Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-21T17:37:51.819Z Has data issue: false hasContentIssue false
  • English
  • Français

Histochemical mapping of NADPH diaphorase in the nervous system of the parasitic nematode Ascaris suum

Published online by Cambridge University Press:  06 April 2009

Z. A. Bascal ,
A. Montgomery ,
L. Holden-Dye ,
R. G. Williams  and
R. J. Walker
Z. A. Bascal
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of SouthamptonSO16 7PX
A. Montgomery
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of SouthamptonSO16 7PX
L. Holden-Dye*
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of SouthamptonSO16 7PX
R. G. Williams
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of SouthamptonSO16 7PX
R. J. Walker
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of SouthamptonSO16 7PX
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Summary

NADPH diaphorase has recently been discovered to be responsible for neuronal nitric oxide (NO) synthase activity in mammals. It thus serves as a histochemical marker for the localization of NO synthase in the nervous system. The histochemical technique was used to map out potential NO-producing neurones in the nervous system of the parasitic nematode, Ascaris suum. Positive staining for NADPH diaphorase was present in various parts of the central nervous system, in particular within selective cell bodies and fibres in the ventral ganglion, the retrovesicular ganglion, ventral and dorsal cords and sublateral lines. Intense staining was also present in the motorneurone commissures, indicating a potential role for NO as a neurotransmitter at the neuromuscular junction. NADPH disphorase-positive neurones were not confined to the central nervous system. Selective staining was also present in the enteric nervous system, in particular the pharynx and in the peripheral nervous system innervating the sensory organs.

Keywords

nematodesAscaris suumNADPH diaphorasenitric oxide synthase
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 625 - 637
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Angstadt, J. D., Donmoyer, J. E. & Stretton, A. O. W. (1989). Retrovesicular ganglion of the nematode Ascaris. Journal of Comparative Neurology 284, 374–88.CrossRefGoogle ScholarPubMed
Barrett, J. (1991). Amino acid metabolism in Helminths. Advances in Parasitology 30, 39–107.CrossRefGoogle ScholarPubMed
Blottner, D. & Baumgarten, H.-G. (1992). Nitric Oxide synthase (NOS)-containing sympathoadrenal cholinergic neurons of the rat IML-cell column: evidence from histochemistry, immunohistochemistry, and retrograde labelling. Journal of Comparative Neurology 316, 45–55.CrossRefGoogle Scholar
Bredt, D. S. & Snyder, H. S. (1990). Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proceedings of the National Academic of Sciences, USA 87, 682–685.CrossRefGoogle ScholarPubMed
Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M. & Snyder, S. H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academic of Sciences, USA 88, 7797–801.CrossRefGoogle ScholarPubMed
Dawson, T. M., Steiner, J. P., Mong, J. A. & Snyder, S. H. (1993). Multiple isoforms of neuronal nitric oxide synthase. Society of Neuroscience Abstract 19, 905.Google Scholar
Elofsson, R., Carlberg, M., Moroz, L., Nezlin, L. & Sakharov, D. (1993). Is nitric oxide (NO) produced by invertebrate neurones? NeuroReport 4, 279–82.CrossRefGoogle ScholarPubMed
Elphick, M. R., Green, I. C. & O'Shea, M. (1993). Nitric oxide synthesis and action in an invertebrate brain. Brain Research 619, 344–6.CrossRefGoogle Scholar
Ernster, L. (1967). DT diaphorase. Methods in Enzymology 10, 329.Google Scholar
Garthwaite, J. (1991). Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends in Neurosciences 14, 60–7.CrossRefGoogle ScholarPubMed
Gelperin, A. (1994). Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature, London 369, 61–3.CrossRefGoogle Scholar
Halton, D. W., Shaw, C., Maule, A. G. & Smart, D. (1994). Regulatory peptides in helminth parasites. Advances in Parasitology 34, 164–227.Google ScholarPubMed
Hope, B. T. & Vincent, s. R. (1989). Histochemical characterization of neuronal NADPH-diaphorase. Journal of Histochemistry and Cytochemistry 37, 653–61.CrossRefGoogle ScholarPubMed
Hope, B. T., Michael, G. J., Knigge, K. M. & Vincent, S. R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences, USA 68, 2811–14.CrossRefGoogle Scholar
Ignarro, L. J. (1991). Signal transduction mechanisms involving nitric oxide. Biochemical Pharmacology 41, 485–90.CrossRefGoogle ScholarPubMed
Lee, D. L. (1982). The Physiology of Nematodes. Oliver & Boyde.Google Scholar
Matsumoto, T., Nakane, M., Pollock, J. S., Kuk, J. E. & Forstermann, U. (1993). A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neuroscience Letters 155, 61–4.CrossRefGoogle ScholarPubMed
Moncada, S., Palmer, R. M. J. & Higgs, E. A. (1991). Nitric oxide: Physiology, pathology and pharmacology. Pharmacological Reviews 43, 109–42.Google Scholar
Montgomery, A., Bascal, Z., Williams, R. G., Holden-Dye, L., Thorndyke, M. C. & Walker, R. J. (1994). Co-localization studies of NADPH-diaphorase positive and peptidergic neurons in the nervous system of Ascaris suum. Regulatory Peptides 51, 287.CrossRefGoogle Scholar
Moroz, L. L., Park, J.-H. & Winlow, W. (1993). Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. NeuroReport 4, 643–6.CrossRefGoogle ScholarPubMed
Moroz, L. L., Radbourne, S. & Winlow, W. (1994) Detection of nitric oxide (NO) production by NO sensitive microelectrodes in invertebrates (snail and leech) and rat aorta. Journal of Physiology 481, 104P.Google Scholar
Nathan, c. (1992). Nitric oxide as a secretory product of mammalian cells. FASEB Journal 6, 3051–64.CrossRefGoogle ScholarPubMed
Schulz, R. & Triggle, c. R. (1994). Role of NO in vascular smooth muscle and cardiac muscle function. Trends in Pharmacological Sciences 15, 255–9.CrossRefGoogle ScholarPubMed
Schuman, E. M. & Madison, D. V. (1994). Nitric oxide and synaptic function. Annual Review of Neurosciences 17, 153–83.CrossRefGoogle ScholarPubMed
Snyder, S. H. & BredtD, S. D, S. (1991). Nitric oxide as a neuronal messenger. Trends in Pharmacological Sciences 12, 125–8.CrossRefGoogle ScholarPubMed
Thalhofer, H. P. & Hofer, H. W. (1989). Purification and properties of cyclic-3′,5′-GMP-dependent protein kinase from the nematode Ascaris suum. Archives of Biochemical Biophysics 273, 535–42.CrossRefGoogle ScholarPubMed
Tracey, W. R., Nakane, M., Pollock, J. S. & Forstermann, U. (1993). Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorase, but represent only a fraction of total cellular NADPH diaphorase activity. Biochemical and Biophysical Research Communications 195, 1035–40.CrossRefGoogle Scholar
Vincent, S. R. (1994). Nitric oxide: a radical neurotransmitter in the central nervous system. Progress in Neurobiology 42, 129–60.CrossRefGoogle ScholarPubMed
Vizzard, M. A., Erdman, S. L., Erickson, V. L., Stewart, R. J., Roppolo, J. R. & De Groat, W. C. (1994). Localization of NADPH diaphorase in the lumbosacral spinal cord and dorsal root ganglia of the cat. Journal of Comparative Neurology 336, 62–75.CrossRefGoogle Scholar
Walker, R. J., Colquhoun, L. M., Parri, H. R., Wiliams, R. G. & Holden-Dye, L. (1992). Pharmacology of the Ascaris nervous system. In Neurotox '91, Molecular Basis of Drug and Pesticide Action, (ed. Duce, I. R.) Cambridge: Elsevier Science Publishers Ltd.Google Scholar
Willett, J.. (1980). Control mechanisms in nematodes. In Nematodes as Biological Models, Vol. 1. Behavioral and Developmental Models, (ed. Zuckerman, I. & Morton, B.) London: Academic Press.Google Scholar