Distribution of glutamate-gated chloride channel subunits in the parasitic nematode Haemonchus contortus

Journal of Comparative Neurology

Volumn 462, Issue 2, 2003, Pages 213-222

  Portillo, Virginia ^a   Jagannathan, Suchitra ^a,b   Wolstenholme, Adrian J ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Anthelmintic; Immunofluorescence; Ivermectin; Motor neuron; Sensory neuron

Indexed keywords

ANTHELMINTIC AGENT; ANTISERUM; AVERMECTIN; CHLORIDE CHANNEL; GLUTAMIC ACID; MILBEMYCIN; RECEPTOR SUBUNIT;

ARTICLE; BRAIN COMMISSURE; CHANNEL GATING; CONTROLLED STUDY; FEMALE; HAEMONCHUS CONTORTUS; IMMUNOFLUORESCENCE; MOTONEURON; NEMATODE; NERVE CORD; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE CELL;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; CHLORIDE CHANNELS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; HAEMONCHUS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; NEURONS, AFFERENT;

EID: 0037665154     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10735     Document Type: Article

References (45)

1. Albertson DG, Thomson JN. 1976. The pharynx of Caenorhabditis elegans. Phil Trans R Soc Lond B Biol Sci 275:299-325.
2. Arena JP, Liu KK, Paress PS, Frazier EG, Cully DF, Mrozik H, Schaeffer JM. 1995. The mechanism of action of avermectins in Caenorhabditis elegans - correlation between activation of glutamate-sensitive chloride current, membrane-binding and biological-acivity. J Parasitol 81:286-294.
3. Ashton FT, Li J, Schad GA. 1999. Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Vet Parasitol 84:297-316.
4. Avery L, Horvitz HR. 1990. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253:263-270.
5. Bernt U, Junkensdorf M, Londenshausen A, Harder A, Schiesenberg E. 1989. Effects of anthelmintics and different modes of action on the behaviour and development of C. elegans. Fund Appl Nematol 21:251-263.
6. Blaxter ML, De ley P, Garey JR, Liu LX, Scheldeman P, Vierstrate A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK. 1998. A molecular evolution framework for the phylum Nematoda. Nature 392:71-75.
7. Cheeseman CL, Delany NS, Woods DJ, Wolstenholme AJ. 2001. High-affinity ivermectin binding to recombinant subunits of the Haemonchus contortus glutamate-gated chloride channel. Mol Biochem Parasitol 114:161-168.
8. Cleland TA. 1996. Inhibitory glutamate receptor channels. Mol Neurobiol 13:97-136.
9. Cully DF, Vassilatis DK, Liu KK, Paress P, Van der Ploeg LHT, Schaeffer JM, Arena JP. 1994. Cloning of an avermectin-sensitive glutamategated chloride channel from Caenorhabditis elegans. Nature 371:707-711.
10. Cully DF, Paress PS, Liu KK, Schaeffer JM, Arena JP. 1996a. Identification of a Drosophila melanogaster glutamate gated chloride channel sensitive to the antiparasite agent avermectin. J Biol Chem 271:20187-20191.
11. Cully DF, Wilkinson H, Vassilatis DK. 1996b. Molecular biology and electrophysiology of glutamate-gated chloride channels of invertebrates. Parasitology 113:S191-S200.
12. Davis RE. 1998. Neurophysiology of glutamatergic signalling and anthelmintic action on Ascaris suum: evidence for a kainate receptor. Parasitology 116:471-486.
13. Delany NS, Laughton DL, Wolstenholme AJ. 1998. Cloning and localisation of an avermectin receptor-related subunit from Haemonchus contortus. Mol Biochem Parasitol 97:177-187.
14. Dent JA, Davis MW, Avery L. 1997. avr-15 Encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. EMBO J 16:5867-5879.
15. Dent JA, Smith MM, Vassilatis DK, Avery L. 2000. The genetics of avermectin resistance in Caenorhabditis elegans. Proc Natl Acad Sci USA 97:2674-2679.
16. Forrester SG, Hamdan FF, Prichard RK, Beech RN. 1999. Cloning, sequencing, and developmental expression levels of a novel glutamategated chloride channel homologue in the parasitic nematode Haemonchus contortus. Biochem Biophys Res Commun 254:529-534.
17. Forrester SG, Prichard RK, Beech RN. 2002. A glutamate-gated chloride channel subunit from Haemonchus contortus: expression in a mammalian cell line, ligand binding, and modulation of anthelmintic binding by glutamate. Biochem Pharmacol 63:1061-1068.
18. Freeman AS, Nghiem C, Li J, Ashton FT, Guerrero J, Shoop WL, Schad GA. 2003. Amphidial structure of ivermectin-resistant and susceptible laboratory and field strains of Haemonchus contortus. Vet Parasitol 110:217-226.
19. Geary TG, Sims SM, Thomas EM, Vanover L, Davis JP, Winterowd CA, Klein R, Norman HO, Thompson DP. 1993. Haemonchus contortus: ivermectin-induced paralysis of the pharynx. Exp Parasitol 77:88-96.
20. Gill JH, Redwin JM, Van Wyk JA, Lacey E. 1991. Detection of resistance to ivermectin in Haemonchus contortus. Int J Parasitol 21:771-776.
21. Gill JH, Kerr CA, Shoop WL, Lacey E. 1998. Evidence of multiple mechanisms of avermectin resistance in Haemonchus contortus - comparison of selection protocols. Int J Parasitol 28:783-790.
22. Grant W. 2000. What is the real target for ivermectin resistance selection in Onchocerca volvulus? Parasitol Today 16:458-459.
23. Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ. 2001. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br J Pharmacol 132:1247-1254.
24. Jagannathan S, Laughton DL, Critten CL, Skinner TM, Horoszok L, Wolstenholme AJ. 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.
25. Johnson CD, Stretton AOW. 1987. GABA-immunoreactivity in inhibitory motor neurons on the nematode Ascaris. J Neurosci 7:223-235.
26. Kass IS, Wang CC, Walrow JP, Stretton AOW. 1980. Avermectin b1A, a paralysing anthelmintic that affects interneurons and inhibitory motorneurons in Ascaris. Proc Natl Acad Sci USA 77:6211-6215.
27. Laughton DL, Lunt GG, Wolstenholme AJ. 1997a. 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.
28. Laughton DL, Lunt GG, Wolstenholme AJ. 1997b. Reporter gene constructs suggest the Caenorhabditis elegans avermectin receptor β-subunit is expressed solely in the pharynx. J Exp Biol 200:1509-1514.
29. Lee RYN, Sawin ER, Chalfie M, Horvitz RH, Avery L. 1999. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J Neurosci 19:159-167.
30. Li J, Ashton FT, Gamble HR, Schad GA. 2000a. Sensory neuroanatomy of a passively ingested nematode parasite, Haemonchus contortus: amphidial neurons of the first stage larva. J Comp Neurol. 417:299-314.
31. Li J, Zhu XD, Boston R, Ashton FT, Gamble HR, Schad GA. 2000b. Thermotaxis and thermosensory neurons in infective larvae of Haemonchus contortus, a passively ingested nematode parasite. J Comp Neurol 424:58-73.
32. Lopez PM, Boston R, Ashton FT, Schad GA. 2000. The neurons of class ALD mediate thermotaxis in the parasitic nematode, Strongyloides stercoralis. Int J Parasitol 30:1115-1121.
33. Martin RJ. 1996. An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutamate-gated chloride channel sensitive to the avermectin analogue, milbemycin D. Parasitology 112:247-252.
34. McIntire SL, Jorgensen EM, Kaplan J, Horvitz HR. 1993. The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337-341.
35. Nonet ML, Grundahl K, Meyer BJ, Rand JB. 1993. Synaptic function is impaired but not eliminated in C-elegans mutants lacking synaptotagmin. Cell 73:1291-1305.
36. Perry RN. 2001. Analysis of the sensory responses of parasitic nematodes using electrophysiology. Int J Parasitol 31:909-918.
37. Rolfe RN, Barrett J, Perry RN. 2001. Electrophysiological analysis of responses of adult females of Brugia pahangi to some chemicals. Parasitology 122:347-357.
38. Rongo C, Kaplan JM. 1999. CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402:195-199.
39. Skinner TM, Bascal ZA, Holden-Dye L, Lunt GG, Wolstenholme AJ. 1998. Immunocytochemical localisation of a putative inhibitory amino acid receptor subunit in the parasitic nematodes Haemonchus contortus and Ascaris suum. Parasitology 117:89-96.
40. Stretton AOW, Davis RE, Angstadt JD, Donmoyer JE, Johnson CD. 1985. Neural control of behavior in Ascaris. Trends Neurosci 8:294-300.
41. Vassilatis DK, Arena JP, Plasterk RHA, Wilkinson H, Schaeffer JM, Cully DF, Van der Ploeg LHT. 1997a. Genetic and biochemical evidence for a novel avermectin sensitive chloride channel in C. elegans isolation and characterisation. J Biol Chem 272:33167-33174.
42. Vassilatis DK, Elliston K, Paress PS, Hamelin M, Arena JP, Schaeffer JM, van der Ploeg LHT, Cully DF. 1997b. Evolutionary relationship of the ligand-gated ion channels and the avermectin sensitive, glutamategated chloride channels. J Mol Evol 44:501-508.
43. Walrond JP, Kass IS, Stretton AOW, Donmoyer JE. 1985. Identification of excitatory and inhibitory motoneurons in the nematode Ascaris by electrophysiological techniques. J Neurosci 5:1-8.
44. White JG, Southgate E, Thompson JN, Brenner S. 1986. The structure of the nervous system of the nematode C. elegans. Phil Trans R Soc Lond B Biol Sci 314:1-340.
45. Yassin L, Gillo B, Kahan T, Halevi S, Eshel M, Treinin M. 2001. Characterisation of the DEG-3/DES-2 receptor: a nicotinic acetylcholine receptor that mutates to cause neuronal degeneration. Mol Cell Neurosci 17:589-599.