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NO nerves in a tapeworm. NADPH-diaphorase histochemistry in adult Hymenolepis diminuta

Published online by Cambridge University Press:  06 April 2009

M. K. S. Gustafsson ,
A. M. Lindholm ,
N. B. Terenina  and
M. Reuter
M. K. S. Gustafsson*
Affiliation:
Department of Biology, Åbo Akademi University, Artillerigatan 6, FIN-20520 Åbo, Finland
A. M. Lindholm
Affiliation:
Department of Biology, Åbo Akademi University, Artillerigatan 6, FIN-20520 Åbo, Finland
N. B. Terenina
Affiliation:
Institute of Parasitology of the Russian Academy of Sciences, Lenin Avenue 33, 117071 Moscow, Russia
M. Reuter
Affiliation:
Department of Biology, Åbo Akademi University, Artillerigatan 6, FIN-20520 Åbo, Finland
*
* Corresponding author: Department of Biology, Åbo Akademi University, Artillerigatan 6, FIN-20520 Åbo, Finland. Tel: + 358 21 2654603. Fax: + 358 21 2654748. E-mail: [email protected].
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Summary

The free radical nitric oxide (NO), which is synthesized by nitric oxide synthase (NOS), has recently been discovered to function as a neuronal messenger. The presence of NOS was detected in the nervous system of adult Hymenolepis diminuta with NADPH-diaphorase (NADPH-d) histochemistry. The NADPH-d histochemical reaction is regarded as a selective marker for NOS in neuronal tissue. NADPH-d staining was observed in nerve fibres in the main and minor nerve cords and the transverse ring commissures, and in cell bodies in the brain commissure, along the main nerve cords, in the suckers and the rostellar sac. NADPH-d staining was also observed in the wall of the internal seminal vesicle and the genital atrium. The pattern of NADPH-d staining was compared with that of the 5-HT immunoreactive nervous elements. The NADPH-d staining reaction and the 5-HT immunoreactivity occur in separate sets of neurons. This is the first time the NADPH-d reaction has been demonstrated in the nervous system of a flatworm, indicating that NOS is present and that NO can be produced at this level of evolution.

Keywords

Hymenolepis diminutanitric oxideNADPH-diaphoraseserotoninnervous system
Type
Research Article
Information
Parasitology , Volume 113 , Issue 6 , December 1996 , pp. 559 - 565
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

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, 625–637.CrossRefGoogle ScholarPubMed
Bred´t, D. S. (1995). Molecular characterization of nitric oxide synthase. In Nitric Oxide in the Nervous System (ed. Vincent, S.), pp. 1–19. Academic Press, London.Google Scholar
Bredt, D. S., Hwang, P. M., Glatt, C. E., Lowenstein, C., Reed, R. R. & Snyder, S. H. (1991 a). Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature, London 351, 714–718.CrossRefGoogle ScholarPubMed
Bredt, D. S., Glatt, C. E., Hwang, P. M., Fothui, M., Dawson, T. M. & Snyder, S. H. (1991 b). Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7, 615–624.CrossRefGoogle ScholarPubMed
Colasanti, M., Lauro, G. M. & Venturini, G. (1995). NO in hydra feeding response. Nature, London 374, 505.CrossRefGoogle ScholarPubMed
Coons, A. H., Leduc, E. H. & Connolly, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study for the hyperimmune rabbit. Journal of Experimental Medicine 102, 49–60.CrossRefGoogle Scholar
Elphick, M., Green, I. C. & O'Shea, M. (1993). Nitric oxide synthesis and action in an invertebrate brain. Brain Research 619, 344–346.CrossRefGoogle Scholar
Elofsson, R., Carlberg, M., Moroz, L., Nezlin, L. & Sakharov, D. (1993). Is nitric oxide (NO) produced by invertebrate neurones? NeuroReport 4, 279–282.CrossRefGoogle ScholarPubMed
Fairweather, I. & Threadgold, L. T. (1983). Hymenolepis nana: the fine structure of the adult nervous system. Parasitology 86, 89–103.CrossRefGoogle ScholarPubMed
Fairweather, I., MaCartney, G. A., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1988). Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) and vertebrate neuropeptides in the nervous system of excysted cysticercoid larvae of the rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology Research 74, 371–379.CrossRefGoogle ScholarPubMed
Feelish, M. & Martin, J. F. (1995). The early role of nitric oxide in evolution. Trends in Ecology and Evolution 10, 496–499.CrossRefGoogle Scholar
Garthwaite, J. (1991). Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends in Neuroscience 14, 60–67.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. (1992). The neuroanatomy of parasitic flatworms. Advances in Neuroimmunology 2, 267–286.CrossRefGoogle Scholar
Hope, B. T., Michael, G. J., Knippe, K. M. & Vincent, S. R. (1991). Neuronal NADPH-diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences, USA 88, 2811–2814.CrossRefGoogle ScholarPubMed
Johansson, K. U. I. & Carlberg, M. (1994). NADPH-diaphorase histochemistry and nitric oxide synthase activity in deutocerebrum of the crayfish, Pacifastacus leniusculus (Crustacea, Decapoda). Brain Research 649, 36–42.CrossRefGoogle ScholarPubMed
Johansson, K. U. I. & Hallberg, E. (1995). Fine structural localization of NADPH-diaphorase in the crayfish olfactory lobe. Proceedings of the International Society for Invertebrate Neurobiology, Tihany, p. 34.Google Scholar
Knowles, R. G., Palacios, M., Palmer, R. M. J. & Moncada, S. (1989). Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proceedings of the National Academy of Sciences, USA 86, 5159–5162.CrossRefGoogle ScholarPubMed
Koesling, D., Humbert, P. & Schultz, G. (1995). The NO receptor: characterization and regulation of soluble guanylyl cyclase. In Nitric Oxide in the Nervous System (ed. Vincent, S.), pp. 43–50. Academic Press, London.CrossRefGoogle Scholar
Leake, L. D. & Moroz, L. L. (1995). Nitric oxide in the CNS of the leech Hirudo medicinalis. Proceedings of the International Society for Invertebrate Neurobiology, Tihany, p. 42.Google Scholar
Lee, M. B., Bueding, E. & Schiller, E. L. (1978). The occurrence and distribution of 5-hydroxytryptamine in Hymenolepis diminuta and H. nana. Journal of Parasitology 64, 254–257.CrossRefGoogle ScholarPubMed
Lumsden, R. D. & Specian, R. (1980). The morphology, histology, and the fine structure of the adult stage of the cyclophyllidean tapeworm Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 157–280. Academic Press, New York.CrossRefGoogle Scholar
McKay, D. M., Fairweather, I., Johnston, C. F., Shaw, C. & Halton, D. W. (1991). Immunocytochemical and radioimmunometrical demonstration of serotonin- and neuropeptide-immunoreactivities in the adult rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology 103, 275–289.CrossRefGoogle ScholarPubMed
Mayer, B. (1995). Biochemistry and molecular pharmacology of nitric oxide synthases. In Nitric Oxide in the Nervous System (ed. Vincent, S.), pp. 21–38. Academic Press, London.CrossRefGoogle Scholar
Moncada, S., Palmer, R. M. J. & Higgs, E. A. (1991). Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacological Reviews 43, 109–142.Google ScholarPubMed
Moroz, L. L. & Gillette, R. (1995). From Polyplacophora to Cephalopoda: Comparative analysis of nitric oxide signalling in the mollusca. Proceedings of the International Society for Invertebrate Neurobiology, Tihany, p. 46.Google ScholarPubMed
Moroz, L. L. & Winlow, W. (1995). Nitric oxide signalling in the gastropod mollusc, Lymnaea stagnalis (L.). Proceedings of the International Society for Invertebrate Neurobiology, Tihany, p. 47.Google Scholar
Rand, M. J. & Li, C. G. (1995). Nitric oxide in the autonomic and enteric nervous system. In Nitric Oxide in the Nervous System (ed. Vincent, S.), pp. 228–279. Academic Press, London.Google Scholar
Reuter, M. & Gustafsson, M. K. S. (1995). The flatworm nervous system: pattern and phylogeny. In The Nervous System of Invertebrates: An Evolutionary and Comparative Approach (ed. Breidbach, O. & Kutsch, W.), pp. 25–59. Birkhäuser Verlag, Basel.CrossRefGoogle Scholar
Schmidt, H. H. H. W., Gagne, G. D., Nakane, M., Pollock, J. S., Miller, M. F. & 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 paraneuronal functions for nitrinergic signal transduction. Journal of Histochemistry and Cytochemistry 40, 1439–1456.CrossRefGoogle ScholarPubMed
Snyder, S. H. (1992). Nitric oxide: first in a new class of neurotransmitters? Science 257, 494–496.CrossRefGoogle Scholar
Sternberger, L. A. (1974). Immunocytochemistry. In Foundation of Immunology Series (ed. Oster, A. & Weiss, L.). Prenctice Hall Inc., Englewood Cliffs, New Jersey.Google Scholar
Sukhdeo, M. V. K., Hsu, S. C., Thompson, C. S. & Mettrick, D. F. (1984). Hymenolepis diminuta: behavioral effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin. Journal of Parasitology 70, 682–688.CrossRefGoogle ScholarPubMed
Sulgostowska, T. (1972). The development of organ systems in cestodes. I. A study of histology of Hymenolepis diminuta (Rudolphi, 1819) (Hymenolepididae). Acta Parasitologica Polonica 20, 449–462.Google Scholar
Thompson, C. S. & Mettrick, D. F. (1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–1262.CrossRefGoogle Scholar
Vincent, S. R. (1995). Localization of nitric oxide neurons in the central nervous system. In Nitric Oxide in the Nervous System (ed. Vincent, S.), pp. 83–102. Academic Press, London.CrossRefGoogle Scholar
Vincent, S. R. & Hope, B. T. (1992). Neurons that say NO. Trends in NeuroScience 15, 108–113.CrossRefGoogle ScholarPubMed