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Neuropeptide signalling systems in flatworms

Published online by Cambridge University Press:  29 March 2006

P. McVEIGH ,
M. J. KIMBER ,
E. NOVOZHILOVA  and
T. A. DAY
P. McVEIGH
Affiliation:
Parasitology Research Group, Queen's University Belfast, Belfast BT9 7BL, Northern Ireland, UK
M. J. KIMBER
Affiliation:
Department of Biomedical Sciences, Iowa State University, Ames IA 50011, USA
E. NOVOZHILOVA
Affiliation:
Department of Biomedical Sciences, Iowa State University, Ames IA 50011, USA
T. A. DAY
Affiliation:
Department of Biomedical Sciences, Iowa State University, Ames IA 50011, USA
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Abstract

Two distinct families of neuropeptides are known to endow platyhelminth nervous systems – the FMRFamide-like peptides (FLPs) and the neuropeptide Fs (NPFs). Flatworm FLPs are structurally simple, each 4–6 amino acids in length with a carboxy terminal aromatic-hydrophobic-Arg-Phe-amide motif. Thus far, four distinct flatworm FLPs have been characterized, with only one of these from a parasite. They have a widespread distribution within the central and peripheral nervous system of every flatworm examined, including neurones serving the attachment organs, the somatic musculature and the reproductive system. The only physiological role that has been identified for flatworm FLPs is myoexcitation. Flatworm NPFs are believed to be invertebrate homologues of the vertebrate neuropeptide Y (NPY) family of peptides. Flatworm NPFs are 36–39 amino acids in length and are characterized by a caboxy terminal GRPRFamide signature and conserved tyrosine residues at positions 10 and 17 from the carboxy terminal. Like FLPs, NPF occurs throughout flatworm nervous systems, although less is known about its biological role. While there is some evidence for a myoexcitatory action in cestodes and flukes, more compelling physiological data indicate that flatworm NPF inhibits cAMP levels in a manner that is characteristic of NPY action in vertebrates. The widespread expression of these neuropeptides in flatworm parasites highlights the potential of these signalling systems to yield new targets for novel anthelmintics. Although platyhelminth FLP and NPF receptors await identification, other molecules that play pivotal roles in neuropeptide signalling have been uncovered. These enzymes, involved in the biosynthesis and processing of flatworm neuropeptides, have recently been described and offer other distinct and attractive targets for therapeutic interference.

Keywords

PlatyhelminthestrematodecestodeturbellarianplanarianFMRFamideneuropeptide Fprohormone convertaseamidation
Type
Research Article
Information
Parasitology , Volume 131 , Supplement S1: Parasite neuromusculature and its utility as a drug target , October 2005 , pp. S41 - S55
Copyright
2005 Cambridge University Press

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References

REFERENCES

AAKERLUND, L., GETHER, U., FUHLENDORFF, J., SCHWARTZ, T. W. & THASTRUP, O. ( 1990). Y1 receptors for neuropeptide Y are coupled to mobilization of intracellular calcium and inhibition of adenylate cyclase. FEBS Letters 260, 73–78.CrossRefGoogle Scholar
AGATA, K., SOEJIMA, Y., KATO, K., KOBAYASHI, C., UMESONO, Y. & WATANABE, K. ( 1998). Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zoological Science 15, 433–440.CrossRefGoogle Scholar
ARMSTRONG, E. P., HALTON, D. W., TINSLEY, R. C., CABLE, J., JOHNSTON, R. N., JOHNSTON, C. F. & SHAW, C. ( 1997). Immunocytochemical evidence for the involvement of an FMRFamide-related peptide in egg production in the flatworm parasite Polystoma nearcticum. Journal of Comparative Neurology 377, 41–48.3.0.CO;2-J>CrossRefGoogle Scholar
ASADA, A., ORII, H., WATANABE, K. & TSUBAKI, M. ( 2005). Planarian peptidylglycine-hydroxylating monooxygenase, a neuropeptide processing enzyme, colocalizes with cytochrome b561 along the central nervous system. FEBS Journal 272, 942–955.CrossRefGoogle Scholar
BALASUBRAMANIAM, A. ( 1997). Neuropeptide Y family of hormones: receptor subtypes and antagonists. Peptides 18, 445–457.CrossRefGoogle Scholar
BALASUBRAMANIAM, A. ( 2003). Neuropeptide Y (NPY) family of hormones: progress in the development of receptor selective agonists and antagonists. Current Pharmaceutical Design 9, 1165–1175.CrossRefGoogle Scholar
BISEROVA, N. M., DUDICHEVA, V. A., TERENINA, N. B., REUTER, M., HALTON, D. W., MAULE, A. G. & GUSTAFSSON, M. K. ( 2000). The nervous system of Amphilina foliacea (Platyhelminthes, Amphilinidea). An immunocytochemical, ultrastructural and spectrofluorometrical study. Parasitology 121, 441–453.Google Scholar
BLAIR, K. & ANDERSON, P. ( 1994). Physiological and pharmacological properties muscle cells isolated from the flatworm Bdelloura candida. Parasitology 109, 325–335.CrossRefGoogle Scholar
BLAIR, K. L., BENNETT, J. L. & PAX, R. A. ( 1988). Schistosoma mansoni: evidence for protein kinase-C-like modulation of muscle activity. Experimental Parasitology 66, 243–252.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, 251–258.CrossRefGoogle Scholar
BOYLE, J. P., WU, X. J., SHOEMAKER, C. B. & YOSHINO, T. P. ( 2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205–215.CrossRefGoogle Scholar
CABLE, J., MARKS, N. J., HALTON, D. W., SHAW, C., JOHNSTON, C. F., TINSLEY, R. C. & GANNICOTT, A. M. ( 1996). Cholinergic, serotoninergic and peptidergic components of the nervous system of Discocotyle sagittata (Monogenea: Polyopisthocotylea). International Journal for Parasitology 26, 1357–1367.CrossRefGoogle Scholar
CHANCE, M. R. & MANSOUR, T. E. ( 1949). A kymographic study of the action of drugs on the liver fluke (Fasciola hepatica). British Journal of Pharmacology 4, 7–13.CrossRefGoogle Scholar
CHANCE, M. R. & MANSOUR, T. E. ( 1953). A contribution to the pharmacology of movement in the liver fluke. British Journal of Pharmacology 8, 134–138.CrossRefGoogle Scholar
COBBETT, P. & DAY, T. A. ( 2003). Functional voltage-gated Ca2+ channels in muscle fibers of the platyhelminth Dugesia tigrina. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology 134, 593–605.CrossRefGoogle Scholar
CURRY, W. J., SHAW, C., JOHNSTON, C. F., THIM, L. & BUCHANAN, K. D. ( 1992). Neuropeptide F: primary structure from the tubellarian, Artioposthia triangulata. Comparative Biochemistry and Physiology. C: Comparative Pharmacology 101, 269–274.CrossRefGoogle Scholar
DAVIS, R. E. & STRETTON, A. O. ( 1996). The motornervous system of Ascaris: electrophysiology and anatomy of the neurons and their control by neuromodulators. Parasitology 113 (Suppl.), S97–S117.CrossRefGoogle Scholar
DAY, T. A., BENNETT, J. L. & PAX, R. A. ( 1994). Serotonin and its requirement for maintenance of contractility in muscle fibres isolated from Schistosoma mansoni. Parasitology 108, 425–432.CrossRefGoogle Scholar
DAY, T. A., HAITHCOCK, J., KIMBER, M. & MAULE, A. G. ( 2000). Functional ryanodine receptor channels in flatworm muscle fibres. Parasitology 120, 417–422.CrossRefGoogle Scholar
DAY, T. A. & MAULE, A. G. ( 1999). Parasitic peptides! The structure and function of neuropeptides in parasitic worms. Peptides 20, 999–1019.CrossRefGoogle Scholar
DAY, T. A., MAULE, A. G., SHAW, C., HALTON, D. W., MOORE, S., BENNETT, J. L. & PAX, R. A. ( 1994). Platyhelminth FMRFamide-related peptides (FaRPs) contract Schistosoma mansoni (Trematoda: Digenea) muscle fibres in vitro. Parasitology 109, 455–459.CrossRefGoogle Scholar
DAY, T. A., MAULE, A. G., SHAW, C. & PAX, R. A. ( 1997). Structure-activity relationships of FMRFamide-related peptides contracting Schistosoma mansoni muscle. Peptides 18, 917–921.CrossRefGoogle Scholar
DOUGAN, P. M., MAIR, G. R., HALTON, D. W., CURRY, W. J., DAY, T. A. & MAULE, A. G. ( 2002). Gene organization and expression of a neuropeptide Y homolog from the land planarian Arthurdendyus triangulatus. Journal of Comparative Neurology 454, 58–64.CrossRefGoogle Scholar
EIPPER, B. A., MILGRAM, S. L., HUSTEN, E. J., YUN, H. Y. & MAINS, R. E. ( 1993). Peptidylglycine alpha-amidating monooxygenase: a multifunctional protein with catalytic, processing, and routing domains. Protein Science 2, 489–497.Google Scholar
EIPPER, B. A., STOFFERS, D. A. & MAINS, R. E. ( 1992). The biosynthesis of neuropeptides: peptide alpha-amidation. Annual Review of Neuroscience 15, 57–85.CrossRefGoogle Scholar
EL-SAYED, N. M., BARTHOLOMEU, D., IVENS, A., JOHNSTON, D. A. & LOVERDE, P. T. ( 2004). Advances in schistosome genomics. Trends in Parasitology 20, 154–157.CrossRefGoogle Scholar
ESPINOZA, E., CARRIGAN, M., THOMAS, S. G., SHAW, G. & EDISON, A. S. ( 2000). A statistical view of FMRFamide neuropeptide diversity. Molecular Neurobiology 21, 35–56.Google Scholar
GARCZYNSKI, S. F., BROWN, M. R., SHEN, P., MURRAY, T. F. & CRIM, J. W. ( 2002). Characterization of a functional neuropeptide F receptor from Drosophila melanogaster. Peptides 23, 773–780.CrossRefGoogle Scholar
GONZALEZ-ESTEVEZ, C., MOMOSE, T., GEHRING, W. J. & SALO, E. ( 2003). Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proceedings of the National Academy of Sciences, USA 100, 14046–14051.CrossRefGoogle Scholar
GRAHAM, M. K., FAIRWEATHER, I. & McGEOWN, J. G. ( 1997). The effects of FaRPs on the motility of isolated muscle strips from the liver fluke, Fasciola hepatica. Parasitology 114, 455–465.CrossRefGoogle Scholar
GRAHAM, M. K., FAIRWEATHER, I. & McGEOWN, J. G. ( 2000). Second messengers mediating mechanical responses to the FaRP GYIRFamide in the fluke Fasciola hepatica. American Journal of Physiology, Regulatory Integrative and Comparative Physiology 279, R2089–R2094.CrossRefGoogle Scholar
GRAHAM, M. K., McGEOWN, J. G. & FAIRWEATHER, I. ( 1999). Ionic mechanisms underlying spontaneous muscle contractions in the liver fluke, Fasciola hepatica. American Journal of Physiology 277, R374–R383.CrossRefGoogle Scholar
GREENBERG, M. J., PAYZA, K., NACHMAN, R. J., HOLMAN, G. M. & PRICE, D. A. ( 1988). Relationships between the FMRFamide-related peptides and other peptide families. Peptides 9, 125–135.CrossRefGoogle Scholar
HALTON, D. W. & GUSTAFSSON, M. K. S. ( 1996). Functional morphology of the platyhelminth nervous system. Parasitology 113 (Suppl.), S47–S72.CrossRefGoogle Scholar
HALTON, D. W. & MAULE, A. G. ( 2004). Flatworm nerve-muscle: structural and functional analysis. Canadian Journal of Zoology 82, 316–333.CrossRefGoogle Scholar
HAUSER, F., WILLIAMSON, M. & GRIMMELIKHUIJZEN, C. J. ( 1997). Molecular cloning of a peptidylglycine alpha-hydroxylating monooxygenase from sea anemones. Biochemical and Biophysical Research Communications 241, 509–512.CrossRefGoogle Scholar
HEYERS, O., WALDUCK, A. K., BRINDLEY, P. J., BLEISS, W., LUCIUS, R., DORBIC, T., WITTIG, B. & KALINNA, B. H. ( 2003). Schistosoma mansoni miracidia transformed by particle bombardment infect Biomphalaria glabrata snails and develop into transgenic sporocysts. Experimental Parasitology 105, 174–178.CrossRefGoogle Scholar
HRčková, G., VELEBNY, S., HALTON, D. W., DAY, T. A. & MAULE, A. G. ( 2004). Pharmacological characterisation of neuropeptide F (NPF)-induced effects on the motility of Mesocestoides corti (syn. Mesocestoides vogae) larvae. International Journal for Parasitology 34, 83–93.CrossRefGoogle Scholar
HUMPHRIES, J. E., KIMBER, M. J., BARTON, Y. W., HSU, W., MARKS, N. J., GREER, B., HARRIOTT, P., MAULE, A. G. & DAY, T. A. ( 2004). Structure and bioactivity of neuropeptide F from the human parasites Schistosoma mansoni and Schistosoma japonicum. Journal of Biological Chemistry 279, 39880–39885.CrossRefGoogle Scholar
HUMPHRIES, J. E., MOUSLEY, A., MAULE, A. G. & HALTON, D. W. ( 2000). Neuromusculature structure and functional correlates. In Echinostomes as Experimental Models for Biological Research ( eds B. Fried & T. K. Graczyk), pp. 213–227. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRef
JOHNSTON, R. N., SHAW, C., BRENNAN, G. P., MAULE, A. G. & HALTON, D. W. ( 1995 a). Localisation, quantitation, and characterisation of neuropeptide F- and FMRFamide-immunoreactive peptides in turbellarians and a monogenean: a comparative study. Journal of Comparative Neurology 357, 76–84.Google Scholar
JOHNSTON, R. N., SHAW, C., HALTON, D. W., VERHAERT, P. & BAGUNA, J. ( 1995 b). GYIRFamide: a novel FMRFamide-related peptide (FaRP) from the triclad turbellarian, Dugesia tigrina. Biochemical and Biophysical Research Communications 209, 689–697.Google Scholar
JOHNSTON, R. N., SHAW, C., HALTON, D. W., VERHAERT, P., BLAIR, K. L., BRENNAN, G. P., PRICE, D. A. & ANDERSON, P. A. V. ( 1996). Isolation, localization, and bioactivity of the FMRFamide-related neuropeptides GYIRFamide and YIRFamide from the marine turbellarian Bdelloura candida. Journal of Neurochemistry 67, 814–821.CrossRefGoogle Scholar
KIM, K. & LI, C. ( 2004). Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Journal of Comparative Neurology 475, 540–550.CrossRefGoogle Scholar
KOLHEKAR, A. S., KEUTMANN, H. T., MAINS, R. E., QUON, A. S. & EIPPER, B. A. ( 1997). Peptidylglycine alpha-hydroxylating monooxygenase: active site residues, disulfide linkages, and a two-domain model of the catalytic core. Biochemistry 36, 10901–10909.CrossRefGoogle Scholar
KOTIKOVA, E. A., RAIKOVA, O. I., REUTER, M. & GUSTAFSSON, M. K. ( 2002). The nervous and muscular systems in the free-living flatworm Castrella truncata (Rhabdocoela): an immunocytochemical and phalloidin fluorescence study. Tissue and Cell 34, 365–374.CrossRefGoogle Scholar
KUMAR, D., McGEOWN, J. G., REYNOSO-ducoing, O., AMBROSIO, J. R. & FAIRWEATHER, I. ( 2003). Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepatica. Parasitology 127, 457–473.CrossRefGoogle Scholar
KUMAR, D., WHITE, C., FAIRWEATHER, I. & McGEOWN, J. G. ( 2004). Electrophysiological and pharmacological characterization of K+-currents in muscle fibres isolated from the ventral sucker of Fasciola hepatica. Parasitology 129, 779–793.CrossRefGoogle Scholar
LARHAMMAR, D. ( 1996). Evolution of neuropeptide Y, peptide YY and pancreatic polypeptide. Regulatory Peptides 62, 1–11.CrossRefGoogle Scholar
LI, C., KIM, K. & NELSON, L. S. ( 1999). FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Research 848, 26–34.CrossRefGoogle Scholar
LOVERDE, P. T., HIRAI, H., MERRICK, J. M., LEE, N. H. & EL-SAYED, N. ( 2004). Schistosoma mansoni genome project: an update. Parasitology International 53, 183–192.CrossRefGoogle Scholar
MAGEE, R. M., FAIRWEATHER, I., SHAW, C., McKILLOP, J. M., MONTGOMERY, W. I., JOHNSTON, C. F. & HALTON, D. W. ( 1991). Quantification and partial characterisation of regulatory peptides in the liver fluke, Fasciola hepatica, from different mammalian hosts. Comparative Biochemistry and Physiology. C: Comparative Pharmacology 99, 201–207.CrossRefGoogle Scholar
MAIR, G. R., HALTON, D. W., SHAW, C. & MAULE, A. G. ( 2000 a). The neuropeptide F (NPF) encoding gene from the cestode, Moniezia expansa. Parasitology 120, 71–77.Google Scholar
MAIR, G. R., MAULE, A. G., DAY, T. A. & HALTON, D. W. ( 2000 b). A confocal microscopical study of the musculature of adult Schistosoma mansoni. Parasitology 121, 163–170.Google Scholar
MAIR, G. R., MAULE, A. G., SHAW, C. & HALTON, D. W. ( 1998). Muscling in on parasitic flatworms. Parasitology Today 14, 73–76.CrossRefGoogle Scholar
MAIR, G. R., NICIU, M. J., STEWART, M. T., BRENNAN, G., OMAR, H., HALTON, D. W., MAINS, R., EIPPER, B. A., MAULE, A. G. & DAY, T. A. ( 2004). A functionally atypical amidating enzyme from the human parasite Schistosoma mansoni. FASEB Journal 18, 114–121.CrossRefGoogle Scholar
MARKS, N. J., HALTON, D. W., MAULE, A. G., BRENNAN, G. P., SHAW, C., SOUTHGATE, V. R. & JOHNSTON, C. F. ( 1995). Comparative analyses of the neuropeptide F (NPF)- and FMRFamide-related peptide (FaRP)-immunoreactivities in Fasciola hepatica and Schistosoma spp. Parasitology 110, 371–381.CrossRefGoogle Scholar
MARKS, N. J., JOHNSON, S., MAULE, A. G., HALTON, D. W., SHAW, C., GEARY, T. G., MOORE, S. & THOMPSON, D. P. ( 1996). Physiological effects of platyhelminth RFamide peptides on muscle-strip preparations of Fasciola hepatica (Trematoda: Digenea). Parasitology 113, 393–401.CrossRefGoogle Scholar
MATZ, M. ( 2002). Amplification of representative cDNA samples from microscopic amounts of invertebrate tissue to search for new genes. Methods in Molecular Biology 183, 3–18.CrossRefGoogle Scholar
MATZ, M. ( 2003). Amplification of representative cDNA pools from microscopic amounts of animal tissue. Methods in Molecular Biology 221, 103–116.CrossRefGoogle Scholar
MAULE, A. G., BRENNAN, G. P., HALTON, D. W., SHAW, C., JOHNSTON, C. F. & MOORE, S. ( 1992 b). Neuropeptide F-immunoreactivity in the monogenean parasite Diclidophora merlangi. Parasitology Research 78, 655–660.Google Scholar
MAULE, A. G., HALTON, D. W., ALLEN, J. & FAIRWEATHER, I. ( 1989 b). Studies on motility in vitro of an ectoparasitic monogenean, Diclidophora merlangi. Parasitology 98, 85–93.Google Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., FAIRWEATHER, I. & SHAW, C. ( 1989 a). Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea). International Journal for Parasitology 19, 307–316.Google Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., SHAW, C. & FAIRWEATHER, I. ( 1990 a). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–273.Google Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., SHAW, C. & FAIRWEATHER, I. ( 1990 b). A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite, Diclidophora merlangi. Parasitology Research 76, 409–419.Google Scholar
MAULE, A. G., HALTON, D. W. & SHAW, C. ( 1995). Neuropeptide F: a ubiquitous invertebrate neuromediator? Hydrobiologia 305, 297–303.Google Scholar
MAULE, A. G., HALTON, D. W., SHAW, C. & JOHNSTON, C. F. ( 1993 a). The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106, 429–440.Google Scholar
MAULE, A. G., MOUSLEY, A., MARKS, N. J., DAY, T. A., THOMPSON, D. P., GEARY, T. G. & HALTON, D. W. ( 2002). Neuropeptide signaling systems – potential drug targets for parasite and pest control. Current Topics in Medicinal Chemistry 2, 733–758.CrossRefGoogle Scholar
MAULE, A. G., SHAW, C., HALTON, D. W., BRENNAN, G. P., JOHNSTON, C. F. & MOORE, S. ( 1992 a). Neuropeptide F (Moniezia expansa): localization and characterization using specific antisera. Parasitology 105, 505–512.Google Scholar
MAULE, A. G., SHAW, C., HALTON, D. W., CURRY, W. J. & THIM, L. ( 1994). RYIRFamide: a turbellarian FMRFamide-related peptide (FaRP). Regulatory Peptides 50, 37–43.CrossRefGoogle Scholar
MAULE, A. G., SHAW, C., HALTON, D. W. & THIM, L. ( 1993 b). GNFFRFamide: a novel FMRFamide-immunoreactive peptide isolated from the sheep tapeworm, Moniezia expansa. Biochemical and Biophysical Research Communications 193, 1054–1060.Google Scholar
MAULE, A. G., SHAW, C., HALTON, D. W., THIM, L., JOHNSTON, C. F., FAIRWEATHER, I. & BUCHANAN, K. D. ( 1991). Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102, 309–316.CrossRefGoogle Scholar
MCVEIGH, P., LEECH, S., MAIR, G. R., MARKS, N. J., GEARY, T. G. & MAULE, A. G. ( 2005). Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. International Journal for Parasitology 35, 1043–1060.CrossRefGoogle Scholar
MICHEL, M. C. ( 1991). Receptors for neuropeptide Y: multiple subtypes and multiple second messengers. Trends in Pharmacological Sciences 12, 389–394.CrossRefGoogle Scholar
MICHEL, M. C., BECK-sickinger, A., COX, H., DOODS, H. N., HERZOG, H., LARHAMMAR, D., QUIRION, R., SCHWARTZ, T. & WESTFALL, T. ( 1998). XVI International Union of Pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacological Reviews 50, 143–150.Google Scholar
MIHARA, S., SHIGERI, Y. & FUJIMOTO, M. ( 1989). Neuropeptide Y-induced intracellular Ca2+ increases in vascular smooth muscle cells. FEBS Letters 259, 79–82.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, 447–455.CrossRefGoogle Scholar
MONEYPENNY, C. G., MAULE, A. G., SHAW, C., DAY, T. A., PAX, R. A. & HALTON, D. W. ( 1997). Physiological effects of platyhelminth FMRF amide-related peptides (FaRPs) on the motility of the monogenean Diclidophora merlangi. Parasitology 115, 281–288.CrossRefGoogle Scholar
MOTULSKY, H. J. & MICHEL, M. C. ( 1988). Neuropeptide Y mobilizes Ca2+ and inhibits adenylate cyclase in human erythroleukemia cells. American Journal of Physiology 255, E880–E885.CrossRefGoogle Scholar
MOUSLEY, A., MARKS, N. J., HALTON, D. W., GEARY, T. G., THOMPSON, D. P. & MAULE, A. G. ( 2004). Arthropod FMRFamide-related peptides modulate muscle activity in helminths. International Journal for Parasitology 34, 755–768.CrossRefGoogle Scholar
NOEL, F., CUNHA, V. M., SILVA, C. L. & MENDONCA-SILVA, D. L. ( 2001). Control of calcium homeostasis in Schistosoma mansoni. Memorias do Instituto Oswaldo Cruz 96S, 85–88.CrossRefGoogle Scholar
OUIMET, T., MAMMARBACHI, A., CLOUTIER, T., SEIDAH, N. G. & CASTELLUCI, V. F. ( 1994). cDNA structure and in situ localization of the Aplysia californica pro-hormone convertase PC2. FEBS Letters 337, 119–120.Google Scholar
PAASONEN, M. K. & VARTIAINEN, A. ( 1958). Pharmacological studies on the body wall musculature of cat tapeworm (Taenia taeniaeformis). Acta Pharmacologica et Toxicologica 15, 29–36.CrossRefGoogle Scholar
PIERCE, S. B., COSTA, M., WISOTZKEY, R., DEVADHAR, S., HOMBURGER, S. A., BUCHMAN, A. R., FERGUSON, K. C., HELLER, J., PLATT, D. M., PASQUINELLI, A. A., LIU, L. X., DOBERSTEIN, S. K. & RUVKUN, G. ( 2001). Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes and Development 15, 672–686.Google Scholar
PRICE, D. A. & GREENBERG, M. J. ( 1977). Structure of a molluscan cardioexcitatory neuropeptide. Science 197, 670–671.CrossRefGoogle Scholar
PRIGGE, S. T., MAINS, R. E., EIPPER, B. A. & AMZEL, L. M. ( 2000). New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cellular and Molecular Life Sciences 57, 1236–1259.CrossRefGoogle Scholar
REDDIEN, P. W., BERMANGE, A. L., MURFITT, K. J., JENNINGS, J. R. & SANCHEZ ALVARADO, A. ( 2005). Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Developmental Cell 8, 635–649.CrossRefGoogle Scholar
REUTER, M., GUSTAFSSON, M. K., SAHLGREN, C., HALTON, D. W., MAULE, A. G. & SHAW, C. ( 1995 b). The nervous system of Tricladida. I. Neuroanatomy of Procerodes littoralis (Maricola, Procerodidae): an immunocytochemical study. Invertebrate Neuroscience 1, 113–122.Google Scholar
REUTER, M., MAULE, A. G., HALTON, D. W., GUSTAFSSON, M. K. S. & SHAW, C. ( 1995 a). The organization of the nervous system in Platyhelminthes. The neuropeptide F-immunoreactive pattern in Catenulida, Macrostomida, Proseriata. Zoomorphology 115, 83–97.Google Scholar
SAMII, S. I. & WEBB, R. A. ( 1996). The stimulatory effect of L-glutamate and related agents on inositol 1,4,5-trisphosphate production in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology. Part C, Pharmacology, Toxicology and Endocrinology 113, 409–420.CrossRefGoogle Scholar
SANCHEZ alvarado, A., NEWMARK, P. A., ROBB, S. M. & JUSTE, R. ( 2002). The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129, 5659–5665.CrossRefGoogle Scholar
šEBELOVÁ, S., STEWART, M. T., MOUSLEY, A., FRIED, B., MARKS, N. J. & HALTON, D. W. ( 2004). The musculature and associated innervation of adult and intramolluscan stages of Echinostoma caproni (Trematoda) visualised by confocal microscopy. Parasitology Research 93, 196–206.CrossRefGoogle Scholar
SEIDAH, N. G., DAY, R., MARCINKIEWICZ, M. & CHRETIEN, M. ( 1998). Precursor convertases: an evolutionary ancient, cell-specific, combinatorial mechanism yielding diverse bioactive peptides and proteins. Annals of the New York Academy of Sciences 839, 9–24.CrossRefGoogle Scholar
SHAW, C., MAULE, A. G. & HALTON, D. W. ( 1996). Platyhelminth FMRFamide-related peptides. International Journal for Parasitology 26, 335–345.CrossRefGoogle Scholar
SKELLY, P. J., DA'DARA, A. & HARN, D. A. ( 2003). Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363–369.CrossRefGoogle Scholar
SKUCE, P. J., JOHNSTON, C. F., FAIRWEATHER, I., HALTON, D. W., SHAW, C. & BUCHANAN, K. D. ( 1990). Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell and Tissue Research 261, 573–581.CrossRefGoogle Scholar
SMIT, A. B., SPIJKER, S. & GERAERTS, W. P. ( 1992). Molluscan putative prohormone convertases: structural diversity in the central nervous system of Lymnaea stagnalis. FEBS Letters 312, 213–218.CrossRefGoogle Scholar
STEWART, M. T., MARKS, N. J. & HALTON, D. W. ( 2003). Neuroactive substances and associated major muscle systems in Bucephaloides gracilescens (Trematoda: Digenea) metacercaria and adult. Parasitology Research 91, 12–21.CrossRefGoogle Scholar
STEWART, M. T., MOUSLEY, A., KOUBKOVA, B., šEBELOVÁ, S., MARKS, N. J. & HALTON, D. W. ( 2003 a). Development in vitro of the neuromusculature of two strigeid trematodes, Apatemon cobitidis proterorhini and Cotylurus erraticus. International Journal for Parasitology 33, 413–424.Google Scholar
STEWART, M. T., MOUSLEY, A., KOUBKOVA, B., šEBELOVÁ, S., MARKS, N. J. & HALTON, D. W. ( 2003 b). Gross anatomy of the muscle systems and associated innervation of Apatemon cobitidis proterorhini metacercaria (Trematoda: Strigeidea), as visualized by confocal microscopy. Parasitology 126, 273–282.Google Scholar
TENSEN, C. P., COX, K. J., BURKE, J. F., LEURS, R., VAN der schors, R. C., GERAERTS, W. P., VREUGDENHIL, E. & HEERIKHUIZEN, H. ( 1998). Molecular cloning and characterization of an invertebrate homologue of a neuropeptide Y receptor. European Journal of Neuroscience 10, 3409–3416.CrossRefGoogle Scholar
TERADA, M., ISHII, A. I., KINO, H. & SANO, M. ( 1982). Studies on chemotherapy of parasitic helminths (VI) effects of various neuropharmacological agents on the motility of Dipylidium caninum. Japanese Journal of Pharmacology 32, 479–488.CrossRefGoogle Scholar
WIEST, P. M., LI, Y. N., BURNHAM, D. C., OLDS, G. R. & BOWEN, W. D. ( 1992). Schistosoma mansoni: characterization of phosphoinositide response. Experimental Parasitology 74, 38–45.CrossRefGoogle Scholar
WILLIAMSON, M., HAUSER, F. & GRIMMELIKHUIJZEN, C. J. ( 2000). Genomic organization and splicing variants of a peptidylglycine alpha-hydroxylating monooxygenase from sea anemones. Biochemical and Biophysical Research Communications 277, 7–12.CrossRefGoogle Scholar
WIPPERSTEG, V., KAPP, K., KUNZ, W., JACKSTADT, W. P., ZAHNER, H. & GREVELDING, C. G. ( 2002). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141–150.CrossRefGoogle Scholar
WIPPERSTEG, V., RIBEIRO, F., LIEDTKE, S., KUSEL, J. R. & GREVELDING, C. G. ( 2003). The uptake of Texas Red-BSA in the excretory system of schistosomes and its colocalisation with ER60 promoter-induced GFP in transiently transformed adult males. International Journal for Parasitology 33, 1139–1143.CrossRefGoogle Scholar
WIPPERSTEG, V., SAJID, M., WALSHE, D., KHIEM, D., SALTER, J. P., McKERROW, J. H., GREVELDING, C. G. & CAFFREY, C. R. ( 2005). Biolistic transformation of Schistosoma mansoni with 5′ flanking regions of two peptidase genes promotes tissue-specific expression. International Journal for Parasitology 35, 583–589.CrossRefGoogle Scholar
YEW, J. Y., KUTZ, K. K., DIKLER, S., MESSINGER, L., LI, L. & STRETTON, A. O. ( 2005). Mass spectrometric map of neuropeptide expression in Ascaris suum. Journal of Comparative Neurology 488, 396–413.CrossRefGoogle Scholar
ZURAWSKI, T. H., MOUSLEY, A., MAIR, G. R., BRENNAN, G. P., MAULE, A. G., GELNAR, M. & HALTON, D. W. ( 2001). Immunomicroscopical observations on the nervous system of adult Eudiplozoon nipponicum (Monogenea: Diplozoidae). International Journal for Parasitology 31, 783–792.CrossRefGoogle Scholar