Nematode cys-loop GABA receptors: biological function, pharmacology and sites of action for anthelmintics

Abdi YA, Gustafsson LL, Ericsson O, Hellgren U (1995) Handbook of drugs for tropical parasitic infections, 2nd edn. Taylor & Francis Ltd, London, pp 123–127

Accardi MV, Forrester SG (2011) The Haemonchus contortus UNC-49B subunit possesses the residues required for GABA sensitivity in homomeric and heteromeric channels. Mol Biochem Parasitol 178:15–22

Amin J, Weiss DS (1993) GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital. Nature 366:565–569

Bamber BA, Beg AA, Twyman RE, Jorgensen EM (1999) The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J Neurosci 19:5348–5359

Bamber BA, Twyman RE, Jorgensen EM (2003) Pharmacological characterization of the homomeric and heteromeric UNC-49 GABA receptors in C. elegans. Br J Pharmacol 138:883–893

Bamber BA, Richmond JE, Otto JF, Jorgensen EM (2005) The composition of the GABA receptor at the Caenorhabditis elegans neuromuscular junction. Br J Pharmacol 144:502–509

Beech R, Levitt N, Cambos M, Zhou S, Forrester SG (2010a) Association of ion-channel genotype and macrocyclic lactone sensitivity traits in Haemonchus contortus. Mol Biochem Parasitol 171:74–80

Beech RN, Wolstenholme AJ, Neveu C, Dent JA (2010b) Nematode parasite genes: what’s in a name? Trend Parasitol 26:334–340

Beg AA, Jorgensen EM (2003) EXP-1 is an excitatory GABA-gated cation channel. Nat Neurosci 6:1145–1152

Boileau AJ, Newell JG, Czajkowski C (2002) GABA(A) receptor beta 2 Tyr97 and Leu99 line the GABA-binding site. Insights into mechanisms of agonist and antagonist actions. J Biol Chem 277:2931–2937

Boisvenue RJ, Brandt MC, Galloway RB, Hendrix JC (1983) In vitro activity of various anthelmintic compounds against Haemonchus contortus larvae. Vet Parasitol 13:341–347

Brown DD, Siddiqui SZ, Kaji MD, Forrester SG (2012) Pharmacological characterization of the Haemonchus contortus GABA-gated chloride channel, Hco-UNC-49: Modulation by macrocyclic lactone anthelmintics and a receptor for piperazine. Vet Parasitol 185:201–209

Chen W, Terada M, Cheng JT (1996) Characterization of subtypes of gamma-aminobutyric acid receptors in an Ascaris muscle preparation by binding assay and binding of PF1022A, a new anthelmintic, on the receptors. Parasitol Res 82:97–101

Cully DF, Vassilatis DK, Liu KK, Paress PS, Van der Ploeg LH, Schaeffer JM, Arena JP (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371:707–711

Del Castillo J, Morales T, Sanchez V (1963) Action of piperazine on the neuromuscular system of Ascaris lumbricoides. Nature 200:706–707

Del Castillo J, De Mello WC, Morales T (1964a) Influence of some ions on the membrane potential of Acaris muscle. J Gen Physiol 48:129–140

Del Castillo J, De Mello WC, Morales TA (1964b) Inhibitory action of gamma-aminobutyric acid (GABA) on Ascaris muscle. Experientia 20:141–143

Dent JA (2010) The evolution of pentameric ligand-gated ion channels. Adv Exp Med Biol 683:11–23

Duittoz AH, Martin RJ (1991a) Antagonist properties of arylaminopyridazine GABA derivatives at the Ascaris muscle GABA receptor. J Exp Biol 159:149–164

Duittoz AH, Martin RJ (1991b) Effects of SR95103 on GABA-activated single-channel currents from Ascaris suum muscle. Comp Biochem Physiol Part C Comp Pharmacol 98:423–432

Duittoz AH, Martin RJ (1991c) Effects of the arylaminopyridazine-GABA derivatives, sr95103 and SR95531 on the Ascaris muscle GABA receptor: the relative potency of the antagonists in Ascaris is different to that at vertebrate GABA, receptors. Comp Biochem Physiol Part C Comp Pharmacol 98:417–422

Feng XP, Hayashi J, Beech RN, Prichard RK (2002) Study of the nematode putative GABA type-A receptor subunits: evidence for modulation by ivermectin. J Neurochem 83:870–878

Gally C, Bessereau JL (2003) GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J Neurosci 23:2591–2599

Gilleard JS (2004) The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128(Suppl 1):S49–S70

Guastella J, Johnson CD, Stretton AO (1991) GABA-immunoreactive neurons in the nematode Ascaris. J Comp Neurol 307:584–597

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. System Biol 52:696–704

Harder A, Schmitt-Wrede HP, Krucken J, Marinovski P, Wunderlich F, Willson J, Amliwala K, Holden-Dye L, Walker R (2003) Cyclooctadepsipeptides—an anthelmintically active class of compounds exhibiting a novel mode of action. Int J Antimicrob Agents 22:318–331

Harrison NJ, Lummis SC (2006) Molecular modeling of the GABA(C) receptor ligand-binding domain. J Mol Model 12:317–324

Hedgecock E (1976) GABA Metabolism in Caenorhabditis elegans. University California Press, Santa Cruz

Holden-Dye L, Walker RJ (1990) Avermectin and avermectin derivatives are antagonists at the 4-aminobutyric acid (GABA) receptor on the somatic muscle cells of Ascaris; is this the site of anthelmintic action? Parasitology 101(Pt 2):265–271

Holden-Dye L, Hewitt GM, Wann KT, Krogsgaard-Larsen P, Walker RJ (1988) Studies involving avermectin and the 4-aminobutyric acid (GABA) receptor of Ascaris suum muscle. Pest Sci 24:231–245

Holden-Dye L, Krogsgaard-Larsen P, Nielsen L, Walker RJ (1989) GABA receptors on the somatic muscle cells of the parasitic nematode, Ascaris suum: stereoselectivity indicates similarity to a GABAA-type agonist recognition site. Br J Pharmacol 98:841–850

Huang J, Casida JE (1997) Avermectin B1a binds to high- and low-affinity sites with dual effects on the gamma-aminobutyric acid-gated chloride channel of cultured cerebellar granule neurons. J Pharmacol Exp Ther 281:261–266

Johnson CD, Stretton AO (1987) GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. J Neurosci 7:223–235

Johnston GA (1986) Multiplicity of GABA receptors, in benzodiazepine/GABA receptors and chloride channels. In: Olsen RW, Venter JC (eds) Receptor biochemistry and methodology, vol 5. Alan R. Liss, Inc., New York, pp 57–71

Johnston GA (2005) GABA(A) receptor channel pharmacology. Curr Pharm Des 11:1867–1885

Jones AK, Sattelle DB (2008) The cys-loop ligand-gated ion channel gene superfamily of the nematode, Caenorhabditis elegans. Invert Neurosci 8:41–47

Jorgensen EM, Nonet ML (1995) Neuromuscular junctions in the nematode C. elegans. Semin Dev Biol 6:207–220

Kass IS, Wang CC, Walrond JP, Stretton AO (1980) Avermectin B1a, a paralyzing anthelmintic that affects interneurons and inhibitory motoneurons in Ascaris. Proc Natl Acad Sci USA 77:6211–6215

Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

Kuriyama T, Ju XL, Fusazaki S, Hishinuma H, Satou T, Koike K, Nikaido T, Ozoe Y (2005) Nematocidal quassinoids and bicyclophosphorothionates: a possible common mode of action on the GABA receptor. Pestic Biochem Physiol 81:176–187

Kusama T, Wang TL, Guggino WB, Cutting GR, Uhl GR (1993) GABA rho 2 receptor pharmacological profile: GABA recognition site similarities to rho 1. Eur J Pharmacol 245:83–84

Laughton DL, Amar M, Thomas P, Towner P, Harris P, Lunt GG, Wolstenholme AJ (1994) Cloning of a putative inhibitory amino acid receptor subunit from the parasitic nematode Haemonchus contortus. Recept Channels 2:155–163

Lummis SC (2009) Locating GABA in GABA receptor binding sites. Biochem Soc Trans 37:1343–1346

Lummis SC, Beene L, Harrison NJ, Lester HA, Dougherty DA (2005) A cation-pi binding interaction with a tyrosine in the binding site of the GABAC receptor. Chem Biol 12:993–997

Lummis SC, McGonigle I, Ashby JA, Dougherty DA (2011) Two amino acid residues contribute to a cation-pi binding interaction in the binding site of an insect GABA receptor. J Neurosci 31:12371–12376

Martin RJ (1980) The effect of gamma-aminobutyric acid on the input conductance and membrane potential of Ascaris muscle. Br J Pharmacol 71:99–106

Martin RJ (1982) Electrophysiological effects of piperazine and diethylcarbamazine on Ascaris suum somatic muscle. Br J Pharmacol 77:255–265

Martin RJ (1985) Gamma-aminobutyric acid- and piperazine-activated single-channel currents from Ascaris suum body muscle. Br J Pharmacol 84:445–461

Martin RJ (1993) Neuromuscular transmission in nematode parasites and antinematodal drug action. Pharmacol Ther 58:13–50

Martin RJ, Pennington AJ, Duittoz AH, Robertson S, Kusel JR (1991) The physiology and pharmacology of neuromuscular transmission in the nematode parasite Ascaris suum. Parasitology 102(Suppl):S41–S58

Martin RJ, Sitamze JM, Duittoz AH, Wermuth CG (1995) Novel arylaminopyridazine-GABA receptor antagonists examined electrophysiologically in Ascaris suum. Eur J Pharmacol 276:9–19

McIntire SL, Jorgensen E, Horvitz HR (1993a) Genes required for GABA function in Caenorhabditis elegans. Nature 364:334–337

McIntire SL, Jorgensen E, Kaplan J, Horvitz HR (1993b) The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337–341

Mehta AK, Ticku MK (1999) An update on GABAA receptors. Brain Res Brain Res Rev 29:196–217

Miller PS, Smart TG (2010) Binding, activation and modulation of Cys-loop receptors. Trends Pharmacol Sci 31:161–174

Nikolaou S, Gasser RB (2006) Prospects for exploring molecular developmental processes in Haemonchus contortus. Int J Parasitol 36:859–868

Padgett CL, Hanek AP, Lester HA, Dougherty DA, Lummis SC (2007) Unnatural amino acid mutagenesis of the GABA(A) receptor binding site residues reveals a novel cation-pi interaction between GABA and beta 2Tyr97. J Neurosci 27:886–892

Parkinson J, Mitreva M, Whitton C, Thomson M, Daub J, Martin J, Schmid R, Hall N, Barrell B, Waterston RH, McCarter JP, Blaxter ML (2004) A transcriptomic analysis of the phylum Nematoda. Nat Genet 36:1259–1267

Polenzani L, Woodward RM, Miledi R (1991) Expression of mammalian gamma-aminobutyric acid receptors with distinct pharmacology in Xenopus oocytes. Proc Natl Acad Sci USA 88:4318–4322

Putrenko I, Zakikhani M, Dent JA (2005) A family of acetylcholine-gated chloride channel subunits in Caenorhabditis elegans. J Biol Chem 280:6392–6398

Qian H, Hyatt G, Schanzer A, Hazra R, Hackam AS, Cutting GR, Dowling JE (1997) A comparison of GABAC and rho subunit receptors from the white perch retina. Vis Neurosci 14:843–851

Ranganathan R, Cannon SC, Horvitz HR (2000) MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature 408:470–475

Rao VT, Siddiqui SZ, Prichard RK, Forrester SG (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

Rao VT, Accardi MV, Siddiqui SZ, Beech RN, Prichard RK, Forrester SG (2010) Characterization of a novel tyramine-gated chloride channel from Haemonchus contortus. Mol Biochem Parasitol 173:64–68

Ringstad N, Abe N, Horvitz HR (2009) Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 325:96–100

Ros-Moreno RM, Moreno-Guzman MJ, Jimenez-Gonzalez A, Rodriguez-Caabeiro F (1999) Interaction of ivermectin with gamma-aminobutyric acid receptors in Trichinella spiralis muscle larvae. Parasitol Res 85:320–323

Schuske K, Beg AA, Jorgensen EM (2004) The GABA nervous system in C. elegans. Trends Neurosci 27:407–414

Shimada S, Cutting G, Uhl GR (1992) Gamma-aminobutyric acid A or C receptor? Gamma-aminobutyric acid rho 1 receptor RNA induces bicuculline-, barbiturate-, and benzodiazepine-insensitive gamma-aminobutyric acid responses in Xenopus oocytes. Mol Pharmacol 41:683–687

Siddiqui SZ, Brown DD, Rao VT, Forrester SG (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

Sigel E, Baur R, Kellenberger S, Malherbe P (1992) Point mutations affecting antagonist affinity and agonist dependent gating of GABAA receptor channels. EMBO J 11:2017–2023

Skinner TM, Bascal ZA, Holden-Dye L, Lunt GG, Wolstenholme AJ (1998) Immunocytochemical localization of a putative inhibitory amino acid receptor subunit in the parasitic nematodes Haemonchus contortus and Ascaris suum. Parasitology 117(Pt 1):89–96

Thompson AJ, Lester HA, Lummis SC (2010) The structural basis of function in Cys-loop receptors. Q Rev Biophys 43:449–499

Walker RJ, Colquhoun L, Holden-Dye L (1992) Pharmacological profiles of the GABA and acetylcholine receptors from the nematode, Ascaris suum. Acta Biol Hung 43:59–68

Wardell B, Marik PS, Piper D, Rutar T, Jorgensen EM, Bamber BA (2006) Residues in the first transmembrane domain of the Caenorhabditis elegans GABA(A) receptor confer sensitivity to the neurosteroid pregnenolone sulfate. Br J Pharmacol 148:162–172

Watanabe I, Koike K, Satou T, Nikaido T (2000) Nematocidal activity of quassinoids against a species of Diplogastridae. Biol Pharm Bull 23:723–726

Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699

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

Wolstenholme AJ (2011) Ion channels and receptor as targets for the control of parasitic nematodes. Int J Parasitol Drug Drug Resist 1:2–13

Zhang HG, Lee HJ, Rocheleau T, Ffrench-Constant RH, Jackson MB (1995) Subunit composition determines picrotoxin and bicuculline sensitivity of Drosophila gamma-aminobutyric acid receptors. Mol Pharmacol 48:835–840