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Signal transduction in larval trematodes: putative systems associated with regulating larval motility and behaviour

Published online by Cambridge University Press:  29 March 2006

J. J. VERMEIRE
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706 USA.
J. E. HUMPHRIES
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706 USA.
T. P. YOSHINO
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706 USA.

Abstract

The multi-host lifestyle of parasitic trematodes necessitates their ability to communicate with their external environment in order to invade and navigate within their hosts' internal environment. Through recent EST and genome sequencing efforts, it has become clear that members of the Trematoda possess many of the elaborate signal transduction systems that have been delineated in other invertebrate model systems like Drosophila melanogaster and Caenorhabditis elegans. Gene homologues representing several well-described signal receptor families including receptor tyrosine kinases, receptor serine tyrosine kinases, G protein-coupled receptors and elements of their downstream signalling systems have been identified in larval trematodes. A majority of this work has focused on the blood flukes, Schistosoma spp. and therefore represents a narrow sampling of the diverse digenean helminth taxon. Despite this fact and given the substantial evidence supporting the existence of such signalling systems, the question then becomes, how are these systems employed by larval trematodes to aid them in interpreting signals received from their immediate environment to initiate appropriate responses in cells and tissues comprising the developing parasite stages? High-throughput, genome-wide analysis tools now allow us to begin to functionally characterize genes differentially expressed throughout the development of trematode larvae. Investigation of the systems used by these parasites to receive and transduce external signals may facilitate the creation of technologies for achieving control of intramolluscan schistosome infections and also continue to yield valuable insights into the basic mechanisms regulating motility and behaviour in this important group of helminths.

Type
Research Article
Copyright
2005 Cambridge University Press

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References

REFERENCES

ABDUL-SALAM, J. & SREELATHA, B. S. ( 2004). Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae). Parasitology International 53, 1121.Google Scholar
AGAISSE, H. & PERRIMON, N. ( 2004). The roles of JAK/STAT signalling in Drosophila immune responses. Immunological Reviews 198, 7282.CrossRefGoogle Scholar
BARGMANN, C. I. ( 1998). Neurobiology of the Caenorhabditis elegans genome. Science 282, 20282033.CrossRefGoogle Scholar
BAYNE, C. J. & GREVELDING, C. G. ( 2003). Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. Journal of Parasitology 89, 10561060.CrossRefGoogle Scholar
BEALL, M. J., McGONIGLE, S. & PEARCE, E. J. ( 2000). Functional conservation of Schistosoma mansoni Smads in TGF-β signalling. Molecular and Biochemical Parasitology 111, 131142.CrossRefGoogle Scholar
BEALL, M. J. & PEARCE, E. J. ( 2001). Human transforming growth factor-β activates a receptor serine/threonine kinase from the intravascular parasite Schistosoma mansoni. Journal of Biological Chemistry 276, 3161331619.CrossRefGoogle Scholar
BOGEA, T. & CAIRA, J. ( 2001). Ultrastructure and chaetotaxy of sensory receptors in the cercaria of a species of Allopodocotyle Pritchard, 1966 (Digenea: Opecoelidae). Memorias do Instituto Oswaldo Cruz 96, 205214.CrossRefGoogle Scholar
BOYLE, J. P., HILLYER, J. F. & YOSHINO, T. P. ( 2003). Pharmacological and autoradiographical characterization of serotonin transporter-like activity in sporocysts of the human blood fluke, Schistosoma mansoni. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioural Physiology 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. & YOSHINO, T. P. ( 2005). Serotonin-induced muscular activity in Schistosoma mansoni larval stages: importance of 5-HT transport and role in daughter sporocyst production. Journal of Parasitology, in press.CrossRefGoogle Scholar
BOYLE, J. P., ZAIDE, J. V. & YOSHINO, T. P. ( 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
BRODY, T. & CRAVCHIK, A. ( 2000). Drosophila melanogaster G protein-coupled receptors. Journal of Cell Biology 150, F838.Google Scholar
CORRENTI, J. M. & PEARCE, E. J. ( 2004). Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Molecular and Biochemical Parasitology 137, 7579.CrossRefGoogle Scholar
DAVIES, S. J., SHOEMAKER, C. B. & PEARCE, E. J. ( 1998). A divergent member of the transforming growth factor-β receptor family from Schistosoma mansoni is expressed on the parasite surface membrane. Journal of Biological Chemistry 273, 1123411240.CrossRefGoogle Scholar
DAVIS, R. E., PARRA, A., LOVERDE, P. T., RIBEIRO, E., GLORIOSO, G. & HODGSON, S. ( 1999). Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proceedings of the National Academy of Sciences, USA 96, 86878692.CrossRefGoogle Scholar
DE JONG-BRINK, M. ( 1995). How schistosomes profit from the stress responses they elicit in their hosts. Advances in Parasitology 35, 177256.CrossRefGoogle Scholar
DORSEY, C. H., COUSIN, C. E., LEWIS, F. A. & STIREWALT, M. A. ( 2002). Ultrastructure of the Schistosoma mansoni cercaria. Micron 33, 279323.CrossRefGoogle Scholar
FALKE, J. J., BASS, R. B., BUTLER, S. L., CHERVITZ, S. A. & DANIELSON, M. A. ( 1997). The two-component signalling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annual Review of Cell and Developmental Biology 13, 457512.CrossRefGoogle Scholar
FALKE, J. J. & HAZELBAUER, G. L. ( 2001). Transmembrane signalling in bacterial chemoreceptors. Trends in Biochemical Sciences 26, 257265.CrossRefGoogle Scholar
FITZPATRICK, J. M., JOHNSTON, D. A., WILLIAMS, G. W., WILLIAMS, D. J., FREEMAN, T. C., DUNNE, D. W. & HOFFMANN, K. F. ( 2005). An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Molecular and Biochemical Parasitology 141, 113.CrossRefGoogle Scholar
FORRESTER, S. G., WARFEL, P. W. & PEARCE, E. J. ( 2004). Tegumental expression of a novel type II receptor serine/threonine kinase (SmRK2) in Schistosoma mansoni. Molecular and Biochemical Parasitology 136, 149156.CrossRefGoogle Scholar
FRANCO, G. R., VALADAO, A. F., AZEVEDO, V. & RABLEO, E. M. ( 2000). The Schistosoma gene discovery program: state of the art. International Journal for Parasitology 30, 453463.CrossRefGoogle Scholar
GETHER, U. & KOBILKA, B. K. ( 1998). G protein-coupled receptors. II. Mechanism of agonist activation. Journal of Biological Chemistry 273, 1797917982.CrossRefGoogle Scholar
HABERL, B., KORNER, M., SPENGLER, Y., HERTEL, J., KALBE, M. & HAAS, W. ( 1999). Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology 120, 479486.Google Scholar
HAMDAN, F. F., ABRAMOVITZ, M., MOUSA, A., XIE, J., DUROCHER, Y. & RIBEIRO, P. ( 2002). A novel Schistosoma mansoni G protein-coupled receptor is responsive to histamine. Molecular and Biochemical Parasitology 119, 7586.CrossRefGoogle Scholar
HAMM, H. E. ( 1998). The many faces of G protein signalling. Journal of Biological Chemistry 273, 669672.CrossRefGoogle Scholar
HILL, C. A., FOX, A. N., PITTS, R. J., KENT, L. B., TAN, P. L., CHRYSTAL, M. A., CRAVCHIK, A., COLLINS, F. H., ROBERTSON, H. M. & ZWIEBEL, L. J. ( 2002). G protein-coupled receptors in Anopheles gambiae. Science 298, 176178.CrossRefGoogle Scholar
HOFFMANN, K. F., DAVIS, E. M., FISCHER, E. R. & WYNN, T. A. ( 2001). The guanine protein coupled receptor rhodopsin is developmentally regulated in the free-living stages of Schistosoma mansoni. Molecular and Biochemical Parasitology 112, 113123.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
HUANG, H. C. & KLEIN, P. S. ( 2004). The frizzled family: receptors for multiple signal transduction pathways. Genome Biology 5, 234 (PMID: 15239825).Google Scholar
ILTZSCH, M. H., BIEBER, D., VIJAYASARATHY, S., WEBSTER, P., ZURITA, M., DING, J. & MANSOUR, T. E. ( 1992). Cloning and characterization of a cDNA coding for the α-subunit of a stimulatory G protein from Schistosoma mansoni. Journal of Biological Chemistry 267, 1450414508.Google Scholar
KALBE, M., HABERL, B. & HAAS, W. ( 2000). Snail host finding by Fasciola hepatica and Trichobilharzia ocellata: compound analysis of “miracidia-attracting glycoproteins”. Experimental Parasitology 96, 231242.CrossRefGoogle Scholar
KAMPKOTTER, A., RIDGERS, I., JOHNSTON, D. A., ROLLINSON, D., KUNZ, W. & GREVELDING, C. G. ( 1999) Schistosoma mansoni: cloning and characterization of the Ras homologue. Experimental Parasitology 91, 280283.CrossRefGoogle Scholar
LARDANS, V. & DISSOUS, C. ( 1998). Snail control strategies for reduction of schistosomiasis transmission. Parasitology Today 14, 413417.CrossRefGoogle Scholar
LEASK, A. & ABRAHAM, D. J. ( 2004). TGF-β signalling and the fibrotic response. FASEB Journal 18, 816827.CrossRefGoogle Scholar
MANSOUR, T. E. ( 1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 136.Google 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
McGONIGLE, S., BEALL, M. J., FEENEY, E. L. & PEARCE, E. J. ( 2001 a). Conserved role for 14-3-3ε downstream of type I TGF-β receptors. FEBS Letters 490, 6569.Google Scholar
McGONIGLE, S., BEALL, M. J. & PEARCE, E. J. ( 2002). Eukaryotic initiation factor 2α associates with TGF-β receptors and 14-3-3ε and acts as a modulator of the TGF-β response. Biochemistry 41, 579587.CrossRefGoogle Scholar
MCGONIGLE, S., FEENEY, E. L., BEALL, M. J. & PEARCE, E. J. ( 2001 b). SIP, a novel SH3 domain–containing protein, interacts with Schistosoma mansoni receptor kinase 1. Molecular and Biochemical Parasitology 114, 119123.Google Scholar
MERRICK, J. M., OSMAN, A., TSAI, J., QUACKENBUSH, J., LOVERDE, P. T. & LEE, N. H. ( 2003). The Schistosoma mansoni gene index: gene discovery and biology by reconstruction and analysis of expressed gene sequences. Journal of Parasitology 89, 261269.CrossRefGoogle Scholar
MORTON, D. B. ( 2004). Invertebrates yield a plethora of atypical guanylyl cyclases. Molecular Neurobiology 29, 96116.CrossRefGoogle Scholar
NEWTON, A. C. ( 1995). Protein kinase C: structure, function, and regulation. Journal of Biological Chemistry 270, 2849528498.CrossRefGoogle Scholar
NODA, M., HIGASHIDA, H., AOKI, S. & WADA, K. ( 2004). Multiple signal transduction pathways mediated by 5-HT receptors. Molecular Neurobiology 29, 3139.CrossRefGoogle Scholar
OSMAN, A., NILES, E. G. & LOVERDE, P. T. ( 2001). Identification and characterization of a Smad2 homologue from Schistosoma mansoni, a transforming growth factor-β signal transducer. Journal of Biological Chemistry 276, 1007210082.CrossRefGoogle Scholar
OSMAN, A., NILES, E. G. & LOVERDE, P. T. ( 2004). Expression of functional Schistosoma mansoni Smad4: Role in Erk-mediated transforming growth factor β (TGF-β) down-regulation. Journal of Biological Chemistry 279, 64746486.CrossRefGoogle Scholar
PAN, S. C. ( 1980). The fine structure of the miracidium of Schistosoma mansoni. Journal of Invertebrate Pathology 36, 307372.CrossRefGoogle Scholar
PAX, R. A., BRICKER, C. S., THOMPSON, D. P., SEMEYN, D. R. & BENNETT, J. L. ( 1983). Neurophysiology of adult male Schistosoma mansoni. Pharmacological Therapeutics 22, 117125.CrossRefGoogle Scholar
PROSDOCIMI, F., FARIA-CAMPOS, A. C., PEIXOTO, F. C., PENA, S. D. J., ORTEGA, J. M. & FRANCO, G. R. ( 2002). Clustering of Schistosoma mansoni mRNA sequences and analysis of the most transcribed genes: implications in metabolism and biology of different developmental stages. Memorias do Instituto Oswaldo Cruz 97, 6169.CrossRefGoogle Scholar
RAMACHANDRAN, H., SKELLY, P. J. & SHOEMAKER, C. B. ( 1996). The Schistosoma mansoni epidermal growth factor receptor homologue, SER, has tyrosine kinase activity and is localized in adult muscle. Molecular and Biochemical Parasitology 83, 110.CrossRefGoogle Scholar
SAKAGUCHI, A., MATSUMOTO, K. & HISAMOTO, N. ( 2004). Roles of MAP kinase cascades in Caenorhabditis elegans. Journal of Biochemistry 136, 711.CrossRefGoogle Scholar
SALZET, M., CAPRON, A. & STEFANO, G. B. ( 2000). Molecular crosstalk in host-parasite relationships: schistosome- and leech-host interactions. Parasitology Today 16, 536540.CrossRefGoogle Scholar
SANTOS, T. M., JOHNSTON, D. A., AZEVEDO, V., RIDGERS, I. L., MARTINEZ, M. F., MAROTTA, G. B., SANTOS, R. L., FONSECA, S. J., ORTEGA, J. M., RABELO, E. M., SABER, M., AHMED, H. M., ROMEIH, M. H., FRANCO, G. R., ROLLINSON, D. & PENA, S. D. ( 1999). Analysis of the gene expression profile of Schistosoma mansoni cercariae using the expressed sequence tag approach. Molecular and Biochemical Parasitology 103, 7997.CrossRefGoogle Scholar
SCHELL, S. C. ( 1985). Handbook of Trematodes of North America. University Press of Idaho ( Moscow, Idaho), 263 pp.
SCHUSSLER, P., GREVELDING, C. G. & KUNZ, W. ( 1997). Identification of Ras, MAP kinases, and a GAP protein in Schistosoma mansoni by immunoblotting and their putative involvement in male-female interaction. Parasitology 115, 629634.CrossRefGoogle Scholar
SCHUTTE, C. H. J. ( 1974). Studies on the South African strain of Schistosoma mansoni. 2. The intra-molluscan larval stages. South African Journal of Science 70, 327346.Google Scholar
SHOEMAKER, C. B., RAMACHANDRAN, H., LANDA, A., MITERMAYER, G. R. & STEIN, L. D. ( 1992). Alternative splicing of the Schistosoma mansoni gene encoding a homologue of epidermal growth factor receptor. Molecular and Biochemical Parasitology 53, 1732.CrossRefGoogle Scholar
SHOOP, W. L. ( 1988). Trematode transmission patterns. Journal of Parasitology 74, 4659.CrossRefGoogle Scholar
SHORT, R. B. & GAGNE, H. T. ( 1975). Fine structure of possible photoreceptor in cercariae of Schistosoma mansoni. Journal of Parasitology 61, 6974.CrossRefGoogle Scholar
SIMON, M. I., STRATHMANN, M. P. & GAUTAN, N. ( 1991). Diversity of G proteins in signal transduction. Science 252, 802808.CrossRefGoogle Scholar
SOPOTT-EHLERS, B., HAAS, W. & EHLERS, U. ( 2003). Ultrastructure of pigmented and unpigmented photoreceptors in cercariae of Trichobilharzia ocellata (Platyhelminthes, Trematoda, Schistosomatidae): evidence for the evolution of parasitism in Neodermata. Parasitology Research 91, 109116.CrossRefGoogle Scholar
STURROCK, R. F. ( 2001). The schistosomes and their intermediate hosts. In Schistosomiasis ( Ed. Mahmoud, A. A. F.). Imperial College Press, London. pp. 784.CrossRef
VERJOVSKI-almeida, S., DEMARCO, R., MARTINS, E. A., GUIMARAES, P. E., OJOPI, E. P., PAQUOLA, A. C., PIAZZA, J. P., NISHIYAMA, M. Y. Jr, kitajima, j. p., ADAMSON, R. E., ASHTON, P. D., BONALDO, M. F., COULSON, P. S., DILLON, G. P., FARIAS, L. P., GREGORIO, S. P., HO, P. L., LEITE, R. A., MALAQUIAS, L. C., MARQUES, R. C., MIYASATO, P. A., NASCIMENTO, A. L., OHLWEILER, F. P., REIS, E. M., RIBEIRO, M. A., SA, R. G., STUKART, G. C., SOARES, M. B., GARGIONI, C., KAWANO, T., RODRIGUES, V., MADEIRA, A. M., WILSON, R. A., MENCK, C. F., SETUBAL, J. C., LEITE, L. C. & DIAS-NETO, E. ( 2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148157.CrossRefGoogle Scholar
VERMEIRE, J. J., BOYLE, J. P. & YOSHINO, T. P. ( 2004). Differential gene expression and the effects of Biomphalaria glabrata embryonic (Bge) cell factors during larval Schistosoma mansoni development. Molecular and Biochemical Parasitology 135, 153157.CrossRefGoogle Scholar
VICOGNE, J., CAILLIAU, K., TULASNE, D., BROWAEYS, E., YAN, Y. T., FAFEUR, V., VILAIN, J. P., LEGRAND, D., TROLET, J. & DISSOUS, C. ( 2004). Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. Journal of Biological Chemistry 279, 3740737414.CrossRefGoogle Scholar
VICOGNE, J. & DISSOUS, C. ( 2003). Schistosoma mansoni receptor tyrosine kinases: towards new therapeutic targets. Journal de la Société de biologie 197, 367373.CrossRefGoogle Scholar
VICOGNE, J., PIN, J. P., LARDANS, V., CAPRON, M., NOEL, C. & DISSOUS, C. ( 2003). An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Molecular and Biochemical Parasitology 126, 5162.CrossRefGoogle Scholar
WILDERING, W. C., HERMANN, P. M. & BULLOCH, A. G. M. ( 2001). Lymnaea epidermal growth factor promotes axonal regeneration in CNS organ culture. Journal of Neuroscience 21, 93459354.Google Scholar
WOLANIN, P. M., THOMASON, P. A. & STOCK, J. B. ( 2002). Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biology 3, reviews 3013.1–3013.8.Google Scholar
WONG, R. W. C. & GUILLARD, L. ( 2004). The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine and Growth Factor Reviews 15, 147156.CrossRefGoogle Scholar
ZDARSKA, Z. ( 1992). Transmission electron microscopy of sensory receptors of Echinostoma revolutum (Froelich 1802) cercaria (Digenea: Echinostomatidae). Parasitology Research 78, 598606.CrossRefGoogle Scholar