Decreased emodepside sensitivity in unc-49 γ-aminobutyric acid (GABA)-receptor-deficient Caenorhabditis elegans

International Journal for Parasitology

Volumn 42, Issue 8, 2012, Pages 761-770

  Miltsch, Sandra M ^a   Krücken, Jürgen ^a   Demeler, Janina ^a   Janssen, I Jana I ^a   Krüger, Nina ^a   Harder, Achim ^b   von Samson Himmelstjerna, Georg ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b BAYER AG   (Germany)

Author keywords

Caenorhabditis elegans; Emodepside; GABA receptor; Rescue; Toxocara canis; Unc 49

Indexed keywords

4 AMINOBUTYRIC ACID; EMODEPSIDE;

DNA; DRUG; NEMATODE; NUMERICAL MODEL; PEPTIDE; PHENOTYPE; SENSITIVITY ANALYSIS;

ANTHELMINTIC SENSITIVITY; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA SEQUENCE; DRUG EFFICACY; DRUG SENSITIVITY; GENE AMPLIFICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS; START CODON; TOXOCARA CANIS; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ANTHELMINTICS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DEPSIPEPTIDES; FEMALE; MALE; MOLECULAR SEQUENCE DATA; MUTATION; PARASITIC SENSITIVITY TESTS; PHYLOGENY; RECEPTORS, GABA-A; SEQUENCE ALIGNMENT;

CAENORHABDITIS ELEGANS; NEMATODA; TOXOCARA CANIS;

EID: 84863815883     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.05.009     Document Type: Article

References (53)

1. Accardi M.V., Forrester S.G. The Haemonchus contortus UNC-49B subunit possesses the residues required for GABA sensitivity in homomeric and heteromeric channels. Mol. Biochem. Parasitol. 2011, 178:15-22.
2. Altreuther G., Gasda N., Adler K., Hellmann K., Thurieau H., Schimmel A., Hutchens D., Krieger K.J. Field evaluations of the efficacy and safety of emodepside plus toltrazuril (Procox® oral suspension for dogs) against naturally acquired nematode and Isospora spp. infections in dogs. Parasitol. Res. 2011, 109(Suppl. 1):S21-S28.
3. Altreuther G., Radeloff I., LeSueur C., Schimmel A., Krieger K.J. Field evaluation of the efficacy and safety of emodepside plus praziquantel tablets (Profender tablets for dogs) against naturally acquired nematode and cestode infections in dogs. Parasitol. Res. 2009, 105(Suppl. 1):S23-29.
4. Bamber B.A., Beg A.A., Twyman R.E., Jorgensen E.M. The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J. Neurosci. 1999, 19:5348-5359.
5. Bamber B.A., Richmond J.E., Otto J.F., Jorgensen E.M. The composition of the GABA receptor at the Caenorhabditis elegans neuromuscular junction. Br. J. Pharmacol. 2005, 144:502-509.
6. Bamber B.A., Twyman R.E., Jorgensen E.M. Pharmacological characterization of the homomeric and heteromeric UNC-49 GABA receptors in C. elegans. Br. J. Pharmacol. 2003, 138:883-893.
7. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
8. Buxton S., Neveu C., Charvet C., Robertson A., Martin R. On the mode of action of emodepside: slow effects on membrane potential and voltage-activated currents in Ascaris suum. Br. J. Pharmacol. 2011, 164:453-470.
9. Chen W., Terada M., Cheng J.T. Characterization of subtypes of gamma-aminobutyric acid receptors in an Ascaris muscle preparation by binding assay and binding of PF1022A, a new anthelmintic, on the receptors. Parasitol. Res. 1996, 82:97-101.
10. Condi G.K., Soutello R.G., Amarante A.F. Moxidectin-resistant nematodes in cattle in Brazil. Vet. Parasitol. 2009, 161:213-217.
11. Costa J.C., Lilley C.J., Atkinson H.J., Urwin P.E. Functional characterisation of a cyst nematode acetylcholinesterase gene using Caenorhabditis elegans as a heterologous system. Int. J. Parasitol. 2009, 39:849-858.
12. Crisford A., Murray C., O'Connor V., Edwards R.J., Kruger N., Welz C., von Samson-Himmelstjerna G., Harder A., Walker R.J., Holden-Dye L. Selective toxicity of the anthelmintic emodepside revealed by heterologous expression of human KCNMA1 in Caenorhabditis elegans. Mol. Pharmacol. 2011, 79:1031-1043.
13. Darriba D., Taboada G.L., Doallo R., Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27:1164-1165.
14. Demeler J., Kuttler U., El-Abdellati A., Stafford K., Rydzik A., Varady M., Kenyon F., Coles G., Hoglund J., Jackson F., Vercruysse J., von Samson-Himmelstjerna G. Standardization of the larval migration inhibition test for the detection of resistance to ivermectin in gastro intestinal nematodes of ruminants. Vet. Parasitol. 2010, 174:58-64.
15. Eddi C., Caracostantogolo J., Pena M., Schapiro J., Marangunich L., Waller P.J., Hansen J.W. The prevalence of anthelmintic resistance in nematode parasites of sheep in southern Latin America: Argentina. Vet. Parasitol. 1996, 62:189-197.
16. El-Abdellati A., Geldhof P., Claerebout E., Vercruysse J., Charlier J. Monitoring macrocyclic lactone resistance in Cooperia oncophora on a Belgian cattle farm during four consecutive years. Vet. Parasitol. 2010, 171:167-171.
17. Gally C., Bessereau J.L. GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J. Neurosci. 2003, 23:2591-2599.
18. Gillan V., Maitland K., McCormack G., Him N.A., Devaney E. Functional genomics of hsp-90 in parasitic and free-living nematodes. Int. J. Parasitol. 2009, 39:1071-1081.
19. Glendinning S.K., Buckingham S.D., Sattelle D.B., Wonnacott S., Wolstenholme A.J. Glutamate-gated chloride channels of Haemonchus contortus restore drug sensitivity to ivermectin resistant Caenorhabditis elegans. PLoS ONE 2011, 6:e22390.
20. Guest M., Bull K., Walker R.J., Amliwala K., O'Connor V., Harder A., Holden-Dye L., Hopper N.A. The calcium-activated potassium channel, SLO-1, is required for the action of the novel cyclo-octadepsipeptide anthelmintic, emodepside, in Caenorhabditis elegans. Int. J. Parasitol. 2007, 37:1577-1588.
21. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
22. Harder A., Schmitt-Wrede H.P., Krücken J., Marinovski P., Wunderlich F., Willson J., Amliwala K., Holden-Dye L., Walker R. Cyclooctadepsipeptides - an anthelmintically active class of compounds exhibiting a novel mode of action. Int. J. Antimicrob. Agents 2003, 22:318-331.
23. Hu Y., Xiao S.H., Aroian R.V. The new anthelmintic tribendimidine is an L-type (levamisole and pyrantel) nicotinic acetylcholine receptor agonist. PLoS Negl. Trop. Dis. 2009, 3:e499.
24. Iravani J. Interrelation between barbiturates, piperazine and GABA in the membrane of crayfish muscles. Naunyn Schmiedebergs Arch. Exp. Pathol. Pharmakol. 1965, 251:265-274.
25. Jex A.R., Liu S., Li B., Young N.D., Hall R.S., Li Y., Yang L., Zeng N., Xu X., Xiong Z., Chen F., Wu X., Zhang G., Fang X., Kang Y., Anderson G.A., Harris T.W., Campbell B.E., Vlaminck J., Wang T., Cantacessi C., Schwarz E.M., Ranganathan S., Geldhof P., Nejsum P., Sternberg P.W., Yang H., Wang J., Gasser R.B. Ascaris suum draft genome. Nature 2011, 479:529-533.
26. Kahsay R.Y., Gao G., Liao L. An improved hidden Markov model for transmembrane protein detection and topology prediction and its applications to complete genomes. Bioinformatics 2005, 21:1853-1858.
27. Kaplan R.M. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 2004, 20:477-481.
28. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
29. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D., Zhang N., Zheng C., Bryant S.H. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011, 39:D225-229.
30. Martin R.J., Harder A., Londershausen M., Jeschke P. Anthelmintic actions of the cyclic depsipeptide PF1022A and its electrophysiological effects on muscle cells of Ascaris suum. Pestic. Sci. 1996, 48:343-349.
31. McIntire S.L., Jorgensen E., Kaplan J., Horvitz H.R. The GABAergic nervous system of Caenorhabditis elegans. Nature 1993, 364:337-341.
32. Miyadoh S., Kawasaki H., Aoyagi K., Yaguchi T., Okada T., Sugiyama J. Taxonomic position of the fungus producing the anthelmintic PF1022 based on the 18S rRNA gene base sequence. Nippon Kingakukai Kaiho 2000, 41:183-188.
33. Nicolay F., Harder A., von Samson-Himmelstjerna G., Mehlhorn H. Synergistic action of a cyclic depsipeptide and piperazine on nematodes. Parasitol. Res. 2000, 86:982-992.
34. Overend D.J., Phillips M.L., Poulton A.L., Foster C.E. Anthelmintic resistance in Australian sheep nematode populations. Aust. Vet. J. 1994, 71:117-121.
35. Petry G., Kruedewagen E., Bach T., Gasda N., Krieger K.J. Efficacy of Procox® oral suspension for dogs (0.1% emodepside and 2% toltrazuril) against experimental nematode Toxocara cati and Ancylostoma tubaeforme infections in cats. Parasitol. Res. 2011, 109(Suppl. 1):S37-S43.
36. Reinemeyer C.R., Charles S.D., Buch J., Settje T., Altreuther G., Cruthers L., McCall J.W., Young D.R., Epe C. Evaluation of the efficacy of emodepside plus praziquantel topical solution against ascarid infections (Toxocara cati or Toxascaris leonina) in cats. Parasitol. Res. 2005, 97(Suppl. 1):S41-S50.
37. Rendell D.K. Anthelmintic resistance in cattle nematodes on 13 south-west Victorian properties. Aust. Vet. J. 2010, 88:504-509.
38. Richmond J.E., Jorgensen E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 1999, 2:791-797.
39. Saeger B., Schmitt-Wrede H.P., Dehnhardt M., Benten W.P., Krücken J., Harder A., Von Samson-Himmelstjerna G., Wiegand H., Wunderlich F. Latrophilin-like receptor from the parasitic nematode Haemonchus contortus as target for the anthelmintic depsipeptide PF1022A. FASEB J. 2001, 15:1332-1334.
40. Sasaki T., Takagi M., Yaguchi T., Miyadoh S., Okada T., Koyama M. A new anthelmintic cyclodepsipeptide, PF1022A. J. Antibiot. (Tokyo) 1992, 45:692-697.
41. Schimmel A., Schroeder I., Altreuther G., Settje T., Charles S., Wolken S., Kok D.J., Ketzis J., Young D., Hutchens D., Krieger K.J. Efficacy of emodepside plus toltrazuril (Procox® oral suspension for dogs) against Toxocara canis, Uncinaria stenocephala and Ancylostoma caninum in dogs. Parasitol. Res. 2011, 109(Suppl. 1):S1-S8.
42. Siddiqui S.Z., Brown D.D., Rao V.T., Forrester S.G. An UNC-49 GABA receptor subunit from the parasitic nematode Haemonchus contortus is associated with enhanced GABA sensitivity in nematode heteromeric channels. J. Neurochem. 2010, 113:1113-1122.
43. Suarez V.H., Cristel S.L. Anthelmintic resistance in cattle nematode in the western Pampeana Region of Argentina. Vet. Parasitol. 2007, 144:111-117.
44. Sullivan K.M., Dean A., Soe M.M. OpenEpi: a web-based epidemiologic and statistical calculator for public health. Public Health Rep. 2009, 124:471-474.
45. Sutherland I.A., Leathwick D.M. Anthelmintic resistance in nematode parasites of cattle: a global issue?. Trends Parasitol. 2010, 27:176-181.
46. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
47. van Wyk J.A., Stenson M.O., Van der Merwe J.S., Vorster R.J., Viljoen P.G. Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort J. Vet. Res. 1999, 66:273-284.
48. von Samson-Himmelstjerna G. Molecular diagnosis of anthelmintic resistance. Vet. Parasitol. 2006, 136:99-107.
49. von Samson-Himmelstjerna G., Harder A., Sangster N.C., Coles G.C. Efficacy of two cyclooctadepsipeptides, PF1022A and emodepside, against anthelmintic-resistant nematodes in sheep and cattle. Parasitology 2005, 130:343-347.
50. Welz C., Krüger N., Schniederjans M., Miltsch S.M., Krücken J., Guest M., Holden-Dye L., Harder A., von Samson-Himmelstjerna G. SLO-1-channels of parasitic nematodes reconstitute locomotor behaviour and emodepside sensitivity in Caenorhabditis elegans slo-1 loss of function mutants. PLoS Pathog. 2011, 7:e1001330.
51. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 2001, 18:691-699.
52. Willson J., Amliwala K., Davis A., Cook A., Cuttle M.F., Kriek N., Hopper N.A., O'Connor V., Harder A., Walker R.J., Holden-Dye L. Latrotoxin receptor signaling engages the UNC-13-dependent vesicle-priming pathway in C. elegans. Curr. Biol. 2004, 14:1374-1379.
53. 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.