Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-20T02:24:31.820Z Has data issue: false hasContentIssue false

Metabolic changes associated with the migration of the schistosomulum of Schistosoma mansoni in the mammal host

Published online by Cambridge University Press:  06 April 2009

J. Ruth Lawson
Affiliation:
Department of Biology, University of York, Heslington, York
R. A. Wilson
Affiliation:
Department of Biology, University of York, Heslington, York

Summary

A variety of measurements was made on small samples of schistosomula recovered from the skin, lungs and hepatic portal system of percutaneously infected mice, on the basis of which development could be divided into a migration and a growth phase. The density of schistosomula, estimated using a Ficoll gradient, was found not to vary significantly between Day 0 and Day 24 post-infection, having a mean value of 1·077. The reduced weight was measured by means of a Cartesian diver balance and used in conjunction with density to estimate the change in wet weight of schistosomula. Wet weight was found to decline slightly during the migration phase and to increase exponentially following arrival of schistosomula in the hepatic portal system. No change in nitrogen content was detected during migration but there was a rapid increase after arrival in the hepatic portal system. The rate of oxygen consumption, measured by Cartesian diver respirometer, declined significantly during migration and then increased exponentially after arrival of worms in the hepatic portal system. No change was detected in the lactic dehydrogenase activity of migrating worms but again, an exponential increase occurred after entry into the hepatic portal system. It was concluded that the migrating schistosomulum is in a semi-quiescent metabolic state, although it possesses the ability to take up nutrients and undergoes morphological changes. Growth is triggered by an unknown mechanism after arrival in the hepatic portal system. Examination of the various sets of data suggests that it is initiated between 10 and 11 days post-infection in the most advanced schistosomula.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1980

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

Becker, W. (1977). Zur Stoffwechselphysiologie der Miracidien von Schistosoma mansoni während ihrer Aktivierung innerhalb der Eischale. Zeitschrift für Parasitenkunde 52, 6979.CrossRefGoogle Scholar
Bergmeyer, H. U. & Bernt, E. (1974). Colorimetric assay with L-Lactate, NAD, phenazine methosulphate and INT. In Methods of Enzymatic Analysis, vol. 2 (ed. Bergmeyer, H. U.), pp. 579–82. New York and London: Academic Press.CrossRefGoogle Scholar
Von Brand, T. (1973). Biochemistry of Parasites. New York and London: Academic Press.Google Scholar
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.CrossRefGoogle ScholarPubMed
Coles, G. C. (1972). Carbohydrate metabolism of larval Schistosoma mansoni. International Journal for Parasitology 2, 341–52.CrossRefGoogle ScholarPubMed
Coles, G. C. (1973). Further studies on the carbohydrate metabolism of immature Schistosoma mansoni. International Journal for Parasitology 3, 783–7.CrossRefGoogle ScholarPubMed
Faust, E. C., Jones, C. A. & Hoffman, W. A. (1934). Studies on schistosomiasis mansoni in Puerto Rico. III. Biological studies. 2. The mammalian phase of the life cycle. Puerto Rico Journal of Public Health and Tropical Medicine 10, 133–96.Google Scholar
Ghandour, A. M. & Webbe, G. (1973). A study of the death of Schistosoma mansoni cercariae during penetration of mammalian host skin: the influences of the ages of the cercariae and of the host. International Journal for Parasitology 3, 789–94.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, 1325.CrossRefGoogle ScholarPubMed
Holter, H., Linderstrøm-Lang, K. & Zeuthen, E. (1956). Manometric techniques for single cells. In Physical Techniques in Biological Research, vol. 3 (ed. Oster, G. and Pollister, A. W.), pp. 557625. New York: Academic Press.Google Scholar
Howells, R. E., Gerken, S. E., Ramalho-Pinto, F. J., Kawazoe, U., Gazzinelli, G. & Pellegrirno, J. (1975). Schistosoma mansoni: tail loss in relation to permeability changes during cercaria-schistosomulum transformation. Parasitology 71, 918.CrossRefGoogle ScholarPubMed
Jacobs, S. (1960). The determination of nitrogen in organic compounds by the indanetrione hydrate method. The Analyst 85, 257–64.CrossRefGoogle Scholar
Jacobs, S. (1962). The quantitative determination of nitrogen by a further modification of the indanetrione hydrate method. The Analyst 87, 53–7.CrossRefGoogle Scholar
Lawson, J. R. (1977). The biology of the cercaria and early schistosomulum of Schistosoma mansoni. D.Phil. thesis, University of York.Google Scholar
Lennox, R. W. & Schiller, E. L. (1972). Changes in dry weight and glycogen content as criteria for measuring the postcercarial growth and development of Schistosoma mansoni. Journal of Parasitology 58, 489–94.CrossRefGoogle ScholarPubMed
Løvtrup, S. (1950 a). Observations on the Cartesian diver balance technique. Comptes Rendus des Travaux du Laboratoire Carlsberg, Série Chimique 27, 125–36.Google Scholar
Løvtrup, S. (1950 b). Determination of density of amoebae by means of a starch density gradient. Comptes Rendus des Travaux du Laboratoire Carlsberg, Série Chimique 27, 137–44.Google Scholar
Miller, P. & Wilson, R. A. (1978). Migration of the schistosomula of Schistosoma mansoni from skin to lungs. Parasitology 77, 281302.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1979). Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80, 267–88.CrossRefGoogle Scholar
Moller, K. M. & Ottolenghi, P. (1964). The manufacture of small standardized glass floats for calibrating density gradients. Comptes Rendus des Travaux du Laboratoire Carlsberg, Série Chimique 34, 169–85.Google ScholarPubMed
Newsholme, E. A. & Start, C. (1973). Regulation in Metabolism. London: John Wiley.Google Scholar
Para, J., Lewert, R. M. & Özcel, M. A. (1970). Schistosoma mansoni: distribution of 14C in isotopically labelled cercariae and its loss during early infection. Experimental Parasitology 27, 273–80.CrossRefGoogle ScholarPubMed
Rabinowitz, Y. (1964). Separation of lymphocytes, polymorphonuclear leukocytes and monocytes on glass columns, including tissue culture observations. Blood 23, 811–28.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695700.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1974). Schistosoma mansoni: cercaria to schistosomula. Advances in Parasitology 12, 115–82.CrossRefGoogle Scholar
Wagenbach, G. E. (1969). Purification of Eimeria tenella sporozoites with glass bead columns. Journal of Parasitology 55, 833–8.CrossRefGoogle ScholarPubMed
Wheater, P. R. & Wilson, R. A. (1979). Schistosoma mansoni: a histological study of migration in the laboratory mouse. Parasitology 79, 4962.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, 5773.CrossRefGoogle Scholar
Wilson, R. A. & Lawson, J. R. (1980). An examination of the skin phase of schistosome migration using a hamster cheek pouch preparation. Parasitology 80, 257–66.CrossRefGoogle ScholarPubMed
Wilson, R. A., Pullin, R. & Denison, J. (1971). An investigation of the mechanism of infection by digenetic trematodes: the penetration of the miracidium of Fasciola hepatica into its snail host Lymnaea truncatula. Parasitology 63, 491506.CrossRefGoogle ScholarPubMed
Yolles, T. K., Moore, D. V. & Meleney, H. E. (1949). Post-cercarial development of Schistosoma mansoni in the rabbit and hamster after intra-peritoneal and percutaneous infection. Journal of Parasitology 35, 276–94.CrossRefGoogle Scholar
Zeuthen, E. (1948). A Cartesian diver balance weighing reduced weights with an accuracy of ± 0.01γ. Comptes Rendus des Travaux du Laboratoire Carlsberg, S´rie Chimique 26, 243–65.Google Scholar
Zeuthen, E. (1953). Growth as related to the cell cycle in single cell cultures of Tetrahymena pyriformis. Journal of Embryology and Experimental Morphology 1, 239–49.Google Scholar