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NADPH diaphorase activity in peptidergic neurones 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 ,
M. C. Thorndyke  and
R. J. Walker
Z. A. Bascal
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of Southampton, Southampton SO16 7PX
A. Montgomery
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of Southampton, Southampton SO16 7PX
L. Holden-Dye
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of Southampton, Southampton SO16 7PX
R. G. Williams
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of Southampton, Southampton SO16 7PX
M. C. Thorndyke
Affiliation:
Department of Biology, School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX
R. J. Walker
Affiliation:
Department of Physiology and Pharmacology, Bassett Crescent East, University of Southampton, Southampton SO16 7PX
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Summary

The histochemical marker for nitric oxide synthase, NADPH diaphorase, is known to co-localize in mammalian neurones with various classical neurotransmitters and neuropeptides. The nervous system of the parasitic nematode Ascaris suum has previously been shown to contain both NADPH diaphorase activity and neuropeptide immunoreactivity. This study examined the possibility that NADPH diaphorase and neuropeptide immunoreactivity may co-exist in the same neurones. Two antisera were used, one raised to KYSALMFamide, a C-terminal synthetic analogue of SALMFamide 1 (GFNSALMFamide), and another that recognizes calcitonin-gene-related peptide (CGRP). We provide evidence that in a distinct subset of neurones in the ventral, dorsal and lateral ganglia NADPH diaphorase staining and SALMFamide- like immunoreactivity are co-localized, suggesting a possible role for nitric oxide in modulating neuropeptide activity in these regions. CGRP-like immunoreactivity was less widely distributed, and was not consistently co-localized with NADPH diaphorase.

Keywords

Ascaris suumnematodenitric oxideNADPH diaphoraseCGRPSALMFamideFMRFamide.
Type
Research Article
Information
Parasitology , Volume 112 , Issue 1 , January 1996 , pp. 125 - 134
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Aimi, Y., Fujimura, M., Vincent, S. R. & Kimura, H. (1991). Localization of NADPH diaphorase containing neurons in sensory ganglia of the rat. Journal of Comparative Neurology 306, 382–92.CrossRefGoogle ScholarPubMed
Bascal, Z. A., Montgomery, A., Holden-Dye, L., Williams, R. G. & Walker, R. J. (1995). Histochemical mapping of NADPH diaphorase in the nervous system of the parasitic nematode Ascaris suum. Parasitology 110, 625–37.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
Bowman, J. W., Thompson, D. P., Friedman, A. R., Winterrowd, C. A., Ichhpurani, A. K., Blair, K. L. & Geary, T. G. (1994). Neuromuscular effects of nematode FMRF-amide-like peptides in Ascaris suum. Society of Neuroscience Abstracts 554, 19.Google Scholar
Brownlee, D. J. A., Fairweather, I., Johnston, C. F., Smart, D., Shaw, C. & Halton, D. W. (1993). Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda: Ascaroidea). Parasitology 106, 305–16.CrossRefGoogle ScholarPubMed
Cowden, C., Stretton, A. O. W. & Davis, R. W. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.CrossRefGoogle ScholarPubMed
Cowden, C. & Stretton, A. O. W. (1993). AF2, an Ascaris neuropeptide: isolation, sequence and bioactivity. Peptides 14, 423–30.CrossRefGoogle ScholarPubMed
Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M. & Snyder, S. L. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences, USA 88, 7797–801.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
Elphick, M. R., Price, D. A., Lee, T. D. & Thorndyke, M. C. (1991 a). The SALMFamides: a new family of neuropeptides isolated from an echinoderm. Proceedings of the Royal Society 243B, 121–7.Google ScholarPubMed
Elphick, M. R., Reeve, J. R., Burke, R. D. & Thorndyke, M. C. (1991 b). Isolation of the neuropeptide SALMFamide-1 from starfish using a new antiserum. Peptides 12, 455–9.CrossRefGoogle ScholarPubMed
Elphick, M. R., Rayne, R. C., Riveros-Moreno, V., Moncada, S. & O'Shea, M. (1995). Nitric oxide synthesis in locust olfactory interneurones. Journal of Experimental Biology 198, 821–9.CrossRefGoogle ScholarPubMed
Franks, C. J., Holden-Dye, L., Williams, R. F., Pang, F- Y. & Walker, F. J. (1994). A nematode FMRFamide- like peptide SDPNFLRFamide (PF1) relaxes the dorsal muscle strip preparation of Ascaris suum. Parasitology 108, 229–36.CrossRefGoogle ScholarPubMed
Geary, R. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14.CrossRefGoogle ScholarPubMed
Holden-Dye, L., Franks, C. J., Williams, R. G. & Walker, R. J. (1995). The effect of the nematode peptides SDPNFLRFamide (PF1) and SADPNFLRFamide (PF2) on synaptic transmission in the parasitic nematode Ascaris suum. Parasitology 110, 449–55.CrossRefGoogle 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
Johansson, K. U. I. & Carlberg, M. (1994). NADPH- diaphorase histochemistry and nitric oxide synthase activity in deutocerebrum of the crayfish, Pacifastacuss leniusculus (Crustacea, Decapoda). Brain Research 649, 36–42.CrossRefGoogle ScholarPubMed
Johnson, C. D. & Stretton, A. O. W. (1987). GABA- immunoreactivity in inhibitory motor neurons of the nematode Ascaris. Journal of Neuroscience 7, 223–35.CrossRefGoogle ScholarPubMed
Keating, C., Thorndyke, M. C., Holden-Dye, L., Franks, C. J., Williams, R. G. & Walker, R. J. (1993). Immunocytochemical detection of SALMFamide-like immunoreactivity in the nervous system of the nematode Haemonchus contortus. British Journal of Pharmacology 111, 307P.Google Scholar
Keating, C., Thorndyke, M. C., Holden-Dye, L., Williams, R. G. & Walker, R. J. (1995). FMRFamide- like neuropeptide AF2 is present in the parasitic nematode Haemonchus contortus. Parasitology (In the press.)CrossRefGoogle ScholarPubMed
Martinez, A., Riveros-Moreno, V., Polak, J. M., Moncada, S. & Sesma, P. (1994). Nitric oxide (NO) synthase immunoreactivity in the starfish Marthasterias glacialis. Cell and Tissue Research 275, 599–603.CrossRefGoogle Scholar
Moore, J. S. & Thorndyke, M. C. (1993). Immunocytochemical mapping of the novel echinoderm neuropeptide SALMFamide 1 (SI) in the starfish Asterias rubens. Cell and Tissue Research 274, 605–18.CrossRefGoogle Scholar
Moroz, L. L., Winlow, W., Turner, R. W., Bulloch, A. G. M., Lukowiak, K. & Syed, N. I. (1994). Nitric oxide synthase immunoreactive cells in the CNS and periphery of Lymnaea. NeuroReport 5, 1277–80.CrossRefGoogle ScholarPubMed
Muller, U. (1994). Ca2+/calmodulin-dependent nitric oxide synthase in Apis mellifera and Drosophila melanogaster. European Journal of Neuroscience 6, 1362–70.CrossRefGoogle ScholarPubMed
Nathan, C. (1992). Nitric oxide as a secretory product of mammalian cells. FASEB Journal 6, 3051–64CrossRefGoogle ScholarPubMed
Neuhuber, W. L., Worl, J., Berthoud, H-R. & Conte, B. (1994). NADPH-diaphorase positive nerve fibres associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric neurons. Cell and Tissue Research 276, 23–30.CrossRefGoogle ScholarPubMed
Okamura, H., Miyagawa, A., Takagi, H., Esumi, H., Yanaihara, N. & Ibata, Y. (1994). Co-existence of PACAP and nitric oxide synthase in the rat hypothalamus. NeuroReport 5, 1177–80.CrossRefGoogle ScholarPubMed
Pang, F-Y., Mason, J., Holden-Dye, L., Franks, C. J., Williams, R. G. & Walker, R. J. (1995). The effects of the nematode peptide, KHEYLFRamide (AF2), on the somatic musculature of the parasitic nematode Ascaris suum. Parasitology 110, 353–62.CrossRefGoogle ScholarPubMed
Pasqualotto, B. A. & Vincent, S. R. (1991). Galanin and NADPH diaphorase coexistence in cholinergic neurons of the rat basal forebrain. Brain Research 551, 78–86.CrossRefGoogle ScholarPubMed
Sanchhez, F., Alonso, J. R., Arevalo, R., Blanco, E., Aijon, J. & Vazquez, F. (1994). Coexistence of NADPH-diaphorase with vasopressin and oxytocin in the hypothalamic magnocellular neurosecretory nuclei of the rat. Cell and Tissue Research 276, 31–4.CrossRefGoogle Scholar
Schuman, E. M. & Madison, D. V. (1994). Nitric Oxide and synaptic function. Annual Review of Neurosciences 17, 153–83.CrossRefGoogle ScholarPubMed
Scott, J. W., McDonald, J. K. & Pemberton, J. L. (1987). Short axon cells of the rat olfactory bulb display NADPH-diaphorase activity, neuropeptide Y-like immunoreactivity, and somatostatin-like immunoreactivity. Journal of Comparative Neurology 260, 378–91.CrossRefGoogle ScholarPubMed
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: an immunocytochemical study. Journal of Comparative Neurology 294, 362–76.CrossRefGoogle ScholarPubMed
Snyder, S. H. & Bredt, D. S. (1991). Nitric oxide as a neuronal messenger. Trends in Pharmacological Sciences 12, 125–8.CrossRefGoogle ScholarPubMed
Spike, R. C., Todd, A. J. & Johnston, H. M. (1993). Coexistence of NADPH diaphorase with GABA, glycine and acetylcholine in rat spinal cord. Journal of Comparative Neurology 335, 320–33.CrossRefGoogle ScholarPubMed
Stretton, A. O. W., Cowden, C., Sithigorngul, P. & Davis, R. W. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–S116.CrossRefGoogle ScholarPubMed
Valtschanoff, J. G., Weinberg, R. J., Kharazia, V. N., Schmidt, H. H., Nakane, M. & Rustioni, A. (1993). Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neuroscience Letters 157, 157–61.CrossRefGoogle ScholarPubMed
Vincent, S. R. (1994). Nitric oxide: a radical neurotransmitter in the central nervous system. Progress in Neurobiology 42, 129–60.CrossRefGoogle ScholarPubMed
Vincent, S. R. & Hope, B. T. (1992). Neurons that say NO. Trends in Pharmacological Sciences 15, 108–13.Google ScholarPubMed
Vincent, S. R., Satoh, K., Armstrong, D. M., Panula, P.,Vale, W. & Fibiger, H. C. (1986). Neuropeptides and NADPH diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience 17, 167–82.CrossRefGoogle ScholarPubMed
Weiler, R. & Kewitz, B. (1993). The marker for nitric oxide synthase, NADPH-diaphorase, co-localizes with GABA in horizontal cells and cells of the inner retina in the carp retina. Neuroscience Letters 158, 151–4.CrossRefGoogle ScholarPubMed
Wikgren, M. & Fagerholm, H. P. (1993). Neuropeptides in sensory structures of nematodes. Acta Biologica Hungarica 44, 133–6.Google ScholarPubMed