Skip to main content
SpringerLink
Log in

Coexistence of NADPH-diaphorase and vasoactive intestinal polypeptide in the enteric nervous system of the Atlantic cod (Gadus morhua) and the spiny dogfish (Squalus acanthias)

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

Abstract

The distribution of NADPH (nicotinamide adenine dinucleotide phosphate)-diaphorase in nerve cells in the gastrointestinal tract has been investigated and compared in three fish species representing different evolutionary branches. In mammals, NADPH-diphorase is identical to nitric oxide synthase (NOS) and can, in the presence of NADPH, reduce the dye nitroblue tetrazolium, resulting in a blue product. Using this method, we have found numerous NADPH-diaphorase-containing nerve cells in the myenteric plexus of the Atlantic cod (Gadus morhua) and the spiny dogfish (Squalus acanthias) but none in the hagfish (Myxine glutinosa). In the cod, nerve fibres were sparsely stained, whereas in the dogfish, they formed a dense pattern of fibre bundles. Double-staining for NADPH-diaphorase and the neuropolypeptides VIP (vasoactive intestinal polypeptide) and PACAP (pituitary adenylate cyclase activating peptide) revealed three separate populations designated VIP/NADPH, VIP/- and NADPH/-. The majority but not all of the NADPH-diaphorase-positive cells also showed VIP or PACAP immunoreactivity and vice versa. The presence of NADPH-diaphorase in neurons and the distribution of these neurons in the gastrointestinal tract of the two species indicate a physiological role for nitric oxide in the control of gut motility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

  • 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 

  • Allescher HD, Sattler D, Piller C, Schusdziarra V, Classen M (1992) Ascending neural pathways in the rat ileum in vitro-effect of capsaicin and involvement of nitric oxide. Eur J Pharmacol 217:153–162

    Google Scholar 

  • Belai A, Schmidt HHHW, Hoyle CHV, Hassall CJS, Saffrey MJ, Moss J, Förstermann U, Murad F, Burnstock G (1992) Colocalization of nitric oxide synthase and NADPH-diaphorase in the myenteric plexus of the rat gut. Neurosci Lett 143:60–64

    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 

  • Bult H, Boeckxstaens G, Pelckmans P, Jordaens F, Van Maercke Y, Herman A (1990) Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature 345:346–347

    Google Scholar 

  • Burnstock G (1959) The innervation of the gut of the brown trout Salmo trutta. Quart J Microsc Sci 100:199–220

    Google Scholar 

  • Costa M, Furness JB, Pompolo S, Brookes SJH, Bornstein JC, Bredt DS, Snyder SH (1992) Projections and chemical coding of neurons with immunoreactivity for nitric oxide synthase in the guinea-pig small intestine. Neurosci Lett 148:121–125

    Google Scholar 

  • Dawson T, Bredt DS, Fotuhi M, Hwang P, 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 

  • De Giorgi R, Parodi JE, Brecha NC, Brunicardi FC, Becker JM, Go VLW, Sternini C (1994) Nitric oxide producing neurons in the monkey and human digestive system. J Comp Neurol 342:619–627

    Google Scholar 

  • Dimaline R (1989) Vasoactive intestinal peptide. In: Holmgren S (ed) The comparative physiology of regulatory peptides. Chapman and Hall, London, pp 150–173

    Google Scholar 

  • Fänge R, Johnels AG, Enger PS (1963) The autonomic nervous system. In: Brodal A, Fänge R (eds) The biology of Myxine. Universitet Forlaget, Oslo, pp 124–136

    Google Scholar 

  • Förstermann U, Schmidt H, Pollock J, Sheng H, Mitchell J, Warner T, Nakane M, Murad F (1991) Isoforms of nitric oxide synthase; characterization and purification from different cell types. Biochem Pharmacol 42:1849–1857

    Google Scholar 

  • Forster ER, Southam E (1993) The intrinsic and vagal extrinsic innervation of the rat stomach contains nitric oxide synthase. Neuroreport 4:275–278

    Google Scholar 

  • Gabella G (1969) Detection of nerve cells by a histochemical technique. Experientia 25:218–219

    Google Scholar 

  • Gabella G (1987) The number of neurons in the small intestine of mice, guinea-pigs and sheep. Neuroscience 22:737–752

    Google Scholar 

  • Grider JR, Jin JG (1993) Vasoactive intestinal peptide release and L-citrulline production from isolated ganglia of the myenteric plexus: evidence for regulation of vasoactive intestinal peptide release by nitric oxide. Neuroscience 54:521–526

    Google Scholar 

  • Holmgren S, Nilsson S (1983) Bombesin-, gastrin/CCK-, 5-hydroxytryptamine-, neurotensin-, somatostatin-, and VIP-like immunoreactivity and catecholeamine fluorescence in the gut of the elasmobranch, Squalus acanthias. Cell Tissue Res 234:595–618

    Google Scholar 

  • Hope B, Michael G, Knigge K, Vincent S (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814

    Google Scholar 

  • Jin JG, Misra S, Grider JR, Makhlouf GM (1993) Functional difference between SP and NKA: relaxation of gastric muscle by SP is mediated by VIP and NO. Am J Physiol 264:G678-G685

    Google Scholar 

  • Kanada A, Hata F, Suthamnatpong N, Maehara T, Ishii T, Takeuchi T, Yagasaki O (1992) Key roles of nitric oxide and cyclic GMP in nonadrenergic and noncholinergic inhibition in rat ileum. Eur J Pharmacol 216:287–292

    Google Scholar 

  • Karila P, Jönsson AC, Jensen J, Holmgren S (1993) Galanin-like immunoreactivity in extrinsic and intrinsic nerves to the gut of the Atlantic cod, Gadus morhua, and the effect of galanin on the smooth muscle of the gut. Cell Tissue Res 271:537–544

    Google Scholar 

  • Li CG, Rand MJ (1990) Nitric oxide and vasoactive intestinal polypeptide mediate non-adrenergic, non-cholinergic inhibitory transmission to smooth muscle of the rat gastric fundus. Eur J Pharmacol 191:303–309

    Google Scholar 

  • Li ZS, Furness JB (1993) Nitric oxide synthase in the enteric nervous system of the rainbow trout, Salmo gairdneri. Arch Histol Cytol 56:185–193

    Google Scholar 

  • Li ZS, Furness JB, Young HM, Campbell G (1992) Nitric oxide synthase immunoactivity and NADPH diaphorase enzyme activity in neurons of the gastrointestinal tract of the toad, Bufo marinus. Arch Histol Cytol 55:333–350

    Google Scholar 

  • Li ZS, Murphy S, Furness JB, Young HM, Campbell G (1993) Relationships between nitric oxide synthase, vasoactive intestinal peptide and substance P immunoreactivities in neurons of the amphibian intestine. J Auton Nerv Syst 44:197–206

    Google Scholar 

  • Maggi CA, Giuliani S (1993) Multiple inhibitory mechanisms mediate non-adrenergic non-cholinergic relaxation in the circular muscle of the guinea-pig colon. Naunyn-Schmiedeberg's Arch Pharmacol 347:630–634

    Google Scholar 

  • Matsumoto T, Nakane M, Pollock JS, Kuk JE, Förstermann U (1993) A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61–64

    Google Scholar 

  • McConalogue K, Furness JB (1993) Projections of nitric oxide synthesizing neurons in the guinea-pig colon. Cell Tissue Res 271:545–553

    Google Scholar 

  • Moncada S, Palmer R, Higgs A (1989) The biological significance of nitric oxide formation from L-arginine. Biochem Soc Trans 17:642–644

    Google Scholar 

  • Nichols K, Krantis A, Staines W (1992) Histochemical localization of nitric oxide-synthesizing neurons and vascular sites in the guinea-pig intestine. Neuroscience 51:791–799

    Google Scholar 

  • Nilsson S (1983) Autonomic nerve function in the vertebrates. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Olsson C, Holmgren S (1994) Distribution of PACAP (pituitary adenylate cyclase-activating polypeptide)-like and helospectin-like peptides in the teleost gut. Cell Tissue Res 277:539–547

    Google Scholar 

  • Scherer-Singler U, Vincent S, Kimura H, McGeer E (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Methods 9:229–234

    Google Scholar 

  • Schober A, Malz CR, Meyer DL (1993) Enzyme histochemical demonstration of nitric oxide synthase in the diencephalon of the rainbow trout (Oncorhynchus mykiss). Neurosci Lett 151:67–70

    Google Scholar 

  • Smart D, Johnston CF, Curry WJ, Shaw C, Halton DW, Fairweather I, Buchanan KD (1992) Immunoreactivity to two specific regions of chromogranin A in the nervous system of Ascaris suum: an immunocytochemical study. Parasitol Res 78:329–335

    Google Scholar 

  • Sogni P, Moreau R, Ohsuga M, Cailmail S, Oberti F, Hadengue A, Pussard E, Lebrec D (1992) Evidence for normal nitric oxide-mediated vasodilator tone in conscious rats with cirrhosis. Hepatology 16:980–983

    Google Scholar 

  • Tam F, Hillier K (1992) The role of nitric oxide in mediating non-adrenergic non-cholinergic relaxation in longitudinal muscle of human taenia-coli. Life Sci 51:1277–1284

    Google Scholar 

  • Timmermans JP, Barbiers M, Scheuermann DW, Bogers JJ, Adriaensen D, Fekete E, Mayer B, Van Marck EA, De Groodt-Lasseel MHA (1994) Nitric oxide synthase immunoreactivity in the enteric nervous system of the developing human digestive tract. Cell Tissue Res 275:235–245

    Google Scholar 

  • Ward SM, Xue C, Shuttleworth CW, Bredt DS, Synder SH, Sanders KM (1992) NADPH diaphorase and nitric oxide synthase colocalization in enteric neurons of canine proximal colon. Am J Physiol 263:G277-G284

    Google Scholar 

  • Young HM, Furness JB, Shuttleworth C, Bredt DS, Synder SH (1992) Co-localization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guinea-pig intestine. Histochemistry 97:375–378

    Google Scholar 

  • Young HM, Furness JB, Sewell P, Burcher EF, Kandiah CJ (1993) Total numbers of neurons in myenteric ganglia of the guinea-pig small intestine. Cell Tissue Res 272:197–200

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoophysiology, Göteborg University, Medicinaregatan 18, S-413 90, Göteborg, Sweden

    Catharina Olsson & Paul Karila

Authors
  1. Catharina Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Karila
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olsson, C., Karila, P. Coexistence of NADPH-diaphorase and vasoactive intestinal polypeptide in the enteric nervous system of the Atlantic cod (Gadus morhua) and the spiny dogfish (Squalus acanthias). Cell Tissue Res 280, 297–305 (1995). https://doi.org/10.1007/BF00307802

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00307802

Key words

Search

Navigation