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

  • R. ALAN WILSON (a1)

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.

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*Contact: Phone: 01904 328600. Fax: 01904 328505. E-mail: raw3@york.ac.uk

References

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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, 243247.
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, 28302837.
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, 215222.
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, 28272838.
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, 284291.
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, 198202.
Ashton, P. D., Harrop, R., Shah, B. and Wilson, R. A. (2001 b). The schistosome egg: development and secretions. Parasitology 122, 329338.
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, 349356.
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, 352358.
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, 42764284.
Bhardwaj, R. and Skelly, P. J. (2011). Characterization of schistosome tegumental alkaline phosphatase (SmAP). PLoS Neglected Tropical Diseases 5, e1011.
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, 205212.
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, 14711482.
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular Cell Proteomics 5, 347356.
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, 241248.
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.
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, 8493.
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.
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, 15191533.
Clegg, J. A. (1965). In Vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133147.
Coulson, P. S. (1997). The radiation-attenuated vaccine against schistosomes in animal models: paradigm for a human vaccine? Advances in Parasitology 39, 271336.
Crabtree, J. E. and Wilson, R. A. (1985). Schistosoma mansoni: an ultrastructural examination of skin migration in the hamster cheek pouch. Parasitology 91, 111120.
Crabtree, J. E. and Wilson, R. A. (1986). Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology 92, 343354.
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, 5766.
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, 835844.
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, 47454755.
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, 233238.
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, 9597.
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, 3931639329.
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, 11121121.
DeMarco, R. and Verjovski-Almeida, S. (2009). Schistosomes–proteomics studies for potential novel vaccines and drug targets. Drug Discovery Today 14, 472478.
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, 357374.
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, 135142.
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, 18.
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, 503514.
Dorsey, C. H., Cousin, C. E., Lewis, F. A. and Stirewalt, M. A. (2002). Ultrastructure of the Schistosoma mansoni cercaria. Micron 33, 279323.
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, 14831494.
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, 12381247.
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, 18251832.
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.
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, 123127.
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, 181187.
Goldring, O. L., Kusel, J. R. and Smithers, S. R. (1977). Schistosoma mansoni: origin in vitro of host-like surface antigens. Experimental Parasitology 43, 8293.
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, 1108211097.
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, 1829.
Harrop, R. and Wilson, R. A. (1993). Protein synthesis and release by cultured schistosomula of Schistosoma mansoni. Parasitology 107, 265274.
Hewitson, J. P., Hamblin, P. A. and Mountford, A. P. (2005). Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunology 27, 271280.
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, 15731594.
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, 1325.
Huang, Y., Qiao, F., Abagyan, R., Hazard, S. and Tomlinson, S. (2006). Defining the CD59-C9 binding interaction. Journal of Biological Chemistry 281, 2739827404.
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, 14851499.
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, 554562.
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, 18621875.
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, 15111520.
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, 12361251.
LoVerde, P. T., Osman, A. and Hinck, A. (2007). Schistosoma mansoni: TGF-beta signaling pathways. Experimental Parasitology 117, 304317.
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/
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, 617628.
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, 327348.
Michaels, R. M. and Prata, A. (1968). Evolution and characteristics of Schistosoma mansoni eggs laid in vitro. Journal of Parasitoogy 54, 921930.
Morris, G. P. and Threadgold, L. T. (1968). Ultrastructure of the tegument of adult Schistosoma mansoni. Journal of Parasitology 54, 1527.
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, 109121.
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, 543554.
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, 236241.
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.
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.
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.
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, 27512756.
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, 112123.
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, 301309.
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, 360372.
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, 301309.
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, 14161427.
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, 105127.
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, 3241.
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, 2461824624.
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, 123131.
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, 919.
Skelly, P. J. and Wilson, R. A. (2006). Making sense of the schistosome surface. Advances in Parasitology 63, 185284.
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.
Stirewalt, M. A. (1959). Isolation and characterization of deposits of secretion from the acetabular gland complex of cercariae of Schistosoma mansoni. Experimental Parasitology 8, 199214.
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, 2028.
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, 146155.
Taylor, J. E. and Rudenko, G. (2006). Switching trypanosome coats: what's in the wardrobe? Trends in Genetics 22, 614620.
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, 10891098.
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, 835840.
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, 958966.
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, 148157.
Wilson, R. A. (2011). The cell biology of schistosomes: a window on the evolution of the early metazoa. Protoplasma Online First™, 6 October.
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, 1420.
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, 239258.
Wilson, R. A. and Barnes, P. E. (1977). The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology 74, 6171.
Wilson, R. A. and Coulson, P. S. (2006). Schistosome vaccines: a critical appraisal. Memorias do Instituto Oswaldo Cruz 101 Suppl 1, 1320.
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, 423431.
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.
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, 12411244.
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, 13471359.
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, 40684078.
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, 3746.
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, 15511559.
Zinn, K., McAllister, L. and Goodman, C. S. (1988). Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53, 577587.

Keywords

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

  • R. ALAN WILSON (a1)

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