Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-30T22:19:45.777Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic variability of glutamate-gated chloride channel genes in ivermectin-susceptible and -resistant strains of Cooperia oncophora

Published online by Cambridge University Press:  18 November 2004

A. I. NJUE  and
R. K. PRICHARD
A. I. NJUE
Affiliation:
Institute of Parasitology, McGill University, 21 111 Lakeshore Road, Ste-Anne-de-Bellevue, Quebec, Canada, H9X 3V9
R. K. PRICHARD
Affiliation:
Institute of Parasitology, McGill University, 21 111 Lakeshore Road, Ste-Anne-de-Bellevue, Quebec, Canada, H9X 3V9
Get access Rights & Permissions [Opens in a new window]

Abstract

The glutamate-gated chloride channels (GluCls) are members of the ligand-gated ion channel superfamily that are thought to be involved in the mode of action of ivermectin and mechanism of resistance. Using reverse-transcriptase PCR techniques, 2 full-length GluCl cDNAs, encoding GluClα3 and GluClβ subunits, were cloned from Cooperia oncophora, a nematode parasite of cattle. The two sequences show a high degree of identity to similar subunits from other nematodes. The C. oncophora GluClα3 subunit is most closely related to the Haemonchus contortus GluClα3B subunit, while C. oncophora GluClβ subunit shares high sequence identity with the H. contortus GluClβ subunit. Using single-strand conformation polymorphism, the genetic variability of these two genes was analysed in an ivermectin-susceptible isolate and an ivermectin-resistant field isolate of C. oncophora. Statistical analysis suggested an association between the C. oncophora GluClα3 gene and ivermectin resistance. No such association was seen with the GluClβ gene.

Keywords

Cooperia oncophoragenetic variationivermectin resistanceglutamate-gated chloride channelsingle-strand conformation polymorphism
Type
Research Article
Information
Parasitology , Volume 129 , Issue 6 , December 2004 , pp. 741 - 751
Copyright
© 2004 Cambridge University Press

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

ANZIANI, O. S., ZIMMERMANN, G., GUGLIELMONE, A. A., VAZQUEZ, R. & SUAREZ, V. ( 2001). Avermectin resistance in Cooperia pectinata in cattle in Argentina. Veterinary Record 149, 58–59.CrossRefGoogle Scholar
ARENA, J. P., LIU, K. K., PARESS, P. S., SCHAEFFER, J. M. & CULLY, D. F. ( 1992). Expression of a glutamate-activated chloride current in Xenopus oocytes injected with Caenorhabditis elegans RNA: evidence for modulation by avermectin. Brain Research Molecular Brain Research 15, 339–348.CrossRefGoogle Scholar
ARENA, J. P., LIU, K. K., PARESS, P. S., FRAZIER, E. G., CULLY, D. F., MROZIK, H. & SCHAEFFER, J. M. ( 1995). The mechanism of action of avermectins in Caenorhabditis elegans: correlation between activation of glutamate-sensitive chloride current, membrane binding, and biological activity. Journal of Parasitology 81, 286–294.CrossRefGoogle Scholar
BARNARD, E. A. ( 1996). The transmitter-gated channels: a range of receptor types and structures. Trends in Pharmacological Sciences 17, 305–309.CrossRefGoogle Scholar
BEECH, R. N., PRICHARD, R. K. & SCOTT, M. E. ( 1994). Genetic variability of the beta-tubulin genes in benzimidazole-susceptible and -resistant strains of Haemonchus contortus. Genetics 138, 103–110.Google Scholar
BENKWITZ, C., OBERDORF-MAASS, S. & NEYSES, L. ( 1999). Combined SSCP and heteroduplex analysis of the human plasma membrane Ca(2+)-ATPase isoform 1 in patients with essential hypertension. Biochemical and Biophysical Research Communications 261, 515–520.CrossRefGoogle Scholar
BLACKHALL, W. J., LIU, H. Y., XU, M., PRICHARD, R. K. & BEECH, R. N. ( 1998 a). Selection at a P-glycoprotein gene in ivermectin- and moxidectin-selected strains of Haemonchus contortus. Molecular and Biochemical Parasitology 95, 193–201.Google Scholar
BLACKHALL, W. J., POULIOT, J. F., PRICHARD, R. K. & BEECH, R. N. ( 1998 b). Haemonchus contortus: selection at a glutamate-gated chloride channel gene in ivermectin- and moxidectin-selected strains. Experimental Parasitology 90, 42–48.Google Scholar
BLOUIN, M. S., DAME, J. B., TARRANT, A. & COURTNEY, C. H. ( 1992). Unusual population genetics of a parasite nematode: mtDNA variation with and among populations. Evolution 46, 470–476.CrossRefGoogle Scholar
CLELAND, T. A. ( 1996). Inhibitory glutamate receptor channels. Molecular Neurobiology 13, 97–136.CrossRefGoogle Scholar
COLES, G. C. ( 2002 a). Cattle nematodes resistant to anthelmintics: why so few cases? Veterinary Research 33, 481–489.Google Scholar
COLES, G. C. ( 2002 b). Sustainable use of anthelmintics in grazing animals. Veterinary Record 151, 165–169.Google Scholar
COLES, G. C., STAFFORD, K. A. & MACKAY, P. H. ( 1998). Ivermectin-resistant Cooperia species from calves on a farm in Somerset. Veterinary Record 142, 255–256.Google Scholar
COLES, G. C., WATSON, C. L. & ANZIANI, O. S. ( 2001). Ivermectin-resistant Cooperia in cattle. Veterinary Record 148, 283–284.Google Scholar
CULLY, D. F., WILKINSON, H., VASSILATIS, D. K., ETTER, A. & ARENA, J. P. ( 1996). Molecular biology and electrophysiology of glutamate-gated chloride channels of invertebrates. Parasitology 113, S191–S200.Google Scholar
CULLY, D. F., VASSILATIS, D. K., LIU, K. K., PARESS, P. S., VAN DER PLOEG, L. H., SCHAEFFER, J. M. & ARENA, J. P. ( 1994). Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature, London 371, 707–711.CrossRefGoogle Scholar
DELANY, N. S., LAUGHTON, D. L. & WOLSTENHOLME, A. J. ( 1998). Cloning and localization of an avermectin receptor-related subunit from Haemonchus contortus. Molecular and Biochemical Parasitology 97, 177–187.CrossRefGoogle Scholar
DENT, J. A., DAVIS, M. W. & AVERY, L. ( 1997). avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. EMBO Journal 16, 5867–5879.CrossRefGoogle Scholar
DENT, J. A., SMITH, M. M., VASSILATIS, D. K. & AVERY, L. ( 2000). The genetics of ivermectin resistance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 97, 2674–2679.CrossRefGoogle Scholar
ELARD, L. & HUMBERT, J. F. ( 1999). Importance of the mutation of amino acid 200 of the isotype 1 beta-tubulin gene in the benzimidazole resistance of the small-ruminant parasite Teladorsagia circumcincta. Parasitology Research 85, 452–456.CrossRefGoogle Scholar
FAMILTON, A. S., MASON, P. & COLES, G. C. ( 2001). Anthelmintic-resistant Cooperia species in cattle. Veterinary Record 149, 719–720.Google Scholar
FENG, X. P., HAYASHI, J., BEECH, R. N. & PRICHARD, R. K. ( 2002). Study of the nematode putative GABA type-A receptor subunits: evidence for modulation by ivermectin. Journal of Neurochemistry 83, 870–878.CrossRefGoogle Scholar
FIEL, C. A., SAUMELL, C. A., STEFFAN, P. E. & RODRIGUEZ, E. M. ( 2001). Resistance of Cooperia to ivermectin treatments in grazing cattle of the Humid Pampa, Argentina. Veterinary Parasitology 97, 211–217.CrossRefGoogle Scholar
FORRESTER, S. G., HAMDAN, F. F., PRICHARD, R. K. & BEECH, R. N. ( 1999). Cloning, sequencing, and developmental expression levels of a novel glutamate-gated chloride channel homologue in the parasitic nematode Haemonchus contortus. Biochemical and Biophysical Research Communications 254, 529–534.CrossRefGoogle Scholar
GILL, J. H., KERR, C. A., SHOOP, W. L. & LACEY, E. ( 1998). Evidence of multiple mechanisms of avermectin resistance in Haemonchus contortus – comparison of selection protocols. International Journal for Parasitology 28, 783–789.CrossRefGoogle Scholar
GRANT, W. N. ( 1994). Genetic variation in parasitic nematodes and its implications. International Journal for Parasitology 24, 821–830.CrossRefGoogle Scholar
GRANT, W. N. & MASCORD, L. J. ( 1996). Beta-tubulin gene polymorphism and benzimidazole resistance in Trichostrongylus colubriformis. International Journal for Parasitology 26, 71–77.CrossRefGoogle Scholar
HOLDEN-DYE, L. & WALKER, R. J. ( 1990). Avermectin and avermectin derivatives are antagonists at the 4-aminobutyric acid (GABA) receptor on the somatic muscle cells of Ascaris; is this the site of anthelmintic action? Parasitology 101, 265–271.Google Scholar
HOROSZOK, L., RAYMOND, V., SATTELLE, D. B. & WOLSTENHOLME, A. J. ( 2001). GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. British Journal of Pharmacology 132, 1247–1254.CrossRefGoogle Scholar
JACKSON, F. ( 1993). Anthelmintic resistance – the state of play. British Veterinary Journal 149, 123–138.CrossRefGoogle Scholar
JACKSON, F. & COOP, R. L. ( 2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107.CrossRefGoogle Scholar
JAGANNATHAN, S., LAUGHTON, D. L., CRITTEN, C. L., SKINNER, T. M., HOROSZOK, L. & WOLSTENHOLME, A. J. ( 1999). Ligand-gated chloride channel subunits encoded by the Haemonchus contortus and Ascaris suum orthologues of the Caenorhabditis elegans gbr-2 (avr-14) gene. Molecular and Biochemical Parasitology 103, 129–140.CrossRefGoogle Scholar
KRAUSE, R. M., BUISSON, B., BERTRAND, S., CORRINGER, P. J., GALZI, J. L., CHANGEUX, J. P. & BERTRAND, D. ( 1998). Ivermectin: a positive allosteric effector of the α7 neuronal nicotinic acetylcholine receptor. Molecular Pharmacology 53, 283–294.CrossRefGoogle Scholar
KUMAR, S., TAMURA, K., JAKOBSEN, I. B. & NEI, M. ( 2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.CrossRefGoogle Scholar
KWA, M. S., KOOYMAN, F. N. J., BOERSEMA, J. H. & ROOS, M. H. ( 1993). Effect of selection for benzimidazole resistance in Haemonchus contortus in β-tubulin isotype 1 and isotype 2 genes. Biochemical and Biophysical Research Communications 191, 413–419.CrossRefGoogle Scholar
LAUGHTON, D. L., LUNT, G. G. & WOLSTENHOLME, A. J. ( 1997). Reporter gene constructs suggest that the Caenorhabditis elegans avermectin receptor beta-subunit is expressed solely in the pharynx. Journal of Experimental Biology 200, 1509–1514.Google Scholar
LE JAMBRE, L. F. ( 1993). Molecular variation in trichostrongylid nematodes from sheep and cattle. Acta Tropica 53, 331–343.CrossRefGoogle Scholar
LIU, J., DENT, J. A., BEECH, R. N. & PRICHARD, R. K. ( 2004). Genomic organization of an avermectin receptor subunit from Haemonchus contortus and expression of its putative promoter region in Caenorhabditis elegans. Molecular and Biochemical Parasitology 134, 267–274.CrossRefGoogle Scholar
MARTIN, R. J. ( 1996). An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutamate-gated chloride channel sensitive to the avermectin analogue, milbemycin D. Parasitology 112, 247–252.CrossRefGoogle Scholar
McKENNA, P. B. ( 1996). Anthelmintic resistance in cattle nematodes in New Zealand: is it increasing? New Zealand Veterinary Journal 44, 76.Google Scholar
NJUE, A. I. & PRICHARD, R. K. ( 2003). Cloning two full-length beta-tubulin isotype cDNAs from Cooperia oncophora, and screening for benzimidazole resistance-associated mutations in two field populations. Parasitology 127, 579–588.CrossRefGoogle Scholar
NJUE, A. I., HAYASHI, J., KINNE, L., FENG, X. P. & PRICHARD, R. K. ( 2004). Mutations in the extracellular domains of glutamate-gated chloride channel α3 and β subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity. Journal of Neurochemistry 89, 1137–1147.CrossRefGoogle Scholar
OTSEN, M., HOEKSTRA, R., PLAS, M. E., BUNTJER, J. B., LENSTRA, J. A. & ROOS, M. H. ( 2001). Amplified fragment length polymorphism analysis of genetic diversity of Haemonchus contortus during selection for drug resistance. International Journal of Parasitology 31, 1138–1143.CrossRefGoogle Scholar
PORTILLO, V., JAGANNATHAN, S. & WOLSTENHOLME, A. J. ( 2003). Distribution of glutamate-gated chloride channel subunits in the parasitic nematode Haemonchus contortus. Journal of Comparative Neurology 462, 213–222.CrossRefGoogle Scholar
POULIOT, J. F., L'HEUREUX, F., LIU, Z., PRICHARD, R. K. & GEORGES, E. ( 1997). Reversal of P-glycoprotein-associated multidrug resistance by ivermectin. Biochemical Pharmacology 53, 17–25.CrossRefGoogle Scholar
PRICHARD, R. K. ( 1990). Anthelmintic resistance in nematodes: extent, recent understanding and future directions for control and research. International Journal for Parasitology 20, 515–523.CrossRefGoogle Scholar
PRICHARD, R. ( 2001). Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445–453.CrossRefGoogle Scholar
SANGSTER, N. C., BANNAN, S. C., WEISS, A. S., NULF, S. C., KLEIN, R. D. & GEARY, T. G. ( 1999). Haemonchus contortus: sequence heterogeneity of internucleotide binding domains from P-glycoproteins. Experimental Parasitology 91, 250–257.CrossRefGoogle Scholar
SCHINKEL, A. H., SMIT, J. J., VAN TELLINGEN, O., BEIJNEN, J. H., WAGENAAR, E., VAN DEEMTER, L., MOL, C. A., VAN DER VALK, M. A., ROBANUS-MAANDAG, E. C., TE RIELE, H. P., BERNS, A. J. & BORST, P. ( 1994). Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77, 491–502.CrossRefGoogle Scholar
VASSILATIS, D. K., ARENA, J. P., PLASTERK, R. H., WILKINSON, H. A., SCHAEFFER, J. M., CULLY, D. F. & VAN DER PLOEG, L. H. ( 1997). Genetic and biochemical evidence for a novel avermectin-sensitive chloride channel in Caenorhabditis elegans. Journal of Biological Chemistry 272, 33167–33174.CrossRefGoogle Scholar
VERMUNT, J. J., WEST, D. M. & POMROY, W. E. ( 1995). Multiple resistance to ivermectin and oxfendazole in Cooperia species of cattle in New Zealand. Veterinary Record 137, 43–45.CrossRefGoogle Scholar
VERMUNT, J. J., WEST, D. M. & POMROY, W. E. ( 1996). Inefficacy of moxidectin and doramectin against ivermectin-resistant Cooperia spp. of cattle in New Zealand. New Zealand Veterinary Journal 44, 188–193.CrossRefGoogle Scholar
WILLIAMS, J. C. ( 1997). Anthelmintic treatment strategies: current status and future. Veterinary Parasitology 72, 461–470.CrossRefGoogle Scholar
XU, M., MOLENTO, M., BLACKHALL, W., RIBEIRO, P., BEECH, R. & PRICHARD, R. ( 1998). Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Molecular and Biochemical Parasitology 91, 327–335.CrossRefGoogle Scholar
ZHENG, Y., HIRSCHBERG, B., YUAN, J., WANG, A. P., HUNT, D. C., LUDMERER, S. W., SCHMATZ, D. M. & CULLY, D. F. ( 2002). Identification of two novel Drosophila melanogaster histamine-gated chloride channel subunits expressed in the eye. Journal of Biological Chemistry 277, 2000–2005.CrossRefGoogle Scholar