Characterization of cys-loop receptor genes involved in inhibitory amine neurotransmission in parasitic and free living nematodes

Parasitology International

Volumn 62, Issue 6, 2013, Pages 599-605

  Beech, Robin N ^b   Callanan, Micah K ^a   Rao, Vijayaraghava T S ^c   Dawe, George B ^d,e   Forrester, Sean G ^a  

^a UNIVERSITY OF ONTARIO INSTITUTE OF TECHNOLOGY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e McGill University Room 457   (Canada)

Author keywords

Bp; CDNA; LGCC; LGIC; NAChR; RACE; RT PCR; TM

Indexed keywords

ACETYLCHOLINE; AMINE; CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR; LIGAND; LIGAND GATED CHLORIDE CHANNEL; SEROTONIN; TRYPTOPHAN; COMPLEMENTARY DNA;

ARTICLE; BRUGIA MALAYI; CONVERGENT EVOLUTION; GENE ISOLATION; GENOME; HAEMONCHUS CONTORTUS; LIGAND BINDING; LOA LOA; NEMATODE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; TRICHINELLA SPIRALIS; WUCHERERIA BANCROFTI; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DNA SEQUENCE; FEMALE; GENETICS; HAEMONCHUS; LARVA; LOA; MALE; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

BRUGIA MALAYI; CAENORHABDITIS ELEGANS; HAEMONCHUS CONTORTUS; LOA LOA; NEMATODA; SCHISTOSOMA MANSONI; TREMATODA; TRICHINELLA SPIRALIS; WUCHERERIA BANCROFTI;

AMINO ACID SEQUENCE; ANIMALS; BRUGIA MALAYI; CYSTEINE LOOP LIGAND-GATED ION CHANNEL RECEPTORS; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; FEMALE; HAEMONCHUS; LARVA; LOA; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; WUCHERERIA BANCROFTI;

EID: 84885372028     PISSN: 13835769     EISSN: 18730329     Source Type: Journal    
DOI: 10.1016/j.parint.2013.03.010     Document Type: Article

References (44)

1. Rogers C.M., Franks C.J., Walker R.J., Burke J.F., Holden-Dye L. Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. Journal of Neurobiology 2001, 49:235-244.
2. Weinshenker D., Garriga G., Thomas J.H. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. Journal of Neuroscience 1995, 15:6975-6985.
3. Horvitz H.R., Chalfie M., Trent C., Sulston J.E., Evans P.D. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 1982, 216:1012-1014.
4. Sulston J., Dew M., Brenner S. Dopaminergic neurons in the nematode Caenorhabditis elegans. The Journal of Comparative Neurology 1975, 163:215-226.
5. Sawin E.R., Ranganathan R., Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619-631.
6. Komuniecki R., Law W.J., Jex A., Geldhof P., Gray J., Bamber B., et al. Monoaminergic signaling as a target for anthelmintic drug discovery: receptor conservation among the free-living and parasitic nematodes. Molecular and Biochemical Parasitology 2012, 183:1-7.
7. Rao V.T., Forrester S.G., Keller K., Prichard R.K. Localisation of serotonin and dopamine in Haemonchus contortus. International Journal of Parasitology 2011, 41:249-254.
8. Ranganathan R., Cannon S.C., Horvitz H.R. MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature 2000, 408:470-475.
9. Ringstad N., Abe N., Horvitz H.R. Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 2009, 325:96-100.
10. Rao V.T., Siddiqui S.Z., Prichard R.K., Forrester S.G. A dopamine-gated ion channel (HcGGR3*) from Haemonchus contortus is expressed in the cervical papillae and is associated with macrocyclic lactone resistance. Molecular and Biochemical Parasitology 2009, 166:54-61.
11. Rao V.T., Accardi M.V., Siddiqui S.Z., Beech R.N., Prichard R.K., Forrester S.G. Characterization of a novel tyramine-gated chloride channel from Haemonchus contortus. Molecular and Biochemical Parasitology 2010, 173:64-68.
12. Dent J.A. Evidence for a diverse cys-loop ligand-gated ion channel superfamily in early bilateria. Journal of Molecular Evolution 2006, 62:523-535.
13. Mu T.W., Lester H.A., Dougherty D.A. Different binding orientations for the same agonist at homologous receptors: a lock and key or a simple wedge?. Journal of the American Chemical Society 2003, 125:6850-6851.
14. Putrenko I., Zakikhani M., Dent J.A. A family of acetylcholine-gated chloride channel subunits in Caenorhabditis elegans. The Journal of Biological Chemistry 2005, 280:6392-6398.
15. Ranjan S., Wang G.T., Hirschlein C., Simkins K.L. Selection for resistance to macrocyclic lactones by Haemonchus contortus in sheep. Veterinary Parasitology 2002, 103:109-117.
16. Weston W.M., LeClair E.E., Trzyna W., McHugh K.M., Nugent P., Lafferty C.M., et al. Differential display identification of plunc, a novel gene expressed in embryonic palate, nasal epithelium, and adult lung. The Journal of Biological Chemistry 1999, 274:13698-13703.
17. Frohman M.A., Dush M.K., Martin G.R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:8998-9002.
18. Harris T.W., Antoshechkin I., Bieri T., Blasiar D., Chan J., Chen W.J., et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Research 2010, 38:D463-D467.
19. Broad Institute Filarial worms Sequencing Project, Broad Institute of Harvard and MIT. http://www.broadinstitute.org/.
20. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 2002, 30:3059-3066.
21. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systems Biology 2003, 52:696-704.
22. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 2007, 24:1586-1591.
23. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology 1993, 234:779-815.
24. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., et al. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003, 50:437-450.
25. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., et al. UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry 2004, 25:1605-1612.
26. Jones A.K., Sattelle D.B. The cys-loop ligand-gated ion channel gene superfamily of the nematode, Caenorhabditis elegans. Invert Neurosci 2008, 8:41-47.
27. Beech R.N., Wolstenholme A.J., Neveu C., Dent J.A. Nematode parasite genes: what's in a name?. Trends in Parasitology 2010, 26:334-340.
28. Williamsom S.M., Walsh T.K., Wolstenholme A.J. The cys-loop ligand-gated ion channel gene family of Brugia malayi and Trichinella spiralis: a comparison with Caenorhabditis elegans. Invertebrate Neuroscience 2007, 7:219-226.
29. Berriman M., Haas B.J., LoVerde P.T., Wilson R.A., Dillon G.P., Cerqueira G.C., et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358.
30. Jones A.K., Davis P., Hodgkin J., Sattelle D.B. The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: an update on nomenclature. Invertebrate Neuroscience 2007, 7:129-131.
31. Zhao H., Ru B., Teeling E.C., Faulkes C.G., Zhang S., Rossiter S.J. Rhodopsin molecular evolution in mammals inhabiting low light environments. PLoS One 2009, 4:e8326.
32. Liu Y., Han N., Franchini L.F., Xu H., Pisciottano F., Elgoyhen A.B., et al. The voltage-gated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats. Molecular Biology and Evolution 2012, 29:1441-1450.
33. Bocquet N., Nury H., Baaden M., Le Poupon C., Changeux J.P., Delarue M., et al. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 2009, 457:111-114.
34. Brejc K., van Dijk W.J., Klaassen R.V., Schuurmans M., van Der Oost J., Smit A.B., et al. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001, 411:269-276.
35. Hibbs R.E., Gouaux E. Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 2011, 474:54-60.
36. Dellisanti C.D., Yao Y., Stroud J.C., Wang Z.Z., Chen L. Crystal structure of the extracellular domain of nAChR alpha1 bound to alpha-bungarotoxin at 1.94 A resolution. Nature Neuroscience 2007, 10:953-962.
37. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. Journal of Molecular Biology 2005, 346:967-989.
38. Beene D.L., Price K.L., Lester H.A., Dougherty D.A., Lummis S.C. Tyrosine residues that control binding and gating in the 5-hydroxytryptamine3 receptor revealed by unnatural amino acid mutagenesis. Journal of Neuroscience 2004, 24:9097-9104.
39. Beene D.L., Brandt G.S., Zhong W., Zacharias N.M., Lester H.A., Dougherty D.A. Cation-pi interactions in ligand recognition by serotonergic (5-HT3A) and nicotinic acetylcholine receptors: the anomalous binding properties of nicotine. Biochemistry 2002, 41:10262-10269.
40. Blaxter M.L., De Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., et al. A molecular evolutionary framework for the phylum Nematoda. Nature 1998, 392:71-75.
41. Yang Z., Wong W.S., Nielsen R. Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution 2005, 22:1107-1118.
42. Zhang J., Nielsen R., Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution 2005, 22:2472-2479.
43. Hernando G., Berge I., Rayes D., Bouzat C. Contribution of subunits to Caenorhabditis elegans levamisole-sensitive nicotinic receptor function. Molecular Pharmacology 2012, 82:550-560.
44. Thompson A.J., Lester H.A., Lummis S.C.R. The structural basis of function of cys-loop receptor. Quarterly Review of Biophysics 2010, 43:449-499.