Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro

Molecular and Biochemical Parasitology

Volumn 76, Issue 1-2, 1996, Pages 257-266

  Frevert, Ute ^a   Sinnis, Photini ^a   Esko, Jeffrey D ^b   Nussenzweig, Victor ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

circumsporozoite protein; heparan sulfate proteoglycan; heparan sulfate deficient CHO mutants; Plasmodium berghei; sporozoite invasion

Indexed keywords

GLYCOSAMINOGLYCAN; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CELL SURFACE; CONTROLLED STUDY; HOST PARASITE INTERACTION; IMMUNOFLUORESCENCE; IN VITRO STUDY; NONHUMAN; PLASMODIUM BERGHEI; PRIORITY JOURNAL; SPOROZOITE;

ANIMALIA; PLASMODIUM BERGHEI;

EID: 0029974996     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/0166-6851(95)02563-4     Document Type: Article

References (43)

1. Nussenzweig, V. and Nussenzweig, R. S. (1989) Rationale for the development of an engineered sporozoite malaria vaccine. Adv. Immunol. 45, 283-334.
2. Robson, K.J.H., Hall, J.R.S., Jennings, M.W., Harris, T.J.R., Marsh, K., Newbold, C.I., Tate, V.E. and Weatherall, D.J. (1988) A highly conserved amino-acid sequence in thrombospondin, properdin, and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335, 79-82.
3. Rogers, W.O., Malik, A., Mellouk, S., Nakamura, K., Rogers, M.D., Szarfman, A., Gordon, D.M., Nüssler, A.K., Aikawa, M. and Hoffman, S.L. (1992) Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc. Natl. Acad. Sci. USA 89, 9176-9180.
4. Clarke, L.E., Tomley, F.M., Wisher, M.H., Foulds, I.J. and Boursnell, M.E.G. (1990) Regions of an Eimeria tenella antigen contain sequences which are conserved in circumsporozoite proteins from Plasmodium spp. and which are related to the thrombospondin gene family. Mol. Biochem. Parasitol. 41, 269-280.
5. Goundis, D. and Reid, K.B.M. (1988) Properdin, the terminal complement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature 335, 82-85.
6. Holt, G.D., Krivan, H.C., Gasic, G.J. and Ginsburg, V. (1989) Antistasin, an inhibitor of coagulation and metastasis, binds to sulfatide (Gal(3-SO4)β 1-1 Cer) and has a sequence homology with other proteins that bind sulfated glycoconjugates. J. Biol. Chem. 264, 12138-12140.
7. Klar, A., Baldassare M. and Jessell, T.M. (1992) F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69, 95-110.
8. Leung-Hagesteijn, C., Spence, A.M., Stern, B.D., Zhou, Y., Su, M.-W., Hedgecock, E.M. and Culotti, J.G. (1992) UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299.
9. Prater, C.A., Plotkin, J., Jaye, D. and Frazier, W.A. (1991) The properdin-like type-I repeats of human thrombospondin contain a cell attachment site. J. Cell. Biol. 112, 1031-1040.
10. Cerami, C., Frevert, U., Sinnis, P., Takacs, B., Clavijo, P., Santos, M.J. and Nussenzweig, V. (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70, 1021-1033.
11. Cerami, C., Frevert, U., Sinnis, P., Takacs, B. and Nussenzweig, V. (1994) Rapid clearance of malaria circumsporozoite protein (CS) by hepatocytes, J. Exp. Med. 179, 695-701.
12. Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B. and Nussenzweig, V. (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J. Exp. Med. 177, 1287-1298,
13. Sinnis, P., Clavijo, P., Fenyö, D., Chait, B.T., Cerami, C. and Nussenzweig, V. (1994) Structural and functional properties of region-II plus of the malaria circumsporozoite protein. J. Exp. Med. 180, 297-306.
14. Frevert, U. (1994) Malaria sporozoite - hepatocyte interactions. Minireview. Exp. Parasitol. 79, 206-210.
15. Nardin, E.H., Nussenzweig, V., Nussenzweig, R.S., Collins, W.E., Harinasuta, K.T., Tapchaisri, P. and Chomcharn, Y. (1982) Circumsporozoite proteins of human malaria parasites Plasmodium falciparum and Plasmodium vivax. J. Exp. Med. 156, 20-30.
16. Yoshida, N., Potocnjak, P., Nussenzweig, V. and Nussenzweig, R.S. (1981) Biosynthesis of Pb44, the protective antigen of sporozoites of Plasmodium berghei. J. Exp. Med. 154, 1225-1236.
17. Tsuji, M., Mattei, D., Nussenzweig, R.S., Eichinger, D. and Zavala, F. (1994) Demonstration of a heat-shock protein 70 in the sporozoite stage of malaria parasites. Parasitol. Res. 80, 16-21.
18. David, G., Bai, X.M., Schueren, B., Cassiman, J.-J. and Berghe, H. (1992) Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol. 119, 961-975.
19. Bame, K.J. and Esko, J.D. (1989) Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264, 8059-8065.
20. Esko, J.D., Stewart, T.E., and Taylor, W.H. (1985) Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA 85, 3197-3201.
21. Hollingdale, M.R., McCullough, M. and Beaudoin, R.L. (1981) In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei from sporozoites. Science 213, 1021-1023.
22. Sinden, R.E., Suhrbier, A., Davies, C.S., Fleck, S.L., Hodivala, K. and Nicholas, J.C. (1990) The development and routine application of high-density exoerythrocyticstage culture of Plasmodium berghei. WHO Bull. 68 (Suppl.), 115-125.
23. Shakibaei, M. and Frevert, U. (1992) Cell surface interactions between Trypanosoma congolense and macrophages during phagocytosis in vitro. J. Protozool. 39, 224-235.
24. Rénia, L., Miltgen, F., Charoenvit, Y., Ponnudurai, T., Verhave, J.P., Collins, W.E. and Mazier, D. (1988) Malaria sporozoite penetration. A new approach by double staining. J. Immunol. Methods 112, 201-205.
25. Linker, A. and Hovingh, P. (1972) Heparinase and heparitinase from flavobacteria. Methods Enzymol. 28, 902-911.
26. Calvo-Calle, J.M., Moreno, A., Eling, W.M.C. and Nardin, E.H. (1994) In vitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp. Parasitol. 79, 362-373.
27. Hollingdale, M.R., Leland, P., Leef, J.L. and Beaudoin, R.L. (1983) The influence of cell type and culture medium on the in vitro cultivation of exoerythrocytic stages of Plasmodium berghei. J. Parasitol. 69, 346-352.
28. Sinden, R.E. and Smith, J. (1980) Culture of the liver stages (exoerythrocytic schizonts) of rodent malaria parasites from sporozoites in vitro. Trans. Roy. Soc. Trop. Med. Hyg. 74, 134-136.
29. Strome, C.P.A., De Santis, P.L. and Beaudoin, R.L. (1979) The cultivation of the exoerythrocytic stages of Plasmodium berghei from sporozoites. In Vitro 15, 531-536.
30. Wisse, E. (1970) An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J. Ultrastruct. Res. 31, 125-150.
31. Robson, K.J.H., Frevert, U., Reckmann, I., Cowan, G., Beier, J., Scragg, I.G., Takehara, K., Bishop, D.H.L., Pradel, G., Sinden, R., Saccheo, S., Müller, H.-M. and Crisanti, A. (1995) Thrombospondin related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and aggregate dependent binding to hepatocytes. EMBO J. 14, 3883-3894.
32. Pancake, S.J., Holt, G.D., Mellouk, S. and Hoffman, S.L. (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J. Cell Biol. 117, 1351-1357.
33. Esko, J.D. (1991) Genetic analysis of proteoglycan structure, function and metabolism. Curr. Opin. Cell Biol. 3, 805-816.
34. Butcher, B.A., Shome, K., Estes, L.W., Choay, J., Petitou, M., Sie, P. and Glew, R.H. (1990) Leishmania donovani: cell-surface heparin receptors of promastigotes are recruited from an internal pool after trypsinization. Exp. Parasitol. 71, 49-59.
35. Butcher, B.A., Sklar, L.A., Seamer, L.C. and Glew, R.H. (1992) Heparin enhances the interaction of infective Leishmania donovani promastigotes with mouse peritoneal macrophages, A fluorescence flow cytometric analysis. J. Immunol. 148, 2879-2886.
36. Love, D.C., Esko, J.D. and Mosser, D.M. (1993) A heparin-binding activity of Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J. Cell Biol. 123, 759-766.
37. Ortega-Barria, E. and Pereira, M.E.A. (1991) A novel T. cruzi heparin-binding protein promotes adhesion and spreading of fibroblasts, and penetration of trypomastigotes and engineered bacteria into non-phagocytic mammalian cells. Cell 67, 411-421.
38. Sibley, L.D. (1993) Interactions between Toxoplasma gondii and its mammalian host cells. Semin. Cell Biol. 4, 335-344.
39. Sim, B.K.L., Chitnis, C.E., Wasniowska, K., Hadley, T.J. and Miller, L.H. (1994) Receptor and ligand domains for Plasmodium falciparum malaria invasion of erythrocytes. Science 264, 1941-1944.
40. Friedman, M.J., Fukuda, M. and Laine, R.A. (1985) Evidence for a malarial parasite interaction site on the major transmembrane protein of the human erythrocyte. Science 228, 73-75.
41. - erythrocytes. Glycobiology 4, 903-908.
42. Hadley, T.J., Klotz, F.W. and Miller, L.H. (1986) Invasion of erythrocytes by malaria parasites: a cellular and molecular overview. Annu. Rev. Microbiol. 40, 451-477.
43. Dalton, J.P., Hudson, D., Adams, J.H. and Miller, L.H. (1991) Blocking of the receptor-mediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulfated polysaccharides and glycosaminoglycans. Eur. J. Biochem. 195, 789-794.