Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T13:25:30.280Z Has data issue: false hasContentIssue false
  • English
  • Français

Electrophysiology of Ascaris muscle and anti-nematodal drug action

Published online by Cambridge University Press:  06 April 2009

R. J. Martin ,
M. A. Valkanov ,
V. M. E. Dale ,
A. P. Robertson  and
I. Murray
R. J. Martin
Affiliation:
Department of Preclinical Veterinary Sciences, R.(D.)S.V.S., Summerhall, University of Edinburgh, Edinburgh, EH9 1QH, UK
M. A. Valkanov
Affiliation:
Department of Preclinical Veterinary Sciences, R.(D.)S.V.S., Summerhall, University of Edinburgh, Edinburgh, EH9 1QH, UK
V. M. E. Dale
Affiliation:
Department of Preclinical Veterinary Sciences, R.(D.)S.V.S., Summerhall, University of Edinburgh, Edinburgh, EH9 1QH, UK
A. P. Robertson
Affiliation:
Department of Preclinical Veterinary Sciences, R.(D.)S.V.S., Summerhall, University of Edinburgh, Edinburgh, EH9 1QH, UK
I. Murray
Affiliation:
Department of Preclinical Veterinary Sciences, R.(D.)S.V.S., Summerhall, University of Edinburgh, Edinburgh, EH9 1QH, UK
Get access Rights & Permissions [Opens in a new window]

Summary

Three groups of anthelmintic drugs act directly and selectively on muscle membrane receptors of parasitic nematodes. These groups of anthelmintics are: (1) The Nicotinic Agonists(levamisole, pyrantel, morantel and oxantel) that act on acetylcholine receptors of nematode somatic muscle; (2) The GAB A Agonist, piperazine, that acts on nematode muscle GABA receptors; and (3) The Avermectins that open glutamate gated Cl- channels on nematode pharyngeal muscle. The electrophysiology and pharmacology of muscle and neuromuscular transmission the nematode parasite, Ascaris suum, is outlined and effects of anthelmintics that interfere with transmission described. Resistance to anthelmintics has appeared in some parasitic nematodes but the mechanisms of this resistance remain to be determined

Keywords

ElectrophysiologyAscaris suummusclepharynxlevamisolepyrantelmoranteloxantelpiperazinemilbemycinavermectins
Type
Research Article
Information
Parasitology , Volume 113 , supplement S1: Molecular biochemistry and physiology of helminth neuromuscular systems , January 1996 , pp. S137 - S156
Copyright
Copyright © Cambridge University Press 1996

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

Aceves, J., Erliji, D. & Martinez-Marnon, R. (1970). The mechanism of the paralyzing action of tetramisole on Ascaris somatic muscle. British Journal of Pharmacology 38, 602–7CrossRefGoogle Scholar
Arena, J. P. (1994). Expression of Caenorhabditis elegans messenger-RNA in Xenopus oocytes: a model system to study the mechanism of action of avermectins. Parasitology Today 10, 35–7CrossRefGoogle Scholar
Arevalo, J. I. & Saz, H. J. (1992). Effects of cholinergic agents on the metabolism of choline in muscle from Ascaris suum. Journal of Parasitology 78, 387–92CrossRefGoogle Scholar
Aubry, M. L., Cowell, P., Davey, M. J. & Shevde, S. (1970). Aspects of the pharmacology of new anthelmintics: pyrantel. British Journal of Pharmacology 38, 332–44CrossRefGoogle ScholarPubMed
Avery, L. (1993). Motor-neuron m3 controls pharyngeal muscle-relaxation timing in Caenorhabditis elegans. Journal of Experimental Biology 175, 283–97CrossRefGoogle ScholarPubMed
Baldwin, E. & Moyle, V. (1949). A contribution to the physiology and pharmacology of Ascaris lumbricoides from the pig. British Journal of Pharmacology 4, 145–52Google Scholar
Brading, A. F. & Caldwell, P. C. (1971). The resting membrane potential of the somatic muscle cells of Ascaris lumbricoides. Journal of Physiology (London) 217, 605–24CrossRefGoogle ScholarPubMed
Campbell, W. C. & Benz, G. W. (1984). Ivermectin: A review of efficacy and safety. Journal of Veterinary Pharmacology and Therapeutics 7, 1–16CrossRefGoogle ScholarPubMed
Cappe De Baillon, P. (1911). Étude sur les fibres musculaires d’Ascaris. I. Fibres parietales. Cellule 27, 165–211Google Scholar
Coles, G. C, East, J. M. & Jenkins, S. N. (1975). The mechanism of action of the anthelmintic levamisole. General Pharmacology 6, 309–13CrossRefGoogle Scholar
Colquhoun, D. & Sakmann, B. (1985). Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. Journal of Physiology (London) 369, 501–57CrossRefGoogle ScholarPubMed
Colquhoun, L., Holden-Dye, L. & Walker, R. J. (1991). The pharmacology of cholinoceptors on the somatic muscle-cells of the parasitic nematode Ascaris suum. Journal of Experimental Biology 158, 509–30CrossRefGoogle ScholarPubMed
Cowden, C. & Stretton, A. O. W. (1993). AF2, an Ascaris neuropeptide-isolation, sequence, and bioactivity. Peptides 14, 423–30CrossRefGoogle Scholar
Cowden, C., Stretton, A. O. W. & Davis, R. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73CrossRefGoogle ScholarPubMed
Cully, D. F., Vassilatis, D. K., Liu, K. K., Paress, P. S., Vanderploeg, L. H. T. & Schaeffer, J. M. (1994). Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371, 707–11CrossRefGoogle ScholarPubMed
Dale, V. M. E. & Martin, R. J. (1995). Oxantel-activated single-channel currents in the muscle membrane of Ascaris suum. Parasitology. 110. 437–48CrossRefGoogle ScholarPubMed
De Bell, J. T. (1965). A long look at neuromuscular junctions in nematodes. Quarterly Reviews of Biology 40, 233–51CrossRefGoogle Scholar
De Bell, J. T., Del Castillo, J. & Sanchez, V. (1963). Electrophysiology of the somatic muscle cells of Ascaris lumbricoides. Journal of Cellular & Comparative Physiology 62, 159–77CrossRefGoogle Scholar
Del Castillo, J., De Mello, W. C. & Morales, T. (1963). The physiological role of acetylcholine in the neuromuscular system of Ascaris lumbricoides. Archives International Physiologie Biochimie 71, 741–57CrossRefGoogle Scholar
Del Castillo, J., De Mello, W. C. & Morales, T. (1964). Influence of some ions on the membrane potential of Ascaris muscle. Journal of General Physiology 48, 129–40CrossRefGoogle Scholar
Del Castillo, J., Rivera, A., Solorzano, S. & Serrato, J. (1989). Some aspects of the neuromuscular system of Ascaris. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences 74, 1071–87CrossRefGoogle ScholarPubMed
Donahue, M. J., Yacoub, N. J. & Harris, B. G. (1982). Correlation of muscle-activity with glycogenmetabolism in muscle of Ascaris suum. American Journal of Physiology 242, R514–R521.Google Scholar
Duittoz, A. H. & Martin, R. J. (1989). SR95103 acts as a GABA antagonist in Ascaris suum muscle. British Journal of Pharmacology 97, 490P.Google Scholar
Duittoz, A. H. & Martin, R. J. (1990). Effects of the arylaminopyridazine-GABA derivatives, SR95103 and SR95531 on the Ascaris muscle GABA receptor: the relative potency of the antagonists in Ascaris is different to that at vertebrate GABAa receptors. Comparative Biochemistry and Physiology C: Pharmacology Toxicology & Endocrinology 98, 417–22CrossRefGoogle Scholar
Duittoz, A. H. & Martin, R. J. (1991a). Effects of SR95103 on GABA-activated single-channel currents from Ascaris suum muscle. Comparative Biochemistry And Physiology C-Pharmacology Toxicology & Endocrinology 98, 423–432Google Scholar
Duittoz, A. H. & Martin, R. J. (1991b). Antagonist properties of arylaminopyridazine GABA derivatives at the Ascaris muscle GABA receptor. Journal of Experimental Biology 159, 149–64CrossRefGoogle ScholarPubMed
Evans, A. M. & Martin, R. J. (1996). Activation and cooperative multi-ion block of single nicotinicacetylcholine channel currents of Ascaris muscle by the tetrahydropyrimidine anthelmintic, morantel. British Journal of Pharmacology 118, 1127–40CrossRefGoogle ScholarPubMed
Geary, T. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992). 2 FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14CrossRefGoogle ScholarPubMed
Goldschmidt, R. (1908). Das Nervensystem von Ascaris lumbricoides und Megalocephala. Ein Versuch, in den Aufbau eines einfachen Nervensystems einzudringan, Zweiter Teil. Zeitschrift filr wissenschaftliche Zoologie 90, 73–136Google Scholar
Goldschmidt, R. (1909). Das Nervensystem von Ascaris lumbricoides und Megalocephala. Ein Versuch, in den Aufbau eines einfachen Nervensystems einzudringen, Zweiter Teil. Zeitschrift fur wissenschaftliche Zoologie 92, 357–396Google Scholar
Guastella, J., Johnson, C. D. & Stretton, A. O. W. (1991). GABA-immunoreactive neurons in the nematode Ascaris. Journal of Comparative Neurology 307, 584–97CrossRefGoogle ScholarPubMed
Guastella, J. & Stretton, A. O. W. (1991). Distribution of H3 GABA uptake sites in the nematode Ascaris. Journal of Comparative Neurology 307, 598–608CrossRefGoogle Scholar
Harrow, I. D. & Gration, K. A. F. (1985). Mode of action of the anthelmintics morantel, pyrantel and levamisole in the muscle cell membrane of the nematode Ascaris suum. Pesticide Science 16, 662–72CrossRefGoogle Scholar
Hobson, A. D., Stephenson, W. & Beadle, L. C. (1952a). Studies on the physiology of Ascaris lumbricoides. I. The relation of total osmotic pressure, conductivity and chloride content of the body fluid to that of the external environment. Journal of Experimental Biology 29, 1–21CrossRefGoogle Scholar
Hobson, A. D., Stephenson, W. & Eden, A. (1952b). Studies on the physiology of Ascaris lumbricoides. II. The inorganic composition of the body fluid in relation to that of the environment. Journal of Experimental Biology 29, 22–9CrossRefGoogle Scholar
Holden-Dye, L., Hewitt, G. M., Wann, K. T., Krogsgaard-Larsen, P. & Walker, R. J. (1988). Studies involving avermectin and the 4-aminobutyric acid (GABA) receptor of Ascaris suum muscle. Pesticide Science 24, 231–245CrossRefGoogle Scholar
Holden-Dye, L., Krogsgaard-Larsen, P., Neilsen, L. & Walker, R. J. (1989). GABA receptors on the somatic muscle cells of the parasitic nematode, Ascaris suum: stereoselectivity indicates similarity to a GABA-type agonist recognition site. British Journal of Pharmacology 98, 841–50CrossRefGoogle Scholar
Holden-Dye, L. & Walker, R. J. (1988). ZAPA, (Z)-3-[(amino iminomethyl)thio]-2-propenoic acid hydrochloride, a potent agonist at GABA receptors on the Ascaris muscle cell. British Journal of Pharmacology 95, 3–5CrossRefGoogle Scholar
Jarman, M. (1959). Electrical activity in the muscle cells of Ascaris lumbricoides. Nature 184, 1244. Johnson, C. D. & Stretton, A. O. w. (1985). Localization of choline acetyltransferase within identified motoneurones of the nematode Ascaris. Journal of Neuroscience 5, 1984–92CrossRefGoogle Scholar
Johnson, C. D. & Stretton, A. O. W. (1987). GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. Journal of Neuroscience 7, 223–35CrossRefGoogle ScholarPubMed
Kostyuk, P. K., Krishtal, O. A. & Pidoplicho, V. I. (1984). Perfusion of isolated neurons fixed in plastic film. In Intracellular Perfusion of Excitable Cells (eds. Kostyuk, P. K. & Krishtal, O. A.), pp. 35–51Chichester, New York, Brisbane, Toronto, Singapore:. John Wiley and Sons.Google Scholar
Laughton, D. L., Wolstenholme, A. J. & Lunt, G. (1995). The beta subunit of the C. elegans inhibitory glutamate receptor is expressed in the pm4 pharyngeal muscle cells. Worm Breeders Gazette 14, 48.Google Scholar
Lewis, J. A., Wu, C.-H., Levine, J. H. & Berg, H. (1980). Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience 5, 967–89CrossRefGoogle ScholarPubMed
Lewis, J. A., Flemming, J. T. & Bird, D. (1992). Cloning nematode acetycholine receptor genes. In Neurotox ‘91, (ed. Duce, I. R.), pp. 155–164London and New York: Elsevier Applied Science.Google Scholar
Martin, R. J. (1980). The effect of y-aminobutyric acid on the input conductance and membrane potential of Ascaris muscle. British Journal of Pharmacology 71, 99–106CrossRefGoogle Scholar
Martin, R. J. (1982). Electrophysiological effects of piperazine and diethylcarbamazine on Ascaris suum somatic muscle. British Journal of Pharmacology 77, 255–65CrossRefGoogle ScholarPubMed
Martin, R. J. (1985). y-Aminobutyric acid- and piperazine-activated single channel currents from Ascaris suum body muscle. British Journal of Pharmacology 84, 445–61CrossRefGoogle Scholar
Martin, R. J. (1987). The y-aminobutyric acid receptor of Ascaris as a target for anthelmintics. Biochemical Society Transactions 17, 61–5CrossRefGoogle Scholar
Martin, R. J. (1993). Neuromuscular-transmission in nematode parasites and antinematodal drug-action. Pharmacology & Therapeutics 58, 13–50CrossRefGoogle ScholarPubMed
Martin, R. J. (1996). An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutarnate-gated chloride channel sensitive to the avermectin analogue milbemycin D. Parasitology 112, 247–52CrossRefGoogle Scholar
Martin, R. J., Pennington, A. J., Duittoz, A. H., Robertson, S. & Kusel, J. R. (1991). The physiology and pharmacology of neuromuscular-transmission in the nematode parasite, Ascaris suum. Parasitology 102, S41–S58.CrossRefGoogle ScholarPubMed
Martin, R. J., Thorn, P., Gration, K. A. F. & Harrow, I. D. (1992). Voltage-activated currents in somatic muscle of the nematode parasite Ascaris suum. Journal of Experimental Biology 173, 75–90CrossRefGoogle ScholarPubMed
Martin, R. J., Sitamze, J. M., Duittoz, A. H. & Wermuth, C. G. (1995). Novel arylaminopyridazine-GABA receptor antagonists examined electrophysiologically in Ascaris suum. European Journal of Pharmacology 276, 9–19CrossRefGoogle ScholarPubMed
Martin, R. J. & Valkanov, M. A. (1995). A chloride channel in isolated muscle vesicles from Ascaris suum conducts products of anaerobic metabolism, suggesting a role in excretion of organic-anions. Journal of Physiology 482P, 8.Google Scholar
Natoff, I. L. (1969). The pharmacology of the cholinoceptor in muscle preparations of Ascaris lumbricoides cat. suum. British Journal of Pharmacology 37, 251–7CrossRefGoogle Scholar
Norton, S. & De Beer, E. J. (1957). Investigations on the action of piperazine on Ascaris lumbricoides. American Journal of Tropical Medicine 6, 889–905Google ScholarPubMed
Pennington, A. J. & Martin, R. J. (1990). A patch-clamp study of acetylcholine-activated ion channels in Ascaris suum muscle. Journal of Experimental Biology 154, 210–21CrossRefGoogle ScholarPubMed
Robertson, S. J., Pennington, A. J., Evans, A. M. & Martin, R. J. (1994). The action of pyrantel as an agonist and an open-channel-blocker at acetylcholinereceptors in isolated Ascaris suum muscle vesicles. European Journal of Pharmacology 271, 273–82CrossRefGoogle Scholar
Robertson, S. J. & Martin, R. J. (1993). Levamisoleactivated single-channel currents from muscle of the nematode parasite Ascaris suum. British Journal of Pharmacology 108, 170–8CrossRefGoogle ScholarPubMed
Robertson, A. P. & Martin, R. J. (1996). Effects of pH on the Ca-dependent chloride channel: a patch-clamp study in Ascaris suum. Parasitology 113, 191–8CrossRefGoogle ScholarPubMed
Rosenbluth, J. (1965). Ultrastructure of somatic muscle cells in Ascaris lumbricoides. II. Intermuscluar junctions, neuromuscular junctions, and glycogen stores. Journal of Cell Biology 26, 579–91CrossRefGoogle ScholarPubMed
Rozhova, E. K., Malyutina, T. A. & Shishov, B. A. (1980). Pharmacological characteristics if cholinoreception in somatic muscle of the nematode Ascaris suum. General Pharmacology 11, 141–46CrossRefGoogle Scholar
Sangster, N. C. & Bjorn, H. (1995). Levamisole resistance in Haemonchus contortus selected at different stages of infection. International Journal for Parasitology 25, 343–8CrossRefGoogle ScholarPubMed
Saz, N. J. & Weil, A. (1962). A pathway of formation of alpha-methyl valerate by Ascaris lumbricoides. Journal of Biological Chemistry 237, 2053–6CrossRefGoogle Scholar
Schneider, A. (1895). Monographie der Nematoden. Berlin.Google Scholar
Stretton, A. O. W., Cowden, C., Sithigorngul, P. & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–S116.CrossRefGoogle ScholarPubMed
Stretton, A. O. W., Fishpool, R. M., Southgate, E., Donmoyer, J. E., Walrond, J. P., Moses, J. E. R. & Kass, I. S. (1978). Structure and physiological activity of the motoneurons of the nematode Ascaris. Proceedings of the National Academy of Sciences, USA 75, 3493–7CrossRefGoogle ScholarPubMed
Tielens, A. G. M. (1994). Energy generation in parasitic helminths. Parasitology Today 10, 346–52 Tsang, V. C. & Saz, H. J. (1973). Demonstration and function of 2-methyl-butyrate racemase in Ascaris lumbricoides. Comparative Biochemistry and Physiology B 45B, 617–23CrossRefGoogle ScholarPubMed
Valkanov, M. A. & Martin, R. J. (1995). A Cl channel selectively conducts dicarboxylic products from anaerobic glucose metabolism and indicates a role in transmembrane transport of waste organic anions. Journal of Membrane Biology 147, 41–9Google Scholar
Valkanov, M. A., Martin, R. J. & Dixon, D. M. (1994). The Ca-activated chloride channel of Ascaris suum conducts volatile fatty-acids produced by anaerobic respiration - a patch-clamp study. Journal of Membrane Biology 138, 133–1.CrossRefGoogle ScholarPubMed
Weisblat, D. A., Byerly, L. & Russel, R. L. (1976). Ionic mechanisms of electrical activity in the somatic muscle cell of the nematode Ascaris lumbricoides. Journal of Comparative Neurology 111, 93–113Google Scholar
Weisblat, D. A. & Russel, R. L. (1976). Propagation of electrical activity in the nerve cord and muscle syncytium of the nematode Ascaris lumbricoides. Journal of Comparative Neurology 107, 293–307Google Scholar
White, J. G., Southgate, E., Thompson, J. N. & Brenner, S. (1976). The structure of the ventral cord of Caenorhabditis elegans. Philosophical Transactions of the Royal Society London, Series B 275, 298–327Google ScholarPubMed
White, J. D., Southgate, E., Thompson, J. N. & Brenner, S. (1986). The structure of the nervous system of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London, Series B 314, 1–340Google ScholarPubMed