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The effect of incubation in vitro on the susceptibility of monkey erythrocytes to invasion by Plasmodium knowlesi

Published online by Cambridge University Press:  06 April 2009

P. I. Trigg
Affiliation:
Division of Parasitology, National Institute for Medical Research Mitt Hill, London NW7 1AA
P. G. Shakespeare
Affiliation:
Division of Parasitology, National Institute for Medical Research Mitt Hill, London NW7 1AA

Extract

Rhesus monkey erythrocytes when incubated in vitro under similar conditions to those used for the cultivation of Plasmodium knowlesi-infected erythrocytes in vitro, exhibit an increase both in their osmotic fragility and in the activity of their acetylthiocholinesterase. No effect was observed on the catabolism of glucose through the glycolytic pathway or through the primary dehydrogenases of the pentose phosphate pathway. The ATP content of normal monkey erythrocytes was also unchanged during incubation in vitro. These observations indicate that incubation of erythrocytes in vitro primarily causes membrane changes. Infection of normal erythrocytes by P. knowlesi was reduced markedly by preincubation in vitro at 37 °C for 24 and 48 h. These results suggest that the maintenance of integrity of the surface of the eythrocyte in vitro is a necessary prerequisite for an efficient culture system for the malaria parasite.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1976

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References

REFERENCES

Aloni, B. & Livne, A. (1974). Acetylcholinesterase as a probe for erythrocyte-membrane intactness. Biochimica et Biophysica Acta 339, 359–66.CrossRefGoogle ScholarPubMed
Anfinsen, C. B, Geiman, Q. M, McKee, R. W, Ormsbee, R. A. & Ball, E. G. (1946). Studies on malarial parasites. VIII. Factors affecting the growth of Plasmodium knowlesi. Journal of Experimental Medicine 84, 607–21.CrossRefGoogle ScholarPubMed
Bannister, L. H, Butcher, G. A, Dennis, E. D. & Mitchell, G. H. (1975). Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71, 483–91.CrossRefGoogle ScholarPubMed
Bertagna, P., Cohen, S., Geiman, Q. M, Haworth, J., Königk, E., Richabds, W. H. G. & Trigg, P. I. (1972). Cultivation techniques for the erythrocytic stages of malaria parasites. Bulletin of the World Health Organization 47, 357–73.Google ScholarPubMed
Brewer, G. J. & Powell, R. D. (1965). A study of the relationship between the content of adenosine triphosphate in human red cells and the course of falciparum malaria: a new system that may confer protection against malaria. Proceedings of the National Academy of Sciences 54, 741–5.CrossRefGoogle ScholarPubMed
Butcher, G. A. & Cohen, S. (1971). Short-term culture of Plasmodium knowlesi. Parasitology 62, 309–20.CrossRefGoogle ScholarPubMed
Butcher, G. A, Mitchell, G. H. & Cohen, S. (1973). Mechanism of host specificity in malarial infection. Nature, London 244, 40–2.CrossRefGoogle ScholarPubMed
Card, R. T, Paulson, E. J. & Valsberg, L. S. (1968). Autohemolysis and osmotic fragility of macrocytic erythrocytes produced in response to hemolysis. American Journal of Physiology 214, 4551.CrossRefGoogle ScholarPubMed
Cooper, R. A. & Jandl, J. H. (1969). The selective and conjoint loss of red cell lipids. Journal of Clinical Investigation 48, 906–14.CrossRefGoogle ScholarPubMed
Dacie, J. V. & Lewis, S. M. (1968). Practical Haematology, 4th ed. London: Churchill.Google Scholar
Dennis, E. D, Mitchell, G. H, Butcher, G. A. & Cohen, S. (1975). In vitro isolation of Plasmodium knowlesi merozoites using polycarbonate sieves. Parasitology 71, 475–82.CrossRefGoogle ScholarPubMed
Dvorak, J. A, Miller, L. H, Whitehouse, W. C. & Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–50.CrossRefGoogle ScholarPubMed
Eaton, J. W. & Brewer, G. J. (1975). Pentose phosphate metabolism. In The Red Blood Cell, vol. 1 (ed. McN Surgenor, D.), pp. 435–78. Academic Press.Google Scholar
Ellman, G. L, Courtney, K. D, Andres, V. & Featherstone, R. H. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7, 8895.CrossRefGoogle ScholarPubMed
Geiman, Q. M, Siddiqui, W. A. & Schnell, J. V. (1966 a). In vitro studies on erythrocytic stages of plasmodia, medium improvements and results with seven species of malarial parasites. Military Medicine 131 (Suppl.), 1015–25.CrossRefGoogle ScholarPubMed
Geiman, Q. M, Siddiqui, W. A. & Schnell, J. V. (1966 b). Plasma replacement for in vitro culture of Plasmodium knowlesi. Science 153, 1129–30.CrossRefGoogle ScholarPubMed
Gompertz, B. D. (1967). Metabolic changes in human red cells during incubation of whole blood in vitro. Biochemical Journal 102, 782–90.CrossRefGoogle Scholar
Hutton, J. J. (1972). Radiometric micromethod for quantitation of glucose utilization by the erythrocyte. Analytical Biochemistry 45, 577–84.CrossRefGoogle ScholarPubMed
Krebs, H. A. & Eggleston, L. V. (1940). The oxidation of pyruvate in pigeon breast muscle. Biochemical Journal 34, 442–59.CrossRefGoogle ScholarPubMed
Ladda, R., Aikawa, M. & Sprinz, H. (1969). Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. Journal of Parasitology 65, 633–44.CrossRefGoogle Scholar
Miller, L. H, Mason, S. J, Dvorak, J. A, McGinnis, M. H. & Rothman, I. K. (1975). Erythrocyte receptors for (Plasmodium knowlesi) malaria. Duffy blood group determinants. Science 189, 361–3.CrossRefGoogle ScholarPubMed
Miller, L. H, Powers, K. G., Finerty, J. & Vanderberg, J. P. (1974). Differences in surface charge between host cells and malarial parasites. Journal of Parasitology 59, 925–7.CrossRefGoogle Scholar
Murphy, J. R. (1962). Erythrocyte metabolism III. Relationship of energy metabolism and serum factors to the osmotic fragility following incubation. Journal of Laboratory and Clinical Medicine 60, 86109.Google Scholar
Powell, R. D, Brewer, G. J, Degowin, R. L. & Carson, P. E. (1966). Effects of glucose-6-phosphate dehydrogenase deficiency upon the host and upon host–drug–malaria parasite interactions. Military Medicine 131 (Suppl.), 1039–56.CrossRefGoogle ScholarPubMed
Rose, I. A. & Warms, J. V. B. (1966). Control of glycolysis in the human red blood cell. Journal of Biological Chemistry 241, 4848–54.CrossRefGoogle ScholarPubMed
Seed, T. M, Aikawa, M., Sterling, C. & Rabbege, J. (1974). Surface properties of extracellular parasites: morphological and cytochemical study. Infection and Immunity 9, 750761.CrossRefGoogle ScholarPubMed
Smalley, M. E. & Butcher, G. A. (1975). The in vitro culture of the blood stages of Plasmodium berghei. International Journal for Parasitology 5, 131–2.CrossRefGoogle ScholarPubMed
Shakespeare, P. G. & Trigg, P. I. (1973). Glucose catabolism by the malaria parasite Plasmodium knowlesi. Nature, London 241, 538–40.CrossRefGoogle ScholarPubMed
Trigg, P. I. (1968). A new continuous perfusion technique for the cultivation of malaria parasites in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 371–8.CrossRefGoogle Scholar
Trigg, P. I. (1969). The use of proprietary tissue culture media for the cultivation in vitro of the erythrocytic stages of Plasmodium knowlesi. Parasitology 59, 925–35.CrossRefGoogle ScholarPubMed
Trigg, P. I. & Gutteridge, W. E. (1971). A minimal medium for the growth of Plasmodium knowlesi in vitro. Parasitology 62, 113–23.CrossRefGoogle Scholar
Trigg, P. I. & Gutteridge, W. E. (1972). A rational approach to the serial culture of malaria parasites: evidence for a deficiency in RNA synthesis during the first cycle in vitro. Parasitology 65, 265–71.CrossRefGoogle Scholar
Williamson, J. & Cover, B. (1966). Separation of blood-cell-free trypanosomes and malaria parasites in a sucrose gradient. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 425–7.CrossRefGoogle Scholar