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Characterization of genes with a putative key role in the parasitic lifestyle of the nematode Strongyloides ratti

Published online by Cambridge University Press:  02 May 2012

W. G. SPINNER ,
F. J. THOMPSON ,
D. C. EMERY  and
M. E. VINEY
W. G. SPINNER
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
F. J. THOMPSON
Affiliation:
University of St Andrews, College Gate, North Street, St Andrews, Fife KY16 9AJ, UK
D. C. EMERY
Affiliation:
Laboratories for Integrative Neuroscience and Endocrinology, University of Bristol, Dorothy Hodgkin Building, Bristol BS1 3NY, UK
M. E. VINEY*
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
*
*Corresponding author: School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK. Tel: + 0117 928 7469. E-mail: [email protected]
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Summary

Parasitic nematodes are significant pathogens of humans and other animals. The molecular and genetic basis of animal parasitism is not yet fully understood. Strongyloides spp. are a genus of gastrointestinal nematodes of which species infect approximately 100–200 million people worldwide. S. ratti is a natural parasite of the rat, and a useful and amenable laboratory model. Previous EST and microarray analyses of the S. ratti life cycle have identified genes whose expression was specific, or biased, to the parasitic adult stage, suggesting that they may play a key role in parasitism in this species. Here we have further investigated the expression of these genes (by RT-PCR) throughout the S. ratti life-cycle. We produced recombinant proteins in vitro for a subset of these genes, which were used in Western blot analyses to investigate the distribution of the gene products among different stages of the S. ratti life cycle. We tested the efficacy of these recombinant proteins as anti-S. ratti vaccines. One of the proteins was detected in the excretory/secretory products of the parasitic stages.

Keywords

Strongyloidesprotein expressiongene expressionvaccination
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1317 - 1328
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Albonico, M., Crompton, D. W. T. and Savioli, F. (1999). Control strategies for human intestinal nematode infections. Advances in Parasitology 42, 277–341. doi: 10.1016/S0065-308X(08)60151-7.CrossRefGoogle ScholarPubMed
Alkharouf, N. W., Klink, V. P., Chouikha, I. B., Beard, H. S., MacDonald, M. H., Meyer, S., Knap, H. T., Khan, R. and Mattews, B. F. (2006). Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224, 838–852. doi: 10.1007/s00425-006-0270-8.CrossRefGoogle ScholarPubMed
Bendtsen, J. D., Nielsen, H., Heijne, G. V. and Brunak, S. (2004). Improved prediction of signal peptides@ SignalP 3.0. Journal of Molecular Biology 340, 783–795. doi: 10.1016/j.jmb.2004.05.028.CrossRefGoogle ScholarPubMed
Blackburn, C. C. and Selkirk, M. E. (1992). Characterisation of the secretory acetylcholinesterases from adult Nippostrongylus brasiliensis . Molecular and Biochemical Parasitology 53, 79–88.CrossRefGoogle ScholarPubMed
Crook, M. and Viney, M. E. (2005). The effect of non-immune stresses on the development of Strongyloides ratti . Parasitology 131, 383–392. doi: 10.1017/S0031182005007675.CrossRefGoogle ScholarPubMed
Devaney, E., O'Neill, K., Harnett, W., Whitesell, L. and Kinnaird, J. H. (2005). Hsp90 is essential in the filarial nematode Brugia pahangi . International Journal for Parasitology 35, 627–636. doi: 10.1016/j.ijpara.2005.01.007.CrossRefGoogle ScholarPubMed
Ding, L. and Candido, E. P. M. (2000). Association of several small heat-shock proteins with reproductive tissues in the nematode Caenorhabditis elegans . The Biochemical Journal 351, 13–17.CrossRefGoogle ScholarPubMed
Fisher, M. C. and Viney, M. E. (1998). The population genetic structure of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London, B 265, 703–709.CrossRefGoogle ScholarPubMed
Gardner, M. P., Gems, D. and Viney, M. E. (2006). Extraordinary plasticity in aging in Strongyloides ratti implies a gene-regulatory mechanism of lifespan evolution. Aging Cell 5, 315–323. doi: 10.1111/j.1474-9726.2006.00226.x.CrossRefGoogle ScholarPubMed
Kadandale, P., Stewart-Michaelis, A., Gordon, S., Rubin, J., Klancer, R., Schweinsberg, P., Grant, B. D. and Singson, A. (2005). The egg surface LDL receptor repeat-containing proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans . Current Biology 15, 2222–2229. doi: 10.1016/j.cub.2005.10.043.CrossRefGoogle ScholarPubMed
Letunic, I., Doerks, T. and Bork, P. (2009). SMART 6: recent updates and new developments. Nucleic Acids Research 37, D229–D232. doi: 10.1093/nar/gkn808.CrossRefGoogle ScholarPubMed
Li, X., Shao, H., Junio, A., Nolan, T. J., Massey, H. C., Pearce, E. J., Viney, M. E. and Lok, J. B. (2011). Transgenesis in the parasitic nematode Strongyloides ratti . Molecular and Biochemical Parasitology 179, 114–119. doi: 10.1016/j.molbiopara.2011.06.002.CrossRefGoogle ScholarPubMed
Lok, J. B. (2011). Nucleic acid transfection and transgensis in parasitic nematodes. Parasitology 31, 1–15. doi: 10.1017/S0031182011001387.Google Scholar
Maizels, R. M., Bundy, D. P., Selkirk, M. E., Smith, D. F. and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature, London 365, 797–805. doi: 10.1038/365797a0.CrossRefGoogle ScholarPubMed
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116. doi: 10.1111/j.0105-2896.2004.00191.x.CrossRefGoogle Scholar
Mizuguchi, S., Uyama, T., Kitagawa, H., Nomura, K. H., Dejima, K., Gengyo-Ando, K., Mitani, S., Sugahara, K. and Nomura, K. (2003). Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans . Nature, London 423, 443–448. doi: 10.1038/nature01635.CrossRefGoogle ScholarPubMed
Nakamoto, H. and Vigh, L. (2007). The small heat shock proteins and their clients. Cellular and Molecular Life Sciences 64, 294–306. doi: 10.1007/s00018-006-6321-2.CrossRefGoogle ScholarPubMed
Olson, S. K., Bishop, J. R., Yates, J. R., Oegema, K. and Esko, J. D. (2006). Identification of novel chondroitin proteoglycans in Caenorhabditis elegans: embryonic cell division depends on CPG-1 and CPG-2. Journal of Cell Biology 173, 985–994. doi: 10.1083/jcb.200603003.CrossRefGoogle ScholarPubMed
Pagni, M., Ioannidis, V., Cerutti, L., Zahn-Zabal, M., Jongeneel, C. V., Hau, J., Martin, O., Kuznetsov, D. and Falquet, L. (2007). MyHits: improvements to an interactive resource for analyzing protein sequences. Nucleic Acids Research 35, W433–W437. doi: 10.1093/nar/gkm352.CrossRefGoogle Scholar
Paterson, S. and Viney, M. E. (2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292. doi: 10.1017/S0031182002002056.CrossRefGoogle ScholarPubMed
Pepling, M. E. (2010). A novel maternal mRNA storage compartment in mouse oocytes. Biology of Reproduction 82, 807–808. doi: 10.1095/biolreprod.110.084376.CrossRefGoogle ScholarPubMed
Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cellular and Molecular Life Sciences 59, 1640–1648. doi: 10.1007/PL00012491.CrossRefGoogle ScholarPubMed
Russnak, R. H., Jones, D. and Candido, M. (1983). Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) in Caenorhabditis elegans: homology with the small hsps of Drosophila . Nucleic Acids Research 11, 3187–3205. doi: 10.1093/nar/11.10.3187.CrossRefGoogle ScholarPubMed
Soblik, H., Younis, A. E., Mitreva, M., Benard, B. Y., Kirchner, M., Geisinger, F., Steen, Hanno, and Brattig, N. W. (2011). Life cycle stage-resolved proteomic analysis of the excretome/secretome from Strongyloides ratti – Identification of stage-specific proteases. Molecular and Cellular Proteomics 10, 1–16. doi: 10.1074/mcp.M111.010157-1.CrossRefGoogle Scholar
Thompson, F. J., Barker, G. L. A., Hughes, L. and Viney, M. E. (2008). Genes important in the parasitic life of the nematode Strongyloides ratti . Molecular and Biochemical Parasitology 158, 112–119. doi: 10.1016/j.molbiopara.2007.11.016.CrossRefGoogle ScholarPubMed
Thompson, F. J., Barker, G. L. A., Hughes, L., Wilkes, C. P., Coghill, J. and Viney, M. E. (2006). A microarray analysis of gene expression in the free-living stages of the parasitic nematode Strongyloides ratti . BMC Genomics 7, 157–177. doi: 10.1186/1471-2164-7-157.CrossRefGoogle ScholarPubMed
Thompson, F. J., Barker, G. L. A., Nolan, T., Gems, D. and Viney, M. E. (2009). Transcript profiles of long- and short-lived adults implicate protein synthesis in evolved differences in aging in the nematode Strongyloides ratti . Mechanisms of Ageing and Development 130, 167–172. doi: 10.1016/j.mad.2008.11.001.CrossRefGoogle ScholarPubMed
Thompson, F. J., Mitreva, M., Barker, G. L. A., Martin, J., Waterston, R. H., McCarter, J. P. and Viney, M. E. (2005). An expressed sequence tag analysis of the life-cycle of the parasitic nematode Strongyloides ratti . Molecular and Biochemical Parasitology 143, 250–250. doi: 10.1016/j.molbiopara.2005.06.005.CrossRefGoogle Scholar
Viney, M. E. (1994). A genetic-analysis of reproduction in Strongyloides ratti . Parasitology 109, 511–515.CrossRefGoogle ScholarPubMed
Viney, M. E. (1996). Developmental switching in the parasitic nematode Strongyloides ratti . Proceedings of the Royal Society of London, B 263, 201–208. doi: 10.1098/rspb.1996.0032.Google ScholarPubMed
Viney, M. E. and Cable, J. (2011). Macroparasite life-histories. Current Biology 21, R767–R774. doi: 10.1016/j.cub.2011.07.023.CrossRefGoogle ScholarPubMed
Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. In Wormbook (ed. The C. elegans Research Community, Wormbook) doi: 10.1895/wormbook.1.7.1, www.wormbook.org CrossRefGoogle Scholar
Viney, M. E., Matthews, B. E. and Walliker, D. (1993). Mating in the nematode parasite Strongyloides ratti: Proof of genetic exchange. Proceedings of the Royal Society of London, B 254, 213–219. doi: 10.1098/rspb.1993.0148.Google ScholarPubMed
Wilkes, C. P., Bleay, C., Paterson, S. and Viney, M. E. (2007). The immune response during a Strongyloides ratti infection of rats. Parasite Immunology 29, 339–346. doi: 10.1111/j.1365-3024.2007.00945.x.CrossRefGoogle ScholarPubMed
Wu, Z., Nagano, I., Boonmars, T. and Takahashi, Y. (2007). Thermally induced and developmentally regulated expression of a small heat shock protein in Trichinella spiralis . Parasitology Research 101, 201–212. doi: 10.1007/s00436-007-0462-6.CrossRefGoogle ScholarPubMed
Yamamoto, T., Davis, C. G., Brown, M. S., Schneider, W. J., Casey, M. L., Goldstein, J. L. and Russell, D. W. (1984). The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39, 27–38. doi: 10.1016/0092-8674(84)90188-0.CrossRefGoogle ScholarPubMed
Yochem, J. and Greenwald, I. (1993). A gene for a low density lipoprotein receptor related protein in the nematode Caenorhabditis elegans . Proceedings of the National Academy of Sciences, USA 90, 4572–4576. doi: 10.1073/pnas.90.10.4572.CrossRefGoogle ScholarPubMed