Teladorsagia circumcincta: Molecular characterisation of the avr-14B subunit and its relatively minor role in ivermectin resistance

International Journal for Parasitology: Drugs and Drug Resistance

Volumn 2, Issue , 2012, Pages 154-161

  Martínez Valladares, María ^a   Geldhof, Peter ^b   Jonsson, Nicholas ^c   Rojo Vázquez, Francisco A ^a,d   Skuce, Philip ^e  

^a Instituto de Ganadería de Montana   (Spain)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF LEÓN   (Spain)

^e MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Anthelmintic resistance; GluCl channels; Ivermectin; Sheep; Teladorsagia circumcincta

Indexed keywords

AMINO ACID; BENZIMIDAZOLE DERIVATIVE; IVERMECTIN; LEVAMISOLE;

ANTIPARASITIC RESISTANCE; ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PYROSEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; TELADORSAGIA CIRCUMCINCTA;

EID: 84861473872     PISSN: 22113207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpddr.2012.03.005     Document Type: Article

References (38)

1. álvarez-Sánchez M.A., Pérez-García J., Bartley D., Jackson F., Rojo-Vázquez F.A. The larval feeding inhibition assay for the diagnosis of nematode anthelmintic resistance. Exp. Parasitol. 2005, 110:56-61.
2. Bartley D.J., Jackson F., Jackson E., Sargison N. Characterisation of two triple resistant field isolates of Teladorsagia from Scottish lowland sheep farms. Vet. Parasitol. 2004, 123:189-199.
3. Blackhall W.J., Pouliot J.F., Prichard R.K., Beech R.N. Haemonchus contortus: selection at a glutamate-gated chloride channel gene in ivermectin- and moxidectin-selected strains. Exp. Parasitol. 1998, 90:42-48.
4. Blackhall W.J., Prichard R.K., Beech R.N. P-glycoprotein selection in strains of Haemonchus contortus resistant to benzimidazoles. Vet. Parasitol. 2008, 152:101-117.
5. Blaxter M.L., De Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J.R., Mackey L.Y., Dorris M., Frisse L.M., Vida J.T., Thomas W.K. A molecular evolutionary framework for the phylum Nematoda. Nature 1998, 392:71-75.
6. Büttner C., Sadtler S., Leyendecker A., Laube B., Griffon N., Betz H., Schmalzing G. Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors. J. Biol. Chem. 2001, 276:42978-42985.
7. Cully D.F., Vassilatis D.K., Liu K.K., Paress P.S., Van der Ploeg L.H., Schaeffer J.M., Arena J.P. Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 1994, 371:707-711.
8. Dent J.A., Davis M.W., Avery L. Avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. EMBO J. 1997, 16:5867-5879.
9. Dent J.A., Smith M.M., Vassilatis D.K., Avery L. The genetics of ivermectin resistance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2000, 97:2674-2679.
10. Dicker A.J., Nisbet A.J., Skuce P.J. Gene expression changes in a p-glycoprotein (Tci-pgp-9) putatively associated with ivermectin resistance in Teladorsagia circumcincta. Int. J. Parasitol. 2011, 41:935-942.
11. El-Abdellati A., De Graef J., Van Zeveren A., Donnan A., Skuce P., Walsh T., Wolstenholme A., Tait A., Vercruysse J., Claerebout E., Geldhof P. Altered avr-14B gene transcription patterns in ivermectin-resistant isolates of the cattle parasites, Cooperia oncophora and Ostertagia ostertagi. Int. J. Parasitol. 2011, 41:951-957.
12. Fucile S., De Saint Jan D., de Carvalho L.P., Bregestovski P. Fast potentiation of glycine receptor channels of intracellular calcium in neurons and transfected cells. Neuron 2000, 28:571-583.
13. geNorm manual, update July 8, 2008. <>. http://www.medgen.ugent.be/~jvdesomp/genorm/.
14. Ghosh R., Andersen E.C., Shapiro J.A., Gerke J.P., Kruglyak L. Natural variation in a chloride channel subunit confers avermectin resistance in C. elegans. Science 2012, 335:574-578.
15. Harvey R.J., Depner U.B., Wässle H., Ahmadi S., Heindl C., Reinold H., Smart T.G., Harvey K., Schütz B., Abo-Salem O.M., Zimmer A., Poisbeau P., Welzl H., Wolfer D.P., Betz H., Zeilhofer H.U., Müller U. GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 2004, 7:884-887.
16. Hejmadi M.V., Jagannathan S., Delany N.S., Coles G.C., Wolstenholme A.J. l-glutamate binding sites of parasitic nematodes: an association with ivermectin resistance?. Parasitology 2000, 120:535-545.
17. Hibbs R.E., Gouaux E. Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 2011, 474:54-60.
18. Horoszok L., Raymond V., Sattelle D.B., Wolstenholme A.J. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, l-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br. J. Pharmacol. 2001, 132:1247-1254.
19. Jagannathan S., Laughton D.L., Critten C.L., Skinner T.M., Horoszok L., Wolstenholme A.J. 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. 1999, 103:129-140.
20. Kaminsky R., Mosimann D., Sager H., Stein P., Hosking B. Determination of the effective dose rate for monepantel (AAD 1566) against adult gastro-intestinal nematodes in sheep. Int. J. Parasitol. 2009, 39:443-446.
21. Kopp S.R., Coleman G.T., Traub R.J., McCarthy J.S., Kotze A.C. Acethylcholine receptor subunit genes from Ancylostoma caninum: altered transcription patterns associated with pyrantel resistance. Int. J. Parasitol. 2009, 39:435-441.
22. Laughton D.L., Lunt G.G., Wolstenholme A.J. 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 1997, 201:119-125.
23. Le Jambre L.F., Lenane I.J., Wardrop A.J. A hybridisation technique to identify anthelmintic resistance genes in Haemonchus. Int. J. Parasitol. 1999, 29:1979-1985.
24. Martínez-Valladares M., Famularo M.R., Fernández-Pato N., Cordero-Pérez C., Castañón-Ordóñez L., Rojo-Vázquez F.A. Characterization of a multidrug resistant Teladorsagia circumcincta isolate from Spain. Parasitol. Res. 2012, 110:2083-2087.
25. McCavera S., Walsh T.K., Wolstenholme A.J. Nematode ligand-gated chloride channels: an appraisal of their involvement in macrocyclic lactone resistance and prospects for developing molecular markers. Parasitology 2007, 134:1111-1121.
26. McCavera S., Rogers A.T., Yates D.M., Woods D.J., Wolstenholme A.J. An ivermectin-sensitive glutamate-gated chloride channel from the parasitic nematode Haemonchus contortus. Mol. Pharmacol. 2009, 75:1347-1355.
27. Mes T.H. Purifying selection and demographic expansion affect sequence diversity of the ligand-binding domain of a glutamate-gated chloride channel gene of Haemonchus placei. J. Mol. Evol. 2004, 58:466-478.
28. Njue A.I., Hayashi J., Kinne L., Feng X.P., Prichard R.K. Mutations in the extracellular domains of glutamate-gated chloride channel alpha3 and beta subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity. J. Neurochem. 2004, 89:1137-1147.
29. Njue A.I., Prichard R.K. Genetic variability of glutamate-gated chloride channel genes in ivermectin-susceptible and -resistant strains of Cooperia oncophora. Parasitology 2004, 129:741-751.
30. Prichard R. Anthelmintic resistance. Vet. Parasitol. 1994, 54:259-268.
31. Sadtler S., Laube B., Lashub A., Nicke A., Betz H., Schmalzing G. A basic cluster determines topology of the cytoplasmic M3-M4 loop of the glycine receptor alpha1 subunit. J. Biol. Chem. 2003, 278:16782-16790.
32. Skuce P., Stenhouse L., Jackson F., Hypsa V., Gilleard J. Benzimidazole resistance allele haplotype diversity in United Kingdom isolates of Teladorsagia circumcincta supports a hypothesis of multiple origins of resistance by recurrent mutation. Int. J. Parasitol. 2010, 40:1247-1255.
33. Tandon R., LePage K.T., Kaplan R.M. Cloning and characterization of genes encoding alpha and beta subunits of glutamate-gated chloride channel protein in Cylicocyclus nassatus. Mol. Biochem. Parasitol. 2006, 150:46-55.
34. Thompson A.J., Lester H.A., Lummis S.C. The structural basis of function in Cys-loop receptors. Q. Rev. Biophys. 2010, 43:449-499.
35. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7), research/0034.
36. Van Zeveren A.M., Visser A., Hoorens P.R., Vercruysse J., Claerebout E., Geldhof P. Evaluation of reference genes for quantitative real-time PCR in Ostertagia ostertagi by the coefficient of variation and geNorm approach. Mol. Biochem. Parasitol. 2007, 153:224-227.
37. Wolstenholme A.J., Fairweather I., Prichard R., von Samson-Himmelstjerna G., Sangster N.C. Drug resistance in veterinary helminths. Trends Parasitol. 2004, 20:469-476.
38. Yates D.M., Wolstenholme A.J. An ivermectin-sensitive glutamate-gated chloride channel subunit from Dirofilaria immitis. Int. J. Parasitol. 2004, 34:1075-1081.