Glutamate-Gated chloride channels of Haemonchus contortus restore drug sensitivity to ivermectin resistant Caenorhabditis elegans

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Glendinning, Susan K ^a   Buckingham, Steven D ^b   Sattelle, David B ^c   Wonnacott, Susan ^a   Wolstenholme, Adrian J ^a,d  

^a UNIVERSITY OF BATH   (United Kingdom)

^b WADHAM COLLEGE   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IVERMECTIN; CHLORIDE CHANNEL; COMPLEMENTARY DNA; GLUTAMATE GATED CHLORIDE CHANNELS; GLUTAMATE-GATED CHLORIDE CHANNELS; GREEN FLUORESCENT PROTEIN;

ARTICLE; AVR 14 GENE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA POLYMORPHISM; DRUG SENSITIVITY; FUNGAL GENE; GENE; GENE EXPRESSION SYSTEM; GENE MUTATION; GENE SEQUENCE; GENE TARGETING; GENETIC VARIABILITY; GLC 2 GENE; GLC 6 GENE; GLUTAMATE GATED CHLORIDE CHANNEL GENE; HAEMONCHUS CONTORTUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROMOTER REGION; RNA SPLICING; ANIMAL; ANIMAL BEHAVIOR; BIOASSAY; DRUG EFFECT; DRUG RESISTANCE; GENETICS; HAEMONCHUS; METABOLISM; MOVEMENT (PHYSIOLOGY); PROTEIN SUBUNIT;

CAENORHABDITIS ELEGANS; CAPRA HIRCUS; HAEMONCHUS CONTORTUS; NEMATODA; OVIS ARIES;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL ASSAY; CAENORHABDITIS ELEGANS; CHLORIDE CHANNELS; DNA, COMPLEMENTARY; DRUG RESISTANCE; GREEN FLUORESCENT PROTEINS; HAEMONCHUS; IVERMECTIN; MOVEMENT; PROMOTER REGIONS, GENETIC; PROTEIN SUBUNITS;

EID: 79960777044     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022390     Document Type: Article

References (52)

1. Brooker S, Hotez PJ, Bundy DAP, (2010) The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Negl Trop Dis 4: e779.
2. Geary TG, Woo K, McCarthy JS, Mackenzie CD, Horton J, et al. (2010) Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int J Parasitol 40: 1-13.
3. Vercruysse J, Rew RS, (2002) Macrocyclic lactones in antiparasitic therapy. Wallingford, U.K. CABI Publishing.
4. Fox LM, (2006) Ivermectin: uses and impact 20 years on. Curr Op Infect Dis 19: 588-593.
5. Omura S, (2008) Ivermectin: 25 years and still going strong. Int J Antimicrob Agents 31: 91-98.
6. Kaplan RM, (2004) Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20: 477-481.
7. Wolstenholme AJ, Fairweather I, Prichard RK, von Samson-Himmelstjerna G, Sangster N, (2004) Drug resistance in veterinary helminths. Trends Parasitol 20: 469-476.
8. Churcher TS, Pion SDS, Osei-Atweneboana MY, Prichard RK, Awadzi K, et al. (2009) Identifying sub-optimal responses to ivermectin in the treatment of River Blindness. Proc Nat'l Acad Sci US A 106: 16716-16721.
9. Osei-Atweneboana MY, Eng JKL, Boakye DA, Gyapong JO, Prichard RK, (2007) Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 369: 2021-2029.
10. Britton C, Murray L, (2006) Using Caenorhabditis elegans for functional analysis of genes of parasitic nematodes. Int J Parasitol 36: 651-659.
11. Wolstenholme AJ, Rogers AT, (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131: S85-S95.
12. Moreno Y, Nabhan JF, Solomon J, Mackenzie CD, Geary TG, (2010) Ivermectin disrupts the function of the excretory-secretory apparatus in microfilariae of Brugia malayi. Pro Nat'l Acad Sci US A 107: 20120-20125.
13. Lok JB, Artis D, (2008) Transgenesis and neuronal ablation in parasitic nematodes: revolutionary new tools to dissect host-parasite interactions. Parasite Immunol 30: 203-214.
14. Liu CH, de Oliveira A, Higazi TB, Ghedin E, DePasse J, et al. (2007) Sequences necessary for trans-splicing in transiently transfected Brugia malayi. Mol Biochem Parasitol 156: 62-73.
15. Lok JB, Massey HC, (2002) Transgene expression in Strongyloides stercoralis following gonadal microinjection of DNA constructs. Mol Biochem Parasitol119: 279-284.
16. Castelletto ML, Massey HC, Lok JB, (2009) Morphogenesis of Strongyloides stercoralis infective larvae requires the DAF-16 ortholog FKTF-1. PLoS Pathogens 5: e1000370.
17. Junio AB, Li XS, Massey HC, Nolan TJ, Lamitina ST, et al. (2008) Strongyloides stercoralis: Cell- and tissue-specific transgene expression and co-transformation with. vector constructs incorporating a common multifunctional 3 ′ UTR. Exp Parasitol 118: 253-265.
18. Geldhof P, Visser A, Clark D, Saunders G, Britton C, et al. (2007) RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134: 609-619.
19. Samarasinghe B, Knox DP, Britton C, (2011) Factors affecting susceptibility to RNA interference in Haemonchus contortus and in vivo silencing of an H11 aminopeptidase gene. Int J Parasitology 41: 51-59.
20. Gillan V, Maitland K, McCormack G, Him N, Devaney E, (2009) Functional genomics of hsp-90 in parasitic and free-living nematodes. Int J Parasitol 39: 1071-1081.
21. Britton C, Murray L, (2002) A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Mol Biochem Parasitol 122: 21-33.
22. Couthier A, Smith J, McGarr P, Craig B, Gilleard JS, (2004) Ectopic expression of a Haemonchus contortus GATA transcription factor in Caenorhabditis elegans reveals conserved function in spite of extensive sequence divergence. Mol Biochem Parasitol 133: 241-253.
23. Kwa MSG, Veenstra JG, van Dujk M, Roos MH, (1995) Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans. J Mol Biol 246: 500-510.
24. Kampkotter A, Volkmann TE, de Castro SH, Leiers B, Klotz LO, et al. (2003) Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): A parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J Mol Biol 325: 25-37.
25. Massey HC, Bhopale MK, Li XS, Castelletto M, Lok JB, (2006) The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans. Int J Parasitol 36: 347-352.
26. Crook M, Grant K, Grant WN, (2010) Failure of Parastrongyloides trichosuri daf-7 to complement a Caenorhabditis elegans daf-7 (e1372) mutant: implications for the evolution of parasitism. Int J Parasitol 40: 1675-1683.
27. Beech RN, Wolstenholme AJ, Neveu C, Dent JA, (2010) Nematode parasite genes: what's in a name? Trends Parasitol 26: 334-340.
28. Welz C, Kruger N, Schniederjans M, Miltsch SM, Krucken J, et al. (2011) SLO-1-channels of parasitic nematodes reconstitute locomotor behaviour and emodepside sensitivity in Caenorhabditis elegans slo-1 loss of function mutants. PLoS Pathogens 7: e1001330.
29. Yates DM, Portillo V, Wolstenholme AJ, (2003) The avermectin receptors of Haemonchus contortus and Caenorhabditis elegans. Int J Parasitol 33: 1183-1193.
30. Jagannathan S, Laughton DL, Critten CL, Skinner TM, Horoszok L, et al. (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.
31. Laughton DL, Lunt GG, Wolstenholme AJ, (1997) 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.
32. Williamson SM, Walsh TK, Wolstenholme AJ, (2007) The cys-loop ligand-gated ion channel gene family of Brugia malayi and Trichinella spiralis: a comparison with Caenorhabditis elegans. Invert Neurosci 7: 219-226.
33. Cook A, Aptel N, Portillo V, Siney E, Sihota R, et al. (2006) Caenorhabditis elegans ivermectin receptors regulate locomotor behaviour and are functional orthologues of Haemonchus contortus receptors. Mol Biochem Parasitol 147: 118-125.
34. Dent JA, Smith MM, Vassilatis DK, Avery L, (2000) The genetics of ivermectin resistance in Caenorhabditis elegans. Proc Nat'l Acad Sci USA 97: 2674-2679.
35. Buckingham SD, Sattelle DB, (2009) Fast, automated measurement of nematode swimming (thrashing) without morphometry. Bmc Neuroscience 10: 84.
36. Cully DF, Vassilatis DK, Liu KK, Paress P, Van der Ploeg LHT, et al. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371: 707-711.
37. Laughton DL, Lunt GG, Wolstenholme AJ, (1997) Reporter gene constructs suggest the Caenorhabditis elegans avermectin receptor β-subunit is expressed solely in the pharynx. J Exp Biol 200: 1509-1514.
38. Pemberton DJ, Franks CJ, Walker RJ, 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 GluClα2 in the function of the native receptor. Mol Pharmacol 59: 1037-1043.
39. Portillo V, Jagannathan S, Wolstenholme AJ, (2003) Distribution of glutamate-gated chloride channel subunits in the parasitic nematode Haemonchus contortus. J Comp Neurol 462: 213-222.
40. Cheeseman CL, Delany NS, Woods DJ, Wolstenholme AJ, (2001) High-affinity ivermectin binding to recombinant subunits of the Haemonchus contortus glutamate-gated chloride channel. Mol Biochem Parasitol 114: 161-168.
41. McCavera S, Walsh TK, Wolstenholme AJ, (2007) Nematode ligand-gated chloride channels: an appraisal of their involvement in macrocyclic lactone resistance and prospects for developing molecular markers. Parasitology 134: 1111-1121.
42. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. (1998) A molecular evolution framework for the phylum Nematoda. Nature 392: 71-75.
43. McCavera S, Rogers AT, Yates DM, Woods DJ, Wolstenholme AJ, (2009) An ivermectin-sensitive glutamate-gated chloride channel from the parasitic nematode, Haemonchus contortus. Mol Pharmacol 75: 1347-1355.
44. Njue AI, Hayashi J, Kinne L, Feng X-P, Prichard RK, (2004) Mutations in the extracellular domain of glutamate-gated chloride channel α3 and β subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity. J Neurochem 89: 1137-1147.
45. Lynagh T, Lynch JW, (2010) A glycine residue essential for high ivermectin sensitivity in Cys-loop ion channel receptors. Int J Parasitol 40: 1477-1481.
46. Hibbs RE, Gouaux E, (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474: 54-60.
47. Fire A, Harrison SW, Dixon D, (1990) A modular set of lacz fusion vectors for studying gene-expression in Caenorhabditis elegans. Gene 93: 189-198.
48. Dent JA, Davis MW, 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.
49. Vassilatis DK, Arena JP, Plasterk RHA, Wilkinson H, Schaeffer JM, et al. (1997) Genetic and biochemical evidence for a novel avermectin sensitive chloride channel in C. elegans; isolation and characterisation. J Biol Chem 272: 33167-33174.
50. Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ, (2001) GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Brit J Pharmacol 132: 1247-1254.
51. Cully DF, Wilkinson H, Vassilatis DK, (1996) Molecular biology and electrophysiology of glutamate-gated chloride channels of invertebrates. Parasitology 113: S191-S200.
52. Forrester SG, Beech RN, Prichard RK, (2004) Agonist enhancement of macrocyclic lactone activity at a glutamate-gated chloride channel subunit from Haemonchus contortus. Biochem Pharmacol 67: 1019-1024.