Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T00:07:10.048Z Has data issue: false hasContentIssue false
  • English
  • Français

Interrelations between the Parasitophorous Vacuole of Toxoplasma gondii and Host Cell Organelles

Published online by Cambridge University Press:  08 March 2005

Rodrigo Cardoso Magno ,
Lorian Cobra Straker ,
Wanderley de Souza  and
Marcia Attias
Rodrigo Cardoso Magno
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, CEP 21949-900—Rio de Janeiro—RJ, Brazil
Lorian Cobra Straker
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, CEP 21949-900—Rio de Janeiro—RJ, Brazil
Wanderley de Souza
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, CEP 21949-900—Rio de Janeiro—RJ, Brazil
Marcia Attias
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, CEP 21949-900—Rio de Janeiro—RJ, Brazil
Get access

Abstract

Toxoplasma gondii, the causative agent of toxoplasmosis, is capable of actively penetrating and multiplying in any nucleated cell of warm-blooded animals. Its survival strategies include escape from fusion of the parasitophorous vacuole with host cell lysosomes and rearrangement of host cell organelles in relation to the parasitophorous vacuole. In this article we report the rearrangement of host cell organelles and elements of the cytoskeleton of LLCMK2 cells, a lineage derived from green monkey kidney epithelial cells, in response to infection by T. gondii tachyzoites. Transmission electron microscopy made on flat embedded monolayers cut horizontally to the apical side of the cells or field emission scanning electron microscopy of monolayers scraped with scotch tape before sputtering showed that association of mitochondria to the vacuole is much less frequent than previously described. On the other hand, all parasitophorous vacuoles were surrounded by elements of the endoplasmic reticulum. These data were complemented by observations by laser scanning microscopy using fluorescent probes from mitochondria and endoplasmic reticulum and reinforced by three-dimensional reconstruction from serial sections observed by transmission electron microscopy and labeling of mitochondria and endoplasmic reticulum by fluorescent probes.

Keywords

LLCMK2mitochondriaendoplasmic reticulum (ER)
Type
BIOLOGICAL APPLICATIONS
Information
Microscopy and Microanalysis , Volume 11 , Issue 2 , April 2005 , pp. 166 - 174
Copyright
© 2005 Microscopy Society of America

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

Attias, M., Vommaro, R.C., & de Souza, W. (1996). Computer aided three-dimensional reconstruction of the free-living protozoan Bodo sp. (Kinetoplastida: Bodonidae). Cell Struct Funct 21, 297–306.Google Scholar
Coppens, I. & Joiner, K.A. (2003). Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 14, 3804–3820.Google Scholar
de Souza, W. (1972). Mise en evidence et structure du systeme microtubulaire de Toxoplasma gondii. [Demonstration and structure of the microtubular system in Toxoplasma gondii]. C R Acad Sci Hebd Seances Acad Sci D 275, 2899–2901.Google Scholar
de Souza, W. (1974). Fine structure of the conoid of Toxoplasma gondii. Rev Inst Med Trop Sao Paulo 16, 32–38.Google Scholar
Dubey, J.P., Lindsay, D.S., & Speer, C.A. (1998). Structures of Toxoplasma gondii: Tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 11, 267–299.Google Scholar
Dubremetz, J.F. (1998). Host cell invasion by Toxoplasma gondii. Trends Microbiol 6, 27–30.Google Scholar
Dubremetz, J.F. & Schwartzman, J.D. (1993). Subcellular organelles of Toxoplasma gondii and host cell invasion. Res Immunol 144, 31–33.Google Scholar
Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P.H., Steele-Mortimer, O., Paiement, J., Bergeron, J.J., & Desjardins, M. (2002). Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119–131.Google Scholar
Hessler, D., Young, S.J., Carragher, B.O., Martone, M.E., Lamont, S., Whittaker, M., Milligan, R.A., Masliah, E., Hinshaw, J.E., & Ellisman, M.H. (1992). Programs for visualization in three-dimensional microscopy. Neuroimage 1, 55–67.Google Scholar
Joiner, K.A., Fuhrman, S.A., Miettinen, H.M., Kasper, L.H., & Mellman, I. (1990). Toxoplasma gondii: Fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249, 641–646.Google Scholar
Joiner, K.A. & Roos, D.S. (2002). Secretory traffic in the eukaryotic parasite Toxoplasma gondii: Less is more. J Cell Biol 157, 557–563.Google Scholar
Jones, T.C. & Hirsch, J.G. (1972). The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J Exp Med 136, 1173–1194.Google Scholar
Jones, T.C., Yeh, S., & Hirsch, J.G. (1972). The interaction between Toxoplasma gondii and mammalian cells. I. Mechanism of entry and intracellular fate of the parasite. J Exp Med 136, 1157–1172.Google Scholar
Kurz, B., Bockeler, W., & Buse, E. (1998). In vitro-model for Toxoplasma gondii invasion into neuroepithelial cells. Anat Anz 180, 299–305.Google Scholar
Lee, C. & Chen, L.B. (1988). Dynamic behavior of endoplasmic reticulum in living cells. Cell 54, 37–46.Google Scholar
Lindsay, D.S., Mitschler, R.R., Toivio-Kinnucan, M.A., Upton, S.J., Dubey, J.P., & Blagburn, B.L. (1993). Association of host cell mitochondria with developing Toxoplasma gondii tissue cysts. Am J Vet Res 54, 1663–1667.Google Scholar
Melo, E.J., de Carvalho, T.U., & de Souza, W. (1992). Penetration of Toxoplasma gondii into host cells induces changes in the distribution of the mitochondria and the endoplasmic reticulum. Cell Struct Funct 17, 311–317.Google Scholar
Melo, E.J. & de Souza, W. (1997). Relationship between the host cell endoplasmic reticulum and the parasitophorous vacuole containing Toxoplasma gondii. Cell Struct Funct 22, 317–323.Google Scholar
Mercier, C., Dubremetz, J.F., Rauscher, B., Lecordier, L., Sibley, L.D., & Cesbron-Delauw, M.F. (2002). Biogenesis of nanotubular network in Toxoplasma parasitophorous vacuole induced by parasite proteins. Mol Biol Cell 13, 2397–2409.Google Scholar
Mordue, D.G., Hakansson, S., Niesman, I., & Sibley, L.D. (1999). Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp Parasitol 92, 87–99.Google Scholar
Nakaar, V., Ngo, H.M., Aaronson, E.P., Coppens, I., Stedman, T.T., & Joiner, K.A. (2003). Pleiotropic effect due to targeted depletion of secretory rhoptry protein ROP2 in Toxoplasma gondii. J Cell Sci 116, 2311–2320.Google Scholar
Pacheco-Soares, C. & de Souza, W. (1998). Redistribution of parasite and host cell membrane components during Toxoplasma gondii invasion. Cell Struct Funct 23, 159–168.Google Scholar
Poot, M., Zhang, Y.Z., Kramer, J.A., Wells, K.S., Jones, L.J., Hanzel, D.K., Lugade, A.G., Singer, V.L., & Haugland, R.P. (1996). Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 44, 1363–1372.Google Scholar
Saliba, K.J. & Kirk, K. (2001). Nutrient acquisition by intracellular apicomplexan parasites: Staying in for dinner. Int J Parasitol 31, 1321–1330.Google Scholar
Schwab, J.C., Beckers, C.J., & Joiner, K.A. (1994). The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci USA 91, 509–513.Google Scholar
Schwartzman, J.D. & Pfefferkorn, E.R. (1982). Toxoplasma gondii: Purine synthesis and salvage in mutant host cells and parasites. Exp Parasitol 53, 77–86.Google Scholar
Sibley, L.D., Niesman, I.R., Parmley, S.F., & Cesbron-Delauw, M.F. (1995). Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci 108, 1669–1677.Google Scholar
Sibley, L.D., Weidner, E., & Krahenbuhl, J.L. (1985). Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 315, 416–419.Google Scholar
Sinai, A.P. & Joiner, K.A. (1997). Safe haven: The cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 51, 415–462.Google Scholar
Sinai, A.P. & Joiner, K.A. (2001). The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 154, 95–108.Google Scholar
Sinai, A.P., Webster, P., & Joiner, K.A. (1997). Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: A high affinity interaction. J Cell Sci 110, 2117–2128.Google Scholar
Suss-Toby, E., Zimmerberg, J., & Ward, G.E. (1996). Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 93, 8413–8418.Google Scholar
Vivier, E. & Petitprez, A. (1972). Données ultrastructurales complémentaires, morphologiques et cytochimiques, sur Toxoplasma gondii. Protistologica T VIII, 199–221.Google Scholar
Young, S.J., Royer, S.M., Groves, P.M., & Kinnamon, J.C. (1987). Three-dimensional reconstruction from serial micrographs using an IBM PC. J Electron Microsc Techn 6, 207–215.Google Scholar