Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-13T03:10:19.655Z Has data issue: false hasContentIssue false
  • English
  • Français

Adhesion and invasion of bovine endothelial cells by Neospora caninum

Published online by Cambridge University Press:  26 March 2010

A. Hemphill ,
B. Gottstein  and
H. Kaufmann
A. Hemphill
Affiliation:
Institute for Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012 Berne, Switzerland
Get access Rights & Permissions [Opens in a new window]

Summary

Neospora caninum is a recently identified coccidian parasite which was, until 1988, misdiagnosed as Toxoplasma gondii. It causes paralysis and death in dogs and neonatal mortality and abortion in cattle, sheep, goats and horses. The life-cycle of Neospora has not yet been elucidated. The only two stages identified so far are tissue cysts and intracellularly dividing tachyzoites. Very little is known about the biology of this species. We have set up a fluorescence-based adhesion/invasion assay in order to investigate the interaction of N. caninum tachyzoites with bovine aorta endothelial (BAE) cells in vitro. Treatment of both host cells and parasites with metabolic inhibitors determined the metabolic requirements for adhesion and invasion. Chemical and enzymatic modifications of parasite and endothelial cell surfaces were used in order to obtain information on the nature of cell surface components responsible for the interaction between parasite and host. Electron microscopical investigations defined the ultrastructural characteristics of the adhesion and invasion process, and provided information on the intracellular development of the parasites.

Keywords

Apicomplexaadhesioninvasioncell adhesion moleculescytoskeleton
Type
Research Article
Information
Parasitology , Volume 112 , Issue 2 , February 1996 , pp. 183 - 197
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

Araujio-Jorge, T. C. & De Souza, W. (1984). Interaction of Trypanosoma cruzi with macrophages: effect of previous incubation of the parasites or host cells with lectins. Zeitschrift fur Parasitenkunde 72, 153–71.CrossRefGoogle Scholar
Augustine, P. C. (1989). The Eimeria: cellular invasion and host-cell parasite interactions. In Coccidia and Intestinal Coccidiomorphs. Collogues de INTRA 49, (ed. Yvore, P.) pp. 205–215. Tours, France.Google Scholar
Bannister, L. H. & Dluzewski, A. R. (1990). The ultrastructure of red cell invasion in malaria infections: a review. Blood Cell 16, 257–92.Google ScholarPubMed
Barr, B. C., Rowe, J. D., Sverlov, K. W., BON Durant, R. H., Ardans, A. A., Oliver, M. N. & Conrad, P. A. (1994). Experimental reproduction of bovine fetal Neospora infection and death with a Neospora isolate. Journal of Veterinary Diagnostic Investigations 6, 207–15.CrossRefGoogle ScholarPubMed
Bonhomme, A., Pingret, L. & Pinon, J. M. (1992). Review: Toxoplasma gondii cellular invasion. Parassitologia 34, 31–43.Google ScholarPubMed
Bonilha, V. L., Do Carmo Ciavaglia, M., DE Souza, W. & E Silva Filho, F. C. (1995). The involvement of terminal carbohydrates of the mammalian cell surface in the cytoadhesion of trichomonads. Parasitology Research 81, 121–6.CrossRefGoogle ScholarPubMed
Chobotar, B., Danforth, H. D. & Entzeroth, R. (1993). Ultrastructural observations of host cell invasion by sporozoites of Eimeria papillata in vivo. Parasitology Research 79, 15–23.CrossRefGoogle ScholarPubMed
Cooper, J. A. (1987). Effects of cytochalasin and phalloidin on actin. Journal of Cell Biology 105, 1473–8.CrossRefGoogle ScholarPubMed
Cross, C. A. M. & Tackle, C. B. (1993). The surface transsialidase family of Trypanosoma cruzi. Annual Reviews in Microbiology 47, 385–411.CrossRefGoogle ScholarPubMed
De Carvalho, L., Van, C. Y. I. & de Souza, W. (1993). Effect of various digestive enzymes on the interaction of Toxoplasma gondii with macrophages. Parasitology Research 79, 114–18.CrossRefGoogle ScholarPubMed
Donelson, J. E. & Fulton, A. B. (1992). Skirmishes on the border. Nature (London) 356, 480–1.CrossRefGoogle ScholarPubMed
Dubey, J. P., Carpenter, J. L., Speer, A., Topper, M. J. & Uggla, A. (1988). Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medicine Association 198, 1269–85Google Scholar
Dubey, J. P. & Lindsay, D. S. (1993). Neosporosis. Parasitology Today 9, 452–8CrossRefGoogle ScholarPubMed
Dvorak, J. A. & Crane, M. S. J. (1981). Vertebrate cell cycle modulates infection by protozoan parasites. Science 214, 1034–6.CrossRefGoogle ScholarPubMed
Ellis, J., Luton, K., Baverstock, P. R., Brindley, P. J., Nimmo, K. A. & Johnson, A. M. (1994). The phylogeny of Neospora caninum. Molecular and Biochemical Parasitology 64, 303–11.CrossRefGoogle ScholarPubMed
Endo, T., Yagita, K., Yasuda, T. & Nakamura, T. (1988). Demonstration and localization of actin in Toxoplasma gondii. Parasitology Research 75, 102–6.CrossRefGoogle ScholarPubMed
Fawcett, D., Musoke, A. & Voigt, W. (1984). Interaction of sporozoites of Theileria parva with bovine lymphocytes in vitro. I. Early events after invasion. Tissue and Cell 16, 873–84.CrossRefGoogle ScholarPubMed
Geiger, B. (1989). Cytoskeleton associated cell-contacts. Current Opinion in Cell Biology 1, 103–9.CrossRefGoogle ScholarPubMed
Gray, M. A., Ross, C. A., Taylor, M. A., Tetley, L. & Luckins, A. C. (1985). In vitro cultivation of Trypanosoma congolense: the production of infective forms of metacyclic trypanosomes cultured on bovine aorta endothelial cell monolayers. Acta Tropica 42, 99–110.Google ScholarPubMed
Griffiths, C. (1993). Fixation for fine structure preservation and immunocytochemistry. In Fine Structure Immunocytochemisty (ed. Griffiths, G.), pp. 26–89. Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Hemphill, A., Affolter, M. & Seebeck, T. (1992). A novel microtubule binding motif identified in a high molecular weight microtubule-associated protein from Trypanosoma brucei. Journal of Cell Biology 117, 95–103.CrossRefGoogle Scholar
Hemphill, A., Frame, I. & Ross, C. A. (1994). The interaction of Trypanosoma congolense with endothelial cells. Parasitology 109, 631–1.Google ScholarPubMed
Hemphill, A. & Ross, C. A. (1995). Flagellum-mediated adhesion of Trypanosoma congolense to bovine aorta endothelial cells. Parasitology Research 81, 412–20.CrossRefGoogle ScholarPubMed
Henriquez, D. R., Piras, R. & Piras, M. M. (1981). The effect of surface membrane modification of fibroblastic cells on the entry process of Trypanosoma cruzi trypomastigotes. Molecular and Biochemical Parasitology 2, 359–66.CrossRefGoogle ScholarPubMed
Hoffman, S. (1992). Assays of cell adhesion. In Cell-Cell Interactions. A Practical Approach, (ed. Rickwood, D. & Hames, B. D. ), pp 1-29. London: IRL press.Google Scholar
Holder, A. A. (1994). Proteins on the surface of the malaria parasite and cell invasion. Parasitology 108, S5-S18.CrossRefGoogle ScholarPubMed
Joiner, K. A. & Dubremetz, J. F. (1993). Toxoplasma gondii: a protozoan for the nineties. Infection and Immunity 61, 1169–72.CrossRefGoogle ScholarPubMed
Rammer, G. M., Boehm, C. A., Rudolph, S. A. & Schultz, L. A. (1988). Mobility of the human T lymphocyte surface molecules CD3, CD4, CDS: regulation by a cAMP-dependent pathway. Proceedings of the National Academy of Sciences, USA 85, 792–6.Google Scholar
Karlsson, K. A., Milh, M. A., Anggstroem, J., Bergstroem, J., Dezfoolian, H., Lanne, B., Leonardson, I. & Teneberg, S. (1992). Membrane proximity and internal binding in the microbial recognition of host cell glycolipids: A conceptual discussion. In Molecular Recognition in Host-Parasite Interactions. FEMS Symposium No. 61. (ed. Korhonen, T. K., Hovi, T. & Maekelae, P. H.), pp. 115–132. New York: Plenum Press.Google Scholar
Rasper, L. H. & Mined, J. R. (1994). Attachment and invasion of host cells by Toxoplasma gondii. Parasitology Today 10, 184–8.Google Scholar
Lander, A. D. (1993). Proteoglycans. In Guidebook to Extracellular Matrix and Adhesion Proteins, (ed. Kreis, T. & Vale, R.), pp. 12–16. Oxford: Oxford University Press.Google Scholar
Lindsay, P. S. & Dubey, J. P. (1989). In vitro development of Neospora caninum (Protozoa: Apicomplexa) from dogs. Journal of Parasitology 75, 163–5.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Blagburn, B. L. & Dubey, J. P. (1990). Infection of mice with Neospora caninum (Protozoa: Apicomplexa) does not protect against challenge with Toxoplasma gondii. Infection and Immunity 58, 2699–700.CrossRefGoogle Scholar
Lindsay, D. S., Speer, C. A., Toivio-Kinnucan, M. A., Dubey, J. P. & Blagburn, B. L. (1993). Use of infected cultured cells to compare ultrastructural features of Neospora caninum from dogs and Toxoplasma gondii. American Journal of Veterinary Research 54, 103–6.CrossRefGoogle ScholarPubMed
Lycke, E., Lund, E. & Strannegard, O. (1965). Enhancement by lysozyme and hyaluronidase of the penetration by Toxoplasma gondii into cultured host cells. British Journal of Experimental Pathology 46, 189–99.Google ScholarPubMed
Mineo, J. R. & Kasper, L. H. (1994). Attachment of Toxoplasma gondii to host cells involves major surface protein SAG-1 (P30). Experimental Parasitology 79, 11–20.CrossRefGoogle Scholar
Norrby, R. (1971). Immunological study on the host cell penetration factor of Toxoplasma gondii. Infection and Immunity 3, 278–86.CrossRefGoogle Scholar
Oebrink, B. (1993). Cell adhesion and cell-cell contact proteins. In Guidebook to the Extracellular Matrix and Adhesion Proteins (ed. Kreis, T. & Vale, R.), pp. 109–114. Oxford: Oxford University Press.Google Scholar
Ortega-Barria, E. & Pereira, M. E. A. (1992). A novel T. cruzi Theparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411–21.CrossRefGoogle Scholar
Pasvol, G., Carlsson, J. & Clough, B. (1992). Recognition of molecules on red cells for malarial parasites. In: Molecular Recognition in Host-Parasite Interactions. FEMS Symposium No. 61, (ed. Korhonen, T. K., Hovi, T. & Maekelae, P. H. ), pp. 173–200. New York: Plenum Press.CrossRefGoogle Scholar
Pegado, M. G. F. & de Souza, W. (1994). Role of surface components in the process of interaction of Giardia duodenialis with epithelial cells in vitro. Parasitology Research 80, 320–6.CrossRefGoogle ScholarPubMed
Ryning, F. W. & Remington, J. S. (1978). Effect of cytochalasin D on Toxoplasma gondii cell entry. Infection and Immunity 20, 739–43.CrossRefGoogle ScholarPubMed
Schenkman, S. & Eichinger, D. (1993). Trypanosoma cruzi trans-sialidase and cell invasion. Parasitology Today 9, 218–22.CrossRefGoogle ScholarPubMed
Schenkman, S., Kurasaki, T., Ravetch, J. V. & Nussenzweig, V. (1992). Evidence for the participation of the ssp3 antigen in the invasion process of non-phagocytic mammalian cells by Trypanosoma cruzi. Journal of Experimental Medicine 175, 567–75.CrossRefGoogle Scholar
Schenkman, S., Robbins, E. S. & Nussenzweig, V. (1991a). Attachment of Trypanosoma cruzi requires parasite energy and invasion can be independent of the target cell cytoskeleton. Infection and Immunity 59, 645–54.CrossRefGoogle ScholarPubMed
Schenkman, S., Diaz, C. & Nussenzweig, V. (1991b). Attachment of Trypanosoma cruzi trypomastigotes to receptors at restricted cell surface domains. Experimental Parasitology 72, 76–86.CrossRefGoogle ScholarPubMed
Schwarzman, J. & Pfefferkorn, E. R. (1983). Immunofluorescent localization of myosin at the anterior pole of coccidian Toxoplasma gondii. Journal of Protozoology 30, 657–61.CrossRefGoogle Scholar
Seefeldt, S. L., Kirkbride, C. A. & Dubey, J. P. (1989). Comparison of enzyme-linked immunosorbent assay, direct fluorescent antibody test, and direct agglutination test for detecting Toxoplasma gondii antibodies in naturally aborted ovine fetuses. Journal of Veterinary Diagnostical Investigations 1, 124–7.CrossRefGoogle ScholarPubMed
Shaw, M. K., Tilney, L. G. & Musoke, A. J. (1991). The entry of Theileria parva sporozoites into bovine lymphocytes: evidence for MHC class I involvement. Journal of Cell Biology 113, 87–101.CrossRefGoogle ScholarPubMed
Sibley, D. L. (1995). Invasion of vertebrate cells by Toxoplasma gondii. Trends in Cell Biology 5, 129–33.CrossRefGoogle ScholarPubMed
Silva, S. R. L., Meirelles, S. R. L. & de Souza, W. (1982). Mechanism of entry of Toxoplasma gondii into vertebrate cells. Journal of Submicroscopical Cytology 14, 471–82.Google ScholarPubMed
Smith, M. & Croft, S. L. (1991). Embedding and thin section preparation. In Electron Microscopy in Biology. A Practical Approach, (ed. Rickwood, D. & Harris, B. D.), pp. 17–37. London: IRL Press.CrossRefGoogle Scholar
Tait, A. & Sacks, D. L. (1988). The cell biology of parasite invasion and survival. Parasitology Today 8, 228–34.CrossRefGoogle Scholar
Trees, A. J., Tennant, B. J. & Kelly, D. F. (1991). Paresis in dogs and Neospora caninum. Veterinary Record 129, 456.CrossRefGoogle ScholarPubMed
Villata, F., Lima, M. F., Ruiz-Ruano, A. & Zhou, I. (1992). Attachment of Trypanosoma cruzi to host cells: a monoclonal antibody recognizing gp83 which is required for parasite attachment. Biochemical and Biophysical Research Communications 182, 6–13.CrossRefGoogle Scholar
Villata, F., Ruiz-Ruano, A., Valentine, A. A. & Lima, M. F. (1993). Purification of a 74 kDa glycoprotein from heart myoblasts that inhibits binding and entry of T. cruzi into heart cells. Molecular and Biochemical Parasitology 61, 217–30.CrossRefGoogle Scholar
Werk, R. (1985). How does Toxoplasma gondii enter host cells? Reviews of Infectious Diseases 7, 449–57.CrossRefGoogle ScholarPubMed
Wilson, M. E., Donelson, J. E., Pearson, R. D. & Ramamoorthy, R. (1992). Macrophage receptors and Leishmania. In: Molecular Recognition in Host-Parasite Interactions. FEMS Symposium No. 61, (ed. Korhonen, T. K., Hovi, T. & Maekelae, P. H. ), pp. 17–30. New York: Plenum Press.CrossRefGoogle Scholar
Woodward, M. P., Young, W. W. & Bloodgood, J. R. (1985). Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. Journal of Immunological Methods 78, 143–53.CrossRefGoogle ScholarPubMed
Zenian, A. & Kierszenbaum, F. (1983). Trypanosoma cruzi: Differences in cell surface interaction of circulating (trypomastigote) and culture (epimastigote) forms with macrophages. Journal of Parasitology 69, 660–5.CrossRefGoogle ScholarPubMed
Zenian, A. & Kierszenbaum, F. (1983). Trypanosoma cruzi: Differences in cell surface interaction of circulating (trypomastigote) and culture (epimastigote) forms with macrophages. Journal of Parasitology 69, 660–5.CrossRefGoogle ScholarPubMed