Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-08T04:47:46.688Z Has data issue: false hasContentIssue false
  • English
  • Français

Protein synthesis and release by cultured schistosomula of Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

R. Harrop  and
R. A. Wilson
R. Harrop
Affiliation:
Department of Biology, University of York, Heslington, York YOl 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, Heslington, York YOl 5DD
Get access Rights & Permissions [Opens in a new window]

Summary

The lung schistosomulum of Schistosoma mansoni is the target of protective immunity in mice singly vaccinated with irradiated cercariae. Since the effector responses are T cell-mediated, their initiation requires the release of antigens from the intact parasite. We have used the technique of biosynthetic labelling with ‘35S’methionine, before and after transformation of the cercariae, to analyse the kinetics of protein synthesis and release by the schistosomulum. In addition, the proteins present in the soluble fraction of the parasite and those released during in vitro culture have been characterized. During a 7-day culture period schistosomula derived from labelled cercariae lost proteins most rapidly within the first 3 h after transformation. Two proteins of molecular weight 61 and 20 kDa were dominant and may correspond to areas of proteolytic activity. Analysis of the rate of protein synthesis of schistosomula labelled after transformation revealed four different phases, which may relate to the developmental processes occurring in vivo. During the first 24 h, synthesis was very low, increasing to a plateau and then rising to a peak at day 8; thereafter the rate declined rapidly. Whilst some stage-specific synthesis of proteins was detected in the soluble fractions of the parasite bodies, the pattern of proteins released by cultured larvae was remarkably uniform. At least 15 proteins were detected by autoradiography with bands at 61, 45 and 20 kDa being particularly prominent. These proteins merit further study as potential mediators of the protective immune response.

Keywords

Schistosoma mansoniprotein synthesisschistosomulumprotective immune response
Type
Research Article
Information
Parasitology , Volume 107 , Issue 3 , September 1993 , pp. 265 - 274
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Basch, P. F. (1981). Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. Journal of Parasitology 67, 179–85.CrossRefGoogle ScholarPubMed
Basch, P. F. & Basch, N. (1982). Schistosoma mansoni: scanning electron microscopy of schistosomula, adults and eggs grown in vitro. Parasitology 85, 333–8.CrossRefGoogle ScholarPubMed
Blanton, R. E. & Licate, L. S. (1992). Developmental regulation of protein synthesis in schistosomes. Molecular and Biochemical Parasitology 51, 201–8.CrossRefGoogle ScholarPubMed
Caulfield, J. P., Cianci, C. M. L., McDiarmid, S. S., Suyemitsu, T. & Schmid, K. (1987). Ultrastructure, carbohydrate, and amino acid analysis of two preparations of the cercarial glycocalyx of Schistosoma mansoni. Journal of Parasitology 73, 514–22.CrossRefGoogle ScholarPubMed
Chavez-Olortegui, C., Resende, M. & Tavares, C. A. P. (1992). Purification and characterization of a 47 kDa protease from Schistosoma mansoni cercarial secretion. Parasitology 105, 211–18.CrossRefGoogle ScholarPubMed
Coulson, P. S. & Mountford, A. P. (1989). Fate of attenuated schistosomula administered to mice by different routes, relative to the immunity induced against Schistosoma mansoni. Parasitology 99, 39–45.CrossRefGoogle Scholar
Coulson, P. S. & Wilson, R. A. (1988). Examination of the mechanisms of pulmonary phase resistance to Schistosoma mansoni in vaccinated mice. American Journal of Tropical Medicine and Hygiene 38, 529–39.CrossRefGoogle ScholarPubMed
Cousin, C. E., Stirewalt, M. A. & Dorsey, C. H. (1981). Schistosoma mansoni: ultrastructure of early transformation of skin- and shear-pressure-derived schistosomules. Experimental Parasitology 51, 341–65.CrossRefGoogle ScholarPubMed
Crabtree, J. E. & Wilson, R. A. (1985). Schistosoma mansoni: an ultrastructural examination of skin migration in the hamster cheek pouch. Parasitology 91, 111–20.CrossRefGoogle ScholarPubMed
Crabtree, J. E. & Wilson, R. A. (1986). Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology 92, 343–54.CrossRefGoogle ScholarPubMed
Dean, D. A., Dioli, D. & Bukowski, M. A. (1981). Resistance induced by normal and irradiated Schistosoma mansoni: Ability of various worm stages to serve as inducers and targets in mice. American Journal of Tropical Medicine and Hygiene 30, 1026–32.CrossRefGoogle ScholarPubMed
Hockley, D. J. & 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
Keene, W. E., Jeong, K. H., McKerrow, J. H. & Werb, Z. (1983). Degradation of extracellular matrix by larvae of Schistosoma mansoni. II. Degradation by newly transformed and developing schistosomula. Laboratory Investigation 49, 201–7.Google ScholarPubMed
Landsperger, W. J., Stirewalt, M. A. & Dresden, M. H. (1982). Purification and properties of a proteolytic enzyme from the cercariae of the human trematode parasite Schistosoma mansoni. The Biochemical Journal 201, 137–44.CrossRefGoogle ScholarPubMed
Lawson, J. R. & Wilson, R. A. (1980). Metabolic changes associated with the migration of the schistosomulum of Schistosoma mansoni in the mammalian host. Parasitology 81, 325–36.CrossRefGoogle Scholar
Lazdins, J. K., Stein, M. J., David, J. R. & Sher, A. (1982). Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Experimental Parasitology 53, 39–44.CrossRefGoogle ScholarPubMed
Lewis, S. A. & Strand, M. (1991). Characterization of proteins and immunogens released by adult Schistosoma mansoni. Journal of Parasitology 77, 263–71.CrossRefGoogle ScholarPubMed
Lockwood, B. C., North, M. J., Scott, K. I., Bremner, A. F. & Coombs, G. H. (1987). The use of a highly sensitive electrophoretic method to compare the proteinases of trichomonads. Molecular and Biochemical Parasitology 24, 89–95.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host–parasite contact in relation to the induction of resistance in mice. Parasitology 88, 249–66.CrossRefGoogle Scholar
Marikovsky, M., Fishelson, Z. & Arnon, R. (1988). Purification and characterization of proteases secreted by transforming schistosomula of Schistosoma mansoni. Molecular and Biochemical Parasitology 30, 45–54.CrossRefGoogle ScholarPubMed
McKerrow, J. H., Keene, W. E., Jeong, K. H. & Werb, Z. (1983). Degradation of extracellular matrix by larvae of Schistosoma mansoni. Laboratory Investigation 49, 195–200.Google ScholarPubMed
McKerrow, J. H., Pino-Heiss, S., Lindquist, R. & Werb, Z. (1985). Purification and characterization of an elastinolytic proteinase secreted by cercariae of Schistosoma mansoni. Journal of Biological Chemistry 260, 3703–7.CrossRefGoogle ScholarPubMed
McKerrow, J. H. & Doenhoff, M. J. (1988). Schistosome proteases. Parasitology Today 4, 334–40.CrossRefGoogle ScholarPubMed
McLaren, D. J., Hockley, D. J., Goldring, O. L. & Hammond, B. J. (1978). A freeze fracture study of the developing tegumental outer membrane of Schistosoma mansoni. Parasitology 76, 327–48.CrossRefGoogle ScholarPubMed
Mountford, A. P., Coulson, P. S. & Wilson, R. A. (1988). Antigen localization and the induction of resistance in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 97, 11–25.CrossRefGoogle ScholarPubMed
Mountford, A. P., Coulson, P. S., Pemberton, R. M., Smythies, L. E. & Wilson, R. A. (1992). The generation of interferon-gamma-producing T lymphocytes in skin-draining lymph nodes, and their recruitment to the lungs, is associated with protective immunity to Schistosoma mansoni. Immunology 75, 250–6.Google Scholar
Mountford, A. P. & Wilson, R. A. (1990). Schistosoma mansoni: the effect of regional lymphadenectomy on the level of protection induced in mice by radiation- attenuated cercariae. Experimental Parasitology 71, 463–9.CrossRefGoogle ScholarPubMed
Nagai, Y., Gazzinelli, G., De Moraes, G. W. G. & Pellegrino, J. (1977). Protein synthesis during cercaria-schistosomulum transformation and early development of the Schistosoma mansoni larvae. Comparative and Biochemical Physiology 57, 27–30.Google ScholarPubMed
Pemberton, R. M., Smythies, L. E., Mountford, A. P. & Wilson, R. A. (1991). Patterns of cytokine production and proliferation by T lymphocytes differ in mice vaccinated or infected with Schistosoma mansoni. Immunology 73, 327–33.Google ScholarPubMed
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. & Pellegrino, J. (1974). Schistosoma mansoni: defined system for stepwise transformation of cercariae to schistosomulae in vitro. Experimental Parasitology 36, 360–72.CrossRefGoogle Scholar
Ratcliffe, E. C. & Wilson, R. A. (1992). The role of mononuclear-cell recruitment to the lungs in the development and expression of immunity to Schistosoma mansoni. Parasitology 104, 299–307.CrossRefGoogle Scholar
Sher, A. & Benno, D. (1982). Decreasing immunogenicity of developing schistosome larvae. Parasite Immunology 4, 101–7.CrossRefGoogle ScholarPubMed
Smythies, L. E., Coulson, P. S. & Wilson, R. A. (1992). monoclonal antibody to interferon-gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. Journal of Immunology 149, 3654–8.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Coulson, P. S. (1986). Schistosoma mansoni: dynamics of migration through the vascular system of the mouse. Parasitology 92, 83–100.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Coulson, P. S. (1989). Lung-phase immunity to schistosomes: a new perspective on an old problem. Parasitology Today 5, 274–8.CrossRefGoogle Scholar
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of the schistosomula of Schistosoma mansoni in mice vaccinated with radiation-attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology 92, 101–16.CrossRefGoogle ScholarPubMed
Wilson, R. A., Draskau, T., Miller, P. & Lawson, J. R. (1978). Schistosoma mansoni: the activity and development of the schistosomulum during migration from the skin to the hepatic portal system. Parasitology 77, 57–73.CrossRefGoogle Scholar
Yuckenburg, P. D., Poupin, F. & Mansour, T. E. (1987). Schistosoma mansoni: protein composition and synthesis during early development; evidence for early synthesis of heat shock proteins. Experimental Parasitology 63, 301–11.CrossRefGoogle Scholar