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Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines?

Published online by Cambridge University Press:  01 May 2012

R. ALAN WILSON
R. ALAN WILSON*
Affiliation:
Centre for Immunology & Infection, Department of Biology, University of York, Heslington, York, YO10 5DD, UK
*
*Contact: Phone: 01904 328600. Fax: 01904 328505. E-mail: raw3@york.ac.uk
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Summary

Since 2004 there has been a remarkable increment in our knowledge of the proteins and glycans that reside at, or are released from the surfaces of schistosomes in the mammalian host. Initial characterization of the soluble proteome permits distinctions to be made between the parasite secretome and its necrotome. The principal proteins secreted by the cercaria to gain access to the skin have been described as well as those released by migrating schistosomula. An inventory of transporters, enzymes and structural proteins has been shown to reside the tegument surface, but also immunoglobulins, complement factors and host CD44. The secreted membranocalyx that overlies the plasma membrane may contain a small number of proteins, not simply acting as physical barrier, but its lipid composition remains elusive. Analysis of worm vomitus has provided insights into blood feeding, increasing the number of known lysosomal hydrolases, and identifying a series of carrier proteins potentially involved in uptake of lipids and inorganic ions by the gut epithelium. The egg secretions that aid escape from the tissues include a mixture of MEG-2 and MEG-3 family variant proteins. The utility of identified proteins for the development of new diagnostics, and their potential as vaccines candidates is evaluated.

Keywords

Acetabular glandhead glandtegumentgut epitheliumegg secretionsmicro exon genesschistosomes
Type
Research Article
Information
Parasitology , Volume 139 , Issue 9: Symposia of the British Society for Parasitology Volume 48 Proteomic insights into parasite biology , August 2012 , pp. 1178 - 1194
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Abath, F. G., Hirst, E. M., Hagan, P. and Simpson, A. J. (1999). Ultrastructural localization of Sm15 and Sm25, two major tegumental adult worm antigens of Schistosoma mansoni. Parasite 6, 243–247.CrossRefGoogle ScholarPubMed
Ahmad, G., Zhang, W., Torben, W., Damian, R. T., Wolf, R. F., White, G. L., Chavez-Suarez, M., Kennedy, R. C. and Siddiqui, A. A. (2009). Protective and antifecundity effects of Sm-p80-based DNA vaccine formulation against Schistosoma mansoni in a nonhuman primate model. Vaccine 27, 2830–2837.CrossRefGoogle Scholar
Ali, P. O., Jeffs, S. A., Meadows, H. M., Hollyer, T., Owen, C. A., Abath, F. G., Allen, R., Hackett, F., Smithers, S. R. and Simpson, A. J. (1991). Structure of Sm25, an antigenic integral membrane glycoprotein of adult Schistosoma mansoni. Molecular and Biochemical Parasitology 45, 215–222.CrossRefGoogle ScholarPubMed
Anderson, S., Shires, V. L., Wilson, R. A. and Mountford, A. P. (1998). In the absence of IL-12, the induction of Th1-mediated protective immunity by the attenuated schistosome vaccine is impaired, revealing an alternative pathway with Th2-type characteristics. European Journal of Immunology 28, 2827–2838.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Araujo-Montoya, B. O., Rofatto, H. K., Tararam, C. A., Farias, L. P., Oliveira, K. C., Verjovski-Almeida, S., Wilson, R. A. and Leite, L. C. (2011). Schistosoma mansoni: Molecular characterization of Alkaline Phosphatase and expression patterns across life cycle stages. Experimental Parasitology 129, 284–291.CrossRefGoogle ScholarPubMed
Ashton, P. D., Curwen, R. S. and Wilson, R. A. (2001 a). Linking proteome and genome: how to identify parasite proteins. Trends in Parasitology 17, 198–202.CrossRefGoogle ScholarPubMed
Ashton, P. D., Harrop, R., Shah, B. and Wilson, R. A. (2001 b). The schistosome egg: development and secretions. Parasitology 122, 329–338.CrossRefGoogle ScholarPubMed
Bendtsen, J. D., Jensen, L. J., Blom, N., Von Heijne, G. and Brunak, S. (2004). Feature-based prediction of non-classical and leaderless protein secretion. Protein Engineering, Design and Selection 17, 349–356.CrossRefGoogle ScholarPubMed
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352–358.CrossRefGoogle ScholarPubMed
Bhardwaj, R., Krautz-Peterson, G., Da'dara, A., Tzipori, S. and Skelly, P. J. (2011). Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes. Infection and Immunity 79, 4276–4284.CrossRefGoogle ScholarPubMed
Bhardwaj, R. and Skelly, P. J. (2011). Characterization of schistosome tegumental alkaline phosphatase (SmAP). PLoS Neglected Tropical Diseases 5, e1011.CrossRefGoogle ScholarPubMed
Braschi, S., Borges, W. C. and Wilson, R. A. (2006 a). Proteomic analysis of the schistosome tegument and its surface membranes. Memorias do Instituto Oswaldo Cruz 101 Suppl 1, 205–212.CrossRefGoogle ScholarPubMed
Braschi, S., Curwen, R. S., Ashton, P. D., Verjovski-Almeida, S. and Wilson, A. (2006 b). The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 1471–1482.CrossRefGoogle ScholarPubMed
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular Cell Proteomics 5, 347–356.CrossRefGoogle ScholarPubMed
Caffrey, C. R., McKerrow, J. H., Salter, J. P. and Sajid, M. (2004). Blood 'n' guts: an update on schistosome digestive peptidases. Trends in Parasitology 20, 241–248.CrossRefGoogle ScholarPubMed
Cardoso, F. C., Macedo, G. C., Gava, E., Kitten, G. T., Mati, V. L., de Melo, A. L., Caliari, M. V., Almeida, G. T., Venancio, T. M., Verjovski-Almeida, S. and Oliveira, S. C. (2008). Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Neglected Tropical Diseases 2, e308.CrossRefGoogle ScholarPubMed
Cass, C. L., Johnson, J. R., Califf, L. L., Xu, T., Hernandez, H. J., Stadecker, M. J., Yates, J. R. 3rd and Williams, D. L. (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155, 84–93.CrossRefGoogle ScholarPubMed
Castro-Borges, W., Dowle, A., Curwen, R. S., Thomas-Oates, J. and Wilson, R. A. (2011 a). Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Neglected Tropical Diseases 5, e993.CrossRefGoogle ScholarPubMed
Castro-Borges, W., Simpson, D. M., Dowle, A., Curwen, R. S., Thomas-Oates, J., Beynon, R. J. and Wilson, R. A. (2011 b). Abundance of tegument surface proteins in the human blood fluke Schistosoma mansoni determined by QconCAT proteomics. Journal of Proteomics 74, 1519–1533.CrossRefGoogle ScholarPubMed
Clegg, J. A. (1965). In Vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–147.CrossRefGoogle ScholarPubMed
Coulson, P. S. (1997). The radiation-attenuated vaccine against schistosomes in animal models: paradigm for a human vaccine? Advances in Parasitology 39, 271–336.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1985). Schistosoma mansoni: an ultrastructural examination of skin migration in the hamster cheek pouch. Parasitology 91, 111–120.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1986). Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology 92, 343–354.CrossRefGoogle ScholarPubMed
Curwen, R. S., Ashton, P. D., Johnston, D. A. and Wilson, R. A. (2004). The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and Biochemical Parasitology 138, 57–66.CrossRefGoogle ScholarPubMed
Curwen, R. S., Ashton, P. D., Sundaralingam, S. and Wilson, R. A. (2006). Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Molecular Cell Proteomics 5, 835–844.CrossRefGoogle ScholarPubMed
Davis, R. E., Davis, A. H., Carroll, S. M., Rajkovic, A. and Rottman, F. M. (1988). Tandemly repeated exons encode 81-base repeats in multiple, developmentally regulated Schistosoma mansoni transcripts. Molecular Cell Biol 8, 4745–4755.Google ScholarPubMed
Deelder, A. M., Qian, Z. L., Kremsner, P. G., Acosta, L., Rabello, A. L., Enyong, P., Simarro, P. P., van Etten, E. C., Krijger, F. W., Rotmans, J. P. et al. (1994). Quantitative diagnosis of Schistosoma infections by measurement of circulating antigens in serum and urine. Tropical and Geographic Medicine 46, 233–238.Google ScholarPubMed
Delcroix, M., Medzihradsky, K., Caffrey, C. R., Fetter, R. D. and McKerrow, J. H. (2007). Proteomic analysis of adult S. mansoni gut contents. Molecular and Biochemical Parasitology 154, 95–97.CrossRefGoogle ScholarPubMed
Delcroix, M., Sajid, M., Caffrey, C. R., Lim, K. C., Dvorak, J., Hsieh, I., Bahgat, M., Dissous, C. and McKerrow, J. H. (2006). A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. Journal of Biological Chemistry 281, 39316–39329.CrossRefGoogle ScholarPubMed
DeMarco, R., Mathieson, W., Manuel, S. J., Dillon, G. P., Curwen, R. S., Ashton, P. D., Ivens, A. C., Berriman, M., Verjovski-Almeida, S. and Wilson, R. A. (2010). Protein variation in blood-dwelling schistosome worms generated by differential splicing of micro-exon gene transcripts. Genome Research 20, 1112–1121.CrossRefGoogle ScholarPubMed
DeMarco, R. and Verjovski-Almeida, S. (2009). Schistosomes–proteomics studies for potential novel vaccines and drug targets. Drug Discovery Today 14, 472–478.CrossRefGoogle ScholarPubMed
Dessein, A., Samuelson, J. C., Butterworth, A. E., Hogan, M., Sherry, B. A., Vadas, M. A. and David, J. R. (1981). Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82, 357–374.CrossRefGoogle ScholarPubMed
Dias Neto, E., Harrop, R., Correa-Oliveira, R., Wilson, R. A., Pena, S. D. and Simpson, A. J. (1997). Minilibraries constructed from cDNA generated by arbitrarily primed RT-PCR: an alternative to normalized libraries for the generation of ESTs from nanogram quantities of mRNA. Gene 186, 135–142.CrossRefGoogle ScholarPubMed
Dillon, G. P., Feltwell, T., Skelton, J. P., Ashton, P. D., Coulson, P. S., Quail, M. A., Nikolaidou-Katsaridou, N., Wilson, R. A. and Ivens, A. C. (2006). Microarray analysis identifies genes preferentially expressed in the lung schistosomulum of Schistosoma mansoni. International Journal for Parasitology 36, 1–8.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Hassounah, O., Murare, H., Bain, J. and Lucas, S. (1986). The schistosome egg granuloma: immunopathology in the cause of host protection or parasite survival? Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 503–514.CrossRefGoogle ScholarPubMed
Dorsey, C. H., Cousin, C. E., Lewis, F. A. and Stirewalt, M. A. (2002). Ultrastructure of the Schistosoma mansoni cercaria. Micron 33, 279–323.CrossRefGoogle ScholarPubMed
Dunne, D. W., Butterworth, A. E., Fulford, A. J., Kariuki, H. C., Langley, J. G., Ouma, J. H., Capron, A., Pierce, R. J. and Sturrock, R. F. (1992). Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. European Journal of Immunology 22, 1483–1494.CrossRefGoogle ScholarPubMed
Eberl, M., Langermans, J. A., Vervenne, R. A., Nyame, A. K., Cummings, R. D., Thomas, A. W., Coulson, P. S. and Wilson, R. A. (2001). Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive? Journal of Infectious Diseases 183, 1238–1247.CrossRefGoogle ScholarPubMed
Elkins, T., Hortsch, M., Bieber, A. J., Snow, P. M. and Goodman, C. S. (1990). Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. Jouranl of Cell Biology 110, 1825–1832.CrossRefGoogle ScholarPubMed
Faghiri, Z., Camargo, S. M., Huggel, K., Forster, I. C., Ndegwa, D., Verrey, F. and Skelly, P. J. (2010). The tegument of the human parasitic worm Schistosoma mansoni as an excretory organ: the surface aquaporin SmAQP is a lactate transporter. PLoS One 5, e10451.CrossRefGoogle ScholarPubMed
Fitzsimmons, C. M., Schramm, G., Jones, F. M., Chalmers, I. W., Hoffmann, K. F., Grevelding, C. G., Wuhrer, M., Hokke, C. H., Haas, H., Doenhoff, M. J. and Dunne, D. W. (2005). Molecular characterization of omega-1: a hepatotoxic ribonuclease from Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 144, 123–127.CrossRefGoogle ScholarPubMed
Goldring, O. L., Clegg, J. A., Smithers, S. R. and Terry, R. J. (1976). Acquisition of human blood group antigens by Schistosoma mansoni. Clinical Experimental Immunology 26, 181–187.Google ScholarPubMed
Goldring, O. L., Kusel, J. R. and Smithers, S. R. (1977). Schistosoma mansoni: origin in vitro of host-like surface antigens. Experimental Parasitology 43, 82–93.CrossRefGoogle ScholarPubMed
Goodrich, S. P., Muller-Steffner, H., Osman, A., Moutin, M. J., Kusser, K., Roberts, A., Woodland, D. L., Randall, T. D., Kellenberger, E., LoVerde, P. T., Schuber, F. and Lund, F. E. (2005). Production of calcium-mobilizing metabolites by a novel member of the ADP-ribosyl cyclase family expressed in Schistosoma mansoni. Biochemistry 44, 11082–11097.CrossRefGoogle ScholarPubMed
Hall, S. L., Braschi, S., Truscott, M., Mathieson, W., Cesari, I. M. and Wilson, R. A. (2011). Insights into blood feeding by schistosomes from a proteomic analysis of worm vomitus. Molecular and Biochemical Parasitology 179, 18–29.CrossRefGoogle ScholarPubMed
Harrop, R. and Wilson, R. A. (1993). Protein synthesis and release by cultured schistosomula of Schistosoma mansoni. Parasitology 107, 265–274.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Hamblin, P. A. and Mountford, A. P. (2005). Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunology 27, 271–280.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Harcus, Y., Murray, J., van Agtmaal, M., Filbey, K. J., Grainger, J. R., Bridgett, S., Blaxter, M. L., Ashton, P. D., Ashford, D. A., Curwen, R. S., Wilson, R. A., Dowle, A. A. and Maizels, R. M. (2011). Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins. Journal of Proteomics 74, 1573–1594.CrossRefGoogle ScholarPubMed
Hockley, D. J. and McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle ScholarPubMed
Huang, Y., Qiao, F., Abagyan, R., Hazard, S. and Tomlinson, S. (2006). Defining the CD59-C9 binding interaction. Journal of Biological Chemistry 281, 27398–27404.CrossRefGoogle ScholarPubMed
Jang-Lee, J., Curwen, R. S., Ashton, P. D., Tissot, B., Mathieson, W., Panico, M., Dell, A., Wilson, R. A. and Haslam, S. M. (2007). Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Molecular Cell Proteomics 6, 1485–1499.CrossRefGoogle ScholarPubMed
Kariuki, T. M., Farah, I. O., Wilson, R. A. and Coulson, P. S. (2008). Antibodies elicited by the secretions from schistosome cercariae and eggs are predominantly against glycan epitopes. Parasite Immunology 30, 554–562.CrossRefGoogle ScholarPubMed
Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E. and McKerrow, J. H. (2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular Cell Proteomics 4, 1862–1875.CrossRefGoogle ScholarPubMed
Kyes, S. A., Kraemer, S. M. and Smith, J. D. (2007). Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family. Eukaryotic Cell 6, 1511–1520.CrossRefGoogle ScholarPubMed
Liu, F., Cui, S. J., Hu, W., Feng, Z., Wang, Z. Q. and Han, Z. G. (2009). Excretory/secretory proteome of the adult developmental stage of human blood fluke, Schistosoma japonicum. Molecular Cell Proteomics 8, 1236–1251.CrossRefGoogle ScholarPubMed
LoVerde, P. T., Osman, A. and Hinck, A. (2007). Schistosoma mansoni: TGF-beta signaling pathways. Experimental Parasitology 117, 304–317.CrossRefGoogle ScholarPubMed
Manuel, S. J. (2010). Patterns of gene expression in Schistosoma mansoni associated with infection of the mammalian host. PhD thesis, University of York, available @ http://etheses.whiterose.ac.uk/1603/Google Scholar
Mathieson, W. and Wilson, R. A. (2010). A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. International Journal for Parasitology 40, 617–628.CrossRefGoogle ScholarPubMed
McLaren, D. J., Hockley, D. J., Goldring, O. L. and Hammond, B. J. (1978). A freeze fracture study of the developing tegumental outer membrane of Schistosoma mansoni. Parasitology 76, 327–348.CrossRefGoogle ScholarPubMed
Michaels, R. M. and Prata, A. (1968). Evolution and characteristics of Schistosoma mansoni eggs laid in vitro. Journal of Parasitoogy 54, 921–930.CrossRefGoogle ScholarPubMed
Morris, G. P. and Threadgold, L. T. (1968). Ultrastructure of the tegument of adult Schistosoma mansoni. Journal of Parasitology 54, 15–27.CrossRefGoogle ScholarPubMed
Mulvenna, J., Hamilton, B., Nagaraj, S. H., Smyth, D., Loukas, A. and Gorman, J. J. (2009). Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Molecular Cell Proteomics 8, 109–121.CrossRefGoogle ScholarPubMed
Mulvenna, J., Moertel, L., Jones, M. K., Nawaratna, S., Lovas, E. M., Gobert, G. N., Colgrave, M., Jones, A., Loukas, A. and McManus, D. P. (2010). Exposed proteins of the Schistosoma japonicum tegument. International Journal for Parasitology 40, 543–554.CrossRefGoogle ScholarPubMed
Nash, T. E. and Deelder, A. M. (1985). Comparison of four schistosome excretory-secretory antigens: phenol sulfuric test active peak, cathodic circulating antigen, gut-associated proteoglycan, and circulating anodic antigen. American Journal of Tropical Medicine and Hygiene 34, 236–241.CrossRefGoogle ScholarPubMed
Nawaratna, S. S., McManus, D. P., Moertel, L., Gobert, G. N. and Jones, M. K. (2011). Gene Atlasing of digestive and reproductive tissues in Schistosoma mansoni. PLoS Neglected Tropical Diseases 5, e1043.CrossRefGoogle ScholarPubMed
Oliveira, K. C., Carvalho, M. L., Venancio, T. M., Miyasato, P. A., Kawano, T., DeMarco, R. and Verjovski-Almeida, S. (2009). Identification of the Schistosoma mansoni TNF-alpha receptor gene and the effect of human TNF-alpha on the parasite gene expression profile. PLoS Neglected Tropical Diseases 3, e556.CrossRefGoogle ScholarPubMed
Parker-Manuel, S. J., Ivens, A. C., Dillon, G. P. and Wilson, R. A. (2011). Gene expression patterns in larval Schistosoma mansoni associated with infection of the mammalian host. PLoS Neglected Tropical Diseases 5, e1274.CrossRefGoogle ScholarPubMed
Pearce, E. J., Hall, B. F. and Sher, A. (1990). Host-specific evasion of the alternative complement pathway by schistosomes correlates with the presence of a phospholipase C-sensitive surface molecule resembling human decay accelerating factor. Journal of Immunology 144, 2751–2756.CrossRefGoogle ScholarPubMed
Perez-Sanchez, R., Valero, M. L., Ramajo-Hernandez, A., Siles-Lucas, M., Ramajo-Martin, V. and Oleaga, A. (2008). A proteomic approach to the identification of tegumental proteins of male and female Schistosoma bovis worms. Molecular and Biochemical Parasitology 161, 112–123.CrossRefGoogle Scholar
Planchart, S., Incani, R. N. and Cesari, I. M. (2007). Preliminary characterization of an adult worm “vomit” preparation of Schistosoma mansoni and its potential use as antigen for diagnosis. Parasitology Research 101, 301–309.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. and Pellegrino, J. (1974). Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro. Experimental Parasitology 36, 360–372.CrossRefGoogle ScholarPubMed
Riengrojpitak, S., Anderson, S. and Wilson, R. A. (1998). Induction of immunity to Schistosoma mansoni: interaction of schistosomula with accessory leucocytes in murine skin and draining lymph nodes. Parasitology 117, 301–309.CrossRefGoogle ScholarPubMed
Rivers, J., Simpson, D. M., Robertson, D. H., Gaskell, S. J. and Beynon, R. J. (2007). Absolute multiplexed quantitative analysis of protein expression during muscle development using QconCAT. Molecular Cell Proteomics 6, 1416–1427.CrossRefGoogle ScholarPubMed
Roberts, S. M., MacGregor, A. N., Vojvodic, M., Wells, E., Crabtree, J. E. and Wilson, R. A. (1983). Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9, 105–127.CrossRefGoogle ScholarPubMed
Rofatto, H. K., Tararam, C. A., Borges, W. C., Wilson, R. A., Leite, L. C. and Farias, L. P. (2009). Characterization of phosphodiesterase-5 as a surface protein in the tegument of Schistosoma mansoni. Molecular and Biochemical Parasitology 166, 32–41.CrossRefGoogle ScholarPubMed
Salter, J. P., Choe, Y., Albrecht, H., Franklin, C., Lim, K. C., Craik, C. S. and McKerrow, J. H. (2002). Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. Journal of Biological Chemistry 277, 24618–24624.CrossRefGoogle ScholarPubMed
Saunders, N., Wilson, R. A. and Coulson, P. S. (1987). The outer bilayer of the adult schistosome tegument surface has a low turnover rate in vitro and in vivo. Molecular and Biochemical Parasitology 25, 123–131.CrossRefGoogle Scholar
Schramm, G., Gronow, A., Knobloch, J., Wippersteg, V., Grevelding, C. G., Galle, J., Fuller, H., Stanley, R. G., Chiodini, P. L., Haas, H. and Doenhoff, M. J. (2006). IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 147, 9–19.CrossRefGoogle Scholar
Skelly, P. J. and Wilson, R. A. (2006). Making sense of the schistosome surface. Advances in Parasitology 63, 185–284.CrossRefGoogle ScholarPubMed
Sprong, H., Suchanek, M., van Dijk, S. M., van Remoortere, A., Klumperman, J., Avram, D., van der Linden, J., Leusen, J. H., van Hellemond, J. J. and Thiele, C. (2006). Aberrant receptor-mediated endocytosis of Schistosoma mansoni glycoproteins on host lipoproteins. PLoS Medicine 3, e253.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1959). Isolation and characterization of deposits of secretion from the acetabular gland complex of cercariae of Schistosoma mansoni. Experimental Parasitology 8, 199–214.CrossRefGoogle ScholarPubMed
Sulbaran, G. S., Ballen, D. E., Bermudez, H., Lorenzo, M., Noya, O. and Cesari, I. M. (2010). Detection of the Sm31 antigen in sera of Schistosoma mansoni- infected patients from a low endemic area. Parasite Immunology 32, 20–28.CrossRefGoogle ScholarPubMed
Tararam, C. A., Farias, L. P., Wilson, R. A. and Leite, L. C. (2010). Schistosoma mansoni Annexin 2: molecular characterization and immunolocalization. Experimental Parasitology 126, 146–155.CrossRefGoogle ScholarPubMed
Taylor, J. E. and Rudenko, G. (2006). Switching trypanosome coats: what's in the wardrobe? Trends in Genetics 22, 614–620.CrossRefGoogle ScholarPubMed
Thornhill, J. A., McVeigh, P., Jurberg, A. D. and Kusel, J. R. (2010). Pathways for the influx of molecules into cercariae of Schistosoma mansoni during skin penetration. Parasitology 137, 1089–1098.CrossRefGoogle ScholarPubMed
Tran, M. H., Pearson, M. S., Bethony, J. M., Smyth, D. J., Jones, M. K., Duke, M., Don, T. A., McManus, D. P., Correa-Oliveira, R. and Loukas, A. (2006). Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835–840.CrossRefGoogle ScholarPubMed
van Balkom, B. W., van Gestel, R. A., Brouwers, J. F., Krijgsveld, J., Tielens, A. G., Heck, A. J. and van Hellemond, J. J. (2005). Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. Journal of Proteome Research 4, 958–966.CrossRefGoogle ScholarPubMed
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. and Dias-Neto, E. (2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.CrossRefGoogle ScholarPubMed
Wilson, R. A. (2011). The cell biology of schistosomes: a window on the evolution of the early metazoa. Protoplasma Online First™, 6 October.Google Scholar
Wilson, R. A., Ashton, P. D., Braschi, S., Dillon, G. P., Berriman, M. and Ivens, A. (2007). 'Oming in on schistosomes: prospects and limitations for post-genomics. Trends in Parasitology 23, 14–20.CrossRefGoogle Scholar
Wilson, R. A. and Barnes, P. E. (1974). The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology 68, 239–258.CrossRefGoogle ScholarPubMed
Wilson, R. A. and Barnes, P. E. (1977). The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology 74, 61–71.CrossRefGoogle ScholarPubMed
Wilson, R. A. and Coulson, P. S. (2006). Schistosome vaccines: a critical appraisal. Memorias do Instituto Oswaldo Cruz 101 Suppl 1, 13–20.CrossRefGoogle ScholarPubMed
Wilson, R. A. and Coulson, P. S. (2009). Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite's armour. Trends in Parasitology 25, 423–431.CrossRefGoogle ScholarPubMed
Wilson, R. A., Langermans, J. A., van Dam, G. J., Vervenne, R. A., Hall, S. L., Borges, W. C., Dillon, G. P., Thomas, A. W. and Coulson, P. S. (2008). Elimination of Schistosoma mansoni adult worms by Rhesus macaques: basis for a therapeutic vaccine? PLoS Neglected Tropical Diseases 2, e290.CrossRefGoogle ScholarPubMed
Wilson, R. A., van Dam, G. J., Kariuki, T. M., Farah, I. O., Deelder, A. M. and Coulson, P. S. (2006). The detection limits for estimates of infection intensity in schistosomiasis mansoni established by a study in non-human primates. International Journal for Parasitology 36, 1241–1244.CrossRefGoogle Scholar
Wilson, R. A., Wright, J. M., de Castro Borges, W., Parker-Manuel, S. J., Dowle, A. A., Ashton, P. D., Young, N. D., Gasser, R. B. and Spithill, T. W. (2011). Exploring the Fasciola hepatica tegument proteome. International Journal for Parasitology 41, 1347–1359.CrossRefGoogle ScholarPubMed
Wynn, T. A., Reynolds, A., James, S., Cheever, A. W., Caspar, P., Hieny, S., Jankovic, D., Strand, M. and Sher, A. (1996). IL-12 enhances vaccine-induced immunity to schistosomes by augmenting both humoral and cell-mediated immune responses against the parasite. Journal of Immunology 157, 4068–4078.CrossRefGoogle ScholarPubMed
Yole, D. S., Pemberton, R., Reid, G. D. and Wilson, R. A. (1996). Protective immunity to Schistosoma mansoni induced in the olive baboon Papio anubis by the irradiated cercaria vaccine. Parasitology 112, 37–46.CrossRefGoogle ScholarPubMed
You, H., Zhang, W., Moertel, L., McManus, D. P. and Gobert, G. N. (2009). Transcriptional profiles of adult male and female Schistosoma japonicum in response to insulin reveal increased expression of genes involved in growth and development. International Journal for Parasitology 39, 1551–1559.CrossRefGoogle ScholarPubMed
Zinn, K., McAllister, L. and Goodman, C. S. (1988). Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53, 577–587.CrossRefGoogle ScholarPubMed