Antinematodal Drugs - Modes of Action and Resistance: And Worms Will Not Come to Thee (Shakespeare: Cymbeline: IV, ii)

Parasitic Helminths: Targets, Screens, Drugs and Vaccines

Volumn , Issue , 2012, Pages 233-249

  Robertson, Alan P ^a   Buxton, Samuel K ^a   Puttachary, Sreekanth ^a   Williamson, Sally M ^b   Wolstenholme, Adrian J ^b   Neveu, Cedric ^c   Cabaret, Jacques ^c   Charvet, Claude L ^c   Martin, Richard J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UR1282   (France)

Author keywords

Anthelmintic; Antinematodal drug; Cholinergic agonist; Mode of action; Resistance

Indexed keywords

EID: 84879462998     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527652969.ch14     Document Type: Chapter

References (79)

1. Bowman, W.C. and Rand, J. (eds) (1980) Textbook of Pharmacology, Blackwell Scientific, Oxford.
2. Kliks, M.M. (1990) Helminths as heirlooms and souvenirs: a review of new world paleoparasitology. Parasitol. Today, 6, 93-100.
3. Fayard, G. (1949) Ascaridiose et piperazine, These de Doctorat, University of Paris.
4. Jones, A.K. and Sattelle, D.B. (2004) Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. Bioessays, 26, 39-49.
5. Boulin, T., Fauvin, A., Charvet, C., Cortet, J., Cabaret, J., Bessereau, J.-L., and Neveu, C. (2001) Functional reconstitution of Haemonchus contortus acetylcholine receptors in Xenopus oocytes provides mechanistic insights into levamisole resistance. Br. J. Pharmacol., 164, 1421-1432.
6. Portillo, V., Jagannathan, S., and Wolstenholme, A.J. (2003) Distribution of glutamate-gated chloride channel subunits in the parasitic nematodes Haemonchus contortus. J. Comp. Neurol., 462, 213-222.
7. Martin, R.J. and Kusel, J.R. (1991) On the distribution of a fluorescent ivermectin probe (400,5,7 dimethyl-bodipy proprionylivermectin) in Ascaris membranes. Parasitology, 104, 549-555.
8. Hibbs, R.E. and Gouaux, E. (2011) Princiciples of activation and permeation in an anion-selective Cys-loop receptor. Nature, 474, 54-60.
9. Boulin, T. et al. (2008) Eight genes are required for functional reconstitution of the Caenorhabditis elegans levamisolesensitive acetylcholine receptor. Proc. Natl. Acad. Sci. USA, 105, 18590-18595.
10. Gottschalk, A. et al. (2005) Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. EMBO J., 24, 2566-2578.
11. Almedom, R.B. et al. (2009) An ERresident membrane protein complex regulates nicotinic acetylcholine receptor subunit composition at the synapse. EMBO J., 28, 2636-2649.
12. Rapti, G., Richmond, J., and Bessereau, J.L. (2011) A singleimunoglobulin-domain protein for clustering acetylcholine receptors in C. elegans. EMBO J., 30, 706-718.
13. Williamson, S.M., Walsh, T.K., and Wolstenholme, A.J. (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.
14. 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.
15. 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.
16. Williamson, S.M. 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.
17. Kaminsky, R. et al. (2008) A new class of anthelmintics effective against drugresistant nematodes. Nature, 452, 176-180.
18. Rufener, L. et al. (2009) Haemonchus contortus acetylcholine receptors of the DEG-3 subfamily and their role in sensitivity to monepantel. PLoS Pathog., 5, e1000380.
19. Rufener, L. et al. (2010) Monepantel allosterically activates DEG-3/DES-2 channels of the gastrointestinal nematode Haemonchus contortus. Mol. Pharmacol., 78, 895-902.
20. Qian, H.,Martin, R.J., and Robertson, A.P. (2006) Pharmacology of N-, L- and Bsubtypes of nematode nAChR resolved at the single-channel level in Ascaris suum. FASEB J., 20, 2606-2608.
21. Zinser, E.W. et al. (2002) Anthelmintic paraherquamides are cholinergic antagonists in gastrointestinal nematodes and mammals. J. Vet. Pharmacol. Ther., 25, 241-250.
22. Cully, D.F. et al. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature, 371, 707-711.
23. Forrester, S.G. et al. (2003) Haemonchus contortus: HcGluCla expressed in Xenopus oocytes forms a glutamate-gated ion channel that is activated by ibotenate and the antiparasitic drug ivermectin. Mol. Biochem. Parasitol., 129, 115-121.
24. Forrester, S.G. and Siddiqui, S.Z. (2008)Anovel member of the ligand-gated chloride channel gene family from Haemonchus contortus. Parasitology, 135, 539-545.
25. Rao, V.T. et al (2010) Characterization of a novel tyramine-gated chloride channel fromHaemonchus contortus. Mol. Biochem. Parasitol., 173, 64-68.
26. Rao, V.T. et al. (2011) Localisation of serotonin and dopamine in Haemonchus contortus. Int. J. Parasitol., 41, 249-254.
27. Rao, V.T. et al. (2009) A dopamine-gated ion channel (HcGGR3_) from Haemonchus contortus is expressed in the cervical papillae and is associated with macrocyclic lactone resistance. Mol. Biochem. Parasitol., 166, 54-61.
28. Siddiqui, S.Z. et al. (2010) An UNC-49 GABA receptor subunit from the parasitic nematode Haemonchus contortus is associated with enhanced GABA sensitivity in nematode heteromeric channels. J. Neurochem., 113, 1113-1122.
29. Mareno, Y. et al. (2010) Ivermectin disrupts the function of the excretorysecretory apparatus in microfilariae of Brugia malayi. Proc. Natl. Acad. Sci. USA, 46, 20120-20125.
30. Horoszok, L. et al. (2001) GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamategated chloride channel subunit from Caenorhabditis elegans. Br. J. Pharmacol., 132, 1247-1254.
31. Jagannathan, S. 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.
32. Cully, D.F. et al. (1996) Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. J. Biol. Chem., 271, 20187-20191.
33. Laughton, D.L., Lunt, G.G., and Wolstenholme, A.J. (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.
34. Dent, J.A. et al. (2000) The genetics of ivermectin resistance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA, 97, 2674-2679.
35. Barnes, T.M. and Hekimi, S. (1997) The Caenorhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J. Neurochem., 69, 2251-2260.
36. Vassilatis, D.K. et al. (1997) Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate-gated chloride channels. J. Mol. Evol., 44, 501-508.
37. Martin, R.J. (1982) Electrophysiological effects of piperazine and diethylcarbamazine on Ascaris suum somatic muscle. Br. J. Pharmacol., 77, 255-265.
38. Martin, R.J. et al. (1996) Anthelmintic actions of the cyclicdepsipeptide PF1022A and its electrophysiological effects on muscle cells of Ascaris suum. Pesticide Sci., 38, 343-349.
39. Guest, M. et al. (2007) The calciumactivated potassium channel, SLO-1, is required for the action of the novel cyclooctadepsipeptide anthelmintic, emodepside, in Caenorhabditis elegans. Int. J. Parasitol., 37, 1577-1588.
40. Crisford, A. et al. (2011) Selective toxicity of the anthelmintic emodepside revealed by heterologous expression of human KCNMA1 in Caenorhabditis elegans. Mol. Pharmacol., 79, 1031-1043.
41. Verma, S., Robertson, A.P., and Martin, R.J. (2009) Effects of SDPNFLRFamide (PF1) on voltage-activated currents in Ascaris suum muscle. Int. J. Parasitol., 39, 315-326.
42. Willson, J. et al. (2003) The effect of the anthelmintic emodepside at the neuromuscular junction of the parasitic nematode Ascaris suum. Parasitology, 126, 79-86.
43. Buxton, S.K., Neveu, C., Charvet, C.L., Robertson, A.P., and Martin, R.J. (2011) On the mode of action of emodepside: effects on membrane potential and voltage-activated currents in Ascaris suum. Br. J. Pharmacol., 164, 453-470.
44. Lacey, E. and Prichard, R.K. (1986) Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus. Mol. Biochem. Parasitol., 19, 171-181.
45. MacDonald, L.M. et al. (2004) Characterisation of benzimidazole binding with recombinant tubulin from Giardia duodenalis, Encephalitozoon intestinalis, and Cryptosporidium parvum. Mol. Biochem. Parasitol., 138, 89-96.
46. Fukushige, T. et al. (1999) MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J. Cell Sci., 112, 395-403.
47. Gogonea, C.B. et al. (1999) Computational prediction of the three-dimensional structures for the Caenorhabditis elegans tubulin family. J. Mol. Graph. Model., 17, 90-100. 126-130.
48. Phillips, J.B. et al. (2004) Roles for two partially redundant alpha-tubulins during mitosis in early Caenorhabditis elegans embryos. Cell Motil. Cytoskeleton, 58, 112-126.
49. Lu, C. andMains, P.E. (2005)Mutations of a redundant alpha-tubulin gene affect Caenorhabditis elegans early embryonic cleavage via MEI-1/katanin-dependent and -independent pathways. Genetics, 170, 115-126.
50. Lu, C., Srayko, M., and Mains, P.E. (2004) The Caenorhabditis elegans microtubulesevering complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotypes. Mol. Biol. Cell, 15, 142-150.
51. Baran, R. et al. (2010) Motor neuron synapse and axon defects in a C. elegans alpha-tubulin mutant. PLoS One, 5, e9655.
52. Driscoll, M. et al. (1989) Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity. J.Cell Biol., 109, 2993-3003.
53. Savage, C. et al. (1989) mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev., 3, 870-881.
54. Luduena, R.F. (1993) Are tubulin isotypes functionally significant. Mol. Biol. Cell, 4, 445-457.
55. Geary, T.G. et al. (1992) Three beta-tubulin cDNAs from the parasitic nematode Haemonchus contortus. Mol. Biochem. Parasitol., 50, 295-306.
56. Van den Bossche, H. et al. (1983) Alterations in rat liver mitochondria caused by Fasciola hepatica. Contrib. Microbiol. Immunol., 7, 30-38.
57. Rothwell, J.T. and Sangster, N.C. (1996) The effects of closantel treatment on the ultrastructure of Haemonchus contortus. Int. J. Parasitol., 26, 49-57.
58. Gloeckner,C. et al. (2010) Repositioning of an existing drug for the neglected tropical disease Onchocerciasis. Proc. Natl. Acad. Sci. USA, 107, 3424-3429.
59. Garner, A.L. et al. (2011) Design, synthesis, and biological activities of closantel analogues: structural promiscuity and its impact on Onchocerca volvulus. J. Med. Chem., 54, 3963-3972.
60. Hawking, F., Sewell, P., and Thurston, J.P. (1948) Mode of action of hetrazan in filariasis. Lancet, ii, 730.
61. Terada, M. and Sano, M. (1986) Effects of diethylcarbamazine on the motility of Angiostrongylus cantonensis and Dirofilaria immitis. Z. Parasitenkd., 72, 375-385.
62. McGarry, H.F., Plant, L.D., and Taylor, M.J. (2005) Diethylcarbamazine activity against Brugia malayi microfilariae is dependent on inducible nitric-oxide synthase and the cyclooxygenase pathway. Filaria J., 4, 4.
63. Queto, T. et al. (2010) Inducible nitric oxide synthase/CD95L-dependent suppression of pulmonary and bone marrow eosinophilia by diethylcarbamazine. Am. J. Respir. Crit. Care Med., 181, 429-437.
64. Anderson, V.R. and Curran, M.P. (2007) Nitazoxanide: a review of its use in the treatment of gastrointestinal infections. Drugs, 67, 1947-1047.
65. Hoffman, P.S. et al. (2007) Antiparasitic drug nitazoxanide inhibits the pyruvate oxidoreductases of Helicobacter pylori, selected anaerobic bacteria and parasites, and Campylobacter jejuni. Antimicrob. Agents Chemother., 51, 868-76.
66. Boray, J.C. et al. (1997) Nitroscanate a new broad-spectrum anthelmintic against nematodes and cestodes of dogs and cats. Aust. Vet. J., 55, 45-53.
67. Voge., E. and Bueding, E. (1980) Schistosoma mansoni: tegmental surface alterations induced by sub-curative does of the schistosmocide, amoscanate. Exp. Parasitol., 50, 251-259.
68. Kohler, P., Davies, K.P., and Zahner, H. (1992) Activity, mechanism of action and pharmacokinetics of 2-tertbutylbenzothiazole and CGP 6140 (amocarzine) antifilarial drugs. Acta Trop., 51, 195-211.
69. Sangster, N.C. et al. (1989) Binding of [3H] m-aminolevamisole to receptors in levamisole-susceptible and -resistant Haemonchus contortus. Int. J. Parasitol., 28, 707-717.
70. Kopp, S.R. et al. (2006) High-level pyrantel resistance in the hookworm Ancylsotoma caninum. Vet. Parasitol., 143, 299-304.
71. Robertson, A.P., Bjorn, H.E., and Martin, R.J. (1999) Resistance to levamisole resolved at the single-channel level. FASEB J., 13, 749-760.
72. Saragoza, P.A. et al. (2003) Identification of an alternatively processed nicotinic receptor alpha7 subunit RNA in mouse brain. Brain Res. Mol. Brain Res., 117, 15-26.
73. Martin, R.J. and Robertson, A.P. (2007) Mode of action of levamisole and pyrantel, anthelmintic resistance, E153 and Q57. Parasitology, 134, 1093-1104.
74. Beech, R.N. et al. (2010) Anthelmintic resistance: markers for resistance, or susceptibility? Parasitology, 138, 160-74.
75. Ardelli, B.F. et al. (2009) A comparison of the effects of ivermectin and moxidectin on the nematode Caenorhabditis elegans. Vet. Parasitol., 165, 96-108.
76. Merino, G. et al. (2009) Natural allelic variants of bovine ATP-binding cassette transporter ABCG2: increased activity of the Ser581 variant and development of tools for the discovery of new ABCG2 inhibitors. Drug Metab. Dispos., 37, 5-9.
77. Mottier, MD. and Prichard, R.K. (2008) Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on Haemonchus contortus. Pharmacogenet. Genomics, 18, 129-140.
78. Kwa, M.S.G. et al. (1995) Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drugresistance in Caenorhabditis elegans. J. Mol. Biol., 246, 500-510.
79. Kavallaris, M. (2010) Microtubules and resistance to tubulin-binding agents. Nat. Rev. Cancer, 10, 194-204.