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. 1986 Mar;51(3):859–864. doi: 10.1128/iai.51.3.859-864.1986

Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies.

M J Stewart, R J Nawrot, S Schulman, J P Vanderberg
PMCID: PMC260977  PMID: 3512436

Abstract

A monoclonal antibody directed against the circumsporozoite protein on the surface of Plasmodium berghei sporozoites inhibited sporozoite motility in vitro. These immobilized sporozoites could adhere to but not invade target cultured cells. Other sporozoite-immobilizing agents also inhibited sporozoite invasion into cultured cells and did not prevent sporozoite adherence. These results indicate that sporozoite invasiveness is associated with sporozoite motility. Thus, the immobilizing effect of this antibody could explain its functional activity against sporozoite invasion in vivo.

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  1. Aikawa M., Schwartz A., Uni S., Nussenzweig R., Hollingdale M. Ultrastructure of in vitro cultured exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. Am J Trop Med Hyg. 1984 Sep;33(5):792–799. doi: 10.4269/ajtmh.1984.33.792. [DOI] [PubMed] [Google Scholar]
  2. Ballou W. R., Rothbard J., Wirtz R. A., Gordon D. M., Williams J. S., Gore R. W., Schneider I., Hollingdale M. R., Beaudoin R. L., Maloy W. L. Immunogenicity of synthetic peptides from circumsporozoite protein of Plasmodium falciparum. Science. 1985 May 24;228(4702):996–999. doi: 10.1126/science.2988126. [DOI] [PubMed] [Google Scholar]
  3. Clyde D. F. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am J Trop Med Hyg. 1975 May;24(3):397–401. doi: 10.4269/ajtmh.1975.24.397. [DOI] [PubMed] [Google Scholar]
  4. Clyde D. F., Most H., McCarthy V. C., Vanderberg J. P. Immunization of man against sporozite-induced falciparum malaria. Am J Med Sci. 1973 Sep;266(3):169–177. doi: 10.1097/00000441-197309000-00002. [DOI] [PubMed] [Google Scholar]
  5. Collins W. E., Contacos P. G. Immunization of monkeys against Plasmodium cynomolgi by X-irradiated sporozoites. Nat New Biol. 1972 Apr 12;236(67):176–177. doi: 10.1038/newbio236176a0. [DOI] [PubMed] [Google Scholar]
  6. Dame J. B., Williams J. L., McCutchan T. F., Weber J. L., Wirtz R. A., Hockmeyer W. T., Maloy W. L., Haynes J. D., Schneider I., Roberts D. Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science. 1984 Aug 10;225(4662):593–599. doi: 10.1126/science.6204383. [DOI] [PubMed] [Google Scholar]
  7. Danforth H. D., Aikawa M., Cochrane A. H., Nussenzweig R. S. Sporozoites of mammalian malaria: attachment to, interiorization and fate within macrophages. J Protozool. 1980 May;27(2):193–202. doi: 10.1111/j.1550-7408.1980.tb04680.x. [DOI] [PubMed] [Google Scholar]
  8. Enea V., Ellis J., Zavala F., Arnot D. E., Asavanich A., Masuda A., Quakyi I., Nussenzweig R. S. DNA cloning of Plasmodium falciparum circumsporozoite gene: amino acid sequence of repetitive epitope. Science. 1984 Aug 10;225(4662):628–630. doi: 10.1126/science.6204384. [DOI] [PubMed] [Google Scholar]
  9. Foley D. A., Vanderberg J. P. Plasmodium berghei: transmission by intraperitoneal inoculation of immature exoerythrocytic schizonts from rats into rats, mice, and hamsters. Exp Parasitol. 1977 Oct;43(1):69–81. doi: 10.1016/0014-4894(77)90009-1. [DOI] [PubMed] [Google Scholar]
  10. Gwadz R. W., Cochrane A. H., Nussenzweig V., Nussenzweig R. S. Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bull World Health Organ. 1979;57 (Suppl 1):165–173. [PMC free article] [PubMed] [Google Scholar]
  11. Hollingdale M. R., Leef J. L., McCullough M., Beaudoin R. L. In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei from sporozoites. Science. 1981 Aug 28;213(4511):1021–1022. doi: 10.1126/science.7022652. [DOI] [PubMed] [Google Scholar]
  12. Hollingdale M. R., Leland P., Leef J. L., Schwartz A. L. Entry of Plasmodium berghei sporozoites into cultured cells, and their transformation into trophozoites. Am J Trop Med Hyg. 1983 Jul;32(4):685–690. doi: 10.4269/ajtmh.1983.32.685. [DOI] [PubMed] [Google Scholar]
  13. Hollingdale M. R., Zavala F., Nussenzweig R. S., Nussenzweig V. Antibodies to the protective antigen of Plasmodium berghei sporozoites prevent entry into cultured cells. J Immunol. 1982 Apr;128(4):1929–1930. [PubMed] [Google Scholar]
  14. Jensen J. B., Edgar S. A. Possible secretory function of the rhoptries of Eimeria magna during penetration of cultured cells. J Parasitol. 1976 Dec;62(6):988–992. [PubMed] [Google Scholar]
  15. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  16. Leland P., Sigler C. I., Danforth H. D., Hollingdale M. R. Inhibition of Plasmodium berghei sporozoite invasion of cultured hepatoma cells. Trans R Soc Trop Med Hyg. 1984;78(5):639–640. doi: 10.1016/0035-9203(84)90226-8. [DOI] [PubMed] [Google Scholar]
  17. Meis J. F., Verhave J. P., Jap P. H., Meuwissen J. H. An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats. Parasitology. 1983 Apr;86(Pt 2):231–242. doi: 10.1017/s003118200005040x. [DOI] [PubMed] [Google Scholar]
  18. Meuwissen J. H., Golenser J., Verhave J. P. Development of effective antisporozoite immunity by natural bites of Plasmodium-berghei-infected mosquitoes in rats under prophylactic treatment with various drug regimens. Isr J Med Sci. 1978 May;14(5):601–605. [PubMed] [Google Scholar]
  19. NISONOFF A. ENZYMATIC DIGESTION OF RABBIT GAMMA GLOBULIN AND ANTIBODY AND CHROMATOGRAPHY OF DIGESTION PRODUCTS. Methods Med Res. 1964;10:134–141. [PubMed] [Google Scholar]
  20. Nardin E. H., Nussenzweig R. S. Stage-specific antigens on the surface membrane of sporozoites of malaria parasites. Nature. 1978 Jul 6;274(5666):55–57. doi: 10.1038/274055a0. [DOI] [PubMed] [Google Scholar]
  21. Potocnjak P., Yoshida N., Nussenzweig R. S., Nussenzweig V. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med. 1980 Jun 1;151(6):1504–1513. doi: 10.1084/jem.151.6.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rieckmann K. H., Beaudoin R. L., Cassells J. S., Sell K. W. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull World Health Organ. 1979;57 (Suppl 1):261–265. [PMC free article] [PubMed] [Google Scholar]
  23. Rieckmann K. H., Carson P. E., Beaudoin R. L., Cassells J. S., Sell K. W. Letter: Sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans R Soc Trop Med Hyg. 1974;68(3):258–259. doi: 10.1016/0035-9203(74)90129-1. [DOI] [PubMed] [Google Scholar]
  24. Russell D. G. Host cell invasion by Apicomplexa: an expression of the parasite's contractile system? Parasitology. 1983 Oct;87(Pt 2):199–209. doi: 10.1017/s0031182000052562. [DOI] [PubMed] [Google Scholar]
  25. Schwartz A. L., Fridovich S. E., Knowles B. B., Lodish H. F. Characterization of the asialoglycoprotein receptor in a continuous hepatoma line. J Biol Chem. 1981 Sep 10;256(17):8878–8881. [PubMed] [Google Scholar]
  26. Shin S. C., Vanderberg J. P., Terzakis J. A. Direct infection of hepatocytes by sporozoites of Plasmodium berghei. J Protozool. 1982 Aug;29(3):448–454. doi: 10.1111/j.1550-7408.1982.tb05431.x. [DOI] [PubMed] [Google Scholar]
  27. Vanderberg J. P. Inactivity of rodent malaria anti-sporozoite antibodies against exoerythrocytic forms. Am J Trop Med Hyg. 1973 Sep;22(5):573–577. doi: 10.4269/ajtmh.1973.22.573. [DOI] [PubMed] [Google Scholar]
  28. Vanderberg J. P. Plasmodium berghei: quantitation of sporozoites injected by mosquitoes feeding on a rodent host. Exp Parasitol. 1977 Jun;42(1):169–181. doi: 10.1016/0014-4894(77)90075-3. [DOI] [PubMed] [Google Scholar]
  29. Vanderberg J. P. Studies on the motility of Plasmodium sporozoites. J Protozool. 1974 Oct;21(4):527–537. doi: 10.1111/j.1550-7408.1974.tb03693.x. [DOI] [PubMed] [Google Scholar]
  30. Vanderberg J., Nussenzweig R., Most H. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. V. In vitro effects of immune serum on sporozoites. Mil Med. 1969 Sep;134(10):1183–1190. [PubMed] [Google Scholar]
  31. Werk R., Bommer W. Toxoplasma gondii: membrane properties of active energy-dependent invasion of host cells. Tropenmed Parasitol. 1980 Dec;31(4):417–420. [PubMed] [Google Scholar]
  32. Yoshida N., Nussenzweig R. S., Potocnjak P., Nussenzweig V., Aikawa M. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science. 1980 Jan 4;207(4426):71–73. doi: 10.1126/science.6985745. [DOI] [PubMed] [Google Scholar]
  33. Young J. F., Hockmeyer W. T., Gross M., Ballou W. R., Wirtz R. A., Trosper J. H., Beaudoin R. L., Hollingdale M. R., Miller L. H., Diggs C. L. Expression of Plasmodium falciparum circumsporozoite proteins in Escherichia coli for potential use in a human malaria vaccine. Science. 1985 May 24;228(4702):958–962. doi: 10.1126/science.2988125. [DOI] [PubMed] [Google Scholar]
  34. Zavala F., Cochrane A. H., Nardin E. H., Nussenzweig R. S., Nussenzweig V. Circumsporozoite proteins of malaria parasites contain a single immunodominant region with two or more identical epitopes. J Exp Med. 1983 Jun 1;157(6):1947–1957. doi: 10.1084/jem.157.6.1947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zavala F., Hollingdale M. R., Schwartz A. L., Nussenzweig R. S., Nussenzweig V. Immunoradiometric assay to measure the in vitro penetration of sporozoites of malaria parasites into hepatoma cells. J Immunol. 1985 Feb;134(2):1202–1205. [PubMed] [Google Scholar]
  36. Zavala F., Tam J. P., Hollingdale M. R., Cochrane A. H., Quakyi I., Nussenzweig R. S., Nussenzweig V. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Science. 1985 Jun 21;228(4706):1436–1440. doi: 10.1126/science.2409595. [DOI] [PubMed] [Google Scholar]

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