Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-28T09:15:31.027Z Has data issue: false hasContentIssue false

Metabolism and inactivation of neurotransmitters in nematodes

Published online by Cambridge University Press:  06 April 2009

R. E. Isaac*
Affiliation:
Department of Biology, University of Leeds, Leeds LS2 9JT, UK
D. Macgregor
Affiliation:
Department of Biology, University of Leeds, Leeds LS2 9JT, UK
D. Coates
Affiliation:
Department of Biology, University of Leeds, Leeds LS2 9JT, UK
*
*Correspondence author.

Summary

The nematode nervous system employs many of the same neurotransmitters as are found in higher animals. The inactivation of neurotransmitters is absolutely essential for the correct functioning of the nervous system, In this article we discuss the various mechanisms used generally in animal nervous systems for synaptic inactivation of neurotransmitters and review the evidence for similar mechanisms operating in parasitic and free-living nematodes. The sequencing of the entire Caenorhabditis elegans genome means that the sequence of nematode genes can be accessed from the C. elegans database (ACeDB) and this wealth of information together with the increasing knowledge of the genetics of this free-living nematode will have great impact on all aspects of nematode neurobiology. The review will provide an insight into how this information may be exploited to identify and characterize target proteins for the development of novel anti-nematode drugs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agarwal, A., Mishra, A., Mishra, S. K. & Ghatak, S. (1985). Monoamine oxidase in Nippostrongylus brasiliensis. Indian Journal of Parasitology 9, 221–4.Google Scholar
Agarwal, A., Shukla, O. P., Ghatak, S. & Tekwani, B. L. (1990). Biogenic amines, metabolites and monoamine oxidase in filarial worm, Setaria cervi, Inernational Journal of Parasitology 20, 873–81.Google Scholar
Alfonso, A., Grundahl, K., Duerr, J. S., Han, H.-P. & Rand, J. B. (1993). The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261, 617–19.Google Scholar
Amara, s. & Kuhar, M. J. (1993). Neurotransmitter transporters: recent progress. Annual Review of Neuroscience 16, 7393.Google Scholar
Avery, L. & Horvitz, H. R. (1990). Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. Journal of Experimental Zoology 253, 263–70.Google Scholar
Barondes, S. H. (1994). Thinking about Prozac. Science 263, 1102–3.CrossRefGoogle ScholarPubMed
Barreteau, H., Trouvin, J. H., Goudey-PERRIERE, F., Jacquot, C. & Gayral, P. (1991). Biogenic amines and GABA in the larval and adult forms of the nematode Nippostrongylus brasiliensis. Comparative Biochemistry and Physiology 100C, 445–9.Google Scholar
Bawab, W., Querido, E., Crines, P. & Desgroseillers, L. (1992). Identification and characterisation of aminopeptidases from Aplysia californica. Biochemical Journal 286, 967–75.Google Scholar
Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G. & Waterston, R. H. (1989). Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 342, 4550.CrossRefGoogle ScholarPubMed
Bergman, J., Madras, B. K., Johnson, S. E. & Spearman, R. D. (1989). Effects of cocaine and related drugs in nonhuman primates III. Self-administration by squirrel monkeys. Journal of Pharmacology and Experimental Therapeutics 251, 150–5.Google Scholar
Berry, M. D., Juoria, A. V. & Paterson, I. A. (1994). The functional role of monoamine oxidases A and B in the mammalian central nervous system. Progress in Neurobiology 42, 375–91.Google Scholar
Borowsky, B., Mezey, E. & Hoffman, B. J. (1993). 2 glycine transporter variants with distinct localization in the CNS and peripheral-tissues are encoded by a common gene. Neuron 10, 851–63.Google Scholar
Borowsky, B. & Hoffman, B. J. (1995). Neurotransmitter transporters: molecular biology, function, and regulation. International Review of Neurobiology 38, 139–99.Google Scholar
Brownlee, D. J. A., Fairweather, I., Johnston, C. F. & Shaw, C. (1993). Immunocytochemical demonstration of peptidergic and serotoninergic components in the enteric nervous system of the round worm, Ascaris suum. Parasitology 108, 89103.CrossRefGoogle Scholar
Chalfie, M. & White, J. (1988). The nervous system. In The Nematode Caenorhabditis elegans. (ed. Wood, W. B.) pp 337–91. New York, Cold Spring Harbor.Google Scholar
Chaudhuri, J., Martin, R. E. & Donahue, M. J (1988). Evidence for the absorption and synthesis of 5-hydroxytryptamine in perfused muscle and intestinal tissue and whole worms of adult Ascaris suum. Parasitology 96, 157–70.Google Scholar
Christensen, N. J. & Henriksen, J. H. (1991). Degradation of endogenous catecholamines. In: Degradation of Bioactive Substances: Physiology and Pathophysiology. (ed. Henriksen, J. H.) pp. 289305. New York, CRC Press.Google Scholar
Corey, J. L., Quick, M. W., Davidson, N., Lester, H. A. & Guastella, J. (1994). A cocaine-sensitive Drosophila serotonin transporter: cloning, expression, and electrophysiological characterization. Proceedings of the National Academy of Sciences, USA 91, 1188–92.Google Scholar
Coyle, J. T. & Axelrod, J. (1972). Dopamine β-hydroxylase in rat brain development characteristics. Journal of Neurochemistry 19, 449–59.Google Scholar
Cowden, S., Stretton, A. O. W. & Davies, R. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.Google Scholar
Croll, N. (1975). Indolealkylamines in the co-ordination of nematode behavioural activities. Canadian Journal of Zoology 53, 894903.Google Scholar
Culotti, J. G., Von EHRENSTEIN, G., Culotti, M. R. & Russell, R. L. (1981). A second class of acetylcholinesterase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 97, 281305.Google Scholar
Davids, G. L., Aisien, S. O. & Walter, R. D. (1994). Characterisation of the N-acetyltransferases respectively responsible for arylalkylamine and diamine acetylation in Ascaris suum. Molecular & Biochemical Parasitology 64, 341–4.Google Scholar
Demchyshyn, L. L., Pristupa, Z. B., Sugamori, K. S., Barker, E. L., Blakely, R. D., Wolfgang, W. J., Forte, M. A. & Niznik, H. B. (1994). Cloning, expression, and localization of a chloride-facilitated, cocaine-sensitive serotonin transporter from Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 91, 5158–62.CrossRefGoogle ScholarPubMed
Desai, C., Garriga, G., Macintire, S. L. & Horvitz, H. R. (1988). A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638–46.Google Scholar
Duve, H., Sewell, J. C., Scott, A. G. & Thorpe, A. (1991). Chromatographic characterization and biological-activity of neuropeptides immunoreactive to antisera against Met5-enkephalin-Arg6-Phe7 (YGGFMRF) extracted from the blowfly Calliphora vomitoria (Diptera). Regulatory Peptides 35, 145–59.Google Scholar
Elkihel, L., Grosclaude, J. M., Nembo, B., Jacquot, C., Gayral, P., Goudey-PERRIERE, F., Letourneux, Y. & Barreteau, H. (1994). Synthesis and determination of N-acetyl octopamine by HPLC with electrochemical detection. Bioassay in Nippostrongylus brasiliensis (Nematoda). Journal of Liquid Chromatography 17, 3421–35.CrossRefGoogle Scholar
Erickson, J. D., Varoqui, H., Schafer, M. K. H., Modi, W., Diebler, M. F., Weihe, E., Rand, J., Eiden, L. E., Bonner, T. I. & Usdin, T. B. (1994). Functional identification of a vesicular acetylcholine transporter and its expression from a cholinergic gene locus. Journal of Biological Chemistry 269, 21929–32.Google Scholar
Fire, A., Harrison, S. W., & Dixon, D. A. (1990). A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189–98.Google Scholar
Galjart, N. J., Morreau, H., Willemsen, R., Gillemans, N., Bonten, E. J. & D'AZZO, A. (1991). Human lysosomal protective protein has cathepsin A-like activity distinct from its protective function. Journal of Biological Chemistry 266, 14754–62.Google Scholar
Gerencser, G. A. & Stevens, B. R. (1994). Thermodynamics of symport and antiport catalyzed by cloned or native transporters. Journal of Experimental Biology 196, 5975.CrossRefGoogle ScholarPubMed
Giros, B., Jaber, M., Jones, S. R., Wightman, R. M. & Caron, M. G. (1996). Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379, 606–12.Google Scholar
Goh, S. L. & Davy, K. G. (1985). Occurrence of noradrenaline in the central nervous system of Phocanema decipiens and its possible role in the control of ecdysis. Canadian Journal of Zoology 63, 475–9.Google Scholar
Grosclaude, J. M., Nembo, B., Barreteau, H., Elkihel, L., Trouvin, J.-H, Jacquot, C., Gayral, P. & Goudey-PERRIERE, F. (1994). Influence of sample recovery techniques on detection of biogenic amines in the rat hookworm, Nippostrongylus brasiliensis. Journal of Liquid Chromatography 17, 2705–21.Google Scholar
Guastella, J., Johnson, C. D. & Stretton, A. O. W. (1991). GABA-immunoreactive neurons in the nematode Ascaris. The Journal of Comparative Neurology 307, 584–97.Google Scholar
Guastella, J., Nelson, N., Nelson, H., Czyzk, L., Keynan, S., Miedel, M. C., Davidson, N., Lester, H. A. & Kanner, B. I. (1990). Cloning and expression of a rat brain GABA transporter. Science 249, 1303–6.Google Scholar
Guastella, J. & Stretton, A. O. W. (1991). Distribution of 3H-GABA uptake sites in the nematode Ascaris. The Journal of Comparative Neurology 307, 598608.CrossRefGoogle ScholarPubMed
Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E. & Evans, P. D. (1982). Serotonin and octopamine in the nematode, Caenorhabditis elegans. Science 216, 1012–14.Google Scholar
Isaac, R. E. (1988). Neuropeptide-degrading endopeptidase activity of locust (Schistocerca gregaria) synaptic membranes. Biochemical Journal 255, 843–7.Google Scholar
Isaac, R. E., Eaves, L., Muimo, R. & Lamango, N. (1991). N-acetylation of biogenic amines in Ascaridia galli. Parasitology 102, 445–50.Google Scholar
Isaac, R. E., Muimo, R. & Macgregor, A. N. (1990). N-acetylation of serotonin, octopamine and dopamine by adult Brugia pahangi. Molecular and Biochemical Parasitology 43, 193–8.CrossRefGoogle ScholarPubMed
Itoh, K., Kase, R., Shimmoto, M., Satake, A., Sakuraba, H. & Suzuki, Y. (1995). Protective protein as an endogenous endothelin degradation enzyme in human tissues. Journal of Biological Chemistry 270, 515–18.Google Scholar
Iversen, L. L. (1975). Uptake process of biogenic amines. In Handbook of Psychopharmacology (eds. Iversen, L. L.Iversen, S. D, Snyder, S. H.), pp. 381442. New York, Plenum.Google Scholar
Iversen, L. L. (1987). Overview: peptides in the nervous system. In Neuropeptides and their Peptidases (ed. Turner, A. J.), pp. 38. Weinheim: Chichester/VCH. Ellis Horwood Series, Ellis Horwood.Google Scholar
Jackman, H. L., Morris, P. W., Deddish, P. A., Skidgel, R. A. & Erdös, E. G. (1991). Inactivation of endothelin I by deamidase (lysosomal protective protein). Journal of Biological Chemistry 267, 2872–5.CrossRefGoogle Scholar
Jackman, H. L., Tan, F., Tamei, H., Harbury, C. B., Li, X. Y., Skidgel, R. A. & Erdös, E. G. (1990). A peptidase of human platelets that deamidates tachykinins. Probable identity with the lysosomal protective protein. Journal of Biological Chemistry 265, 11265–72.Google Scholar
Jacquot, C., Barreteau, H., Trouvin, J. H., Gayral, P. & Leroy, J. P. (1986). Putative neurotransmitters in three experimental filiariasis models. Life Sciences 39, 1539–42.CrossRefGoogle Scholar
Jiang, J., Gu, B., Albright, L. M. & Nixon, B. T. (1989). Conservation between coding and regulatory elements of Rhizobium meliloti and Rhizobium leguminosarum dct genes. Journal of Bacteriology 171, 5244–53.Google Scholar
Johnson, C. D., Duckett, J. G., Culotti, J. G., Herman, R. K., Meneely, P. M. & Russell, R. L. (1981). An acetylcholinesterase-deficient mutant of the nematode Cenorhabditis elegans. Genetics 97, 261–79.CrossRefGoogle Scholar
Johnson, C. D., Rand, J. B., Herman, R. K. & Stern, B. D. (1988). The acetylcholinesterase genes of C. elegans; identification of a third gene (ace-3) and mosaic mapping of a synthetic lethal phenotype. Neuron 1, 165–73.Google Scholar
Kanner, B. I. (1994). Sodium-coupled neurotransmitter transport structure, function and regulation. Journal of Experimental Biology 196, 237–49.Google Scholar
Kanner, B. I., Bendahan, A., Pantanowitz, S. & Su, H. (1994). The number of amino acid residues in hydrophilic loops connecting transmembrane domains of the GABA transportert GAT-1 is critical for its function. Federation of European Biochemical Societies Letters 356, 191–4.Google Scholar
Karlson, p. & Sekeris, c. E. (1962). N-acetyl dopamine as a sclerotizing agent of the insect cuticle. Nature 195, 183–4.Google Scholar
Kempton, L. R. C., Pillmoor, J. B., Willis, R. J. & Isaac, R. E. (1990). Tyramine γ-hydroxylase activity in the synganglion of the cattle tick Boophilus microplus. In Insect Neurochemistry and Neurophysiology (eds. Borkovec, A. B. & Masler, E. P.), pp. 281284. Humana Press, Clifton, New Jersey.Google Scholar
Kempton, L. R. C., Isaac, R. E., Pillmoor, J. B. & Willis, R. J. (1992). Octopamine N-acetyltransferase activity from the cattle tick, Boophilus microplus. Insect Biochemistry & Molecular Biology 22, 777–83.Google Scholar
Kenny, A. J. (1993). Endopeptidase 24.11: putative substrates and possible roles. Biochemical Transactions 21, 663–8.Google Scholar
Kenny, A. J. & Hooper, N. M. (1991). Peptidases involved in the metabolism of bioactive peptides. In Degradation of Bioactive Substances: Physiology and Pathophysiology (ed. Henriksen, J. H.), pp. 4779, Boca Raton, Florida, CRC Press.Google Scholar
Kenny, A. J., Stephenson, S. L. & Turner, A. J. (1987). Cell surface peptidases. In Mammalian Ectoenzymes (eds. Kenny, A. J. and Turner, A. J.), pp. 169209. Amsterdam, Elsevier.Google Scholar
Keshet, G. I., Bendahan, A., Su, H., Mager, S., Lester, H. A. & Kanner, B. I. (1995). Glutamate-101 is critical for the function of the sodium and chloride-coupled GABA transporter GAT-1. Federation of European Biochemical Societies Letters 371, 3942.Google Scholar
Kleinberger-DORON, N. & Kanner, B. I. (1994). Identification of tryptophan residues critical for the function and targeting of the ³-aminobutyric acid transporter (subtype A). Journal of Biological Chemistry 269, 3063–7.Google Scholar
Lamango, N. S. & Isaac, R. E. (1994). Identification and properties of a peptidyl dipeptidase in the housefly, Musca domestica, that resembles mammalian angiotensin converting enzyme. Biochemical Journal 29, 651–7.Google Scholar
Lee, D. L. (1962). The distribution of esterase enzymes in Ascaris lumbricoides. Parasitology 52, 241–60.Google Scholar
Lee, D. L. (1996). Why do some nematode parasites of the alimentary tract secrete acetylcholinesterase? International Journal for Parasitology 26, 499508.Google Scholar
Lee, D. L. & Ko, R. C. (1991). Catecholaminergic neurons in Trichinella spiralis (Nematoda). Parasitology Research 77, 269–70.Google Scholar
Lester, H. A., Mager, S., Quick, M. W. & Corey, J. L. (1994). Permeation properties of neurotransmitter transporters. Annual Review of Pharmacology and Toxicology 34, 219–49.CrossRefGoogle ScholarPubMed
Li, j. & Nappi, A. J. (1992). N-acetyltransferase activity during ovarian development in the mosquito Aedes aegypti following blood feeding. Insect Biochemistry & Molecular Biology 22, 4952.Google Scholar
Liu, Q.-R., Mandiyan, S., Lopez-Corcuera, B., Nelson, H. & Nelson, N. (1993). A rat brain cDNA encoding the neurotransmitter transporter with an unusual structure. Federation of European Biochemical Societies Letters 315, 114–18.Google Scholar
Liu, Q.-R., Mandiyan, S., Nelson, H. & Nelson, N. (1992). A family of genes encoding neurotransmitter transporters. Proceedings of the National Academy of Sciences, USA 89, 6639–43.CrossRefGoogle ScholarPubMed
Loer, C. M. & Kenyon, C. J. (1993). Serotonin-deficient mutants and male mating behaviour in the nematode Caenorhabditis elegans. Journal of Neuroscience 13, 5407–17.CrossRefGoogle ScholarPubMed
Lynch, A. S., Briggs, D. & Hope, I. A. (1995). Developmental expression pattern screen for genes predicted in the C. elegans genome sequencing project. Nature Genetics 11, 309–13.Google Scholar
Macgregor, D., Hope, I. A. & Isaac, R. E. (1995). Nematodes, neurobiology and development of. In Molecular Biology and Biotechnology (ed. Meyers, R. A.), pp. 587–9. New York: VCH Publishers Inc.Google Scholar
Martin, R. J. (1993). Neuromuscular transmission in nematode parasites and antinematodal drug action. Pharmacology and Therapeutics 58, 1350.Google Scholar
Mayser, w., Schloss, P. & Betz, H. (1992). Primary structure and functional expression of a choline transporter expressed in the rat nervous sytem. Federation of European Biochemical Societies Letters 37, 31–6.CrossRefGoogle Scholar
Mbungu, D., Ross, L. S. & Gill, S. S. (1995). Cloning, functional expression, and pharmacology of a GABA transporter from Manduca sexta. Archives of Biochemistry and Biophysics 318, 489–97.Google Scholar
Mckelvy, J. P. & Blumberg, S. (1986). Inactivation of neuropeptides. Annual Review of Neuroscience 9, 415–34.Google Scholar
Miklos, G. L. G. (1993). Molecules and cognition: the latterday lessons of levels, language and lac. Evolutionary overview of brain structure and function in some vertebrates and invertebrates. Journal of Neurobiology 24, 842–90.Google Scholar
Mishra, S. K., Ramanuj, S. & Ghatak, S. (1983). Monoamine oxidase in adult A. galli. Journal of Helminthology 57, 313–8.Google Scholar
Mishra, S. K., Ramanuj, S. & Ghatak, S. (1984) Ascaris lumbricoides and Ascaridia galli: biogenic amines in adults and developmental stages. Experimental Parasitology 57, 34–9.Google Scholar
Mishra, s. K., Sen, R. & Ghatak, s. (1978). Monoamine oxidase and metabolites of biogenic amines in human Ascaris. Indian Journal of Parasitology 2, 153–5.Google Scholar
Muimo, R. & Isaac, R. E. (1993). Properties of arylalkylamine N-acetyltransferase from the nematode Ascaridia galli. Comparative Biochemistry & Physiolology 106B, 969–76.Google Scholar
Mukherjee, S., Tripathi, L. M., Tekwani, B. L., Katiyah, J. C. & Ghatak, s. (1989). Pattern of biogenic amines in various tissues of hamster during infection with Ancylostoma ceylanicum, a human hookworm. Clinical and Chemistry Enzymology Communications 1, 229–34.Google Scholar
Nathanson, J. A., Hunnicutt, E. J., Kantham, L., Scavone, C. (1993). Cocaine as a naturally occurring insecticide. Proceedings of the National Academy of Sciences, USA 90, 9645–8.Google Scholar
Nelson, N. & Lill, H. (1994). Porters and neurotransmitter transporters. Journal of Experimental Biology 196, 213–28.Google Scholar
Nyberg, F. & Terenius, L. (1991). Enzymatic inactivation of neuropeptides. In: Degradation of Bioactive Substances: Physiology and Pathophysiology (ed. Henriksen, J. H.), pp. 189200, Boca Raton, Florida, CRC Press.Google Scholar
Opperman, C. H. & Chang, S. (1992). Nematode acetylcholinesterases: molecular forms and their potential role in nematode behaviour. Parasitology Today 8, 406–11.Google Scholar
Pacholczyk, T., Blakely, R. D. & Amara, S. (1991). Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature 350, 350–4.Google Scholar
Plasterk, R. H. A. (1995). Reverse genetics: from gene sequence to mutant worm. In: Methods in Cell Biology 48 (eds. Epstein, H. F. & Shakes, D. C), pp. 5981. San Diego Academic Press.Google Scholar
Powell, J. F. (1991). Molecular biological studies of monoamine oxidase: structure and function. Biochemical Society Transactions 19, 199201.Google Scholar
Pritchard, D. I. (1993). Why do some parasitic nematodes secrete acetylcholinesterase (AChE) International Journal for Parasitology 23, 549–50.CrossRefGoogle ScholarPubMed
Radian, R., Bendahan, A. & Kanner, B. I. (1986). Purification and identification of the functional sodium- and chloride-coupled γ-aminobutyric acid transport glycoprotein from rat brain. Journal of Biological Chemistry 261, 15437–41.CrossRefGoogle ScholarPubMed
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, 755–68.Google Scholar
Ritz, M., Lamb, R. J., Goldberg, S. R. & Kuhar, M. J. (1987). Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237, 1219–23.Google Scholar
Roques, B. P., Noble, F., Dauge, V., Fournie-ZALUSKI, M.-C. & Beaumont, A. (1993). Neutral endopeptidase 24.11: structure, inhibition, and experimental and clinical pharmacology. Pharmacology Reviews 45, 87146.Google ScholarPubMed
Rudnick, G. & Wall, S. C. (1992). The molecular mechanism of ‘ecstasy’ [ 3,4–methylenedioxy-methamphetamine (MDMA)]: serotonin transporters are targets for MDMA-induced serotonin release. Proceedings of the National Academy of Sciences, USA 89, 1817–21.Google Scholar
Sajid, M. & Isaac, R. E. (1994). Metabolism of AF1 (Lys-Asn-Glu-Phe-Ile-Arg-Phe-NH2) the nematode Ascaris suum. Biochemical Society Transactions 22, 293S.Google Scholar
Sajid, M. & Isaac, R. E. (1995). Identification and properties of a neuropeptide-degrading endopeptidase (neprilysin) of Ascaris suum muscle. Parasitology 111, 599608.Google Scholar
Sajid, M., Keating, C., Holden-DYE, L., Harrow, I. D. & Isaac, R. E. (1996). Metabolism of AF1 (KNEFIRF-NH2) in the nematode, Ascaris suum, by aminopeptidase, endopeptidase and deamidase enzymes. Molecular & Biochemical Parasitology 75, 159–68.Google Scholar
Schafer, W. R. &. Kenyon, C. J. (1995). A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375, 73–8Google Scholar
Schinkman, K. & Li, C. (1992). Localisation of FMRFamide-like peptides in Caenorhabditis elegans. Journal of Comparative Neurology 316, 251–60.Google Scholar
Shafqat, S., Velaz-FAIRCLOTH, M., Guadano-FERRAZ, A. & Fremeau, R. T. (1993). Molecular characterization of neurotransmitter transporters. Molecular Endocrinology 7, 1517–29.Google Scholar
Shahkolahi, A. M. & Donahue, M. J. (1993). Bacterial flora, a possible source of serotonin in the intestine of adult female Ascaris suum. Journal of Parasitology 79, 1722.Google Scholar
Sharpe, M. J. & Atkinson, H. J. (1980). Improved visualisation of dopaminergic neurons in nematodes using the glyoxylic acid fiourescence method. Journal of Zoology 190, 273–84.Google Scholar
Shisov, B. A. (1980). Biogenic amines in helminths. In Neurotransmitters. Comparative Aspects (eds. Salanki, J. & Turpaev, T. M.), pp. 3156. Budapest, Akademiai Kiado.Google Scholar
Smart, D. (1988a). Investigations of the synthesis and metabolism of 5-hydroxytryptamine in Ascaridia galli (nematoda). International Journal for Parasitology 18, 747–52.Google Scholar
Smart, D. (1988b). Catecholamine synthesis in Ascaridia galli (Nematoda). International Journal for Parasitology 18, 458–92.Google Scholar
Smart, D. (1989). What are the functions of the catecholamines and 5-hydroxytryptamine in parasitic nematodes? In Comparative Biochemistry of Parasitic Helminths (eds. Bennet, E. M., Behn, C. & Bryant, C.), pp. 2534. London, Chapman & Hall.Google Scholar
Soubrier, F., Hubert, C., Testut, P., Nadaud, S., Alhenc-GELAS, F. & Corvol, P. (1993). Molecular biology of the angiotensin I converting enzyme: I. Biochemistry and structure of the gene. Journal of Hypertension 11, 471–6.Google Scholar
Stretton, A. O. W. (1992). Ascaris neural signalling molecules. In Molecular Basis of Drug and Pesticide Action (ed. Duce, I. R.), pp. 123–38. London, Elsevier Applied Science.Google Scholar
Sulston, J., Dew, M. & Brenner, S. (1975). Dopaminergic neurons in the nematode Caenorhabditis elegans. The Journal of Comparative Neurology 163, 215–26.Google Scholar
Talesa, V., Culetto, E., Schirru, N., Bernardi, H., Fedon, Y., Toutant, J.-P. & Arpagaus, M. (1995). Characterisation of a null mutation in ace-1, the gene encoding class A acetylcholinesterase in the nematode Caenorhabditis elegans. Federation of European Biochemical Societies Letters 357, 265–8.Google Scholar
Tolner, B., Poolman, B., Wallace, B. & Konings, W. (1992). Revised nucleotide sequence of the gltP gene, which encodes the proton-glutamate-aspartate transport protein of Escherichia coli K-12. Journal of Bacteriology 174, 2391–3.Google Scholar
Uchida, S., Kwon, H. M., Yamauchi, A., Preston, A. S., Marumo, F., & Handler, J. S. (1992). Molecular cloning of the cDNA for an MDCK cell NA+-and Cl--dependent taurine transporter that is regulated by hypertonicity. Proceedings of the National Academy of Sciences, USA 89, 8230–4.Google Scholar
Uhl, G. R. & Johnson, P. S. (1994). Neurotransmitter transporters: three important gene families for neuronal function. Journal of Experimental Biology 196, 229–36.Google Scholar
Uhl, G. R., Kitayama, S., Gregor, P., Nanthakumar, E., Persico, A. & Shimada, s. (1992). Neurotransmitter transporter family cDNAs in a rat midbrain library: ‘orphan transporters’ suggest sizeable structural variations. Molecular Brain Research 16, 353–9.Google Scholar
Usdin, T. B., Mezey, E., Chen, C., Brownstein, M. J. & Hoffman, B. J. (1991). Cloning of the cocaine-sensitive bovine dopamine transporter. Proceedings of the National Academy of Sciences, USA 88, 11168–71.Google Scholar
Walker, R. J. & Holden-DYE, L. (1991). Evolutionary aspects of transmitter molecules, their receptors and channels. Parasitology 102, S7–S29.Google Scholar
Weber, W. W. (1973). Acetylation of drugs. In Metabolic Conjugation and Metabolic Hydrolysis (ed. Fishman, W. H.), vol. 3. pp. 249–96. New York, Academic Press.Google Scholar
Weinshenker, D., Garriga, G. & Thomas, J. H. (1995). Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. The Journal of Neuroscience 15, 6975–85.Google Scholar
Wright, D. J. & Awan, F. A. (1978). Catecholaminergic structures in the nervous system of three nematode species, with observations on related enzymes. Journal of Zoology 185, 477–89.Google Scholar
White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B 314, 1340.Google Scholar