Skip to main content
Log in

Ultrastructural investigation of nitric oxide synthase-immunoreactive nerves associated with coronary blood vessels of rat and guinea-pig

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

Abstract

Ultrastructural investigation of nitrix oxide synthase-immunoreactive nerves closely associated with blood vessels in rat and guinea-pig hearts revealed many labelled nerve fibres in the walls of the main branches of the coronary arteries, and in arterioles, capillaries and post-capillary venules. The number of nitric oxide synthase-containing nerve fibres associated with different vessels, even those of the same calibre, varied. Terminal regions of nitric oxide synthase-immunoreactive fibres were observed in the endocardium and myocardium. Nitric oxide synthase-labelled fibres displayed electrondense immunoproduct in both varicose and intervaricose regions. Immunoreactive axonal varicosities contained both small and large synaptic vesicles. The characteristics of the nitric oxide synthase-immunoreactive nerve fibres observed in the heart and the possibility that these fibres represent the processes of intracardiac neurones and/or sensory neurones of extrinsic origin are discussed.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Afework M, Tomlinson A, Burnstock G (1994) Distribution and colocalization of nitric oxide synthase and NADPH-diaphorase in adrenal gland of developing, adult and aging Sprague-Dawley rats. Cell Tissue Res 276:133–141

    Google Scholar 

  • Aimi Y, Fujimura M, Vincent SR, Kimura H (1991) Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J Comp Neurol 306:382–392

    Google Scholar 

  • Aimi Y, Kimura H, Kinoshita T, Minami Y, Fujimura M, Vincent SR (1993) Histochemical localization of nitric oxide synthase in rat enteric nervous system. Neuroscience 53:553–560

    Google Scholar 

  • Belai A, Burnstock G (1994) Evidence for coexistence of ATP and nitric oxide in non-adrenergic, non-cholinergic (NANC) inhibitory neurones in the rat ileum, colon and anococcygeus muscle. Cell Tissue Res 278:197–200

    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 

  • Burnstock G (1993) Introduction: changing face of autonomic and sensory nerves in the circulation. In: Edvinsson L, Uddman R (eds) Vascular innervation and receptor mechanisms: new perspectives. Academic Press, San Diego, pp 1–22

    Google Scholar 

  • Burnstock G, Chamley J, Campbell GR (1980) The innervation of the arteries. In: Schwartz CJ, Werthessen NT, Wolf S (eds) Structure and function of the circulation. Plenum Press, New York, pp 729–767

    Google Scholar 

  • Fischer A, Mundel P, Mayer B, Preisler U, Philippin B, Kummer W (1993) Nitric oxide synthase in guinea pig lower airway innervation. Neurosci Lett 149:157–160

    Google Scholar 

  • Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376

    Google Scholar 

  • Furness JB, Pompolo S, Shuttleworth CWR, Burleigh DE (1992) Light-and electron-microscopic immunochemical analysis of nerve fibre types innervating the taenia of the guinea-pig caecum. Cell Tissue Res 270:125–137

    Google Scholar 

  • Gardiner SM, Bennett T (1993) Endothelial-derived relaxing factors: focus on nitric oxide. In: Edvinsson L, Uddman R (eds) Vascular innervation and receptor mechanisms: new perspectives. Academic Press, San Diego, pp 41–85

    Google Scholar 

  • Garthwaite J (1991) Glutamate nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci 14:60–67

    Google Scholar 

  • Gruetter CA, Barry BK, McNamara DB, Gruetter DY, Kadowitz PJ, Ignarro LJ (1979) Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. j Cyclic Nucleotide Res 5:211–224

    Google Scholar 

  • Gulbenkian S, Edvinsson L, Opgaard OS, Wharton J, Polak JM, David-Ferreìra JF (1990) Peptide-containing nerve fibres in guinea-pig coronary arteries: immunohistochemistry, ultrastructure and vasomotility. J Auton Nerv Syst 31:153–168

    Google Scholar 

  • Hassall CJS, Saffrey MJ, Belai A, Hoyle CHV, Moules EW, Moss J, Schmidt HHHW, Murad F, Förstermann U, Burnstock G (1992) Nitric oxide synthase-immunoreactivity and NADPH-diaphorase activity in a subpopulation of intrinsic neurones of the guinea-pig heart. Neurosci Lett 143:65–68

    Google Scholar 

  • Klimaschewski L, Kummer W, Mayer B, Couraud JY, Preissler U, Philippin B, Heym C (1992) Nitric oxide synthase in cardiac nerve fibres and neurons of rat and guinea pig heart. Circ Res 71:1533–1537

    Google Scholar 

  • Klimaschewski L, Kummer W, Mayer B (1994) Co-localization of nitric oxide synthase with vasoactive intestinal polypeptide and neuropeptide Y in the guinea pig heart. Cell Vision 1:131–137

    Google Scholar 

  • Knowles RG, Moncada S (1992) Nitric oxide as a signal in blood vessels. Trends Biochem Sci 17:399–402

    Google Scholar 

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

    Google Scholar 

  • Loesch A, Burnstock G (1993) Ultrastructural localization of nitric oxide synthase in intima of rabbit aorta. Endothelium 1:23–29

    Google Scholar 

  • Loesch A, Belai A, Burnstock G (1994) An ultrastructural study of NADPH-diaphorase and nitric oxide synthase in the perivascular nerves and vascular endothelium of the rat basilar artery. J Neurocytol 23:49–59

    Google Scholar 

  • Parent R, Al-Obaidi M, Lavallée M (1993) Nitric oxide formation contributes to β-adrenergic dilation of resistance coronary vessels in conscious dogs. Circ Res 73:241–251

    Google Scholar 

  • Pasqualotto BA, Vincent SR (1991) Galanin and NADPH-diaphorase coexistence in cholinergic neurons of the rat basal forebrain. Brain Res 551:78–86

    Google Scholar 

  • Santer RM, Symons D (1993) Distribution of NADPH-diaphorase activity in rat paravertebral, prevertebral and pelvic sympathetic ganglia. Cell Tissue Res 271:115–121

    Google Scholar 

  • Schmidt HHHW, Gagne GD, Nakane M, Pollock JS, Miller M, Murad F (1992) Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40:1439–1456

    Google Scholar 

  • Schmidt HHHW, Lohmann SM, Walter U (1993) The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochem Biophys Acta 1178:153–175

    Google Scholar 

  • Sheng H, Gagne GD, Matsumoto T, Miller MF, Förstermann U, Murad F (1993) Nitric oxide synthase in bovine superior cervical ganglion. J Neurochem 61:1120–1126

    Google Scholar 

  • Shepherd JT, Vanhoutte PM (1991) Endothelium-derived relaxing (EDRF) and contracting factors (EDCF) in the control of cardiovascular homeostasis: the pioneering observations. In: Rubanyi GM (ed) Cardiovascular significance of endothelium-derived vasoactive factors. Futura, Mount Kisco, NY, pp 39–64

    Google Scholar 

  • Smith TP, Canty JM (1993) Modulation of coronary autoregulatory responses by nitric oxide. Circ Res 73:232–240

    Google Scholar 

  • Tanaka K, Hassall CJS, Burnstock G (1993a) Distribution of intracardiac neurones and nerve terminals that contain a marker for nitric oxide, NADPH-diaphorase, in the guinea-pig heart. Cell Tissue Res 273:293–300

    Google Scholar 

  • Tanaka K, Ohshima H, Esumi H, Chiba T (1993b) Direct synaptic contacts of nitric oxide synthase-immunoreactive nerve terminals on the neurons of the intracardiac ganglia of the guinea pig. Neurosci Lett 158:67–70

    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 

  • Ursell PC, Mayes M (1993) The majority of nitric oxide synthase in pig heart is vascular and not neural. Cardiovasc Res 27:1920–1924

    Google Scholar 

  • Vincent SR (1994) Nitric oxide: a radical neurotransmitter in the central nervous system. Prog Neurobiol 42:129–160

    Google Scholar 

  • Vincent SR, Johansson O, Hökfelt T, Skirboll L, Elde RP, Terenius L, Kimmel J, Goldstein M (1983) NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin and avian pancreatic polypeptide (APP)-like immunoreactivities. J Comp Neurol 217:252–263

    Google Scholar 

  • Ward SM, Xue C, Sanders KM (1994) Localization of nitric oxide synthase in canine ileocolonic and pyloric sphincters. Cell Tissue Res 275:513–527

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sosunov, A.A., Hassall, C.J.S., Loesch, A. et al. Ultrastructural investigation of nitric oxide synthase-immunoreactive nerves associated with coronary blood vessels of rat and guinea-pig. Cell Tissue Res 280, 575–582 (1995). https://doi.org/10.1007/BF00318361

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318361

Key words

Navigation