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Neuromuscular function in plant parasitic nematodes: a target for novel control strategies?

Published online by Cambridge University Press:  29 March 2006

M. J. KIMBER  and
C. C. FLEMING
M. J. KIMBER
Affiliation:
Department of Biomedical Sciences, Iowa State University, Ames, IA. 50011, USA
C. C. FLEMING
Affiliation:
Applied Plant Science, Queen's University Belfast, Newforge Lane, Belfast. BT9 5PX, UK Department of Agriculture and Rural Development for Northern Ireland, Newforge Lane, Belfast, BT9 5PX, UK
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Abstract

Over the last decade the need for new strategies and compounds to control parasitic helminths has become increasingly urgent. The neuromuscular systems of these worms have been espoused as potential sources of target molecules for new drugs which may address this need. One facet of helminth neuromuscular biology which has garnered considerable research interest is that of neuropeptidergic neurotransmission, particularly regarding parasites of humans and animals, as well as free-living nematode model species. This research interest has been piqued by the fact that neuropeptides have been demonstrated to be fundamentally important to nematode biology and thus may be of utility in this search for new drug targets. This review focuses on the neuropeptide biology of plant parasitic nematodes, a subject which has been comparatively neglected despite the fact that the search for alternative control measures also extends to these economically important parasites. We focus on the FMRFamide-like peptide (FLP) neuropeptides and the complexity and distribution of this peptide family in plant parasitic nematodes. Possible roles for FLPs in plant parasitic nematode behaviour, as elucidated by a combination of molecular imaging techniques and RNA interference (RNAi), are discussed. We propose that disruption of FLP neurosignalling in plant parasitic nematodes represents a novel form of pest control and speculate as to how this may be achieved.

Keywords

Nematodeplant parasitic nematodeneuropeptideFMRFamide-like peptideFLPindirect immunocytochemistryin situ hybridizationRNAi

Information

Type
Research Article
Information
Parasitology , Volume 131 , Supplement S1: Parasite neuromusculature and its utility as a drug target , October 2005 , pp. S129 - S142
Copyright
2005 Cambridge University Press

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References

REFERENCES

ABOOBAKER, A. A. & BLAXTER, M. L. ( 2003). Use of RNA interference to investigate gene function in the human filarial nematode parasite Brugia malayi. Molecular and Biochemical Parasitology 129, 41–51.CrossRefGoogle Scholar
ANDERSON, R. V. & BYERS, J. R. ( 1975). Ultrastructure of the esophageal procorpus in the plant parasitic nematode, Tylenchorhynchus dubius, and functional aspects in relation to feeding. Canadian Journal of Zoology 53, 1581–1595.CrossRefGoogle Scholar
ATKINSON, H. J., ISAAC, R. E., HARRIS, P. D. & SHARPE, C. M. ( 1988). FMRFamide immunoreactivity within the nervous system of the nematodes Panagrellus redivivus, Caenorhabditis elegans and Heterodera glycines. Journal of Zoology 216, 663–671.Google Scholar
BOUTLA, A., KALANTIDIS, K., TAVERNARAKIS, N., TSAGRIS, M. & TABLER, M. ( 2002). Induction of RNA interference in Caenorhabditis elegans by RNAs derived from plants exhibiting post-transcriptional gene silencing. Nucleic Acids Research 30, 1688–1694.CrossRefGoogle Scholar
BOWMAN, J. W., FRIEDMAN, A. R., THOMPSON, D. P., ICHHPURANI, A. K., KELLMAN, M. F., MARKS, N., MAULE, A. G. & GEARY, T. G. ( 1996). Structure-activity relationships of KNEFIRFamide (AF1), a nematode FMRFamide-related peptide, on Ascaris suum muscle. Peptides 17, 381–387.CrossRefGoogle Scholar
BROWNLEE, D. J. A., BRENNAN, G. P., HALTON, D. W., FAIRWEATHER, I. & SHAW, C. ( 1994). Ultrastructural localization of pancreatic polypeptide- and FMRFamide immunoreactivities within the central nervous system of the nematode, Ascaris suum (Nematoda: Ascaroidea). Parasitology 108, 587–593.CrossRefGoogle Scholar
BROWNLEE, D. J. A., FAIRWEATHER, I., JOHNSTON, C. F., SMART, D. & SHAW, C. ( 1993). Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology Research 79, 302–308.CrossRefGoogle Scholar
BROWNLEE, D. J. A., HOLDEN-DYE, L., FAIRWEATHER, I. & WALKER, R. J. ( 1995). The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the nematode Ascaris suum. Parasitology 111, 379–384.CrossRefGoogle Scholar
BROWNLEE, D. J. A. & WALKER, R. J. ( 1999). Actions of nematode FMRFamide-related peptides on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Annals of the New York Academy of Sciences 897, 228–238.CrossRefGoogle Scholar
COWDEN, C., SITHIGORNGUL, P., BRACKLEY, P., GUASTELLA, J. & STRETTON, A. O. W. ( 1993). Localisation and differential expression FMRFamide-like immunoreactivity in the nematode Ascaris suum. Journal of Comparative Neurology 333, 455–468.CrossRefGoogle Scholar
COWDEN, C. & STRETTON, A. O. W. ( 1993). AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides 14, 423–430.CrossRefGoogle Scholar
COWDEN, C. & STRETTON, A. O. W. ( 1995). Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16, 491–500.CrossRefGoogle Scholar
DAVIS, E. L., HUSSEY, R. S. & BAUM, T. J. ( 2004). Getting to the roots of parasitism by nematodes. Trends in Parasitology 20, 134–141.CrossRefGoogle Scholar
DAVIS, E. L., HUSSEY, R. S., BAUM, T. J., BAKKER, J., SCHOTS, A., ROSSO, M.-N. & ABAD, P. ( 2000). Nematode parasitism genes. Annual Review of Phytopathology 38, 365–396.CrossRefGoogle Scholar
DAVIS, R. E. & STRETTON, A. O. W. ( 1996). The motornervous system of Ascaris: electrophysiology and anatomy of the neurones and their control by neuromodulators. Parasitology 113, S99–S117.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
EDISON, A. S., MESSINGER, L. A. & STRETTON, A. O. W ( 1997). Afp-1: a gene encoding multiple transcripts of a new class of FMRFamide-like neuropeptides in the nematode Ascaris suum. Peptides 18, 929–935.CrossRefGoogle Scholar
ESCOBAR, M. A., CIVEROLO, E. L., SUMMERFELT, K. R. & DANDEKAR, A. M. ( 2001). RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proceedings of the National Academy of Sciences, USA 98, 13437–13442.CrossRefGoogle Scholar
FANELLI, E., DI VITO, M., JONES, J. T. & DE giorgi, C. ( 2005). Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene 349, 87–95.CrossRefGoogle Scholar
FELLOWES, R. A., MAULE, A. G., MARKS, N. J., GEARY, T. G., THOMPSON, D. P. & HALTON, D. W. ( 2000). Nematode neuropeptide modulation of the vagina vera of Ascaris suum: in vitro effects of PF1, PF2, PF4, AF3 and AF4. Parasitology 120, 79–89.CrossRefGoogle Scholar
FELLOWES, R. A., MAULE, A. G., MARKS, N. J., GEARY, T. G., THOMPSON, D. P., SHAW, C. & HALTON, D. W. ( 1998). Modulation of the vagina vera of Ascaris suum in vitro by FMRFamide-related peptides. Parasitology 116, 277–287.CrossRefGoogle Scholar
FIRE, A., XU, S., MONTGOMERY, M. K., KOSTAS, S. A., DRIVER, S. E. & MELLO, C. C. ( 1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.CrossRefGoogle Scholar
FRASER, A. G., KAMATH, R. S., ZIPPERLEN, P., MARTINEZ-CAMPOS, M., SOHRMANN, M. & AHRINGER, J. ( 2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325–330.Google Scholar
GEARY, T. G., MARKS, N. J., MAULE, A. G., BOWMAN, J. W., ALEXANDER-BOWMAN, S. J., DAY, T. A., LARSEN, M. J., KUBIAK, T. M., DAVIS, J. P. & THOMPSON, D. P. ( 1999). Pharmacology of FMRFamide-related peptides in helminths. Annals of the New York Academy of Sciences 897, 212–227.CrossRefGoogle Scholar
HUSSEIN, A. S., KICHENIN, K. & SELKIRK, M. E. ( 2002). Suppression of secreted acetylcholinesterase expression in Nippostrongylus brasiliensis by RNA interference. Molecular and Biochemical Parasitology 122, 91–94.CrossRefGoogle Scholar
JAGDALE, G. B. & GORDON, R. ( 1994). Distribution of FMRFamide-like peptide in the nervous system of a mermithid nematode, Romanomermis culicivorax. Parasitology Research 80, 467–473.CrossRefGoogle Scholar
KALANTIDIS, K., PSARADAKIS, S., TABLER, M. & TSAGRIS, M. ( 2002). The occurrence of CMV-specific short RNAs in transgenic tobacco expressing virus-derived double-stranded RNA is indicative of resistance to the virus. Molecular Plant-Microbe Interactions 15, 826–833.CrossRefGoogle Scholar
KAMATH, R. S., MARTINEZ-CAMPOS, M., ZIPPERLEN, P., FRAZER, A. G. & AHRINGER, J. ( 2000). Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biology 2, 1–10.Google Scholar
KEATING, C., THORNDYKE, M. C., HOLDEN-DYE, L., WILLIAMS, R. G. & WALKER, R. J. ( 1995). The isolation of a FMRFamide-like peptide from the nematode Haemonchus contortus. Parasitology 111, 515–521.CrossRefGoogle Scholar
KIMBER, M. J., FLEMING, C. C., BJOURSON, A. J., HALTON, D. W. & MAULE, A. G. ( 2001). FMRFamide-related peptides in potato cyst nematodes. Molecular and Biochemical Parasitology 116, 199–208.CrossRefGoogle Scholar
KIMBER, M. J., FLEMING, C. C., PRIOR, A., JONES, J. T., HALTON, D. W. & MAULE, A. G. ( 2002). Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. International Journal for Parasitology 32, 1095–1105.CrossRefGoogle Scholar
KOVALEVA, E. S., YAKOVLEV, A., MASLER, E. P. & CHITWOOD, D. J. ( 2002). Human proprotein convertase 2 homologue from a plant nematode: cloning, characterization, and comparison with other species. FASEB Journal 16, 1099–1101.CrossRefGoogle Scholar
KUBIAK, T. M., LARSEN, M. J., NULF, S. C., ZANTELLO, M. R., BURTON, K. J., BOWMAN, J. W., MODRIC, T. & LOWERY, D. E. ( 2003 a). 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, 33724–33729.Google Scholar
KUBIAK, T. M., LARSEN, M. J., ZANTELLO, M. R., BOWMAN, J. W., NULF, S. C. & LOWERY, D. E. ( 2003 b). Functional annotation of the putative orphan Caenorhabditis elegans G-protein-coupled receptor C10C6.2 as a FLP15 peptide receptor. Journal of Biological Chemistry 278, 42115–42120.Google Scholar
LI, C., KIM, K. H. & NELSON, L. S. ( 1999). FMRFamide-related gene family in Caenorhabditis elegans. Brain Research 848, 26–34.CrossRefGoogle Scholar
LUSTIGMAN, S., ZHANG, J., LIU, J., OKSOV, Y. & HASHMI, S. ( 2004). RNA interference targeting cathepsin L and Z-like cysteine proteases of Onchocerca volvulus confirmed their essential function during L3 molting. Molecular and Biochemical Parasitology 138, 165–170.CrossRefGoogle Scholar
MAEDA, I., KOHARA, Y., YAMAMOTO, M. & SUGIMOTO, A. ( 2001). Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Current Biology 11, 171–176.CrossRefGoogle Scholar
MARKS, N. J., MAULE, A. G., GEARY, T. G., THOMPSON, D. P., LI, C., HALTON, D. W. & SHAW, C. ( 1998). KSAYMRFamide (PF3/AF8) is present in the free-living nematode, Caenorhabditis elegans. Biochemical and Biophysical Research Communications 248, 422–425.CrossRefGoogle Scholar
MARKS, N. J., SANGSTER, N. C., MAULE, A. G., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & SHAW, C. ( 1999). Structural characterisation and pharmacology of KHEYLRFamide (AF2) and KSAYMRFamide (PF3/AF8) from Haemonchus contortus. Molecular and Biochemical Parasitology 100, 185–194.CrossRefGoogle Scholar
MARKS, N. J., SHAW, C., MAULE, A. G., DAVIS, J. P., HALTON, D. W., VERHAERT, P., GEARY, T. G. & THOMPSON, D. P. ( 1995). Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide-encoding gene. Biochemical and Biophysical Research Communications 217, 845–851.CrossRefGoogle Scholar
MASLER, E. P., KOVALEVA, E. S. & SARDANELLI, S. ( 1999). Comparison of FLP immunoreactivity in free-living nematodes and in the plant-parasitic nematode Heterodera glycines. Annals of the New York Academy of Sciences 897, 253–263.CrossRefGoogle Scholar
MAULE, A. G., GEARY, T. G., BOWMAN, J. W., MARKS, N. J., BLAIR, K. L., HALTON, D. W., SHAW, C. & THOMPSON, D. P. ( 1995). Ascaris suum: Comparative studies on the effects of nematode FMRFamide-related peptides (FLPs) on muscle strip preparations. Invertebrate Neuroscience 1, 255–265.CrossRefGoogle 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., BOWMAN, J. W., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & THIM, L. ( 1994 a). KSAYMRFamide: a novel FMRFamide-related heptapeptide from the free-living nematode, Panagrellus redivivus, which is myoactive in the parasitic nematode, Ascaris suum. Biochemical and Biophysical Research Communications 200, 973–980.Google Scholar
MAULE, A. G., SHAW, C., BOWMAN, J. W., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & THIM, L. ( 1994 b) The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free-living nematode Panagrellus redivivus (Nematoda, Rhabditida). Parasitology 109, 351–356.Google 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
MERTENS, I., VANDINGENEN, A., CLYNEN, E., NACHMAN, R. J., DE LOOF, A. & SCHOOFS, L. ( 2005 a). Characterization of an RFamide-related peptide orphan GPCR in C. elegans. Annals of the New York Academy of Sciences 1040, 410–412.Google Scholar
MERTENS, I., MEEUSEN, T., JANSSEN, T., NACHMAN, R. & SCHOOFS, L. ( 2005 b). Molecular characterization of two G protein-coupled receptor splice variants as FLP2 receptors in Caenorhabditis elegans. Biochemical and Biophysical Research Communications 330, 967–974.Google Scholar
MERTENS, I., VANDINGENEN, A., MEEUSEN, T., JANSSEN, T., LUYTEN, W., NACHMAN, R. J., DE LOOF, A. & SCHOOFS, L. ( 2004). Functional characterization of the putative orphan neuropeptide G-protein coupled receptor C26F1.6 in Caenorhabditis elegans. FEBS Letters 573, 55–60.Google Scholar
MONTGOMERY, M. K., XU, S. & FIRE, A. ( 1998). RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 95, 15502–15507.CrossRefGoogle Scholar
NELSON, L. S., ROSOFF, M. L. & LI, C. ( 1998). Disruption of a neuropeptide gene, flp-1, causes multiple behavioural defects in Caenorhabditis elegans. Science 281, 1686–1690.CrossRefGoogle Scholar
PERRY, R. N. ( 1996). Chemoreception in plant parasitic nematodes. Annual Review of Phytopathology 34, 181–199.CrossRefGoogle Scholar
PERRY, R. N. ( 2001). Analysis of the sensory responses of parasitic nematodes using electrophysiology. International Journal for Parasitology 31, 909–918.CrossRefGoogle Scholar
PURCELL, J., ROBERTSON, A. P., THOMPSON, D. P. & MARTIN, R. J. ( 2002). PF4, a FMRFamide-related peptide, gates low-conductance Cl− channels in Ascaris suum. European Journal of Pharmacology 456, 11–17.CrossRefGoogle Scholar
RACKE, K. D. & COATS, J. R. ( 1990). Enhanced biodegradation of insecticides in midwestern corn soils. American Chemical Society Symposium Series 426, 68–81.CrossRefGoogle Scholar
RICH, J. R., DUNN, R. A. & NOLING, J. W. ( 2004). Nematicides: Past and Present Uses. In Nematology – Advances and Perspectives Volume II: Nematode Management and Utilization ( ed. Chen, Z. X., Chen, S. Y. & Dickson, D. W.), pp. 1179–1200. CABI Publishing, Wallingford, UK.CrossRef
ROGERS, C., REALE, V., KIM, K., CHATWIN, H., LI, C., EVANS, P. & DE BONO, M. ( 2003). Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature Neuroscience 6, 1178–1185.CrossRefGoogle Scholar
SASSER, J. N. & FRECKMAN, D. W. ( 1987). A world perspective on nematology: The role of society, In Vistas on Nematology ( ed. Veech, J. A. & Dickinson, D. W.), pp. 7–14. Society of Nematologists Inc., Hyattsville, MD, USA.
SCHINKMANN, K. & LI, C. ( 1992). Localization of FMRFamide-like peptides in Caenorhabditis elegans. Journal of Comparative Neurology 316, 251–260.CrossRefGoogle Scholar
SCHINKMANN, K. & LI, C. ( 1994). Comparison of two Caenorhabditis genes encoding FMRFamide (Phe-Met-Arg-Phe-NH2)-like peptides. Molecular Brain Research 24, 238–246.CrossRefGoogle Scholar
SMITH, N. A., SINGH, S. P., WANG, M.-B., STOUTJESDIJK, P. A., GREEN, A. G. & WATERHOUSE, P. M. ( 2000). Total silencing by intron-spliced hairpin RNAs. Nature 407, 319–320.Google Scholar
STEWART, G. R., PERRY, R. N. & WRIGHT, D. J. ( 1994). Immunocytochemical studies on the occurrence of gamma-aminobutyric acid in the nervous system of the nematodes, Panagrellus redivivus, Meloidogyne incognita and Globodera rostochiensis. Fundamental and Applied Nematology 17, 433–439.Google Scholar
TABARA, H., GRISHOK, A. & MELLO, C. ( 1998). RNAi in C. elegans: Soaking in the Genome Sequence. Science 282, 430–431.Google Scholar
TAVERNARAKIS, N., WANG, S. L., DOROVKOV, M., RYAZANOV, A. & DRISCOLL, M. ( 2000). Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nature Genetics 24, 180–183.CrossRefGoogle Scholar
TOMARI, Y. & ZAMORE, P. D. ( 2005). Perspective: machines for RNAi. Genes and Development 19, 517–529.CrossRefGoogle Scholar
URWIN, P. E., LILLEY, C. J. & ATKINSON, H. J. ( 2002). Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions 15, 747–752.CrossRefGoogle Scholar
VARSHAVSKY, A. ( 2004). ‘Spalog’ and ‘sequelog’: neutral terms for spatial and sequence similarity. Current Biology 14, 181–183.CrossRefGoogle Scholar
WATERHOUSE, P. M., GRAHAM, M. W. & WANG, M.-B. ( 1998). Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proceedings of the National Academy of Sciences, USA 95, 13959–13964.CrossRefGoogle Scholar
WESLEY, S. V., HELLIWELL, C. A., SMITH, N. A., WANG, M.-B., ROUSE, D. T., LIU, Q., GOODING, P. S., SINGH, S. P., ABBOTT, D., STOUTJESDIJK, P. A., ROBINSON, S. P., GLEAVE, A. P., GREEN, A. G. & WATERHOUSE, P. M. ( 2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant Journal 27, 581–590.CrossRefGoogle Scholar
WHITE, J. G., SOUTHGATE, E., THOMPSON, J. N. & BRENNER, S. ( 1986). The structure of the nervous system of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 314, 1–340.CrossRefGoogle Scholar
WILLIAMSON, V. M. & GLEASON, C. A. ( 2003). Plant-nematode interactions. Current Opinion in Plant Biology 6, 327–333.CrossRefGoogle Scholar
WINTER, M. D., MCPHERSON, M. J. & ATKINSON, H. J. ( 2002). Neuronal uptake of pesticides disrupts chemosensory cells of nematodes. Parasitology 125, 561–565.Google Scholar
ZUCKERMAN, B. M. ( 1983). Hypotheses and possibilities of intervention in nematode chemoresponses. Journal of Nematology 15, 173–182.Google Scholar