Selective toxicity of the anthelmintic emodepside revealed by heterologous expression of human KCNMA1 in Caenorhabditis elegans

Molecular Pharmacology

Volumn 79, Issue 6, 2011, Pages 1031-1043

  Crisford, Anna ^a   Murray, Caitriona ^a   O'Connor, Vincent ^a   Edwards, Richard J ^a   Kruger, Nina ^b   Welz, Claudia ^b   Von Samson Himmelstjerna, Georg ^c   Harder, Achim ^d   Walker, Robert J ^a   Holden Dye, Lindy ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d BAYER AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 HYDROXY 5 TRIFLUOROMETHYLPHENYL) 5 TRIFLUOROMETHYL 2(3H) BENZIMIDAZOLONE; CALCIUM ACTIVATED POTASSIUM CHANNEL; EMODEPSIDE; KCNMA1 CHANNEL; ROTTLERIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTHELMINTIC ACTIVITY; ARTICLE; CAENORHABDITIS ELEGANS; CELL SPECIFICITY; CELL STIMULATION; DRUG SENSITIVITY; FEEDING; HETEROLOGOUS EXPRESSION; NERVOUS SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARMACOPHORE; PHARYNGEAL MUSCLE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTHELMINTICS; CAENORHABDITIS ELEGANS; DEPSIPEPTIDES; HUMANS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNITS; LOCOMOTION; POTASSIUM CHANNELS, CALCIUM-ACTIVATED;

EID: 79956336717     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.071043     Document Type: Article

References (37)

1. Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, and North RA (1992) Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 9:209-216.
2. Altschul SF, Gish W, Miller W, Myers EW, and Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410.
3. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
4. Bull K, Cook A, Hopper NA, Harder A, Holden-Dye L, and Walker RJ (2007) Effects of the novel anthelmintic emodepside on the locomotion, egg-laying behaviour and development of Caenorhabditis elegans. Int J Parasitol 37:627-636. (Pubitemid 46442834)
5. Butler A, Tsunoda S, McCobb DP, Wei A, and Salkoff L (1993) mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science 261: 221-224.
6. Carre-Pierrat M, Grisoni K, Gieseler K, Mariol MC, Martin E, Jospin M, Allard B, and Ségalat L (2006) The SLO-1 BK channel of Caenorhabditis elegans is critical for muscle function and is involved in dystrophin-dependent muscle dystrophy. J Mol Biol 358:387-395.
7. Chiang JT, Steciuk M, Shtonda B, and Avery L (2006) Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. J Exp Biol 209: 1859-1873. (Pubitemid 43965862)
8. Chiba CM and Rankin CH (1990) A developmental analysis of spontaneous and reflexive reversals in the nematode. Caenorhabditis elegans. J Neurobiol 21:543-554. (Pubitemid 20201680)
9. Cook A, Franks CJ, and Holden-Dye L (2006) Electrophysiological recordings from the pharynx, in WormBook (C. elegans Research Community ed) pp 1-7, doi: 10.1895/wormbook.1.110.1.
10. Dillon J, Andrianakis I, Bull K, Glautier S, O'Connor V, Holden-Dye L, and James C (2009) AutoEPG: software for the analysis of electrical activity in the microcircuit underpinning feeding behaviour of Caenorhabditis elegans. PLoS ONE 4:e8482.
11. Du W, Bautista JF, Yang H, Diez-Sampedro A, You SA, Wang L, Kotagal P, Lüders HO, Shi J, Cui J, et al. (2005) Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat Genet 37:733-738. (Pubitemid 41754890)
12. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Chen Y, Clapham P, Coates G, Fairley S, Fitzgerald S, Gordon L, Hendrix M, Hourlier T, Johnson N, Kähäri A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Larsson P, Longden I, McLaren W, Overduin B, Pritchard B, Riat HS, Rios D, Ritchie GR, Ruffier M, Schuster M, Sobral D, Spudich G, Tang YA, Trevanion S, Vandrovcova J, Vilella AJ, White S, Wilder SP, Zadissa A, Zamora J, Aken BL, Birney E, Cunningham F, Dunham I, Durbin R, Fernández-Suarez XM, Herrero J, Hubbard TJ, Parker A, Proctor G, Vogel J, and Searle SM. et al. (2011) Ensembl 2011. Nucleic Acids Res 39:D800-D806.
13. Geary TG, Woo K, McCarthy JS, Mackenzie CD, Horton J, Prichard RK, de Silva NR, Olliaro PL, Lazdins-Helds JK, Engels DA, et al. (2010) Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int J Parasitol 40:1-13.
14. Gilleard JS (2006) Understanding anthelmintic resistance: the need for genomics and genetics. Int J Parasitol 36:1227-1239.
15. Guest M, Bull K, Walker RJ, Amliwala K, O'Connor V, Harder A, Holden-Dye L, and Hopper NA (2007) 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 37:1577-1588. (Pubitemid 47542465)
16. Harder A, Schmitt-Wrede HP, Krücken J, Marinovski P, Wunderlich F, Willson J, Amliwala K, Holden-Dye L, and Walker R (2003) Cyclooctadepsipeptides- an anthelmintically active class of compounds exhibiting a novel mode of action. Int J Antimicrob Agents 22:318-331. (Pubitemid 37103217)
17. Harder A and von Samson-Himmelstjerna G (2002) Cyclooctadepsipeptides - a new class of anthelmintically active compounds. Parasitol Res 88:481-488. (Pubitemid 34810711)
18. Holden-Dye L, O'Connor V, Hopper NA, Walker RJ, Harder A, Bull K, and Guest M (2007) SLO, SLO, quick, quick, slow: calcium-activated potassium channels as regulators of Caenorhabditis elegans behaviour and targets for anthelmintics. Invert Neurosci 7:199-208. (Pubitemid 350164927)
19. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, and Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5-W9.
20. Lee K, Rowe IC, and Ashford ML (1995) NS 1619 activates BKCa channel activity in rat cortical neurones. Eur J Pharmacol 280:215-219.
21. McCobb DP, Fowler NL, Featherstone T, Lingle CJ, Saito M, Krause JE, and Salkoff L (1995) A human calcium-activated potassium channel gene expressed in vascular smooth muscle. Am J Physiol 269:H767-H777.
22. Mitchell PH, Bull K, Glautier S, Hopper NA, Holden-Dye L, and O'Connor V (2007) The concentration-dependent effects of ethanol on Caenorhabditis elegans behaviour. Pharmacogenomics J 7:411-417. (Pubitemid 350187453)
23. Nonet ML, Saifee O, Zhao H, Rand JB, and Wei L (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J Neurosci 18:70-80. (Pubitemid 28046768)
24. Okkema PG, Harrison SW, Plunger V, Aryana A, and Fire A (1993) Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135:385-404. (Pubitemid 23307595)
25. + channels by novel benzimidazolone. Eur J Pharmacol 251:53-59.
26. Rogers CM, Franks CJ, Walker RJ, Burke JF, and Holden-Dye L (2001) Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamidelike neuropeptides. J Neurobiol 49:235-244. (Pubitemid 33000769)
27. Saeger B, Schmitt-Wrede HP, Dehnhardt M, Benten WP, Krücken J, Harder A, Von Samson-Himmelstjerna G, Wiegand H, and Wunderlich F (2001) Latrophilin-like receptor from the parasitic nematode Haemonchus contortus as target for the anthelmintic depsipeptide PF1022A. FASEB J 15:1332-1334.
28. Salkoff L, Butler A, Ferreira G, Santi C, and Wei A (2006) High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7:921-931.
29. Townson S, Freeman A, Harris A, and Harder A (2005) Activity of the cyclooctadepsipeptide emodepside against Onchocerca gutterosa, Onchocerca lienalis and Brugia pahangi (Abstract). Am J Trop Med Hyg 73 (6 Suppl):93.
30. von Samson-Himmelstjerna G, Harder A, Sangster NC, and Coles GC (2005) Efficacy of two cyclooctadepsipeptides, PF1022A and emodepside, against anthelminticresistant nematodes in sheep and cattle. Parasitology 130:343-347. (Pubitemid 40444953)
31. Wang ZW, Saifee O, Nonet ML, and Salkoff L (2001) SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32:867-881. (Pubitemid 34024847)
32. Willson J, Amliwala K, Davis A, Cook A, Cuttle MF, Kriek N, Hopper NA, O'Connor V, Harder A, Walker RJ, and Holden-Dye L (2004) Latrotoxin receptor signaling engages the UNC-13-dependent vesicle-priming pathway in C. elegans. Curr Biol 14:1374-1379. (Pubitemid 39081640)
33. Willson J, Amliwala K, Harder A, Holden-Dye L, and Walker RJ (2003) The effect of the anthelmintic emodepside at the neuromuscular junction of the parasitic nematode Ascaris suum. Parasitology 126:79-86. (Pubitemid 36246202)
34. 3) cells and in cortical neuronal (HCN-1A) cells. J Cell Physiol 210:655-666.
35. + channel. Nature 466:393-397.
36. Zakharov SI, Morrow JP, Liu G, Yang L, and Marx SO (2005) Activation of the BK (SLO1) potassium channel by mallotoxin. J Biol Chem 280:30882-30887.
37. Zhang XF, Gopalakrishnan M, and Shieh CC (2003) Modulation of action potential firing by iberiotoxin and NS1619 in rat dorsal root ganglion neurons. Neuroscience 122:1003-1011. (Pubitemid 37485850)