

    Google Scholar 

  • Richards AN, Barnwell JB, Bradley RC (1927) The effect of small amounts of adrenaline upon the glomerular blood vessels of the frog's kidney perfused at constant rate. Am J Physiol 79:410–418

    Google Scholar 

  • Schultzberg M, Hökfelt T, Terenius L, Elfvin LG, Lundberg JM, Brandt J, Elde RP, Goldstein M (1979) Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neurosci 4:249–270

    Google Scholar 

  • Siggins GR, Bloom FE (1970) Cytochemical and physiological effects of 6-hydroxydopamine on periarteriolar nerves of frogs. Circ Res 27:23–38

    Google Scholar 

  • Silva DG, Ross G (1974) Ultrastructure and fluorescence histochemical studies on the innervation of the tracheo-bronchial muscle of normal cats treated with 6-hydroxydopamine. J Ultrastruct Res 47:310–328

    Google Scholar 

  • Simpson FO, Devine CE (1966) The fine structure of autonomic neuromuscular contacts in arterioles of sheep renal cortex. J Anat 100:127–137

    Google Scholar 

  • Thureson-Klein A, Stjärne L, Brundin J (1976) Ultrastructure of the nerves in veins from human omentum. Neurosci 1:333–337

    Google Scholar 

  • Thureson-Klein A, Klein RL, Johansson O (1979) Catecholamine-rich cells and varicosities in the bovine splenic nerve, vesicle contents and evidence for exocytosis. J Neurobiol 10:309–337

    Google Scholar 

  • Tilton RG, Kilo C, Williamson JR, Murch DW (1979) Differences in pericyte contractile function in rat cardiac and skeletal muscle microvasculatures. Microvasc Res 18:336–352

    Google Scholar 

  • Toh BH, Yildiz A, Sotelo J, Osung O, Holborow EJ, Fairfax A (1976) Distribution of actin and myosin in muscle and non-muscle cells. Cell Tissue Res 199:117–126

    Google Scholar 

  • Tranzer JP, Richards JG (1976) Ultrastructural cytochemistry of biogenic amines in nervous tissue: methodological improvements. J Histochem Cytochem 24:1178–1193

    Google Scholar 

  • Unsicker K, Axelsson S, Owman C, Svensson K-G (1975) Innervation of the male genital tract and kidney in the Amphibia Xenopus laevis Daudin, Rana temporaria L. and Bufo bufo L. Cell Tissue Res 160:453–484

    Google Scholar 

  • Uranga J (1973) Effect of glomerulopressin, oxytocin and norepinephrine on glomerular pressure in the toad. Gen Comp Endocrinol 20:515–521

    Google Scholar 

  • Verity MA, Bevan JA (1968) Fine structural study of the terminal effector plexus, neuromuscular and intermuscular relationships in the pulmonary artery. J Anat 103:49–63

    Google Scholar 

  • Wilson SP, Klein RL, Chang K-J, Gasparis MS, Viveros OH, Yang W-H (1980) Are opioid peptides co-transmitters in noradrenergic vesicles of sympathetic nerves? Nature 288:707–708

    Google Scholar 

  • Yamagishi W, Azuma T (1963) The innervation of the renal blood vessels of the toad. Jpn J Physiol 13:399–412

    Google Scholar 

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  1. Department of Zoology, University of Melbourne, Parkville, Victoria, Australia

    Judith L. Morris & Ian L. Gibbins

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  1. Judith L. Morris
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Morris, J.L., Gibbins, I.L. Innervation of the renal vasculature of the toad (Bufo marinus). Cell Tissue Res. 231, 357–376 (1983). https://doi.org/10.1007/BF00222187

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Key words

  • Kidney
  • Amphibia
  • Vasculature
  • Innervation