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Classical transmitters and their receptors in flatworms

Published online by Cambridge University Press:  29 March 2006

P. RIBEIRO
Affiliation:
Institute of Parasitology, McGill University, Macdonald Campus, 21,111 Lakeshore Road, Ste. Anne de Bellevue Quebec, Canada H9X 3V9.
F. EL-SHEHABI
Affiliation:
Institute of Parasitology, McGill University, Macdonald Campus, 21,111 Lakeshore Road, Ste. Anne de Bellevue Quebec, Canada H9X 3V9.
N. PATOCKA
Affiliation:
Institute of Parasitology, McGill University, Macdonald Campus, 21,111 Lakeshore Road, Ste. Anne de Bellevue Quebec, Canada H9X 3V9.

Abstract

The flatworm nervous system employs a wide repertoire of neuroactive substances, including small chemical messengers, the so called classical transmitters, and several types of neuropeptides. A large body of research accumulated over four decades has provided a wealth of information on the tissue localization and effects of these substances, their biochemistry and, recently, their molecular modes of action in all major classes of flatworms. This evidence will be reviewed, with particular emphasis on the small (classical) transmitters and the receptors that mediate their effects. One of the themes that will emerge from this discussion is that classical transmitters regulate core activities such as movement, metabolism and transport, and thus are essential for survival of the organism. In addition, the evidence shows that flatworms have multiple neurotransmitter receptors, many with unusual pharmacological features, which make them particularly attractive as drug targets. Understanding the molecular basis of these distinctive properties, and developing new, more specific receptor agonists and antagonists will undoubtedly become a major challenge in future research.

Type
Research Article
Copyright
2005 Cambridge University Press

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References

REFERENCES

ABD EL-RAZEK, M. A. & WEBB, R. A. ( 1997). Transport of exogenous 5-hydroxytryptamine across the outer plasma membrane of the syncytial tegument of Hymenolepis diminuta is by simple diffusion. Canadian Journal of Zoology 75, 16051617.CrossRefGoogle Scholar
BARKER, L. R., BUEDING, E. & TIMMS, A. R ( 1966). The possible role of acetylcholine in Schistosoma mansoni. British Journal of Pharmacology 26, 656665.CrossRefGoogle Scholar
BENNETT, J. L. & BUEDING, E. ( 1973). Uptake of 5-hydroxytryptamine in Schistosoma mansoni. Molecular Pharmacology 9, 311319.Google Scholar
BENNETT, J. L. & GIANUTSOS, G. ( 1977). Distribution of catecholamines in immature Fasciola hepatica: a histochemical and biochemical study. International Journal for Parasitology 7, 221225.CrossRefGoogle Scholar
BENTLEY, G. N., JONES, A. K., PARRA, W. G. O. & AGNEW, A. ( 2004). ShAR1 alpha and ShAR1 beta: novel putative nicotinic acetylcholine receptor subunits from the platyhelminth blood fluke Schistosoma. Gene 329, 2738.Google Scholar
BLAIR, K. L. & ANDERSON, P. A. V. ( 1994). Physiological and pharmacological properties of muscle cells isolated from the flatworm Bdelloura candida (Tricladia). Parasitology 109, 325335.CrossRefGoogle Scholar
BLAIR, K. L., DAY, T. A., LEWIS, M. C., BENNETT, J. L. & PAX, R. A. ( 1991). Studies on muscle cells isolated from Schistosoma mansoni: A Ca2+-dependent K+ channel. Parasitology 102, 251258.CrossRefGoogle Scholar
BOESS, F. G. & MARTIN, I. L. ( 1994). Molecular biology of 5HT receptors. Neuropharmacology 33, 275317.CrossRefGoogle Scholar
BOYLE, J. P., HILLYER, J. F. & YOSHINO, T. P. ( 2003). Pharmacological and autoradiographical studies of serotonin transporter-like activity in sporocysts of the human blood fluke, Schistosoma mansoni. Journal of Comparative Physiology A 189, 631641.CrossRefGoogle Scholar
BOYLE, J. P. & YOSHINO, T. P. ( 2003). Gene manipulation in parasitic helminths. International Journal for Parasitology 33, 12591268.CrossRefGoogle Scholar
BOYLE, J. P., ZAIDE, J. V. & YOSHINO, T. ( 2000). Schistosoma mansoni: effects of serotonin and serotonin receptor antagonists on motility and length of primary sporocysts in vitro. Experimental Parasitology 94, 217226.CrossRefGoogle Scholar
BROWNLEE, D. J. A. & FAIRWEATHER, I. ( 1996). Immunocytochemical localization of glutamate-like immunoreactivity within the nervous system of the cestode, Mesocestoides corti and the trematode, Fasciola hepatica. Parasitology Research 82, 423427.CrossRefGoogle Scholar
BUTTARELLI, F. R., PONTIERI, F. E., MARGOTTA, V. & PALLADINI, G. ( 2000). Acetylcholine/dopamine interaction in planaria. Comparative Biochemistry and Physiology C 125, 225231.CrossRefGoogle Scholar
CAMACHO, M. & AGNEW, A. ( 1995). Schistosoma: rate of glucose transport is altered by acetylcholine interaction with tegumental acetylcholine receptors and acetylcholinesterase. Experimental Parasitology 81, 584591.CrossRefGoogle Scholar
CAMACHO, M., ALSFORD, S., JONES, A. & AGNEW, A. ( 1995). Nicotinic acetylcholine receptors on the surface of the blood fluke Schistosoma. Molecular and Biochemical Parasitology 71, 127134.CrossRefGoogle Scholar
CAPENER, C. E., KIM, H. J., ARINAMINPATHY, Y. & SANSOM, S. P. ( 2002). Ion channels: Structural bioinformatics and modelling. Human Molecular Genetics 11, 24252433.CrossRefGoogle Scholar
CARONTI, B., MARGOTTA, V., MERANTE, A., PONTERI, F. E. & PALLADINI, G. ( 1999). Treatment with 6-hydroxydopamine in planaria (Dugesia gonocephala s.l.) morphological and behavioural study. Comparative Biochemistry and Physiology Part C 123, 201207.Google Scholar
CATTO, B. A., LEWIS, F. A. & OTTESEN, E. A. ( 1980). Cercaria-induced histamine release: a factor in the pathogenesis of schistosome dermatitis? American Journal of Tropical Medicine and Hygiene 29, 886889.Google Scholar
CATTO, B. A. & OTTENSEN, E. A. ( 1979). Serotonin uptake in schistosomules of Schistosoma mansoni. Comparative Biochemistry and Physiology 63C, 235242.CrossRefGoogle Scholar
CEBRIA, F., KUDOME, T., NAKAZAWA, M., MINETA, K., IKEO, K., GOJOBORI, T. & AGATA, K. ( 2002). The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mechanisms of Development 116, 199204.CrossRefGoogle Scholar
CHOU, T.-C. T., BENNETT, J. L. & BUEDING, E. ( 1972). Occurrence and concentrations of biogenic amines in trematodes. Journal of Parasitology 58, 10981102.CrossRefGoogle Scholar
COWARD, P., CHAN, S. D. H., WADA, H. G., HUMPHRIES, G. M. & CONKLIN, B. R. ( 1999). Chimeric G proteins allow a high-throughput signaling assay of Gi-coupled receptors. Analytical Biochemistry 270, 242248.CrossRefGoogle Scholar
CYR, D., GRUNER, S. & METTRICK, D. F. ( 1983). Hymenolepis diminuta: Uptake of 5-hydroxytryptamine (serotonin), glucose and changes in worm glycogen levels. Canadian Journal of Zoology 61, 14691474.CrossRefGoogle Scholar
DAVIS, R. & STRETTON, A. O. W. ( 1995). Neurotransmitters of helminths. In Biochemistry and Molecular Biology of Parasites ( ed. Marr, J. J. and Muller, M.), pp. 257287. Academic Press, London.CrossRef
DAVIS, R. E., PARRA, A., LOVERDE, P. T., RIBEIRO, E., GLORIOSO, G. & HODGSON, S. ( 1999). Transient expression of DNA and RNA in parasitic helminths using particle bombardment. Proceedings of the National Academy of Sciences, USA 96, 86878692.CrossRefGoogle Scholar
DAY, T. A., BENNETT, J. L. & PAX, R. A. ( 1994). Serotonin and its requirement for maintenance of contractility in muscle fibers isolated from Schistosoma mansoni. Parasitology 108, 425432.CrossRefGoogle Scholar
DAY, T. A., CHEN, G.-Z., MILLER, C., TIAN, M., BENNETT, J. L. & PAX, R. A. ( 1996). Cholinergic inhibition of muscle fibers isolated from Schistosoma mansoni (Trematoda: Digenea). Parasitology 113, 5561.CrossRefGoogle Scholar
DUROCHER, Y., PERRET, S., THIBAUDEAU, E., GAUMOND, M. H., KAMEN, A., STOCCO, R. & ABRAMOVITZ, M. ( 2000). A reporter gene assay for high-throughput screening of G-protein-coupled receptors stably or transiently expressed in HEK293 EBNA cells grown in suspension culture. Analytical Biochemistry 284, 316326.CrossRefGoogle Scholar
ERCOLI, N., PAYARES, G. & NUNEZ, D. ( 1985). Schistosoma mansoni: Neurotransmitters and the mobility of cercaria and schistosomules. Experimental Parasitology 59, 204216.CrossRefGoogle Scholar
ERIKSSON, K., PANULA, P. & REUTER, M. ( 1995 a). GABA in the nervous system of the planarian Polycelis nigra. Hydrobiologia 305, 285289.Google Scholar
ERIKSSON, K. S., JOHNSTON, R. N., SHAW, C., HALTON, D. W. & PANULA, P. A. J. ( 1996). Widespread distribution of histamine in the nervous system of a trematode flatworm. Journal of Comparative Neurology 373, 220227.3.0.CO;2-5>CrossRefGoogle Scholar
ERIKSSON, K. S., MAULE, A. G., HALTON, D. W., PANULA, P. A. J. & SHAW, C. ( 1995 b). GABA in the nervous system of parasitic flatworms. Parasitology 110, 339346.Google Scholar
ERIKSSON, K. S. & PANULA, P. ( 1994). Gamma-aminobutyric acid in the nervous system of a planarian. Journal of Comparative Neurology 345, 528536.CrossRefGoogle Scholar
FAIRWEATHER, I., MAULE, A. G., MITCHELL, S. H., JOHNSTON, C. F. & HALTON, D. W. ( 1987). Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology Research 73, 255258.CrossRefGoogle Scholar
FALCONE, F. H., DAHINDEN, C. A., GIBBS, B. F., NOLL, T., AMON, U., HEBESTREIT, H., ABRAHAMSEN, O., KLAUCKE, J., SCHLAAK, M. & HAAS, H. ( 1996). Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. European Journal of Immunology 26, 11471155.CrossRefGoogle Scholar
FITCH, R. W., XIAO, Y., KELLAR, K. J. & DALY, J. W. ( 2003). Membrane potential fluorescence: A rapid and highly sensitive assay for nicotinic receptor channel function. Proceedings of the National Academy of Sciences, USA 100, 49094914.CrossRefGoogle Scholar
FRANQUINET, R., LE MOIGNE, A. & HANOUNE, J. ( 1978). The adenylate cyclase system of planaria Polycelis tenuis: Activation by serotonin and guanine nucleotides. Biochimica et Biophysica Acta 539, 8897.CrossRefGoogle Scholar
GIANUTSOS, G. & BENNETT, J. L. ( 1977). The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Comparative Biochemistry and Physiology 58C, 157159.CrossRefGoogle Scholar
GUSTAFSSON, M. K. S. ( 1987). Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitology Research 74, 168174.CrossRefGoogle Scholar
GUSTAFSSON, M. K. S. & ERIKSSON, K. ( 1991). Localization and identification of catecholamines in the nervous system of Diphyllobothrium dendriticum (Cestoda). Parasitology Research 77, 498502.CrossRefGoogle Scholar
GUSTAFSSON, M. K. S., LINDHOLM, A. M., TERENINA, N. & REUTER, M. ( 1996). NO nerves in a tapeworm! NADPDH diaphorase histochemistry in adult Hymenolepis diminuta. Parasitology 113, 559565.CrossRefGoogle Scholar
GUSTAFSSON, M. K. S., TERENINA, N. B., KRESHCHENKO, N. D., REUTER, M., MAULE, A. G. & HALTON, D. W. ( 2001). Comparative study of the spatial relationship between nicotinamide adenine dinucleotide phosphate-diaphorase activity, serotonin immunoreactivity, and GYIRFamide immunoreactivity and the musculature of the adult liver fluke, Fasciola hepatica. Journal of Comparative Neurology 429, 7179.3.0.CO;2-M>CrossRefGoogle Scholar
GUSTAFSSON, M. K. S., WIKGREN, M. C., KARHI, T. J. & SCHOT, L. P. C. ( 1987). Immunocytochemical demonstration of neuropeptides and serotonin in the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 240, 255260.Google Scholar
HALTON, D. W. ( 1967). Histochemical studies of carboxylic esterase activity in Fasciola hepatica. Journal of Parasitology 53, 12101216.CrossRefGoogle Scholar
HALTON, D. W. ( 2004). Microscopy and the helminth parasite. Micron 35, 361390.CrossRefGoogle Scholar
HALTON, D. W. & GUSTAFSSON, M. K. S. ( 1996). Functional morphology of the platyhelminth nervous system. Parasitology 113, S47S72.CrossRefGoogle Scholar
HALTON, D. W. & MAULE, A. G. ( 2004). Flatworm nerve-muscle: structural and functional analysis. Canadian Journal of Zoology 82, 316333.CrossRefGoogle Scholar
HAMDAN, F., ABRAMOVITZ, M., MOUSA, A., XIE, J., DUROCHER, Y. & RIBEIRO, P. ( 2002 a). A novel Schistosoma mansoni G protein-coupled receptor is responsive to histamine. Molecular and Biochemical Parasitology 119, 7586.Google Scholar
HAMDAN, F., MOUSA, A. & RIBEIRO, P. ( 2002 b). Codon-optimization improves heterologous expression of a Schistosoma mansoni cDNA in HEK293 cells. Parasitology Research 88, 583586.Google Scholar
HAMDAN, F. & RIBEIRO, P. ( 1998). Cloning, functional expression and characterization of a novel form of tyrosine hydroxylase from the human parasite, Schistosoma manson. Journal of Neurochemistry 71, 13691380.Google Scholar
HAMDAN, F. & RIBEIRO, P. ( 1999). Characterization of a stable form of tryptophan hydroxylase from the human parasite, Schistosoma mansoni. Journal of Biological Chemistry 274, 2174621754.CrossRefGoogle Scholar
HAMDAN, F., UNGRIN, M., ABRAMOVITZ, M. & RIBEIRO, P. ( 1999). Characterization of a novel serotonin receptor from Caenorhabditis elegans: Cloning and functional expression of two splice variants. Journal of Neurochemistry 72, 13721383.CrossRefGoogle Scholar
HILLMAN, G. R. & SENFT, A. W. ( 1973). Schistosome motility measurements: response to drugs. Journal of Pharmacological and Experimental Therapeutics 185, 177184.Google Scholar
HOLMES, S. D. & FAIRWEATHER, I. ( 1984). Fasciola hepatica: The effects of neuropharmacological agents upon in vitro motility. Experimental Parasitology 58, 194208.CrossRefGoogle Scholar
HU, W., YAN, Q., SHEN, D. K., LIU, F., ZHU, Z. D., SONG, H. D., XU, X. R., WANG, Z. J., RONG, Y. P., ZENG, L. C., WU, J., ZHANG, X., WANG, J. J., XU, X. N., WANG, S. Y., FU, G., ZHANG, X. L., WANG, Z. Q., BRINDLEY, P. J., MCMANUS, D. P., XUE, C. L., FENG, Z., CHEN, Z. & HAN, Z. G. ( 2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139147.CrossRefGoogle Scholar
JENSEN, A. A. & KRISTIANSEN, U. ( 2004). Functional characterization of the human α1 glycine receptor in a fluorescence-based membrane potential assay. Biochemical Pharmacology 67, 17891799.CrossRefGoogle Scholar
JOFFE, B. I. & KOTIKOVA, E. A. ( 1991). Distribution of catecholamines in turbellarians. In Simpler Nervous Systems. Studies in Neuroscience 13 ( ed. Sakharov, D. A. and Winlow, W.), pp. 77112. Manchester University Press, Manchester, UK.
JONES, A. K., BENTLEY, G. N., PARRA, W. G. O. & AGNEW, A. ( 2002). Molecular acetylcholinesterase in the regulation of glucose scavenging. FASEB Journal 16, 5169.Google Scholar
JONES, A. K. & SATTELLE, D. B. ( 2003). Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. BioEssays 26, 3949.Google Scholar
KARLIN, A. ( 2002). Emerging structure of the nicotinic acetylcholine receptors. Nature Reviews (Neuroscience) 3, 102114.CrossRefGoogle Scholar
KAUFMAN, S. & RIBEIRO, P. ( 1996). Properties of the Neuronal Aromatic Amino Acid Hydroxylases. In Encyclopedia of Molecular Biology and Molecular Medicine (ed. Meyers, R. A.), pp. 207220. VCH Publishers, Inc., Weinheim, Germany.
KEENAN, L. & KOOPOWITZ, H. ( 1982). Physiology and in situ identification of putative aminergic transmitters in the nervous system of Gyrocotyle fimbriata, a parasitic flatworm. Journal of Neurobiology 13, 921.CrossRefGoogle Scholar
KEENAN, L., KOOPOWITZ, H. & BERNARDO, K. ( 1979). Primitive nervous systems: action of aminergic drugs and blocking agents on activity in the ventral nerve cord of the flatworm Notoplana acticola. Journal of Neurobiology 10, 397407.CrossRefGoogle Scholar
KEHOE, J. & MCINTOSH, J. M. ( 1998). Two distinct nicotinic receptors, one pharmacologically similar to the vertebrate alpha7-containing receptor, mediate Cl currents in Aplysia neurons. Journal of Neuroscience 18, 81988213.Google Scholar
KLEIN, C., PAUL, J., SAUVE, K., SCHMIDT, M., ARCANGELI, L., RANSOM, J., TRUEHEART, J., MANFREDI, J., BROACH, J. & MURPHY, A. ( 1998). Identification of surrogate agonists for the human FPRL-1 receptor by autocrine selection in yeast. Nature Biotechnology 16, 13341337.CrossRefGoogle Scholar
KOHN, A. B., MOROZ, L. L., LEA, J. M. & GREENBERG, R. M. ( 2001). Distribution of nitric oxide synthase immunoreactivity in the nervous system and peripheral tissues of Schistosoma mansoni. Parasitology 122, 8792.CrossRefGoogle Scholar
KOMUNIECKI, R. W., HOBSON, R. J., REX, E. B., HAPIAK, V. M. & KOMUNIECKI, P. R. ( 2004). Biogenic amine receptors in parasitic nematodes: what can be learned from Caenorhabditis elegans? Molecular and Biochemical Parasitology 137, 111.Google Scholar
KUBIAK, T., LARSEN, M., NULF, S., ZANTELLO, M., BURTON, K., BOWMAN, J., MODRIC, T. & LOWERY, D. ( 2003). Differential activation of “social and solitary” variants of the Caenorhabditis elegans G protein-coupled receptor NPR-1 by its cognate ligand AF9. Journal of Biological Chemistry 278, 3372433729.CrossRefGoogle Scholar
LEURS, R., SMIT, M. J. & TIMMERMAN, H. ( 1995). Molecular pharmacological aspects of histamine receptors. Pharmacology and Therapeutics 66, 413463.CrossRefGoogle Scholar
LIN, S. H. S. & CIVELLI, O. ( 2004). Orphan G protein-coupled receptors: Targets for new therapeutic interventions. Annals of Medicine 36, 204214.CrossRefGoogle Scholar
MANGER, P., LI, J., CHRISTENSEN, B. M. & YOSHINO, T. P. ( 1996). Biogenic monoamines in the freshwater snail, Biomphalaria glabrata: influence of infection by the human fluke, Schistosoma mansoni. Comparative Biochemistry and Physiology A 114, 227234.CrossRefGoogle Scholar
MANSOUR, T. E. ( 1979). Chemotherapy of parasitic worms: New biochemical strategies. Science 205, 462469.CrossRefGoogle Scholar
MANSOUR, T. E. ( 1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 136.Google Scholar
MANSOUR, J. M. & MANSOUR, T. E. ( 1986). GTP-binding proteins associated with serotonin-activated adenylate cyclase in Fasciola hepatica. Molecular and Biochemical Parasitology 21, 139149.CrossRefGoogle Scholar
MANSOUR, J. M. & MANSOUR T. E. ( 1989). Identification of GTP-binding proteins in Fasciola hepatica and Schistosoma mansoni by immunoblotting. Molecular and Biochemical Parasitology 36, 1118.CrossRefGoogle Scholar
MARTELLY, I. & FRANQUINET, R. ( 1984). Planarian regeneration as a model for cellular activation studies. Trends in Biological Sciences 9, 468471.CrossRefGoogle Scholar
MAULE, A. G., HALTON, D. W., ALLEN, J. M. & FAIRWEATHER, I. ( 1989). Studies on motility in vitro of an ectoparasitic monogenean Diclidophora merlangi. Parasitology 98, 8593.CrossRefGoogle Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., SHAW, C. & FAIRWEATHER, I. ( 1990). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255273.CrossRefGoogle Scholar
MAULE, A. G., HALTON, D. W., SHAW, C. & JOHNSTON, C. F. ( 1993). The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106, 429440.CrossRefGoogle Scholar
McKAY, D. M., HALTON, D. W., ALLEN, J. M. & FAIRWEATHER, I. ( 1989). The effects of cholinergic and serotoninergic drugs on motility in vitro of Haplometra cylindracea (Trematoda: Digenea). Parasitology 99, 241252.CrossRefGoogle Scholar
McNALL, S. J. & MANSOUR, T. E. ( 1984). Novel serotonin receptors in Fasciola: Characterization by studies on adenylate cyclase activation and [3H]LSD binding. Biochemical Pharmacology 33, 27892797.CrossRefGoogle Scholar
MELLIN, T. N., BUSCH, R. D., WANG, C. C. & KATH, G. ( 1983). Neuropharmacology of the parasitic trematode, Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 32, 8393.CrossRefGoogle Scholar
MENDONça-silva, D. L., GARDINO, P. F., KUBRUSLY, R. C. C., MELLO, F. G. & NOEL, F. ( 2004). Characterization of GABAergic neurotransmission in adult Schistosoma mansoni. Parasitology 129, 137146.CrossRefGoogle Scholar
MENDONça-silva, D. L., PESSOA, R. F. & NOEL, F. ( 2002). Evidence for the presence of glutamatergic receptors in adult Schistosoma mansoni. Biochemical Pharmacology 64, 13371344.CrossRefGoogle Scholar
METTRICK, D. F. & TELFORD, J. M. ( 1963). Histamine in the phylum Platyhelminthes. Journal of Parasitology 49, 653656.CrossRefGoogle Scholar
MILLER, C. L., DAY, T. A., BENNETT, J. L. & PAX, R. A. ( 1996). Schistosoma mansoni: L-glutamate-induced contractions in isolated muscle fibers – evidence for a glutamate transporter. Experimental Parasitology 84, 410419.CrossRefGoogle Scholar
MONEYPENNY, C. G., KRESHCHENKO, N., MOFFETT, C. L., HALTON, D. W., DAY, T. A. & MAULE, A. G. ( 2001). Physiological effects of FMRFamide-related peptides and classical transmitters on dispersed muscle fibres of the turbellarian. Procerodes littoralis. Parasitology 122, 447455.CrossRefGoogle Scholar
MOUSA, A. ( 2002). Characterization of a novel histamine-responsive G protein-coupled receptor from Schistosoma mansoni (SmGPCR). MSc. Thesis, McGill University, Montreal, Qc.
NIMMO-SMITH, R. H. & RAISON, C. G. ( 1968). Monoamine oxidase activity of Schistosoma mansoni. Comparative Biochemistry and Physiology 62C, 403416.CrossRefGoogle Scholar
ORII, H., MOCHII, M. & WATANABE, K. ( 2003). A simple “soaking method” for RNA interference in the planarian Dugesia japonica. Developmental Genes and Evolution 213, 138141.Google Scholar
OSLOOBI, N. & WEBB, R. A. ( 1999). Localization of a sodium-dependent high-affinity serotonin transporter and recruitment of exogenous serotonin by the cestode Hymenolepis diminuta: an autoradiographic and immunohistochemical study. Canadian Journal of Zoology 77, 12651277.CrossRefGoogle Scholar
PALCZEWSKI, K., KUMASAKA, T., HORI, T., BEHNKE, C. A., MOTOSHIMA, H., FOX, B. A., LE trong, I., TELLER, D. C., OKADA, T., STENKAMP, R. E., YAMAMOTO, M. & MIYANO, M. ( 2000). Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739745.CrossRefGoogle Scholar
PALLADINI, G., RUGGIERI, S., STOCCHI, F., DE PANDIS, M. F., VENTURINI, G. & MARGOTTA, V. ( 1996). A pharmacological study of cocaine activity in Planaria. Comparative Biochemistry and Physiology 115C, 4145.CrossRefGoogle Scholar
PAX, R. A., SIEFKER, C. & BENNETT, J. L. ( 1984). Schistosoma mansoni: Differences in acetylcholine, dopamine and serotonin control of circular and longitudinal parasite muscles. Experimental Parasitology 58, 312324.CrossRefGoogle Scholar
PAX, R. A., SIEFKER, C., HICKOX, T. & BENNETT, J. L. ( 1981). Schistosoma mansoni: Neurotransmitters, longitudinal musculature and effects of electrical stimulation. Experimental Parasitology 52, 346355.CrossRefGoogle Scholar
PAX, R. A., DAY, T. A., MILLER, C. L. & BENNETT, J. L. ( 1996). Neuromuscular physiology and pharmacology of parasitic flatworms. Parasitology 113, S83S96.CrossRefGoogle Scholar
RAFFA, R. B., HOLLAND, L. J. & SCHULINGKAMP, R. J. ( 2001). Quantitative assessment of dopamine D2 antagonist activity using invertebrate (Planaria) locomotion as a functional endpoint. Journal of Pharmacological and Toxicological Methods 45, 223226.CrossRefGoogle Scholar
RAHMAN, M. S., METTRICK, D. F. & PODESTA, R. B. ( 1983). Effects of 5-hydroxytryptamine on carbohydrate metabolism in Hymenolepis diminuta (Cestoda). Canadian Journal of Physiology and Pharmacology 61, 137143.CrossRefGoogle Scholar
RAHMAN, M. S., METTRICK, D. F. & PODESTA, R. B. ( 1985). Schistosoma mansoni: Effects of in vitro serotonin (5HT) on aerobic and anaerobic carbohydrate metabolism. Experimental Parasitology 60, 1017.CrossRefGoogle Scholar
RAO, K. V. N., CHEN, L., GNANASEKAR, M. & RAMASWAMY, K. ( 2002). Cloning and characterization of a calcium-binding, histamine—releasing protein from Schistosoma mansoni. Journal of Biological Chemistry 277, 3120731213.CrossRefGoogle Scholar
RAYMOND, V. & SATTELLE, D. B. ( 2002). Novel animal-health drug targets from ligand-gated chloride channels. Nature Reviews (Drug Discovery) 1, 427436.CrossRefGoogle Scholar
REUTER, M., GUSTAFSSON, M. K. S., SHEIMAN, I. M., TERENINA, N., HALTON, D. W., MAULE, A. G. & SHAW, C. ( 1995). The nervous system of Tricladida II. Neuroanatomy of Dugesia tigrina (Paludicola Dugesiidae): an immunocytochemical study. Invertebrate Neuroscience 1, 133143.Google Scholar
RIBEIRO, P. & WEBB, R. A. ( 1983 a). The synthesis of 5-hydroxytryptamine from tryptophan and 5-hydroxytryptophan in the cestode Hymenolepis diminuta. International Journal for Parasitology 13, 101106.Google Scholar
RIBEIRO, P. & WEBB, R. A. ( 1983 b). The occurrence and synthesis of octopamine and other biogenic amines in the cestode Hymenolepis diminuta. Molecular and Biochemical Parasitology 7, 5362.Google Scholar
RIBEIRO, P. & WEBB, R. A. ( 1984). The occurrence, synthesis and metabolism of 5-hydroxytryptamine and 5-hydroxytryptophan in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 79, 159164.Google Scholar
RIBEIRO, P. & WEBB, R. A. ( 1986). Demonstration of specific high-affinity binding sites for [3H] 5-hydroxytryptamine in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 84, 353358.CrossRefGoogle Scholar
RIBEIRO, P. & WEBB, R. A. ( 1987). Characterization of a serotonin transporter and an adenylate cyclase-linked serotonin receptor in the cestode Hymenolepis diminuta. Life Sciences 40, 755768.CrossRefGoogle Scholar
RIBEIRO, P. & WEBB, R. A. ( 1991). Serotonin stimulates protein phosphorylation in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 100, 483489.CrossRefGoogle Scholar
ROTH, B. L. & KRISTIANSEN, K. ( 2004). Molecular mechanisms of ligand binding, signaling and regulation within the superfamily of G protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacology and Therapeutics 103, 2180.Google Scholar
SAITOH, O., YURUZUME, E. & NAKATA, H. ( 1996). Identification of a planarian serotonin receptor by ligand binding and PCR studies. NeuroReport 8, 173178.CrossRefGoogle Scholar
SAITOH, O., YURUZUME, E., WATANABE, K. & NAKATA, H. ( 1997). Molecular identification of a G protein-coupled receptor family which is expressed in planarians. Gene 195, 5561.CrossRefGoogle Scholar
SAMII, S. I. & WEBB, R. A. ( 1990). Acetylcholine-like immunoreactivity in the cestode Hymenolepis diminuta. Brain Research 513, 161165.CrossRefGoogle Scholar
SINE, S. M. ( 2002). The nicotinic receptor ligand binding domain. Journal of Neurobiology 53, 431446.CrossRefGoogle Scholar
SIXMA, T. K. & SMIT, A. B. ( 2003). Acetylcholine binding protein (AChBP): a secreted glial protein that provides a high-resolution model for the extracellular domain of pentameric ligand-gated ion channels. Annual Review of Biophysical and Biomolecular Structure 32, 311334.CrossRefGoogle Scholar
SMITH, M. W., BORTS, T. L., EMKEY, R., COOK, C., WIGGINNS, C. J. & GUTIERREZ, J. A. ( 2003). Characterization of a novel G protein-coupled receptor from the parasitic nematode Haemonchus contortus with high affinity for serotonin. Journal of Neurochemistry 86, 255266.Google Scholar
SOLIS-SOTO, J. M. & BRINK, M. D. ( 1994). Immunocytochemical study on biologically active neurosubstances in daughter sporocysts and cercaria of Trichobilharzia ocellata and Schistosoma mansoni. Parasitology 108, 301311.CrossRefGoogle Scholar
SUKHDEO, M. V. K., HSU, S. C., THOMPSON, C. S. & METTRICK, D. F. ( 1984). Hymenolepis diminuta: behavioural effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin. Journal of Parasitology 70, 682688.CrossRefGoogle Scholar
SUKHDEO, M. V. K., SANGSTER, N. C. & METTRICK, D. F. ( 1986). Effects of cholinergic drugs on longitudinal muscle contractions of Fasciola hepatica. Journal of Parasitology 72, 858864.CrossRefGoogle Scholar
TEMBE, E. A., HOLDEN-DYE, L., SMITH, S. W. G., JACQUES, P. A. & WALKER, R. J. ( 1993). Pharmacological profile of the 5-hydroxytryptamine receptor of Fasciola hepatica body wall muscle. Parasitology 106, 6773.CrossRefGoogle Scholar
THOMPSON, C. S. & METTRICK, D. F. ( 1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 12571262.CrossRefGoogle Scholar
THOMPSON, C. S., SANGSTER, N. C. & METTRICK, D. F. ( 1986). Cholinergic inhibition of muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 64, 21112115.CrossRefGoogle Scholar
THOMPSON, D. P., KLEIN, R. D. & GEARY, T. G. ( 1996). Prospects for rational approaches to anthelmintic discovery. Parasitology 113, S217S238.CrossRefGoogle Scholar
TOMOSKY, T. K., BENNETT, J. L. & BUEDING, E. ( 1974). Tryptaminergic and dopaminergic responses of Schistosoma mansoni. Journal of Pharmacology and Experimental Therapeutics 190, 260271.Google Scholar
UNGRIN, M., SINGH, L., STOCCO, R., SAS, D. & ABRAMOVITZ, M. ( 1999). An automated aqueorin luminescence-based functional calcium assay for G protein-coupled receptors. Analytical Biochemistry 272, 3442.CrossRefGoogle Scholar
VASSILATIS, D. K., HOHMANN, J. G., ZENG, H., LI, F., RANCHALIS, J. E., MORTRUD, M. T., BROWN, A., RODRIGUEZ, S. S., WELLER, J. R., WRIGHT, A. C., BERGMANN, J. E. & GAITANARIS, G. A. ( 2003). The G protein-coupled receptor repertoires of human and mouse. Proceedings of the National Academy of Sciences, USA 100, 49034908.CrossRefGoogle Scholar
VENTURINI, G., STOCCHI, F., MARGOTTA, V., RUGGIERI, S., BRAVI, D., BALLANTUONO, P. & PALLADINI, G. ( 1989). A pharmacological study of dopaminergic receptors in Planaria. Neuropharmacology 28, 13771382.CrossRefGoogle Scholar
VERJOVSKI-ALMEIDA, S., DEMARCO, R., MARTINS, E. A. L., GUIMARAES, P. E. M., OJOPI, E. P. B., PAQUOLA, A. C. M., PIAZZA, J. P., NISHIYAMA, M. Y., KITAJIMA, J. P., ADAMSON, R. E. et al. ( 2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148157.CrossRefGoogle Scholar
VISIERS, I., BALLESTEROS, J. & WEINSTEIN, H. ( 2002). Three-dimensional representations of G protein-coupled receptor structures and mechanisms. Methods in Enzymology 343, 329371.CrossRefGoogle Scholar
WALKER, R. J., BROOKS, H. L. & HOLDEN-DYE, L. ( 1996). Evolution and overview of classical transmitter molecules and their receptors. Parasitology 113, S3S33.CrossRefGoogle Scholar
WEBB, R. A. ( 1985). Uptake and metabolism of 5-hydroxytryptamine by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 80, 305312.CrossRefGoogle Scholar
WEBB, R. A. ( 1986). The uptake and metabolism of L-glutamate by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 85, 151162.CrossRefGoogle Scholar
WEBB, R. A. ( 1988). Release of exogenously supplied L-[3H]-glutamate and endogenous glutamate from tissue slices of the cestode Hymenolepis diminuta. Canadian Journal of Physiology and Pharmacology 66, 889894.CrossRefGoogle Scholar
WEBB, R. A. ( 1995). Electrical field-stimulated release of L-[3H]-glutamate from tissue slices of the cestode Hymenolepis diminuta. Parasitology Research 81, 173174.CrossRefGoogle Scholar
WEBB, R. A. ( 1997). Glutamatergic inositol 1,4,5- triphosphate production in tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology C 118, 1926.Google Scholar
WEBB, R. A. & EKLOVE, H. ( 1989). Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode, Hymenolepis diminuta. Parasitology Research 75, 545548.CrossRefGoogle Scholar
WEBB, R. A. & MIZUKAWA, K. ( 1985). Serotonin-like immunoreactivity in the cestode Hymenolepis diminuta. Journal of Comparative Neurology 234, 431440.CrossRefGoogle Scholar
WIKGREN, M., REUTER, M., GUSTAFSSON, M. K. S. & LINDROOS, P. ( 1990). Immunocytochemical localization of histamine in flatworms. Cell and Tissue Research 260, 479484.CrossRefGoogle Scholar
WILSON, V. C. L. C. & SCHILLER, E. L. ( 1969). The neuroanatomy of Hymenolepis diminuta and H. nana. Journal of Parasitology 55, 261270.CrossRefGoogle Scholar
WIPPERSTEG, V., KAPP, K., KUNZ, W. & GREVELDING, C. ( 2002). Characterization of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. International Journal for Parasitology 32, 12191224.CrossRefGoogle Scholar
WOOD, P. J. & MANSOUR, T. E. ( 1986). Schistosoma mansoni: Serotonin uptake and its drug inhibition. Experimental Parasitology 62, 114119.CrossRefGoogle Scholar
XIE, J., DERNOVICI, S. & RIBEIRO, P. ( 2005). Mutagenesis analysis of the serotonin 5HT2C receptor and a Caenorhabditis elegans 5HT2 homologue: Conserved residues of helix 4 and 7 contribute to agonist-dependent activation of 5HT2 receptors. Journal of Neurochemistry 92, 375387.CrossRefGoogle Scholar
YONGE, K. A. & WEBB, R. A. ( 1992). Uptake and metabolism of histamine by the rat tapeworm Hymenolepis diminuta: an in vitro study. Canadian Journal of Zoology 70, 4350.CrossRefGoogle Scholar