Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T16:11:11.221Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of the parasite-host cell interactions involved in Theileria parva sporozoite invasion of bovine lymphocytes

Published online by Cambridge University Press:  06 April 2009

M. K. Shaw
M. K. Shaw
Affiliation:
International Laboratory for Research on Animal Diseases, Nairobi, Kenya
Get access Rights & Permissions [Opens in a new window]

Summary

Sporozoite invasion of bovine lymphocytes by Theileria parva is a pH-dependent process that occurs without the need for de novo protein synthesis. The process was inhibited by RGD(S) peptides, fibronectin and, in the presence of serum, by antibodies reactive with fibronectin. Invasion was also blocked by a range of sulphated glycoconjugates, but treatment of lymphocytes with heparitinase did not inhibit entry. Enzymic modifications of the lymphocyte surface demonstrated that trypsin-insensitive glycoproteins containing O- and N-linked carbohydrates as well as phospholipase-sensitive molecules on the host cell surface were critical to sporozoite entry. Modification of the lymphocyte surface with NEM and DTT had only marginal effects on sporozoite binding but blocked parasite internalization. Invasion was also blocked by several antibodies which cross-reacted with sporozoite surface molecules. While only a few experimental conditions specifically blocked sporozoite binding, a wider range of reagents and treatments inhibited parasite entry. The reasons for this are discussed in terms of the nature of the zippering process that facilitates sporozoite internalization.

Keywords

Theileria parvasporozoite invasionlymphocytesparasite-host interactionsglycoproteins
Type
Research Article
Information
Parasitology , Volume 113 , Issue 3 , September 1996 , pp. 267 - 277
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ayad, S., Boot-Handford, R. P., Humphries, M. J., Kadler, K. E. & Shuttleworth, C. A. (1994). The Extracellular Matrix Facts Book. Academic Press Ltd, London.Google Scholar
Bergelson, J. M. & Finberg, R. W. (1993). Integrins as receptors for virus attachment and cell entry. Trends in Microbiology 1, 287–288.CrossRefGoogle ScholarPubMed
Brown, C. G. D. (1987). Theileriidae. In: In vitro Methods of Parasite Cultivation, (ed. Taylor, A. E. R. & Baker, J. R.), pp. 230–253. Academic Press, London.Google Scholar
Cerami, C., Kwakye-Berko, F. & Nussenzweig, V. (1992). Binding of malarial circumsporozoite protein to sulfatides (Gal{3-SO4}B1-Cer) and cholesterol-3-sulfate and its dependence on disulfide bond formation between cysteines in region II. Molecular and Biochemical Parasitology 54, 1–12.CrossRefGoogle ScholarPubMed
Dalton, J. P., Hudson, D., Adams, J. H. & Miller, L. H. (1991). Blocking of the receptor-mediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulphated polysaccharides and glycosaminoglycans. European Journal of Biochemistry 195, 789–794.CrossRefGoogle ScholarPubMed
Damon, D. H., D'Amore, P. A. & Wagner, J. A. (1988). Sulfated glycosaminoglycans modify growth factorinduced neurite outgrowth in PC12 cells. Journal of Cellular Physiology 135, 293–300.CrossRefGoogle ScholarPubMed
Damon, D. H., Lobb, R. R., D'Amore, P. A. & Wagner, J. A. (1989). Heparin potentiates the action of acidic fibroblast growth factor by prolonging its biological half-life. Journal of Cellular Physiology 138, 221–226.Google Scholar
Dobbelaere, D. A. E., Spooner, P. R., Barry, W. C. & Irvin, A. D. (1984). Monoclonal antibody neutralizes the sporozoite stage of different Theileria parva stocks. Parasite Immunology 6, 361–370.CrossRefGoogle ScholarPubMed
Elbein, A. D. (1987). Inhibitors of the biosynthesis and processing of N-linked oligosaccharides. Annual Review of Biochemistry 56, 497–534.CrossRefGoogle Scholar
Fawcett, D. W., Doxsey, S., Stagg, D. A. & Young, A. S. (1982). The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Electron microscopic observations. European Journal of Cell Biology 27, 10–21.Google Scholar
Finlay, B. B. (1990). Cell adhesion and invasion mechanisms in microbial pathogenesis. Current Opinion in Cell Biology 2, 815–820.Google Scholar
Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B. & Nussenzweig, V. (1993). Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. Journal of Experimental Medicine 177, 1287–1298.Google Scholar
Furtado, G. C., Slowik, M., Kleinman, H. K. & Joiner, K. A. (1992). Laminin enhances binding of Toxoplasma gondii tachyzoites to J774 murine macrophage cells. Infection and Immunity 60, 2337–2342.Google Scholar
Hall, B. F. & Joiner, K. A. (1991). Strategies of obligate intracellular parasites for invading host defences. Parasitology Today (Immunoparasitology Today) 7, A22–A27.CrossRefGoogle Scholar
Hall, R., Hunt, P. D., Carrington, M., Simmons, D., Williamson, S., Mecham, R. P. & Tait, A. (1992). Mimicry of elastin repetitive motifs by Theileria annulata sporozoite surface antigen. Molecular and Biochemical Parasitology 53, 105–112.Google Scholar
Herrera, E. M., Ming, M., Ortega-Barria, E. & Pereira, M. E. A. (1994). Mediation of Trypanosoma cruzi invasion by heparan sulfate receptors on host cells and penetrin counter-receptors on the trypanosomes. Molecular and Biochemical Parasitology 65, 73–83.CrossRefGoogle ScholarPubMed
Hynes, R. O. & Yamada, K. M. (1982). Fibronectins: multifunctional molecular glycoproteins. Journal of Cell Biology 95, 369–377.Google Scholar
Isberg, R. R. & Leong, J. M. (1990). Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60, 861–871.CrossRefGoogle Scholar
Katzer, F., Carrington, M., Knight, P., Williamson, S., Tait, A., Morrison, W. I. & Hall, R. (1994). Polymorphism of SPAG-1, a candidate antigen for inclusion in a sub-unit vaccine against Theileria annulata. Molecular and Biochemical Parasitology 67, 1–10.Google Scholar
Kuhn, K. & Eble, J. (1994). The structural basis of integrin-ligand interactions. Trends in Cell Biology 4, 256–261.CrossRefGoogle Scholar
Kulane, A., Ekre, H. P., Perlmann, P., Rombo, L., Wahlgren, M. & Wahlin, B. (1992). Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. American Journal of Tropical Medicine and Hygiene 46, 589–594.Google Scholar
Lalor, P. A., Morrison, W. I., Goddeeris, B. M., Jack, R. J. & Black, S. J. (1986). Monoclonal antibodies identify phenotypically and functionally distinct cell types in the bovine lymphoid system. Veterinary Immunology and Immunopathology 13, 121–140.Google Scholar
Leong, J. M., Morrissey, P. E., Marra, A. & Isberg, R. R. (1995). An aspartate residue of the Yersinia pseudotuberculosis invasin protein that is critical for integrin binding. EMBO Journal 14, 422–431.Google Scholar
Love, D. C., Esko, J. D. & Mosser, D. M. (1993). A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. Journal of Cell Biology 123, 759–766.Google Scholar
Muller, H-M., Reckmann, I., Hollingdale, M. R., Bujard, H., Robson, K. J. H. & Crisanti, A. (1993). Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glyconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO Journal 12, 2881–2889.CrossRefGoogle Scholar
Duller, S. N., Thomas, K. A., Salvo, J. D. & Levine, E. M. (1989). Stabilization by heparin of fibroblastic growth factor mitogenicity for human endothelial cells in vitro. Journal of Cellular Physiology 140, 439–448.Google Scholar
Musoke, A. J., Nantulya, V. M., Rurangirwa, F. R. & Buscher, G. (1984). Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52, 231–238.Google Scholar
Naessens, J. & Williams, D. J. L. (1992). Characterization and measurement of CD5 + B cells in normal and Trypanosoma congolense-infected cattle. European Journal of Immunology 22, 1713–1718.Google Scholar
Nene, V., Iams, K. P., Gobright, E. & Musoke, A. J. (1992). Characterisation of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51, 17–28.Google Scholar
Neyts, J., Snoeck, R., Schols, D., Balzarini, J., Esko, J. D., Van Schepdael, A. & De Clercq, E. (1992). Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparin sulfate. Virology 189, 48–58.Google Scholar
Noisin, E. L. & Villalta, F. (1989). Fibronectin increases Trypanosoma cruzi amastigote binding to and uptake by murine macrophages and human monocytes. Infection and Immunity 57, 1030–1034.CrossRefGoogle ScholarPubMed
Ortega-Barria, E. & Pereira, M. E. A. (1991). A novel T. cruzi heparin binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411–421.CrossRefGoogle ScholarPubMed
Ouaissi, M. A. (1988). Role of the RGD sequence in parasite adhesion to host cells. Parasitology Today 4, 169–173.Google Scholar
Ouaissi, M. A., Afchain, D., Capron, A. & Grimaud, J. A. (1984). Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature, London 308, 380–382.CrossRefGoogle ScholarPubMed
Pancake, S. J., Holt, G. D., Mellouk, S. & Hoffman, S. L. (1992). Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. Journal of Cell Biology 117, 1351–1357.Google Scholar
Patti, J. M., Allen, B. L., McGavin, M. J. & Hook, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annual Review of Microbiology 48, 585–617.Google Scholar
Peyrol, S., Ouaissi, M. A., Capron, A. & Grimaud, J. A. (1987). Trypanosoma cruzi: ultrastructural visualization of fibronectin bound to culture cells. Experimental Parasitology 63, 112–114.Google Scholar
Rosengart, T. K., Johnson, W. V., Friesel, R., Clark, R. & Maciag, T. (1988). Heparin protects heparin-binding growth factor-1 from proteolytic inactivation in vitro. Biochemical Biophysical Research Communications 152, 432–440.CrossRefGoogle ScholarPubMed
Ruoslahti, E. & Pierschbacher, M. D. (1986). Arg-Gly-Asp: a versatile cell recognition signal. Cell 44, 517–518.Google Scholar
Shaw, M. K., Tilney, L. G. & Musoke, A. J. (1991). The entry of Theileria parva sporzoites into bovine lymphocytes: evidence for MHC class I involvement. Journal of Cell Biology 113, 87–101.CrossRefGoogle Scholar
Shaw, M. K., Tilney, L. G., Musoke, A. J. & Teale, A. J. (1995). MHC class I molecules are an essential cell surface component involved in Theileria parva sporozoite binding to bovine lymphocytes. Journal of Cell Science 108, 1587–1596.Google Scholar
Shieh, M-T., Wudunn, D., Montgomery, R. I., Esko, J. D. & Spear, P. G. (1992). Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. Journal of Cell Biology 116, 1273–1281.Google Scholar
Sommer, A. & Rifkin, D. B. (1989). Interaction of heparin with human basic growth factor: protection of the angiogenic protein from proteolytic degradation by a glycosaminoglycan. Journal of Cellular Physiology 138, 215–220.Google Scholar
Ward, G. E., Chitnis, C. E. & Miller, L. H. (1994). The invasion of erythrocytes by malarial merozoites. Bailliere's Clinical Infectious Diseases 1, 155–190.Google Scholar
Webster, P., Dobbelaere, D. A. E. & Fawcett, D. A. (1985). The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Immunoelectron microscopic observations. European Journal of Cell Biology 36, 157–162.Google Scholar
Wyler, D. J., Sypek, J. P. & McDonald, J. A. (1985). In vitro parasite-monocyte interactions in human leishmaniasis: possible role of fibronectin in parasite attachment. Infection and Immunity 49, 305–311.Google Scholar
Zabrentzky, V. S., Kohn, E. C. & Roberts, D. D. (1990). Suramin inhibits laminin- and thrombospondin mediated melanoma cell adhesion and migration and binding of these adhesive proteins to sulphatide. Cancer Research 50, 5937–5942.Google Scholar
Zhang, J. P. & Stephens, R. S. (1992). Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell 69, 861–869.CrossRefGoogle ScholarPubMed