Skip to main content
Log in

Electron microscopic studies on the interaction of rat Kupffer cells andPlasmodium berghei sporozoites

  • Original Investigations
  • Published:
Zeitschrift für Parasitenkunde Aims and scope Submit manuscript

Abstract

The interactions betweenPlasmodium berghei sporozoites and Kupffer cells in rat liver were studied by transmission electron microscopy. Between 10 and 45 min after inoculation, sporozoites were found in the process of entering Kupffer cells and inside phagolysosomes. The sporozoites entered the Kupffer cells by phagocytosis as determined by the presence of pseudopods and local accumulations of aggregated microfilaments and the resulting exclusion of other organelles in the phagocyte cytoplasm beneath the attached parasite. Sporozoites were taken up either with their anterior end first, or backwards. Scanning electron microscopy of in vitro sporozoite Kupffer cell interaction confirmed these observations. It was concluded that sporozoites are taken up in a normal phagocytic way by the Kupffer cells, regardless of their initial place of contact or position. Thirty min after inoculation sporozoites found in phagolysosomes were still morphologically intact but after 45 min we could encounter completely digested sporozoites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aikawa M, Yoshida N, Nussenzweig RS, Nussenzweig V (1981) The protective antigen of malaria sporozoites (Plasmodium berghei) is a differentiation antigen. J Immunol 126:2494–2495

    Google Scholar 

  • Blackwell JM, Alexander J (1983) The macrophage and parasitic protozoa. Trans Roy Soc Trop Med Hyg 77:636–645

    Google Scholar 

  • Brouwer A, Knook DL (1982) Endocytosis of heat-denaturated albumin by cultured rat Kupffer cells. J Reticuloendothel Soc 32:259–268

    Google Scholar 

  • Cochrane AH, Aikawa M, Jeng M, Nussenzweig RS (1976) Antibody-induced ultrastructural changes of malarial sporozoites. J Immunol 116:859–867

    Google Scholar 

  • Danforth HD, Aikawa M, Cochrane AH, Nussenzweig RS (1980) Sporozoites of mammalian malaria: Attachment to, interiorization and fate within macrophages. J Protozool 27:193–202

    Google Scholar 

  • Danforth HD, Moon RJ, Jensen JB, Vrable RG, Beaudoin RL (1982) Retention ofPlasmodium berghei sporozoites within perfused mouse livers. Acta Trop (Basel) 39:5–10

    Google Scholar 

  • Goldmacher VS (1984) Macrophages. Inhibition of endocytosis by anchorage to substrate. Exp Cell Res 154:632–635

    Google Scholar 

  • Hollingdale MR, Schwartz AL (1983) Sporozoites recognize specific hepatocyte receptors. In: Molecular biology of host-parasite interactions. J Cell Biochem (supl.) 7A p. 37

    Google Scholar 

  • Knook DL, Sleyster EC (1976) Separation of Kupffer and endothelial cells of the rat liver by centrifugal elutriation. Exp Cell Res 99:449

    Google Scholar 

  • Langreth SG, Nguyen-Dinh P, Trager W (1978)Plasmodium falciparum: merozoite invasion in vitro in the presence of chloroquine. Exp Parasitol 46:235–238

    Google Scholar 

  • Meis JFGM, Verhave JP, Jap PHK, Hess F, Meuwissen JHETh (1981) An ultrastructural study of developing stages of exoerythrocyticPlasmodium berghei in rat hepatocytes. Parasitology 82:195–204

    Google Scholar 

  • Meis JFGM, Verhave JP, Jap PHK, Meuwissen JHETh (1982) The role of Kupffer cells in the trapping of malarial sporozoites in the liver and the subsequent infection of hepatocytes. In: Knook DL, Wisse E (eds.) Sinusoidal liver cells. Elsevier Biomedical Press, Amsterdam, 429–436

    Google Scholar 

  • Meis JFGM, Verhave JP, Jap PHK, Meuwissen JHETh (1983a) An ultrastructural study on the role of Kupffer cells in the process of infection byPlasmodium berghei sporozoites in rats. Parasitology 86:231–242

    Google Scholar 

  • Meis JFGM, Verhave JP, Jap PHK, Sinden RE, Meuwissen JHETh (1983b) Ultrastructural observations on the infection of rat liver byPlasmodium berghei sporozoites in vivo. J Protozool 30:361–366

    Google Scholar 

  • Miller LH, Aikawa M, Johnson JG, Shiroishi T (1979) Interaction between cytochalasin B-treated malaria parasites and red cells: attachment and junction formation. J Exp Med 149:172–184

    Google Scholar 

  • Potocnjak P, Yoshida N, Nussenzweig RS, Nussenzweig V (1980) Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med 151:1504–1513

    Google Scholar 

  • Shin SCJ, Vanderberg JP, Terzakis JA (1982) Direct infection of hepatocytes by sporozoites ofPlasmodium berghei. J Protozool 29:448–454

    Google Scholar 

  • Sinden RE, Smith JE (1982) The role of the Kupffer cell in the infection of rodents by sporozoites ofPlasmodium: uptake of sporozoites by perfused liver and the establishment of infection in vivo. Acta Trop (Basel) 39:11–27

    Google Scholar 

  • Sleyster EC, Knook DL (1982) Relation between localization and function of rat liver Kupffer cells. Lab Invest 47:484–490

    Google Scholar 

  • Thorne KJI, Blackwell JM (1983) Cell-mediated killing of protozoa. Adv Parasitol 22:43–151

    Google Scholar 

  • Verhave JP, Meuwissen JHETh, Golenser J (1980) The dual role of macrophages in the sporozoite-induced malaria infection. A hypothesis. Int J Nucl Med Biol 7:149–156

    Google Scholar 

  • Verhave JP, Meis JFGM, De Boo Th, Meuwissen JHETh (1985) The delivery of exoerythrocytic malaria parasites. Ann Soc belge Med Trop (in press)

  • Vermeulen AN, Van Munster JC, Meuwissen JHETh (1982)Plasmodium berghei: immunologically active proteins on the sporozoite surface. Exp Parasitol 53:199–208

    Google Scholar 

  • Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M (1980) Hybridroma produces protective antibodies directed against the sporozoite stage of malaria parasites. Science 207:71–73

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meis, J.F.G.M., Verhave, J.P., Brouwer, A. et al. Electron microscopic studies on the interaction of rat Kupffer cells andPlasmodium berghei sporozoites. Z. Parasitenkd. 71, 473–483 (1985). https://doi.org/10.1007/BF00928350

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00928350

Keywords

Navigation