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Nitric oxide synthase-immunoreactive axons innervating the guinea-pig lingual artery: an ultrastructural immunohistochemical study using elastic brightfield imaging

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Abstract

The ultrastructure of nitric oxide synthase-immunoreactive (NOS-IR) axons innervating the guineapig lingual artery was investigated by means of pre-embedding immunohistochemistry using an indirect peroxidase technique and diaminobenzidine. Sections ranging in thickness from 60 to 500 nm were ultrastructurally evaluated in elastic brightfield imaging mode. Thick sections (optimum at 300 nm) were advantageous for enhancement of the labelling intensity, whilst some subcellular details were better revealed by thin sections. NOS-IR axon terminals often contained aggregations of large, dense-cored vesicles, consistent with a previous light microscopical report on colocalization of NOS and vasoactive intestinal peptide-immunoreactivity in these fibres. NOS-IR axons formed direct neuro-muscular junctions (width less than 50 nm) at the outer surface of the tunica media, thus providing a structural basis for “nitrergic” vasodilation. In addition, NOS-IR axons made direct contacts with non-varicose and varicose segments of non-reactive axons, suggesting interneuronal communication between these elements.

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References

  • Bachelard H, St-Pierre S, Rioux F (1987) Participation of capsaicin-sensitive neurons in the cardiovascular effects of neurotensin in guinea pigs. Peptides 8:1079–1087

    Google Scholar 

  • Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87:682–685

    Google Scholar 

  • Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768–770

    Google Scholar 

  • Burnett AL, Lowenstein CJ, Bredt DS, Chang TSK, Snyder SH (1992) Nitric oxide: a physiologic mediator of penile erection. Science 257:401–403

    Google Scholar 

  • Cederqvist B, Wiklund NP, Persson MG, Gustafsson LE (1991) Modulation of neuroeffector transmission in the guinea pig pulmonary artery by endogenous nitric oxide. Neurosci Lett 127:67–69

    Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801

    Google Scholar 

  • Edvinsson L, Emson P, McCulloch J, Tatemoto K, Uddman R (1983) Neuropeptide Y: cerebrovascular innervation and vasomotor effects in the cat. Neurosci Lett 43:79–84

    Google Scholar 

  • Edvinsson L, Gulbenkian S, Jansen I, Wharton J, Cervantes C, Polak JM (1989) Comparison of peptidergic mechanisms in different parts of the guinea pig superior mesenteric artery: immunocytochemistry at the light and ultrastructural levels and responses in vitro of large and small arteries. J Autonom Nerv Syst 28:141–154

    Google Scholar 

  • Grozdanovic Z, Baumgarten HG, Brüning G (1992) Histochemistry of NADPH-diaphorase, a marker for neuronal nitric oxide synthase, in the peripheral autonomic nervous system of the mouse. Neuroscience 48:225–235

    Google Scholar 

  • Hope BT, Micheal GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814

    Google Scholar 

  • Ignarro LJ, Bush PA, Buga GM, Wood KS, Fukuto JM, Rajfer J (1990) Nitric oxide and cyclic GMP formation upon electrical field stimulation cause relaxation of corpus cavernosum smooth muscle. Biochem Biophys Res Commun 170:843–850

    Google Scholar 

  • Inoue K, Kitada Y (1991) Parasympathetic postganglionic cells in the glossopharyngeal nerve trunk and their relationship to unmyelinated nerve fibres in the fungiform papillae of the frog. Anat Rec 230:131–135

    Google Scholar 

  • Kawasaki H, Nuki C, Saito A, Takasaki K (1990) Adrenergic modulation of calcitonin gene-related peptide (CGRP)-containing nerve-mediated vasodilation in the rat mesenteric resistance vessels. Brain Res 506:287–290

    Google Scholar 

  • Klatt P, Heinzel B, John M, Kastner M, Böhme E, Mayer B (1992) Ca2+/calmodulin-dependent cytochrome c reductase activity of brain nitric oxide synthase. J Biol Chem 267:11374–11378

    Google Scholar 

  • Klemm M, Hirst GDS, Campbell G (1992) Structure of autonomic neuromuscular junctions in the sinus venosus of the toad. J Autonom Nerv Syst 39:139–150

    Google Scholar 

  • Kummer W, Fischer A, Mundel P, Mayer B, Hoba B, Philippin B, Preissler U (1992) Nitric oxide synthase in VIP-containing vasodilator nerve fibres in the guinea pig. Neuro Report 3:653–655

    Google Scholar 

  • Kurkowski R, Kummer W, Heym C (1990) Substance P-immunoreactive nerve fibres in tracheobronchial lymph nodes of the guinea pig: origin, ultrastructure and coexistence with other peptides. Peptides 11:13–20

    Google Scholar 

  • Lee TJ-F, Sarwinski SJ (1991) Nitric oxidergic vasodilation in the porcine basilar artery. Blood Vessels 28:407–412

    Google Scholar 

  • Llewellyn-Smith IJ, Song Z-M, Costa M, Bredt DS, Snyder SH (1992) Ultrastructural localization of nitric oxide synthase immunoreactivity in guinea-pig enteric neurons. Brain Res 577:337–342

    Google Scholar 

  • Luff SE, McLachlan EM (1989) Frequency of neuromuscular junctions on arteries of different dimensions in the rabbit, guinea pig and rat. Blood Vessels 26:95–106

    Google Scholar 

  • Luff SE, McLachlan EM, Hirst GDS (1987) An ultrastructural analysis of the sympathetic neuromuscular junctions on arterioles of the submucosa of the guinea pig ileum. J Comp Neurol 257:578–594

    Google Scholar 

  • Luff SE, Hengstberger SG, McLachlan EM, Anderson WP (1991) Two types of sympathetic axon innervating the juxtaglomerular arterioles of the rabbit and rat kidney differ structurally from those supplying other arteries. J Neurocytol 20:781–795

    Google Scholar 

  • Mayer B, John M, Böhme E (1990) Purification of Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum: cofactor-role of tetrahydro-biopterin. FEBS Lett 277:215–219

    Google Scholar 

  • Moncada S, Palmer RMJ, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142

    Google Scholar 

  • Morris JL, Murphy R (1988) Evidence that neuropeptide Y released from noradrenergic axons causes prolonged contraction of the guinea-pig uterine artery. J Autonom Nerv Syst 24:241–249

    Google Scholar 

  • Pernow J, Öhlén A, Hökfelt T, Nilsson O, Lundberg JM (1987) Neuropeptide Y: presence in perivascular noradrenergic neurons and vasoconstrictor effects on skeletal muscle blood vessels in experimental animals and man. Regul Pept 19:313–324

    Google Scholar 

  • Pickel VM (1981) Immunocytochemical methods. In: Heimer L, Robards MJ (eds) Neuroanatomical tract-tracing methods. Plenum Press, New York, pp 483–509

    Google Scholar 

  • Toda N, Okamura T (1990) Possible role of nitric oxide in transmitting information from vasodilator nerve to cerebroarterial muscle. Biochem Biophys Res Commun 170:308–313

    Google Scholar 

  • Toda N, Okamura T (1991) Role of nitric oxide in neurally induced cerebroarterial relaxation. J Pharmacol Exp Ther 258:1027–1032

    Google Scholar 

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  1. Wolfgang Kummer

    Present address: Institute for Anatomy and Cell Biology, Philipps-University, Robert-Koch-Strasse 6, W-3550, Marburg, Germany

Authors and Affiliations

  1. Institute for Anatomy and Cell Biology, Ruprecht-Karls-University, Heidelberg, Germany

    Wolfgang Kummer

  2. Institute for Pharmacology and Toxicology, Karl-Franzens-University, Graz, Austria

    Bernd Mayer

Authors
  1. Wolfgang Kummer
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  2. Bernd Mayer
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Kummer, W., Mayer, B. Nitric oxide synthase-immunoreactive axons innervating the guinea-pig lingual artery: an ultrastructural immunohistochemical study using elastic brightfield imaging. Histochemistry 99, 175–179 (1993). https://doi.org/10.1007/BF00571878

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