Phylogenomics of ligand-gated ion channels predicts monepantel effect

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Rufener, Lucien ^a,b   Keiser, Jennifer ^c,d   Kaminsky, Ronald ^a   Mäser, Pascal ^c,d   Nilsson, Daniel ^b  

^a Novartis Centre de Recherche Santé Animale   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACR 23 PROTEIN; ANTHELMINTIC AGENT; CAENORHABDITIS ELEGANS PROTEIN; ION CHANNEL; MONEPANTEL; MONEPANTEL 1 PROTEIN; UNCLASSIFIED DRUG; ZOLVIX;

AMINO ACID SEQUENCE; ANTHELMINTIC SENSITIVITY; ARTICLE; CAENORHABDITIS ELEGANS; CHANNEL GATING; DRUG SENSITIVITY; GENE SEQUENCE; GENOME; HAEMONCHUS CONTORTUS; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRISTIONCHUS PACIFICUS; SENSITIVITY ANALYSIS; STRONGYLOIDES RATTI;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; HAEMONCHUS CONTORTUS; NEMATODA; OVIS ARIES; PRISTIONCHUS PACIFICUS; STRONGYLOIDES RATTI;

EID: 78149325386     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001091     Document Type: Article

References (53)

1. Perry BD, Randolph TF (1999) Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Vet Parasitol 84: 145-168.
2. Drudge JH, Leland SE, Jr., Wyant ZN (1957) Strain variation in the response of sheep nematodes to the action of phenothiazine. II. Studies on pure infections of Haemonchus contortus. Am J Vet Res 18: 317-325.
3. Atanasio A, Boomker J, Sitoe C (2002) A survey on the occurrence of resistance to anthelmintics of gastrointestinal nematodes of goats in Mozambique. Onderstepoort J Vet Res 69: 215-220.
4. Coles GC, Rhodes AC, Wolstenholme AJ (2005) Rapid selection for ivermectin resistance in Haemonchus contortus. Vet Parasitol 129: 345-347.
5. Jackson F, Coop RL (2000) The development of anthelmintic resistance in sheep nematodes. Parasitology 120 Suppl: S95-107.
6. Traversa D, Paoletti B, Otranto D, Miller J (2007) First report of multiple drug resistance in trichostrongyles affecting sheep under field conditions in Italy. Parasitol Res 101: 1713-1716.
7. Waghorn TS, Leathwick DM, Rhodes AP, Lawrence KE, Jackson R, et al. (2006) Prevalence of anthelmintic resistance on sheep farms in New Zealand. N ZVet J54: 271-277.
8. Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, et al. (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452: 176-180.
9. Kaminsky R, Gauvry N, Schorderet Weber S, Skripsky T, Bouvier J, et al. (2008) Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate. Parasitol Res 103: 931-939.
10. Rufener L, Maser P, Roditi I, Kaminsky R (2009) Haemonchus contortus acetylcholine receptors of the DEG-3 subfamily and their role in sensitivity to monepantel. PLoS Pathog 5: e1000380.
11. Millar NS, Gotti C (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56: 237-246.
12. Kohler P (2001) The biochemical basis of anthelmintic action and resistance. Int J Parasitol 31: 336-345.
13. Robertson AP, Clark CL, Burns TA, Thompson DP, Geary TG, et al. (2002) Paraherquamide and 2-deoxy-paraherquamide distinguish cholinergic receptor subtypes in Ascaris muscle. J Pharmacol Exp Ther 302: 853-860.
14. Holden-Dye L, Walker RJ (2006) Actions of glutamate and ivermectin on the pharyngeal muscle of Ascaridia galli: a comparative study with Caenorhabditis elegans. Int J Parasitol 36: 395-402.
15. Arena JP, Liu KK, Paress PS, Schaeffer JM, Cully DF (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.
16. Culetto E, Baylis HA, Richmond JE, Jones AK, Fleming JT, et al. (2004) The Caenorhabditis elegans unc-63 gene encodes a levamisole-sensitive nicotinic acetylcholine receptor alpha subunit. J Biol Chem 279: 42476-42483.
17. Fleming JT, Squire MD, Barnes TM, Tornoe C, Matsuda K, et al. (1997) Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17: 5843-5857.
18. Brown LA, Jones AK, Buckingham SD, Mee CJ, Sattelle DB (2006) Contributions from Caenorhabditis elegans functional genetics to antiparasitic drug target identification and validation: nicotinic acetylcholine receptors, a case study. Int J Parasitol 36: 617-624.
19. 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.
20. Chen N, Harris TW, Antoshechkin I, Bastiani C, Bieri T, et al. (2005) WormBase: a comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res 33: D383-389.
21. The UniProt Consortium (2009) The Universal Protein Resource (UniProt). Nucleic Acids Res 37: D169-174.
22. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
23. Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14: 988-995.
24. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-288.
25. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
26. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
27. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, et al. (2007) Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460.
28. Bingham J, Sudarsanam S (2000) Visualizing large hierarchical clusters in hyperbolic space. Bioinformatics 16: 660-661.
29. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71-75.
30. Tasneem A, Iyer LM, Jakobsson E, Aravind L (2005) Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol 6: R4.
31. Chiu J, DeSalle R, Lam HM, Meisel L, Coruzzi G (1999) Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged. Mol Biol Evol 16: 826-838.
32. Philippe G, Angenot L, Tits M, Frederich M (2004) About the toxicity of some Strychnos species and their alkaloids. Toxicon 44: 405-416.
33. Kall L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338: 1027-1036.
34. Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res 35: W429-432.
35. Jones AK, Sattelle DB (2004) Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. Bioessays 26: 39-49.
36. Williamson SM, Robertson AP, Brown L, Williams T, Woods DJ, et al. (2009) The nicotinic acetylcholine receptors of the parasitic nematode Ascaris suum: formation of two distinct drug targets by varying the relative expression levels of two subunits. PLoS Pathog 5: e1000517.
37. Rufener L, Baur R, Kaminsky R, Maser P, Sigel E (2010) Monepantel allosterically activates DEG-3/DES-2 channels of the gastrointestinal nematode Haemonchus contortus. Molecular Pharmacology, In Press.
38. Sager H, Hosking B, Bapst B, Stein P, Vanhoff K, et al. (2009) Efficacy of the amino-acetonitrile derivative, monepantel, against experimental and natural adult stage gastro-intestinal nematode infections in sheep. Vet Parasitol 159: 49-54.
39. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.
40. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, et al. (2008) Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proc Natl Acad Sci U S A 105: 14802-14807.
41. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, et al. (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26: 909-915.
42. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, et al. (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1: E45.
43. C. elegans Seq Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282: 2012-2018.
44. Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, et al. (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40: 1193-1198.
45. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
46. Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, et al. (2002) Whole- genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301-1310.
47. Int. Chicken Genome Seq. Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-716.
48. She X, Jiang Z, Clark RA, Liu G, Cheng Z, et al. (2004) Shotgun sequence assembly and recent segmental duplications within the human genome. Nature 431: 927-930.
49. Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, et al. (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324: 522-528.
50. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803-819.
51. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
52. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, et al. (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316: 1718-1723.
53. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.