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An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats

Published online by Cambridge University Press:  06 April 2009

J. F. G. M. Meis ,
J. P. Verhave ,
P. H. K. Jap  and
J. H. E. Th. Meuwissen
J. F. G. M. Meis
Affiliation:
Department of Medical Parasitology, Geert Grooteplein Zuid 24, University of Nijmegen, 6500 HB Nijmegen, The Netherlands
J. P. Verhave
Affiliation:
Department of Medical Parasitology, Geert Grooteplein Zuid 24, University of Nijmegen, 6500 HB Nijmegen, The Netherlands
P. H. K. Jap
Affiliation:
Department of Cytology and Histology, Geert Grooteplein Noord 21, University of Nijmegen, 6500 HB Nijmegen, The Netherlands
J. H. E. Th. Meuwissen
Affiliation:
Department of Medical Parasitology, Geert Grooteplein Zuid 24, University of Nijmegen, 6500 HB Nijmegen, The Netherlands
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Summary

The interactions in vivo between Plasmodium berghei sporozoites and Kupffer cells in rat livers were studied by transmission electron microscopy. By 10 and 15 min after inoculation, sporozoites were both free in the liver sinusoids and inside endocytotic vacuoles of the Kupffer cells. The latter cells were very active in phagocytosing sporozoites, bacteria and red blood cells. The sporozoites retained their integrity inside the endocytotic vacuoles and no signs of lysosomal digestion were observed. Sporozoites seen within endocytotic vacuoles 1 h after inoculation were still morphologically intact, although bristle-coated vesicles fused with the vacuole membrane. Evidence is presented which suggests that Kupffer cells transport sporozoites towards the space of Disse and adjacent hepatocytes. No sporozoites were seen to penetrate an endothelial cell or its narrow fenestrae. It is proposed that Kupffer cell passage, rather than gaps in the sinusoidal lining, represents the normal route that sporozoites take to circumvent the endothelial barrier. The localization of exo-erythrocytic forms was made easier by the use of Brown Norway rats in which many more parasites develop than in the Wistar rats. The distribution pattern of the parasites was found to be mainly around the ‘periportal’ zones of the acini of liver tissue.

Type
Research Article
Information
Parasitology , Volume 86 , Issue 2 , April 1983 , pp. 231 - 242
Copyright
Copyright © Cambridge University Press 1983

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References

REFERENCES

Bradfield, J. W. B., Payne, H. R. & Small, D. (1982). The fate of colloidal carbon after hepatic phagocytosis. In Sinusoidal Liver Cells (ed. Knook, D. L. and Wisse, E.), pp. 453–4. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Danforth, H. D., Aikawa, M., Cochrane, A. H. & Nussenzweig, R. S. (1980). Sporozoites of mammalian malaria; Attachment to, interiorization and fate within macrophages. Journal of Protozoology 27, 193–202.CrossRefGoogle Scholar
Danforth, H. D., Moon, R. J., Jensen, J. B., Vrable, R. G. & Beaudoin, R. L. (1982). Retention of Plasmodium berghei sporozoites within perfused mouse livers. Acta tropica 39, 5–10.Google Scholar
De Zanger, R. & Wisse, E. (1982). The filtration-effect of rat liver fenestrated sinusoidal endothelium on the passage of remnant chylomicrons in the space of Disse. In Sinusoidal Liver Cells (ed. Knook, D. L. and Wisse, E.), pp. 69–79. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Gendrault, J. L., Montecino-Rodriguez, F. & Cinqualbre, J. (1982). Structure of the normal human liver sinusoid after perfusion fixation. In Sinusoidal Liver Cells (ed. Knook, D. L. and Wisse, E.), pp. 93–100. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Golenser, J., Heeren, J., Verhave, J. P., Van der Kaay, H. J. & Meuwissen, J. H. E. Th. (1977). Crossreactivity with sporozoites, exoerythrocytic forms and blood schizonts of Plasmodium berghei in indirect fluorescent antibody tests with sera of rats immunized with sporozoites or infected blood. Clinical and Experimental Immunology 29, 43–51.Google ScholarPubMed
Hollingdale, M. R., Leef, J. L., McCullough, M. & Beaudoin, R. L. (1981). In vitro cultivation of the exo-erythrocytic stage of Plasmodium berghei from sporozoites. Science 213, 1021–3.Google Scholar
Holmberg, S., Schulman, S. & Vanderberg, J. P. (1981). Role of a serum factor in enhancement of in vitro interactions between Plasmodium berghei sporozoites and hamster peritoneal macrophages. Journal of Parasitology 67, 893–7.Google Scholar
Jap, P. H. K., Meis, J. F. G. M., Verhave, J. P. & Meuwissen, J. H. E. Th. (1982). Degenerating exoerythrocytic forms of Plasmodium berghei in rat liver: an ultrastructural and eytochemical study. Parasitology 85, 263–9.CrossRefGoogle ScholarPubMed
Kirn, A., Gendrault, J. L., Gut, J. P., Steffan, A. M. & Bingen, A. (1982). Isolement et culture de cellules sinusoidales de foies humain et murin: une nouvelle approche pour l'éetude des infections virales du foie. Gastroenterologie Clinique et Biologique 6, 283–93.Google Scholar
Krotoski, W. A., Garnham, P. C. C., Bray, R. S., Krotoski, D. M., Killick-Kendrick, R., Draper, C. C., Targett, G. A. T. & Guy, M. W. (1982 a). Observations on early and late post-sporozoite tissue stages in primate malaria. I. Discovery of a new latent form of Plasmodium cynomolgi (the hypnozoite), and failure to detect hepatic forms within the first 24 hours after infection. American Journal of Tropical Medicine and Hygiene 31, 24–35.CrossRefGoogle ScholarPubMed
Krotoski, W. A., Bray, R. S., Garnham, P. C. C., Gwadz, R. W., Killick-Kendrick, R., Draper, C. C., Targett, G. A. T., Krotoski, D. M., Guy, M. W., Koontz, L. C. & Cogswell, F. B. (1982 b). Observations on early and late post-sporozoite tissue stages in primate malaria. II. The hypnozoite of Plasmodium cynomolgi bastianellii from 3 to 105 days after infection, and detection of 36-to 40-hour pre-erythrocytic forms. American Journal of Tropical Medicine and Hygiene 31, 211–25.CrossRefGoogle Scholar
Lambiotte, M., Landau, I., Thierry, N. & Miltgen, F. (1981). Dévelopment de schizontes dans des hepatocytes de rat adulte en culture après infestation in vitro par des sporozoites de Plasmodium yoelii. Comptes Rendus Hebdomadaires des Seances de l'Academe des Sciences, III (Paris) 293, 431–3.Google Scholar
Lojda, Z., Gossrau, R. & Schiebler, T. H. (1979). Enzyme Histochemistry. A Laboratory Manual. Berlin, Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Long, P. L. & Speer, C. A. (1977). Invasion of host cells by Coccidia. In Parasite Invasion (ed. Taylor, A. E. R. and Muller, R.). Symposium of the British Society of Parasitology 15, 1–26.Google Scholar
Mauel, J. (1982). Macrophages as host cells and reactive defence cells. In Immune Reactions to Parasites (ed. Frank, W.). Zentralblatt fur Bakteriologie, Mikrobiologie und Hygiene, l eAbteilung (Suppl.) 12, 43–56. Stuttgart, New York: Gustav Fischer Verlag.Google Scholar
Meis, J. F. G. M., Verhave, J. P., Jap, P. H. K., Hess, F. & Meuwissen, J. H. E. Th. (1981). An ultrastructural study of developing stages of exoerythrocytic Plasmodium berghei in rat hepatocytes. Parasitology 82, 195–204.Google Scholar
Meis, J. F. G. M., Verhave, J. P., Jap, P. H. K. & Meuwissen, J. H. E. Th. (1982 a). The demonstration of Plasmodium berghei sporozoites in rat hepatocytes one hour after inoculation. Zeitschrift für Parasitenkunde 67, 345–8.CrossRefGoogle ScholarPubMed
Meis, J. F. G. M., Verhave, J. P., Jap, P. H. K. & Meuwissen, J. H. E. Th. (1982 b). The role of Kupffer cells in the trapping of malarial sporozoites in the liver and the subsequent infection of hepatocytes. In Sinusoidal Liver Cells (ed. Knook, D. L. and Wisse, E.), pp. 429–36. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Pirson, Ph. (1982). Culture of the exoerythrocytic liver stages of Plasmodium berghei sporozoites in rat hepatocytes. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 422.CrossRefGoogle ScholarPubMed
Rappaport, A. M. (1982). Physioanatomic considerations. In Diseases of the Liver (ed. Schiff, L. and Schiff, E. R.), 5th ed, pp. 1–57. Philadelphia: Lippincot.Google Scholar
Seljelid, R. (1980). Properties of Kupffer cells. In Mononuclear Phagocytes: Functional Aspects (ed. Van Furth, R.), pp. 157–199. The Hague: Martinus Nijhoff.CrossRefGoogle Scholar
Shin, S. C. J., Vanderberg, J. P. & Terzakis, J. A. (1982). Direct infection of hepatocytes by sporozoites of Plasmodium berghei. Journal of Protozoology 29, 448–54.Google Scholar
Sinden, R. E. (1978). Cell biology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 85–168. London: Academic Press.Google Scholar
Sinden, R. E. & Smith, J. E. (1980). Culture of the liver stages (exoerythrocytic schizonts) of rodent malaria parasites from sporozoites in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 134–6.Google Scholar
Sinden, R. E. & Smith, J. E. (1982). The role of the Kupffer cell in the infection of rodents by sporozoites of Plasmodium: uptake of sporozoites by perfused liver and the establishment of infection in vivo. Acta tropica 39, 11–27.Google Scholar
Smith, J. E. & Sinden, R. E. (1982 a). Studies on the role of host serum in the retention of malarial sporozoites by isolated perfused rat liver. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 45–7.CrossRefGoogle ScholarPubMed
Smith, J. E. & Sinden, R. E. (1982 b). On the relationship between Kupffer cell activity in the uptake and infectivity of sporozoites of Plasmodium yoelii yoelii. In Sinusoidal Liver Cells (ed. Knook, D. L. and Wisse, E.), pp. 437–44. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Smith, J. E., Pirson, Ph. & Sinden, R. E. (1983). Studies on the kinetics of uptake and distribution of free and liposome entrapped primaquine, and of malarial sporozoites by isolated perfused rat liver. Annals of Tropical Medicine and Parasitology (in the Press).Google Scholar
Strome, C. P. A., DeSantis, P. L. & Beaudoin, R. L. (1979). The cultivation of the exo-erythrocytic stages of Plasmodium berghei from sporozoites in vitro. In Vitro 15, 531–6.Google Scholar
Vanderberg, J. P. (1981). Plasmodium berghei exo-erythrocytic forms develop only in the liver. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 904–5.CrossRefGoogle Scholar
Verhave, J. P. (1975). Immunization with sporozoites. An experimental study of Plasmodium berghei malaria. Ph.D. thesis, Catholic University Nijmegen, The Netherlands, 121 pp.Google Scholar
Verhave, J. P., Meuwissen, J.H, E. Th. & Golenser, J. (1980). The dual role of macrophages in the sporozoite-induced malaria infection. A hypothesis. International Journal of Nuclear Medicine and Biology 7, 149–56.Google Scholar
Wisse, E. (1977). Ultrastructure and function of Kupffer cells and other sinusoidal cells in the liver. In Kupffer Cells and Other Liver Sinusoidal Cells (ed. Wisse, E. and Knook, D. L.), pp. 33–60. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Wisse, E. (1980). On the fine structure and function of rat liver Kupffer cells. In The Reticuloendothelial System, vol. 1, (ed. Carr, I. and Daems, W. Th.), pp. 361–379. New York: Plenum Press.Google Scholar
Wisse, E. De, Zanger, R. B. & Jacobs, R. (1982). Lobular gradients in endothelial fenestrae and sinusoidal diameter favour centralobular exchange processes in scanning EM study. In Sinusoidal Liver Cells (ed. Knook, D. L. & Wisse, E.), pp. 61–7. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar