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Biology of the schistosome lung-stage schistosomulum

  • G. N. GOBERT (a1), M. CHAI (a1) and D. P. McMANUS (a1)


Past and more recent research has examined the ultrastructure, metabolism, cell biology, genomics and post-genomics of schistosome schistosomula. These areas are considered and discussed in this review with particular emphasis on (1) the early migration phases through the host, (2) interaction of the host immune response with the parasite surface, (3) glucose uptake mechanisms, and (4) defining the transcriptional profiles of lung-stage schistosomula compared with other developmental stages using microarrays. The microarray profiling studies suggest caution is required when considering the use of schistosomes obtained by in vitro means for molecular or biochemical studies.


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Agoston, K., Kerekgyarto, J., Hajko, J., Batta, G., Lefeber, D., Kamerling, J. and Vliegenthart, J. F. G. ( 2001). Synthesis of fragments of the glycocalyx glycan of the parasite Schistosoma mansoni. Chemistry – A European Journal 8, 151161.
Ahmed, S. F., Oswald, I. P., Caspar, P., Hieny, S., Keefer, L., Sher, A. and James, S. L. ( 1997). Developmental differences determine larval susceptibility to nitric oxide-mediated killing in a murine model of vaccination against Schistosoma mansoni. Infection and Immunity 65, 219226.
Basch, P. F. ( 1981). Cultivation of Schistosoma mansoni in vitro. 1. Establishment of cultures from cercariae and development until pairing. Journal of Parasitology 67, 179185.
Basch, P. F. and Basch, N. ( 1982). Schistosoma mansoni: scanning electron microscopy of schistosomula, adults and eggs grown in vitro. Parasitology 85, 333338.
Brink, L. H., McLaren, D. J. and Smithers, S. R. ( 1977). Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74, 7386.
Brouwers, J. F. H. M., Skelly, P. J., VanGolde, L. M. G. and Tielens, G. M. ( 1999). Studies on phospholipid turnover argue against sloughing of tegumental membranes in adult Schistosoma mansoni. Parasitology 119, 287294.
Bruce, J. I., Weis, E. M., Stirewalt, M. A. and Lincicome, D. R. ( 1969). Schistosoma mansoni: glycogen content and utilization of glucose, pyruvate, glutamate, and citric acid cycle intermediates by cercariae and schistosomules. Experimental Parasitology 26, 2940.
Chai, M., McManus, D. P., McInnes, R., Moertel, L. P., Tran, M., Loukas, A., Jones, M. K. and Gobert, G. N. ( 2006). Transcriptome profiling of lung schistosomula, in vitro cultured schistosomula and the adult Schistosoma japonicum. Cellular and Molecular Life Sciences 63, 919929.
Clegg, J. A. ( 1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133147.
Contreras, V. T., De Lima, A. R. and Zorrilla, G. ( 1998). Trypanosoma cruzi: maintenance in culture modify gene and antigenic expression of metacyclic trypomastigotes. Memorias do Instituto Oswaldo Cruz 93, 753760.
Correnti, J. M., Brindley, P. J. and Pearce, E. J. ( 2005). Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Molecular and Biochemical Parasitology 143, 209215.
Cousin, C. E., Stirewalt, M. A. and Dorsey, C. H. ( 1981). Schistosoma mansoni: ultrastructure of early transformation of skin- and shear-pressure-derived schistosomules. Experimental Parasitology 51, 341365.
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.
Dean, D. A. ( 1977). Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover. The Journal of Parasitology 63, 418426.
Dean, D. A. and Mangold, B. L. ( 1992). Evidence that both normal and immune elimination of Schistosoma mansoni take place at the lung stage of migration prior to parasite death. American Journal of Tropical Medicine and Hygiene 47, 238248.
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.
El-Ridi, R., Mohamed, S. H. and Tallima, H. ( 2003). Incubation of Schistosoma mansoni lung-stage schistosomula in corn oil exposes their surface membrane antigenic specificities. The Journal of Parasitology 89, 10641067.
Ford, M. J., Bickle, Q. D., Taylor, M. G. and Andrews, B. J. ( 1984). Passive transfer of resistance and the site of immune-dependent elimination of the challenge infection in rats vaccinated with highly irradiated cercariae of Schistosoma mansoni. Parasitology 89, 461482.
Gobert, G. N., Stenzel, D. J., Jones, M. K., Allen, D. E. and McManus, D. P. ( 1997). Schistosoma japonicum: immunolocalization of paramyosin during development. Parasitology 114, 4552.
Gobert, G. N., Stenzel, D. J., McManus, D. P. and Jones, M. K. ( 2003). The ultrastructural architecture of the adult Schistosoma japonicum tegument. International Journal for Parasitology 33, 15611575.
Gold, D. and Fletcher, E. ( 2000). Influence of mechanical tail-detachment techniques of schistosome cercariae on the production, viability, and infectivity of resultant schistosomula: a comparative study. Parasitology Research 86, 570572.
Grossmann, G., Opekarova, M., Novakova, L., Stolz, J. and Tanner, W. ( 2006). Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryotic Cell 5, 945953.
Gui, M., Kusel, J. R., Shi, R. E. and Ruppel, A. ( 1995). Schistosoma japonicum and S. mansoni: comparison of larval migration patterns in mice. Journal of Helminthology 69, 1925.
Halton, D. W. ( 1997). Nutritional adaptations to parasitism within the platyhelminthes. International Journal for Parasitology 27, 693704.
Harrop, R., Coulson, P. S. and Wilson, R. A. ( 1999). Characterization, cloning and immunogenicity of antigens released by lung-stage larvae of Schistosoma mansoni. Parasitology 118, 583594.
Harrop, R. and Wilson, R. A. ( 1993). Protein synthesis and release by cultured schistosomula of Schistosoma mansoni. Parasitology 107, 265274.
He, Y. X. ( 1993). Biology of Schistosoma japonicum from cercaria penetrating into host skin to producing egg. Chinese Medical Journal 106, 576583.
He, Y. X., Chen, L. and Ramaswamy, K. ( 2002). Schistosoma mansoni, S. haematobium, and S. japonicum: early events associated with penetration andmigration of schistosomula through human skin. Experimental Parasitology 102, 99108.
He, Y. X., Salafsky, B. and Ramaswamy, K. ( 2005). Comparison of skin invasion among three major species of Schistosoma. Trends in Parasitology 21, 201203.
Hewitson, J. P., Hamblin, P. A. and Mountford, A. P. ( 2005). Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunology 27, 271280.
Hockley, D. 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.
Horemans, A. M. C., Tielens, A. and van den Bergh, S. G. ( 1992). The reversible effect of glucose on the energy metabolism of Schistosoma mansoni cercariae and schistosomula. Molecular and Biochemical Parasitology 51, 7380.
Jiang, J., Skelly, P. J., Shoemaker, C. B. and Caulfield, J. P. ( 1996). Schistosoma mansoni: the glucose transport protein SGTP4 is present in tegumental multilamellar bodies, discoid bodies, and the surface lipid bilayers. Experimental Parasitology 82, 201210.
Knopf, P. M., Cioli, D., Mangold, B. L. and Dean, D. A. ( 1986). Migration of Schistosoma mansoni in normal and passively immunized laboratory rats. American Journal of Tropical Medicine and Hygiene 35, 11731184.
Lawson, B. W. L., Bickle, Q. D. and Taylor, M. G. ( 1993). Mechanisms involved in the loss of antibody-mediated adherence of macrophages to lung-stage schistosomula of Schistosoma mansoni in vitro. Parasitology 106, 463469.
Loukas, A., Jones, M. K., King, L. T., Brindley, P. J. and McManus, D. P. ( 2001). Receptor for Fc on the surface of schistosomes. Infection and Immunity 69, 36463651.
Marikovsky, M., Parizade, M. and Arnon, R. ( 1990). Complement regulation on the surface of cultured schistosomula and adult worms of Schistosoma mansoni. European Journal of Immunology 20, 221227.
McLaren, D. J. ( 1980). Schistosoma mansoni: the parasite surface in relation to host immunity. In Tropical Medicine Research Studies Series, Vol. 1 ( ed. Brown, K. N.), pp. 229. Research Studies Press, London.
Mitchell, G. F., Tiu, W. U. and Garcia, E. G. ( 1991). Infection characteristics of Schistosoma japonicum in mice and relevance to the assessment of schistosome vaccines. Advances in Parasitology 30, 167200.
Moser, G., Wassom, D. L. and Sher, A. ( 1980). Studies of the antibody-dependent killing of schistosomula of Schistosoma mansoni employing haptenic target antigens. I. Evidence that the loss in susceptibility to immune damage undergone by developing schistosomula involves a change unrelated to the masking of parasite antigens by host molecules. Journal of Experimental Medicine 152, 4153.
Mountford, A. P. and Harrop, R. ( 1998). Vaccination against schistosomiasis: the case for lung-stage antigens. Parasitology Today 14, 109114.
Mountford, A. P., Harrop, R. and Wilson, A. ( 1995). Antigens derived from lung-stage larvae of Schistosoma mansoni are efficient stimulators of proliferation and gamma interferon secretion by lymphocytes from mice vaccinated with attenuated larvae. Infection and Immunity 63, 19801986.
Parizade, M., Arnon, R., Lachmann, P. J. and Fishelson, Z. ( 1994). Functional and antigenic similarities between a 94-kD protein of Schistosoma mansoni (SCIP-1) and human CD59. Journal of Experimental Medicine 179, 16251636.
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. and Pellegrino, J. ( 1974). Schistosoma mansoni: a defined system for the step-wise transformation of the cercaria to schistsomule. Experimental Parasitology 36, 360372.
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E. and Pellegrino, J. ( 1975). Factors affecting surface changes in intact cercariae and cercarial bodies of Schistosoma mansoni. Parasitology 71, 1925.
Salafsky, B., Fusco, A. C., Whitley, K., Nowicki, D. and Ellenberger, B. ( 1988). Schistosoma mansoni: Analysis of cercarial transformation methods. Experimental Parasitology 67, 116127.
Samuelson, J. C., Caulfield, J. P. and David, J. R. ( 1980). Schistosoma mansoni: post-transformational surface changes in schistosomula grown in vitro and in mice. Experimental Parasitology 50, 369383.
Santoro, F., Lachmann, P. J., Capron, A. and Capron, M. ( 1979). Activation of complement by Schistosoma mansoni schistosomula: killing of parasites by the alternative pathway and requirement of IgG for classical pathway activation. Journal of Immunology 123, 15511557.
Sher, A., Sacks, D. L., Simpson, A. J. and Singer, A. ( 1984). Dichotomy in the tissue origin of schistosome acquired class I and class II major histocompatibility complex antigens. Journal of Experimental Medicine 159, 952957.
Skelly, P. J. and Shoemaker, C. B. ( 1995). A molecular genetic study of the variations in metabolic function during schistosome development. Memorias do Instituto Oswaldo Cruz 90, 281284.
Skelly, P. J. and Shoemaker, C. B. ( 1996). Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 93, 36423646.
Skelly, P. J. and Shoemaker, C. B. ( 2000). Induction cues for tegument formation during the transformation of Schistosoma mansoni cercariae. International Journal for Parasitology 30, 625631.
Skelly, P. J., Tielens, A. G. M. and Shoemaker, C. B. ( 1998). Glucose transport and metabolism in mammalian-stage schistosomes. Parasitology Today 14, 402406.
Stirewalt, M. A. ( 1974). Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology 12, 115182.
Stirewalt, M. A. and Dorsey, C. H. ( 1974). Schistosoma mansoni: cercarial penetration of host epidermis at the ultrastructural level. Experimental Parasitology 35, 115.
Tallima, H. and El Ridi, R. ( 2005). Methyl-beta-Cyclodextrin treatment and filipin staining reveal the role of cholesterol in surface membrane antigen sequestration of Schistosoma mansoni and S. haematobium lung-stage larvae. Journal of Parasitology 91, 720725.
Wilson, R. A. and Coulson, P. S. ( 1989). Lung-phase immunity to schistosomes: a new perspective on an old problem. Parasitology Today 5, 274278.
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