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Besnoitia besnoiti and Toxoplasma gondii: two apicomplexan strategies to manipulate the host cell centrosome and Golgi apparatus

Published online by Cambridge University Press:  03 June 2014

RITA CARDOSO
Affiliation:
Instituto de Investigação Científica Tropical, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, Av. Universidade Técnica, 1300-447 Lisboa, Portugal Centro de Investigação Interdisciplinar em Sanidade Animal, FMV, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal Instituto Gulbenkian de Ciência, 2781-901 Oeiras, Portugal
SOFIA NOLASCO
Affiliation:
Centro de Investigação Interdisciplinar em Sanidade Animal, FMV, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal Instituto Gulbenkian de Ciência, 2781-901 Oeiras, Portugal Escola Superior de Tecnologia da Saúde de Lisboa, 1990-096 Lisboa, Portugal
JOÃO GONÇALVES
Affiliation:
Instituto Gulbenkian de Ciência, 2781-901 Oeiras, Portugal Centro de Química e Bioquímica, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
HELDER C. CORTES
Affiliation:
Laboratório de Parasitologia Victor Caeiro, ICAAM – Instituto de Ciências Agrárias e Ambientais Mediterrânicas – Universidade de Évora – Núcleo da Mitra, Ap. 94, 7002-554 Évora, Portugal
ALEXANDRE LEITÃO*
Affiliation:
Instituto de Investigação Científica Tropical, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, Av. Universidade Técnica, 1300-447 Lisboa, Portugal Centro de Investigação Interdisciplinar em Sanidade Animal, FMV, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal
HELENA SOARES*
Affiliation:
Instituto Gulbenkian de Ciência, 2781-901 Oeiras, Portugal Escola Superior de Tecnologia da Saúde de Lisboa, 1990-096 Lisboa, Portugal Centro de Química e Bioquímica, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
*
*Corresponding author: IICT, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, Av. Universidade Técnica, 1300-447 Lisboa, Portugal. E-mail: alexandre@fmv.ulisboa.pt
*Corresponding author: Centro de Química e Bioquímica, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal. E-mail: mhsoares@fc.ul.pt

Summary

Besnoitia besnoiti and Toxoplasma gondii are two closely related parasites that interact with the host cell microtubule cytoskeleton during host cell invasion. Here we studied the relationship between the ability of these parasites to invade and to recruit the host cell centrosome and the Golgi apparatus. We observed that T. gondii recruits the host cell centrosome towards the parasitophorous vacuole (PV), whereas B. besnoiti does not. Notably, both parasites recruit the host Golgi apparatus to the PV but its organization is affected in different ways. We also investigated the impact of depleting and over-expressing the host centrosomal protein TBCCD1, involved in centrosome positioning and Golgi apparatus integrity, on the ability of these parasites to invade and replicate. Toxoplasma gondii replication rate decreases in cells over-expressing TBCCD1 but not in TBCCD1-depleted cells; while for B. besnoiti no differences were found. However, B. besnoiti promotes a reorganization of the Golgi ribbon previously fragmented by TBCCD1 depletion. These results suggest that successful establishment of PVs in the host cell requires modulation of the Golgi apparatus which probably involves modifications in microtubule cytoskeleton organization and dynamics. These differences in how T. gondii and B. besnoiti interact with their host cells may indicate different evolutionary paths.

Type
Special Issue Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Bornens, M. (2008). Organelle positioning and cell polarity. Nature Reviews Molecular Cell Biology 9, 874886. doi: 10.1038/nrm2524.CrossRefGoogle ScholarPubMed
Bornens, M. (2012). The centrosome in cells and organisms. Science 335, 422426. doi: 10.1126/science.1209037.Google Scholar
Coppens, I., Dunn, J. D., Romano, J. D., Pypaert, M., Zhang, H., Boothroyd, J. C. and Joiner, K. A. (2006). Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125, 261274. doi: 10.1016/j.cell.2006.01.056.Google Scholar
Cortes, H., Reis, Y., Waap, H., Vidal, R., Soares, H., Marques, I., Pereira da Fonseca, I., Fazendeiro, I., Ferreira, M. L., Caeiro, V., Shkap, V., Hemphill, A. and Leitão, A. (2006). Isolation of Besnoitia besnoiti from infected cattle in Portugal. Veterinary Parasitolology 141, 226233. doi: 10.1016/j.vetpar.2006.05.002.Google Scholar
De Anda, F. C., Pollarolo, G., Da Silva, J. S., Camoletto, P. G., Feiguin, F. and Dotti, C. G. (2005). Centrosome localization determines neuronal polarity. Nature 436, 704708. doi: 10.1038/nature03811.CrossRefGoogle ScholarPubMed
Dupin, I., Camand, E. and Etienne-Manneville, S. (2009). Classical cadherins control nucleus and centrosome position and cell polarity. Journal of Cell Biology 185, 779786. doi: 10.1083/jcb.200812034.Google Scholar
Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P. M., Andreyeva, N., Gleeson, P., Galjart, N., Maia, A. R., McLeod, I. X., Maiato, H., Khodjakov, A., Akhmanova, A. and Kaverina, I. (2007). Asymmetric CLASP-dependent nucleation of non centrosomal microtubules at the trans-Golgi network. Developmental Cell 12, 917930. doi: 10.1016/j.devcel.2007.04.002.Google Scholar
Ellis, J. T., Holmdahl, O. J., Ryce, C., Njenga, J. M., Harper, P. A. and Morrison, D. A. (2000). Molecular phylogeny of Besnoitia and the genetic relationships among Besnoitia of cattle, wildebeest and goats. Protist 151, 329336.Google Scholar
Etienne-Manneville, S. (2008). Polarity proteins in migration and invasion. Oncogene 27, 69706980. doi: 10.1038/onc.2008.347.Google Scholar
European Food Safety Authority (2010). Scientific Statement on Bovine Besnoitiosis. EFSA Journal No. 8. European Food Safety Authority, Parma, Italy.Google Scholar
Gomes, E. R., Jani, S. and Gundersen, G. G. (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451463.Google Scholar
Gonçalves, J., Nolasco, S., Nascimento, R., Fanarraga, M., Zabala, J. C. and Soares, H. (2010 a). TBCCD1, a new centrosomal protein, is required for centrosome and Golgi apparatus positioning. EMBO Reports 11, 194200. doi: 10.1038/embor.2010.5.CrossRefGoogle ScholarPubMed
Gonçalves, J., Tavares, A., Carvalhal, S. and Soares, H. (2010 b). Revisiting the tubulin folding pathways: new roles in centrosomes and cilia. Biomolecular Concepts 1, 423434. doi: 10.1515/bmc.2010.033.Google Scholar
Hurtado, L., Caballero, C., Gavilan, M. P., Cardenas, J., Bornens, M. and Rios, R. M. (2011). Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. Journal of Cell Biology 193, 917933. doi: 10.1083/jcb.201011014.Google Scholar
Innes, E. A. (2010). A brief history and overview of Toxoplasma gondii . Zoonoses and Public Health 57, 17. doi: 10.1111/j.1863-2378.2009.01276.x.Google Scholar
Kodani, A. and Sütterlin, C. (2008). The Golgi protein GM130 regulates centrosome morphology and function. Molecular Biology of the Cell 19, 745753. doi: 10.1091/ mbc.E07-08-0847.Google Scholar
Kodani, A., Kristensen, I., Huang, L. and Sütterlin, C. (2009). GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome organization. Molecular Biology of the Cell 20, 11921200. doi: 10.1091/mbc.E08-08-0834.Google Scholar
Lambert, H., Hitziger, N., Dellacasa, I., Svensson, M. and Barragan, A. (2006). Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cellular Microbiology 8, 16111623. doi: 10.1111/j.1462-5822.2006.00735.x.Google Scholar
Lambert, H., Dellacasa-Lindberg, I. and Barragan, A. (2010). Migratory responses of leukocytes infected with Toxoplasma gondii . Microbes and Infection 13, 96102. doi: 10.1016/j.micinf.2010.10.002.Google Scholar
Luxton, G. W. G. and Gundersen, G. G. (2011). Orientation and function of the nuclear-centrosomal axis during cell migration. Current Opinion in Cell Biology 23, 579588. doi: 10.1016/j.ceb.2011.08.001.Google Scholar
Marcelino, E., Martins, T. M., Morais, J. B., Nolasco, S., Cortes, H., Hemphill, A., Leitão, A. and Novo, C. (2011). Besnoitia besnoiti protein disulfide isomerase (BbPDI): molecular characterization, expression and in silico modelling. Experimental Parasitology 129, 164174. doi: 10.1016/j.exppara.Google Scholar
Miller, P. M., Folkmann, A. W., Maia, A. R., Efimova, N., Efimov, A. and Kaverina, I. (2009). Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nature Cell Biology 11, 10691080. doi: 10.1038/ncb1920.Google Scholar
Pols, J. W. (1960). Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort Journal of Veterinary Research 28, 265356.Google Scholar
Pouthas, F., Girard, P., Lecaudey, V., Gilmour, D., Boulin, C., Pepperkok, R. and Reynaud, E. G. (2008). In migrating cells, the Golgi complex and the position of the centrosome depend on geometrical constraints of the substratum. Journal of Cell Science 121, 24062414. doi: 10.1242/jcs.026849.Google Scholar
Reis, Y., Cortes, H., Viseu Melo, L., Fazendeiro, I., Leitão, A. and Soares, H. (2006). Microtubule cytoskeleton behavior in the initial steps of host cell invasion by Besnoitia besnoiti . FEBS Letters 580, 46734682.Google Scholar
Rivero, S., Cardenas, J., Bornens, M. and Rios, R. M. (2009). Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO Journal 28, 10161028. doi: 10.1038/emboj.2009.47.Google Scholar
Salpingidou, G., Smertenko, A., Hausmanowa-Petrucewicz, I., Hussey, P. J. and Hutchison, C. J. (2007). A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. Journal of Cell Biology 178, 897904. doi: 10.1083/jcb.200702026.Google Scholar
Schmoranzer, J., Fawcett, J. P., Segura, M., Tan, S., Vallee, R. B., Pawson, T. and Gundersen, G. G. (2009). Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Current Biology 19, 10651074. doi: 10.1016/j.cub.2009.05.065.Google Scholar
Sehgal, A., Bettiol, S., Pypaert, M., Wenk, M. R., Kaasch, A., Blader, I. J., Joiner, K. A. and Coppens, I. (2005). Peculiarities of host cholesterol transport to the unique intracellular vacuole containing Toxoplasma . Traffic 6, 11251141. doi: 10.1111/j.1600-0854.2005.00348.x.Google Scholar
Shaw, M. K., Compton, H. L., Roos, D. S. and Tilney, L. G. (2000). Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii . Journal of Cell Science 113, 12411254.Google Scholar
Sütterlin, C. and Colanzi, A. (2010). The Golgi and the centrosome: building a functional partnership. Journal of Cell Biology 188, 621628. doi: 10.1083/jcb.200910001.Google Scholar
Sweeney, K. R., Morrissette, N. S., LaChapelle, S. and Blader, I. J. (2010). Host cell invasion by Toxoplasma gondii is temporally regulated by the host microtubule cytoskeleton. Eukaryotic Cell 9, 16801689. doi: 10.1128/EC.00079-10.Google Scholar
Thyberg, J. and Moskalewski, S. (1999). Role of microtubules in the organization of the Golgi complex. Experimental Cell Research 246, 263279. doi: 10.1006/ excr.1998.4326.Google Scholar
Vinogradova, T., Miller, P. M. and Kaverina, I. (2009). Microtubule network asymmetry in motile cells: role of Golgi-derived array. Cell Cycle 8, 21682174.CrossRefGoogle ScholarPubMed
Walker, M. E., Hjort, E. E., Smith, S. S., Tripathi, A., Hornick, J. E., Hinchcliffe, E. H., Archer, W. and Hager, K. M. (2008). Toxoplasma gondii actively remodels the microtubule network in host cells. Microbes and Infection 10, 14401449. doi: 10.1016/j.micinf.2008.08.014.Google Scholar
Wang, Y., Weiss, L. and Orlofsky, A. (2010). Coordinate control of host centrosome position, organelle distribution, and migratory response by Toxoplasma gondii via host mTORC2. Journal of Biological Chemistry 285, 1561115618. doi: 10.1074/jbc.M109.095778.Google Scholar
Weidner, J. M., Kanatani, S., Hernández-Castañeda, M. A., Fuks, J. M., Rethi, B., Wallin, R. P. and Barragan, A. (2013). Rapid cytoskeleton remodelling in dendritic cells following invasion by Toxoplasma gondii coincides with the onset of a hypermigratory phenotype. Cellular Microbiology 15, 17351752. doi: 10.1111/cmi.12145.Google Scholar
Yadav, S., Puri, S. and Linstedt, A. D. (2009). A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Molecular Biology of the Cell 20, 17281736. doi: 10.1091/mbc.E08-10-1077.Google Scholar
Yvon, A. M., Walker, J. W., Danowski, B., Fagerstrom, C., Khodjakov, A. and Wadsworth, P. (2002). Centrosome reorientation in wound-edge cells is cell type specific. Molecular Biology of the Cell 13, 18711880. doi: 10.1091/mbc.01-11-0539.Google Scholar
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