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

Volumn 89, Issue 5, 2004, Pages 1137-1147

  Njue, Annete I ^a   Hayashi, Jon ^b   Kinne, Lyle ^b   Feng, Xiao Peng ^a   Prichard, Roger K ^a  

^a MCGILL UNIVERSITY   (Canada)

^b FMC CORPORATION   (United States)

Author keywords

Anthelmintic resistance; Cooperia oncophora; Glutamate gated chloride channel; Ivermectin; Moxidectin; Two electrode voltage clamp

Indexed keywords

4 AMINOBUTYRIC ACID; ASPARTIC ACID; CHLORIDE CHANNEL; COMPLEMENTARY DNA; GLUTAMIC ACID; GLYCINE; IBOTENIC ACID; IVERMECTIN; KAINIC ACID; MOXIDECTIN; N METHYL DEXTRO ASPARTIC ACID; QUISQUALIC ACID;

AGONIST; AMINO ACID SUBSTITUTION; ARTICLE; COOPERIA ONCOPHORA; DOSE RESPONSE; DRUG RESISTANCE; GLUTAMATE GATED CHLORIDE CHANNEL; MOLECULAR CLONING; MUTATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; VOLTAGE CLAMP; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTINEMATODAL AGENTS; CELLS, CULTURED; CHLORIDE CHANNELS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE; GLUTAMIC ACID; IVERMECTIN; LIGANDS; MACROLIDES; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; TRICHOSTRONGYLOIDEA; XENOPUS LAEVIS;

COOPERIA; COOPERIA ONCOPHORA; NEMATODA; ONCOPHORA; TRIXIS; XENOPUS LAEVIS;

EID: 2642551393     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02379.x     Document Type: Article

References (52)

1. Anziani O. S., Zimmermann G., Guglielmone A. A., Vazquez R. and Suarez V. (2001) Avermectin resistance in Cooperia pectinata in cattle in Argentina. Vet. Rec. 149, 58-59.
2. Arena J. P., Liu K. K., Paress P. S., Schaeffer J. M. and 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 Res. Mol. Brain Res. 15, 339-348.
3. Arena J. P., Liu K. K., Paress P. S., Frazier E. G., Cully D. F., Mrozik H. and 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. J. Parasitol. 81, 286-294.
4. Bechade C., Sur C. and Triller A. (1994) The inhibitory neuronal glycine receptor. Bioessays 16, 735-744.
5. Brejc K., van Dijk W. J., Klaassen R. V., Schuurmans M., van Der Oost J., Smit A. B. and Sixma T. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411, 269-276.
6. Campbell W. C. (1989) Ivermectin and Abamectin, pp. xviii, 363. Springer-Verlag, New York.
7. Chang Y., Wang R., Barot S. and Weiss D. S. (1996) Stoichiometry of a recombinant GABAA receptor. J. Neurosci. 16, 5415-5424.
8. Cheeseman C. L., Delany N. S., Woods D. J. and Wolstenholme A. J. (2001) High-affinity ivermectin binding to recombinant subunits of the Haemonchus contortus glutamate-gated chloride channel. Mol. Biochem. Parasitol. 114, 161-168.
9. Cleland T. A. (1996) Inhibitory glutamate receptor channels. Mol. Neurobiol. 13, 97-136.
10. Coles G. C., Stafford K. A. and MacKay P. H. (1998) Ivermectin-resistant Cooperia species from calves on a farm in Somerset. Vet. Rec. 142, 255-256.
11. Coles G. C., Watson C. L. and Anziani O. S. (2001) Ivermectin-resistant Cooperia in cattle. Vet. Rec. 148, 283-284.
12. Conder G. A., Thompson D. P. and Johnson S. S. (1993) Demonstration of co-resistance of Haemonchus contortus to ivermectin and moxidectin. Vet. Rec. 132, 651-652.
13. Corringer P. J., Galzi J. L., Eisele J. L., Bertrand S., Changeux J. P. and Bertrand D. (1995) Identification of a new component of the agonist binding site of the nicotinic alpha 7 homooligomeric receptor. J. Biol. Chem. 270, 11749-11752.
14. Corringer P. J., Le Novere N. and Changeux J. P. (2000) Nicotinic receptors at the amino acid level. Annu. Rev. Pharmacol. Toxicol. 40, 431-458.
15. Craig T. M., Hatfield T. A., Pankavich J. A. and Wang G. T. (1992) Efficacy of moxidectin against an ivermectin-resistant strain of Haemonchus contortus in sheep. Vet. Parasitol. 41, 329-333.
16. Cully D. F., Vassilatis D. K., Liu K. K., Paress P. S., Van der Ploeg L. H., Schaeffer J. M. and Arena J. P. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371, 707-711.
17. Cully D. F., Paress P. S., Liu K. K., Schaeffer J. M. and Arena J. P. (1996) Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. J. Biol. Chem. 271, 20187-20191.
18. Dascal N. (1987) The use of Xenopus oocytes for the study of ion channels. CRC Crit. Rev. Biochem. 22, 317-387.
19. Delany N. S., Laughton D. L. and Wolstenholme A. J. (1998) Cloning and localization of an avermectin receptor-related subunit from Haemonchus contortus. Mol. Biochem. Parasitol. 97, 177-187.
20. Dent J. A., Davis M. W. and Avery L. (1997) avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. EMBO J. 16, 5867-5879.
21. Dent J. A., Smith M. M., Vassilatis D. K. and Avery L. (2000) The genetics of ivermectin resistance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 97, 2674-2679.
22. Etter A., Cully D. F., Schaeffer J. M., Liu K. K. and Arena J. P. (1996) An amino acid substitution in the pore region of a glutamate-gated chloride channel enables the coupling of ligand binding to channel gating. J. Biol. Chem. 271, 16035-16039.
23. Familton A. S., Mason P. and Coles G. C. (2001) Anthelmintic-resistant Cooperia species in cattle. Vet. Rec. 149, 719-720.
24. Feng X. P., Hayashi J., Beech R. N. and Prichard R. K. (2002) Study of the nematode putative GABA type-A receptor subunits: evidence for modulation by ivermectin. J. Neurochem. 83, 870-878.
25. Ffrench-Constant R. H., Rocheleau T. A., Steichen J. C. and Chalmers A. E. (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363, 449-451.
26. Ffrench-Constant R. H., Pittendrigh B., Vaughan A. and Anthony N. (1998) Why are there so few resistance-associated mutations in insecticide target genes? Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1685-1693.
27. Fiel C. A., Saumell C. A., Steffan P. E. and Rodriguez E. M. (2001) Resistance of Cooperia to ivermectin treatments in grazing cattle of the Humid Pampa, Argentina. Vet Parasitol. 97, 211-217.
28. Fleming J. T., Squire M. D., Barnes T. M., Tomoe C., Matsuda K., Ahnn J., Fire A., Sulston J. E., Barnard E. A., Sattelle D. B. and Lewis J. A. (1997) Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J. Neurosci. 17, 5843-5857.
29. Geary T. G., Sims S. M., Thomas E. M., Vanover L., Davis J. P., Winterrowd C. A., Klein R. D., Ho N. F. and Thomson D. P. (1993) Haemonchus contortus: ivermectin-induced paralysis of the pharynx. Exptl. Parasitol. 77, 88-96.
30. Holden-Dye L. and 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 Part 2, 265-271.
31. Horoszok L., Raymond V., Sattelle D. B. and Wolstenholme A. J. (2001) GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, 1-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br. J. Pharmacol. 132, 1247-1254.
32. Jagannathan S., Laughton D. L., Critten C. L., Skinner T. M., Horoszok L. and 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. Mol. Biochem. Parasitol. 103, 129-140.
33. Kane N. S., Hirschberg B., Qian S., Hunt D., Thomas B., Brochu R., Ludmerer S. W., Zheng Y., Smith M., Arena J. P., Cohen C. J., SchmatZ. D., Warmke J. and Cully D. F. (2000) Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. Proc. Natl. Acad. Sci. USA 97, 13949-13954.
34. Laughton D. L., Lunt G. G. and Wolstenholme A. J. (1997a) Alternative splicing of a Caenorhabditis elegans gene produces two novel inhibitory amino acid receptor subunits with identical ligand binding domains but different ion channels. Gene 201, 119-125.
35. Laughton D. L., Lunt G. G. and Wolstenholme A. J. (1997b) Reporter gene constructs suggest that the Caenorhabditis elegans avermectin receptor beta-subunit is expressed solely in the pharynx. J. Exp. Biol. 200, 1509-1514.
36. Lea T. J. and Usherwood P. N. R. (1973) Effect of ibotenic acid on chloride permeability of insect muscle-fibres. Comp. Gen. Pharmacol. 4, 351-363.
37. Ludmerer S. W., Warren V. A., Williams B. S. et al. (2002) Ivermectin and nodulisporic acid receptors in Drosophila melanogaster contain both gamma-aminobutyric acid-gated Rdl and glutamate-gated GluCl alpha chloride channel subunits. Biochemistry 41, 6548-6560.
38. Macdonald R. L. and Olsen R. W. (1994) GABAA receptor channels. Annu. Rev. Neurosci. 17, 569-602.
39. McKellar Q. A. and Benchaoui H. A. (1996) Avermectins and milbemycins. J. Vet. Pharmacol. Therap 19, 331-351.
40. Ortells M. O. and Lunt G. G. (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci. 18, 121-127.
41. Pankavich J. A., Berger H. and Simkins K. L. (1992) Efficacy of moxidectin, nemadectin and ivermectin against an ivermectin-resistant strain of Haemonchus contortus in sheep. Vet. Rec. 130, 243.
42. Parmentier H. K., Ploeger H. W., Nieuwland M. G., Souren P. J., Van Pinxteren L. A., Rietveld F. W., De Vries Reilingh G. and Kloosterman A. (1995) Low molecular weight Cooperia oncophora antigens: characterization and humoral immune responses in calves mono-infected with 100,000 infective larvae. Vet. Parasitol. 59, 219-230.
43. Pemberton D. J., Franks C. J., Walker R. J. and Holden-Dye L. (2001) Characterization of glutamate-gated chloride channels in the pharynx of wild-type and mutant Caenorhabditis elegans delineates the role of the subunit GluClalpha2 in the function of the native receptor. Mol. Pharmacol. 59, 1037-1043.
44. Portillo V., Jagannathan S. and Wolstenholme A. J. (2003) Distribution of glutamate-gated chloride channel subunits in the parasitic nematode Haemonchus contortus. J. Comp. Neurol. 462, 213-222.
45. Ranganathan R., Cannon S. C. and Horvitz H. R. (2000) MOD-1 is a serotonin-gated chloride channel that modulates locomotory behavior in C. elegans. Nature 408, 470-475.
46. Ranjan S., Wang G. T., Hirschlein C. and Simkins K. L. (2002) Selection for resistance to macrocyclic lactones by Haemonchus contortus in sheep. Vet. Parasitol. 103, 109-117.
47. Shoop W. L., Haines H. W., Michael B. F. and Eary C. H. (1993) Mutual resistance to avermectins and milbemycins: oral activity of ivermectin and moxidectin against ivermectin-resistant and susceptible nematodes. Vet. Rec. 133, 445-447.
48. Shoop W. L., Mrozik H. and Fisher M. H. (1995) Structure and activity of avermectins and milbemycins in animal health. Vet. Parasitol. 59, 139-156.
49. Unwin N. (1993) Nicotinic acetylcholine receptor at 9 A resolution. J. Mol. Biol. 229, 1101-1124.
50. Vassilatis D. K., Arena J. P., Plasterk R. H., Wilkinson H. A., Schaeffer J. M., Cully D. F. and Van der Ploeg L. H. (1997) Genetic and biochemical evidence for a novel avermectin-sensitive chloride channel in Caenorhabditis elegans. Isolation and characterization. J. Biol. Chem. 272, 33167-33174.
51. Vermunt J. J., West D. M. and Pomroy W. E. (1996) Inefficacy of moxidectin and doramectin against ivermectin-resistant Cooperia spp. of cattle in New Zealand. NZ Vet. J. 44, 188-193.
52. Zheng Y., Hirschberg B., Yuan J., Wang A. P., Hunt D. C., Ludmerer S. W., SchmatZ. D. M. and Cully D. F. (2002) Identification of two novel Drosophila melanogaster histamine-gated chloride channel subunits expressed in the eye. J. Biol. Chem. 277, 2000-2005.