Levamisole receptors: A second awakening

Trends in Parasitology

Volumn 28, Issue 7, 2012, Pages 289-296

  Martin, Richard J ^a   Robertson, Alan P ^a   Buxton, Samuel K ^a   Beech, Robin N ^b   Charvet, Claude L ^c,d   Neveu, Cédric ^c,d  

^a IOWA STATE UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UR1282   (France)

^d UNIVERSITÉ DE TOURS   (France)

Author keywords

Acetylcholine; Anthelmintic; Ion channel receptor; Levamisole; Nematode; Oocyte expression; Resistance; Subtypes

Indexed keywords

CHOLINERGIC RECEPTOR; DRUG RECEPTOR; ION CHANNEL; LEVAMISOLE;

ANTHELMINTIC ACTIVITY; ASCARIS SUUM; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; GENE FUNCTION; GENETIC VARIABILITY; HAEMONCHUS CONTORTUS; HUMAN; MICROFLUIDICS; NEMATODIASIS; NONHUMAN; OESOPHAGOSTOMUM; PHENOTYPE; REVIEW;

ANIMALS; ANTHELMINTICS; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; DEPSIPEPTIDES; DRUG RESISTANCE; GENES, HELMINTH; HUMANS; ION CHANNEL GATING; ION CHANNELS; LEVAMISOLE; MODELS, MOLECULAR; PYRANTEL; RECEPTORS, CHOLINERGIC; SPECIES SPECIFICITY; XENOPUS;

ANIMALIA; NEMATODA;

EID: 84862339518     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2012.04.003     Document Type: Review

References (51)

1. Puttachary S., et al. Levamisole and ryanodine receptors. II: an electrophysiological study in Ascaris suum. Mol. Biochem. Parasitol. 2010, 171:8-16.
2. Robertson, A.P. et al. (2010) Levamisole and ryanodine receptors. I: a contraction study in Ascaris suum. Mol. Biochem. Parasitol. 171, 1-7.
3. Robertson S.J., Martin R.J. Levamisole-activated single-channel currents from muscle of the nematode parasite Ascaris suum. Br. J. Pharmacol. 1993, 108:170-178.
4. Robertson A.P., et al. Resistance to levamisole resolved at the single-channel level. FASEB J. 1999, 13:749-760.
5. Robertson A.P., et al. Single-channel recording from adult Brugia malayi. Invert. Neurosci. 2011, 11:53-57.
6. Qian H., et al. Pharmacology of N-, L- and B-subtypes of nematode nAChR resolved at the single-channel level in Ascaris suum. FASEB J. 2006, 20:2606-2608.
7. Qian H., et al. Levamisole resistance resolved at the single-channel level in Caenorhabditis elegans. FASEB J. 2008, 22:3247-3254.
8. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
9. Changeux J.P., Edelstein S.J. Allosteric mechanisms of signal transduction. Science 2005, 308:1424-1428.
10. Corringer P.J., et al. Critical elements determining diversity in agonist binding and desensitization of neuronal nicotinic acetylcholine receptors. J. Neurosci. 1998, 18:648-657.
11. Jones A.K., Sattelle D.B. Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. Bioessays 2004, 26:39-49.
12. Boulin T., et al. Eight genes are required for functional reconstitution of the Caenorhabditis elegans levamisole-sensitive acetylcholine receptor. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18590-18595.
13. Culetto E., et al. The Caenorhabditis elegans unc-63 gene encodes a levamisole-sensitive nicotinic acetylcholine receptor alpha subunit. J. Biol. Chem. 2004, 279:42476-42483.
14. Fleming J.T., et al. Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J. Neurosci. 1997, 17:5843-5857.
15. Towers P.R., et al. The Caenorhabditis elegans lev-8 gene encodes a novel type of nicotinic acetylcholine receptor alpha subunit. J. Neurochem. 2005, 93:1-9.
16. Seo S., et al. The positive allosteric modulator morantel binds at noncanonical subunit interfaces of neuronal nicotinic acetylcholine receptors. J. Neurosci. 2009, 29:8734-8742.
17. Wu T.Y., et al. Morantel allosterically enhances channel gating of neuronal nicotinic acetylcholine alpha 3 beta 2 receptors. Mol. Pharmacol. 2008, 74:466-475.
18. Evans A.M., Martin R.J. Activation and cooperative multi-ion block of single nicotinic-acetylcholine channel currents of Ascaris muscle by the tetrahydropyrimidine anthelmintic, morantel. Br. J. Pharmacol. 1996, 118:1127-1140.
19. Martin R.J., Robertson A.P. Mode of action of levamisole and pyrantel, anthelmintic resistance, E153 and Q57. Parasitology 2007, 134:1093-1104.
20. Fleming J.T., et al. Molecular cloning and in vitro expression of C. elegans and parasitic nematode ionotropic receptors. Parasitology 1996, 113(Suppl.):S175-S190.
21. Gally C., et al. A transmembrane protein required for acetylcholine receptor clustering in Caenorhabditis elegans. Nature 2004, 431:578-582.
22. Maryon E.B., et al. unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J. Cell Biol. 1996, 134:885-893.
23. Almedom R.B., et al. An ER-resident membrane protein complex regulates nicotinic acetylcholine receptor subunit composition at the synapse. EMBO J. 2009, 28:2636-2649.
24. Eimer S., et al. Regulation of nicotinic receptor trafficking by the transmembrane Golgi protein UNC-50. EMBO J. 2007, 26:4313-4323.
25. Gottschalk A., et al. Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. EMBO J. 2005, 24:2566-2578.
26. Halevi S., et al. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J. 2002, 21:1012-1020.
27. Haugstetter J., et al. Identification and characterization of a novel thioredoxin-related transmembrane protein of the endoplasmic reticulum. J. Biol. Chem. 2005, 280:8371-8380.
28. Simon D.J., et al. The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions. Cell 2008, 133:903-915.
29. Williamson S.M., et al. The cys-loop ligand-gated ion channel gene family of Brugia malayi and Trichinella spiralis: a comparison with Caenorhabditis elegans. Invert. Neurosci. 2007, 7:219-226.
30. Neveu, C. et al. (2010) Genetic diversity of levamisole receptor subunits in parasitic nematode species and abbreviated transcripts associated with resistance. Pharmacogenet. Genomics 20, 414-425.
31. Boulin T., et al. Functional reconstitution of Haemonchus contortus acetylcholine receptors in Xenopus oocytes provides mechanistic insights into levamisole resistance. Br. J. Pharmacol. 2011, 164:1421-1432.
32. Fauvin, A. et al. (2010) cDNA-AFLP analysis in levamisole-resistant Haemonchus contortus reveals alternative splicing in a nicotinic acetylcholine receptor subunit. Mol. Biochem. Parasitol. 170, 105-107.
33. Raymond V., et al. Anthelmintic actions on homomer-forming nicotinic acetylcholine receptor subunits: chicken alpha7 and ACR-16 from the nematode Caenorhabditis elegans. Neuroscience 2000, 101:785-791.
34. Williamson S.M., et al. 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. 2009, 5:e1000517.
35. Chen G.Q., et al. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 1999, 402:817-821.
36. Brejc K., et al. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001, 411:269-276.
37. 2+-binding sites. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3210-3215.
38. Abin-Carriquiry, J.A. et al. (2010) In silico characterization of cytisinoids docked into an acetylcholine binding protein. Bioorg. Med. Chem. Lett. 20, 3683-3687.
39. Unwin N. Acetylcholine receptor channel imaged in the open state. Nature 1995, 373:37-43.
40. Brandsdal B.O., et al. Free energy calculations and ligand binding. Adv. Protein Chem. 2003, 66:123-158.
41. Robertson A.P., et al. Pyrantel resistance alters nematode nicotinic acetylcholine receptor single-channel properties. Eur. J. Pharmacol. 2000, 394:1-8.
42. Chen, B. et al. (2011) Microfluidic bioassay to characterize parasitic nematode phenotype and anthelmintic resistance. Parasitology 138, 80-88.
43. Carr, J.A. et al. (2011) A microfluidic platform for high-sensitivity, real-time drug screening on C. elegans and parasitic nematodes. Lab. Chip 11, 2385-2396.
44. Kopp S.R., et al. High-level pyrantel resistance in the hookworm Ancylostoma caninum. Vet. Parasitol. 2007, 143:299-304.
45. Williamson S.M., et al. Candidate anthelmintic resistance-associated gene expression and sequence polymorphisms in a triple-resistant field isolate of Haemonchus contortus. Mol. Biochem. Parasitol. 2011, 180:99-105.
46. Halevi S., et al. Conservation within the RIC-3 gene family. Effectors of mammalian nicotinic acetylcholine receptor expression. J. Biol. Chem. 2003, 278:34411-34417.
47. Levandoski M.M., et al. Single-channel properties of N- and L-subtypes of acetylcholine receptor in Ascaris suum. Int. J. Parasitol. 2005, 35:925-934.
48. Pennington A.J., Martin R.J. A patch-clamp study of acetylcholine-activated ion channels in Ascaris suum muscle. J. Exp. Biol. 1990, 154:201-221.
49. Robertson S.J., et al. The action of pyrantel as an agonist and an open channel blocker at acetylcholine receptors in isolated Ascaris suum muscle vesicles. Eur. J. Pharmacol. 1994, 271:273-282.
50. Abin-Carriquiry J.A., et al. In silico characterization of cytisinoids docked into an acetylcholine binding protein. Bioorg. Med. Chem. Let. 2010, 20:3683-3687.
51. Brandsdal B.O., et al. Free energy calculations and ligand binding. Advances in Protein Chemistry 2003, 123-158. Academic Press. D. Valerie (Ed.).