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Molecular cloning and in vitro expression of C. elegans and parasitic nematode ionotropic receptors

Published online by Cambridge University Press:  06 April 2009

J. T. Fleming ,
H. A. Baylis ,
D. B. Sattelle  and
J. A. Lewis
J. T. Fleming
Affiliation:
Massachusetts General Hospital Cancer Center, Building 149, 13th Street, Charlestown, MA 02129, USA
H. A. Baylis
Affiliation:
The Babraham Institute Laboratory of Molecular Signalling, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
D. B. Sattelle*
Affiliation:
The Babraham Institute Laboratory of Molecular Signalling, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
J. A. Lewis
Affiliation:
Division of Life Sciences, University of Texas at San Antonio, San Antonio, Texas 78249-0662, USA
*
*Corresponding author.
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Summary

The free living nematode, C. elegans is understood at a level of detail equalled by few other organisms, and much of the cell biology and sequence information is proving of considerable utility in the study of parasitic nematodes. Already, C. elegans provides a convenient vehicle for investigating anthelmintic drug action and resistance mechanisms. Among the ionotropic receptors, with their important roles in the behaviour and development of the organism, are targets for anthelmintics. The subunits of nicotinic acetylcholine receptors of C. elegans form a large and diverse multigene family. Members of this family are among the 11 genes associated with resistance to the anthelmintic drug levamisole.

Keywords

Caenorhabditis elegansionotropic receptorsacetylcholine receptorsanthelmintic drug targetsresistance mechanisms
Type
Research Article
Information
Parasitology , Volume 113 , supplement S1: Molecular biochemistry and physiology of helminth neuromuscular systems , January 1996 , pp. S175 - S190
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Abramson, S. N., Culver, P., Kline, T., Li, Y., Guest, P., Gutman, L., & Taylor, p. (1988). Lophotoxin and related coral toxins covalently label the α-subunit of the nicotinic acetylcholine receptor. Journal of Biological Chemistry 263, 18568–18573.CrossRefGoogle ScholarPubMed
Abramson, S. N., Li, Y., Culver, P. & Taylor, P. (1989). An analog of lophotoxin reacts covalently with tyr190 in the-α-subunit of the nicotinic acetylcholine receptor. Journal of Biological Chemistry 264, 12666–12672.CrossRefGoogle Scholar
Ajuh, P. & Egwang, T. (1994). Cloning of a cDNA encoding a putative nicotinic acetylcholine receptor subunit of the human filarial parasite Onchocerca volvulus. Gene 144, 127–129.CrossRefGoogle ScholarPubMed
Barnard, E. A. (1992). Receptor classes and neurotransmiter-gated ion channels. Trends in Biochemical Sciences 17, 368–374.Google Scholar
Bai, D., Abramson, S. N. & Sattelle, D. B. (1993). Actions of a coral toxin analogue (Bipinnatin-B) on an insect nicotinic acetylcholine receptor. Archives of Insect Biochemistry and Physiology 23, 155–159.Google Scholar
Ballivet, M., Alliod, C., Bertrand, S. & Bertrand, D. (1996). Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. Journal of Molecular Biology 258, 261–269.CrossRefGoogle ScholarPubMed
Berridge, M. J. (1993). Inositol trisphosphate and calcium signalling. Nature 361, 315–325.CrossRefGoogle ScholarPubMed
Birchall, P. S., Fishpool, R. M. & Albertson, D. G. (1995). Expression patterns of predicted genes from the C. elegans genome sequence visualized by FISH in whole organisms. Nature Genetics 11, 314–320.Google Scholar
Bossy, B., Ballivet, M. & Spierer, P. (1988). Conservation of neuronal nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EMBO Journal, 7 611–618.CrossRefGoogle ScholarPubMed
Brenner, s. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71–94.CrossRefGoogle ScholarPubMed
Campbell, W. C., Fisher, M. H., Stapley, E. O., Albersschonberg, G. & Jacob, T. A. (1983). Ivermectin: a potent new antiparasitic agent. Science 221, 823–828.Google Scholar
Chalfie, M. & White, J. (1988). The nervous system. In The Nematode Caenorhabditis elegans (ed. Wood, W. B.), pp. 337–392. Cold Spring Harbor Laboratory, New York: Cold Spring Harbor Laboratory Press.Google Scholar
Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. & Prasher, D. c. (1994). Green fluorescent protein as a marker for gene expression Science 263, 802–805.CrossRefGoogle ScholarPubMed
Colquhoun, L., Holden-Dye, L., & Walker, R. J. (1991). The pharmacology of cholinoceptors on the somatic muscle cells of the parasitic nematode Ascaris suum. Journal of Experimental Biology 158, 509–530.CrossRefGoogle ScholarPubMed
Colquhoun, L., Holden-Dye, L., & Walker, R. J. (1993). The action of nicotinic receptor specific toxins on the somatic muscle cells of the parasitic nematode Ascaris suum. Molecular Neuropharmacology 3, 11–16.Google Scholar
Coulson, A., Sulston, J., Brenner, S. & Karn, J. (1986). Towards a physical map of the genome of the nematode Caenorhabditis elegans. Proceedings of the National Academy of Science, USA 83, 7821–7825.CrossRefGoogle Scholar
Cully, D. F. & Paress, P. s. (1991). Solubilization and characterization of a high-affinity ivermectin binding site from Caenorhabditis elegans. Molecular Pharmacology 40, 326–332.Google Scholar
Cully, D. F., Vassilatis, D. K., Liu, K. K., Paress, P. S., Van Der Ploeg, L. H. T., Schaeffer, J. M. & Arena, J. P. (1994). Cloning of an avermectin-sensitive glutamategated chloride channel from Caenorhabditis elegans. Nature 371, 707–711.CrossRefGoogle ScholarPubMed
Devillers-Thiery, A., Galzi, J. L.Eisele, J. L.Bertrand, s., Bertrand, D. & Changeux, J. p. (1993). Functional architecture of the nicotinic acetylcholine receptor: a prototype of ligand-gated ion channels. Journal of Membrane Biology 136, 97–112.CrossRefGoogle ScholarPubMed
Donelson, J. E., Duke, B. O. L., Moser, D., Zeng, W., Erondu, N. E.Lucius, R., Renz, A., Kjaram, M. & Flores, G. z. (1988). Construction of Onchocerca volvulus cDNA libraries and partial characterization of the cDNA for a major antigen. Molecular and Biochemical Parasitology 31, 241–250.Google Scholar
Edgley, M. L., Baillie, D. L., Riddle, D. L., & Rose, A. M. (1995). Genetic balancer. In Methods in Cell Biology. Caenorhabditis elegans: Modern Biological Analysis of an Organism, Vol. 48 (ed. Epstein, H. F. & Shakes, D. C.), pp. 147–184. San Diego: Academic Press.Google Scholar
Epstein, H. F. & Shakes, D. c. (EDS). (1995). Methods in Cell Biology. Caenorhabditis elegans: Modern Biological Analysis of an Organism, Vol. 48, pp. 1–654. San Diego: Academic Press.Google Scholar
Fire, A., Albertson, D., Harrison, S. W. & Moerman, D. G. (1991). Production of antisense RNA leads to effective and specific inhibition of gene expression in C. elegans muscle. Development 113, 503–514.Google Scholar
Fire, A., Harrison, s. w. & Dixon, D. (1990). A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189–198.Google Scholar
Fleming, J. T., Riina, H. A., & Sattelle, D. B. (1991). Acetylcholine and GABA receptors of Caenorhabditis elegans expressed in Xenopus oocytes. Journal of Physiology {London) 438, 371p.Google Scholar
Fleming, J. T., Tornøe, C., Riina, H. A., Coadwell, J., Lewis, J. A. & Sattelle, D. B. (1993). Acetylcholine receptor molecules of the nematode Caenorhabditis elegans. In Comparative Molecular Neurobiology (ed. Pichon, Y.), pp. 65–80. Birkhauser Verlag, Basel, Switzerland.CrossRefGoogle Scholar
Furuichi, T., Kohda, K., Miyawaki, A. & Mikoshiba, K. (1994). Intracellular channels. Current Opinion in Neurobiology 4, 294–303.CrossRefGoogle ScholarPubMed
Gundelfinger, E. D. (1992). How complex is the nicotinic receptor system of insects? Trends in Neurosciences 15, 206–211.CrossRefGoogle ScholarPubMed
Harrow, i. D. & Gration, K. A. F. (1985). Mode of action of the anthelmintics morantel, pyrantel and levamisole on muscle cell membrane of the nematode Ascaris suum. Pestic. Sci. 16, 662–672.Google Scholar
Hart, A. c., Sims, S. & Kaplan, J. M. (1995). Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378, 82–85.Google Scholar
Hermans-Borgmeyer, I., Zopf, D., Ryseck, R-P., Hovemann, B., Betz, H. & Gundelfinger, E. D. (1986). Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. EMBO Journal 5, 1503–1508.Google Scholar
Hodgkin, J., Plasterk, R. H. A. & Waterston, R. H. (1995). The nematode Caenorhabditis elegans and its genome. Science 270, 410–14.CrossRefGoogle ScholarPubMed
Johnsen, R. c. & Baillie, D. L. (1991). Genetic analysis of a major segment [LGV(left)] of the genome of Caenorhabditis elegans. Genetics 129, 735–752.Google Scholar
Kao, p. N. & Karlin, A. (1986). Acetylcholine receptor binding site contains a disulfide crosslink between adjacent half-cystinyl residues. Journal of Biological Chemistry 261, 8085–8088.CrossRefGoogle ScholarPubMed
Karlin, A. (1993). Structure of nicotinic acetylcholine receptors. Current Opinions in Neurobiology 3, 299–309.CrossRefGoogle ScholarPubMed
Karlin, A. & Akabas, M. H. (1995). Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15, 1231–1244.Google Scholar
Kim, Y-K., Valdivia, H. H., Maryon, E. B., Anderson, P. & Coronado, R. (1992). High molecular weight proteins in the nematode C. elegans bind [3H]ryanodine and form a large conductance channel. Biophysical Journal 63, 1379–1384.CrossRefGoogle Scholar
Laughton, D. L., Amar, M., Thomas, P., Towner, P., Harris, P., Lunt, G. G. & Wolstenholme, A. J. (1994). Cloning of a putative inhibitory amino acid receptor subunit from the parasitic nematode Haemonchus contortus. Receptors & Channels 2, 155–163.Google ScholarPubMed
Laughton, D. L., Wheeler, S. V., Lunt, G. G. & Wolstenholme, A. J. (1995). The 6-subunit of Caenorhabditis elegans avermectin receptor responds to glycine and is encoded by chromosome I. Journal of Neurochemistry 64, 2354–2357.Google Scholar
Lewis, J. A., Elmer, J. S., Skimming, J., Mclafferty, S., Fleming, J. & Mcgee, T. (1987a). Cholinergic receptor mutants of the nematode Caenorhabditis elegans. Journal of Neuroscience 7, 3059–3071.CrossRefGoogle ScholarPubMed
Lewis, J. A., Fleming, J. T., Mclafferty, S., Murphy, J. & Wu, c. (1987b). The levamisole receptor, a cholinergic receptor of the nematode Caenorhabditis elegans. Molecular Pharmacology 31, 185–193.Google Scholar
Lewis, J. A., Wu, C.-H., Berg, H. & Levine, J. H. (1980a). The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95, 905–928.Google Scholar
Lewis, J. A., Wu, C.-H., Levine, J. H. & Berg, H. (1980b). Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience 5, 967–989.Google Scholar
Maricq, A. V., Peckol, E., Driscoll, M. & Bargmann, c. I. (1995). Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378, 78–81.Google Scholar
Marshall, J., Buckingham, S. D., Shingai, R., Lunt, G. G., Goosey, M. W., Darlison, M. G., Sattelle, D. B. & Barnard, E. A. (1990). Sequence and functional expression of a single a. subunit of an insect nicotinic acetylcholine receptor. EMBO Journal 9, 4391–398.Google Scholar
Mccombie, W. R., Adams, M. D., Kelley, J. M., Fitzgerald, M. G., Utterback, T. R., Khan, M., Dubnick, M., Kerlavage, A. R., Venter, J. C. & Fields, c. (1992). Caenorhabditis elegans expressed sequence tags identify gene families and potential disease gene homologues. Nature Genetics 1, 124–131.Google Scholar
Mcintire, S. L., Jorgensen, E. & Horvitz, H. R. (1993a). Genes required for GABA function in Caenorhabditis elegans. Nature 364, 334–337.Google Scholar
Mcintire, S. L., Jorgensen, E., Kaplan, J. & Horvitz, H. R. (1993a). The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337–341.Google Scholar
Mckim, K. s., Starr, T. & Rose, A. M. (1992). Genetic and molecular analysis of the dpy-14 region in Caenorhabditis elegans. Molecular & General Genetics 233, 241–251.Google Scholar
Nakai, J., Imagawa, T., Hakamata, Y., Shigekawa, M., Takeshima, H. & Numa, s. (1990). Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel. FEBS Letters 271, 169–177.Google Scholar
Rushforth, A. M., Saari, B., & Anderson, p. (1993). Siteselected insertion of the transposon Tel into a Caenorhabditis elegans myosin light chain gene. Molecular & Cellular Biology 13, 902–910.Google Scholar
Sakube, Y., Ando, H. & Kagawa, H. (1993). Cloning and mapping of a ryanodine receptor homolog gene of Caenorhabditis elegans. Annals of the New York Academy of Science 707, 540–545.Google Scholar
Sargent, p. B. (1993). The diversity of neural nicotinic acetylcholine receptors. Annual Review of Neuroscience 16, 403–443.Google Scholar
Sattelle, D. B. (1990). GABA receptors of insects. Advances in Insect Physiology 22, 1–113.CrossRefGoogle Scholar
Sattelle, D. B. (1992). Receptors for L-glutamate and GABA in the nervous system of an insect Periplaneta americana. Comparative Biochemistry & Physiology 103C, 429–438.Google Scholar
Sattelle, D. B., Lummis, S. C. R., Riina, H. A., Fleming, J. T.Anthony, N. M. & Marshall, J. (1992). Functional expression in Xenopus oocytes of invertebrate ligand-gated ion channels. In Neurotox 91: Molecular basis of drug and pesticide action (ed. Duce, I. R.), pp. 203–219. London: Elsevier Applied Science.CrossRefGoogle Scholar
Sattelle, D. B., Marshall, J., Lummis, S. C. R., Leech, C. A., Miller, K. W. P., Anthony, N. M. A., Bai, D., Wafford, K. A., Harrison, J. B., Chapaitis, L. A., Watson, M. K., Benner, E. A., Vassallo, J. G., Wong, J. F. H. & Rauh, J. J. (1991). γ-Aminobutyric acid and L-glutamate receptors of insect nervous tissues. In Transmitter Amino Acid Receptors, Structures, Transduction and Models for Drug Development (eds. Barnard, E. A. & Costa, E.) Fidia Research Foundation Symposium Series Vol. 6, pp. 273–291. New York, Thieme Medical Publishers.Google Scholar
Schuster, C. M., Ultsch, A., Schmitt, B. & Betz, H. (1993). Molecular analysis of Drosophila glutamate receptors In Comparative Molecular Neurobiology (ed. Pichon, Y.), pp. 234–249. Basel: Birkhauser-VerlagGoogle Scholar
Squire, M. D., Tornøe, C., Baylis, H. A., Fleming, J. T., Barnard, E. A. & Sattelle, D. B. (1995). Molecular cloning and functional co-expression of a Caenorhabditis elegans nicotinic acetylcholine receptor (acr-2). Receptors & Channels 3, 107–115.Google Scholar
Strader, C. D., Fong, T. M., Tota, M. R. & Underwood, D. (1994). Structure and function of G protein-coupled receptors. Annual Review of Biochemistry 63, 101–132.Google Scholar
Sulston, J., Du, Z., Thomas, K., Wilson, R., Hillier, L., Staden, R., Hallorhan, N., Green, P., Thierry-Mieg, J., Qui, L., Dear, S., Coulson, A., Craxton, M., Durbin, R., Berks, M., Metzstein, M., Hawkins, T., Ainscough, R. & Waterston, R., (1992). The C. elegans genome sequencing project: a beginning. Nature 356, 37–41.CrossRefGoogle Scholar
Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.Google Scholar
Takeshima, H., Nishimura, J., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T. & Numa, s. (1989). Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339, 439–45.Google Scholar
Tornøe, C., Bai, D., Holden-DYE, L., Abramson, S. N. & Sattelle, D. B. (1995). Actions of neurotoxins (bungarotoxins, neosurugatoxin and lophotoxins) on insect and nematode nicotinic acetylcholine receptors. Toxicon 33, 411–24.CrossRefGoogle ScholarPubMed
Tornøe, C., Holden-Dye, L., Bai, D., Abramson, S. N. & Sattelle, D. B. (1994). A nematode nicotinic acetylcholine receptor displays insensitivity to lophotoxin analogue Bipinnatin B. Physiology 480, 96P.Google Scholar
Tornøe, C., Holden-DYE, L., Garland, C., Abramson, S. N., Fleming, J. T. & Sattelle, D. B. (1996) Lophotoxin-insensitive nematode nicotinic acetylcholine receptors. Journal of Experimental Biology 199 (in press).CrossRefGoogle ScholarPubMed
Treinin, M. & Chalfie, M. (1995). A mutated acetylcholine receptor subunit causes neuronal degeneration in C. elegans. Neuron 14, 871–877.CrossRefGoogle ScholarPubMed
Unwin, N. (1993a) Neurotransmitter action: opening of ligand-gated ion channels. Cell 72 Neuron 10 (Suppl.), 31–41.Google Scholar
Unwin, N. (1993b). Nicotinic acetylcholine receptor at 9 A resolution. Journal of Molecular Biology 299, 1101–1124.Google Scholar
Unwin, N. (1995). Acetylcholine receptor channel imaged in the open state. Nature 373, 37–43.Google Scholar
Waterston, R., Martin, C., Craxton, M., Hyunh, C., Coulson, A., Hillier, L., Durbin, R., Green, P., Shownkeen, R., Hallorhan, N., Metzstein, M., Hawkins, T., Wilson, R., Berks, M., Du, Z., Thomas, K., Thierry-Mieg, J. & Sulston, J. (1992). A survey of expressed genes in Caenorhabditis elegans. Nature Genetics 1, 114–123.Google Scholar
White, J. G., Southgate, E., Thompson, J. N. & Brenner, s. (1986). The structure of the nervous system of Caenorhabditis elegans. PhilosophicalTransactions of the Royal Society of London B. (Biological Sciences) 314, 1–340.Google Scholar
Zwaal, R. R., Broeks, A., Van Meurs, J., Groenen, J. T. & Plasterk, R. H. (1993). Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proceedings of the National Academy of Sciences, USA 90, 7431–7435.Google Scholar