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Apicomplexans pulling the strings: manipulation of the host cell cytoskeleton dynamics

Published online by Cambridge University Press:  04 April 2016

RITA CARDOSO Open the ORCID record for RITA CARDOSO [Opens in a new window] ,
HELENA SOARES ,
ANDREW HEMPHILL  and
ALEXANDRE LEITÃO
RITA CARDOSO*
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, Länggass-Strasse 122, Bern 3012, Switzerland Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal
HELENA SOARES
Affiliation:
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
ANDREW HEMPHILL
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, Länggass-Strasse 122, Bern 3012, Switzerland
ALEXANDRE LEITÃO
Affiliation:
Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal
*
*Corresponding author: Institute of Parasitology, Vetsuisse Faculty, University of Berne, Länggass-Strasse 122, Bern 3012, Switzerland. Tel: +41 31 631 2396. Fax: +41 31 631 2477. E-mail: [email protected]
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Summary

Invasive stages of apicomplexan parasites require a host cell to survive, proliferate and advance to the next life cycle stage. Once invasion is achieved, apicomplexans interact closely with the host cell cytoskeleton, but in many cases the different species have evolved distinct mechanisms and pathways to modulate the structural organization of cytoskeletal filaments. The host cell cytoskeleton is a complex network, largely, but not exclusively, composed of microtubules, actin microfilaments and intermediate filaments, all of which are modulated by associated proteins, and it is involved in diverse functions including maintenance of cell morphology and mechanical support, migration, signal transduction, nutrient uptake, membrane and organelle trafficking and cell division. The ability of apicomplexans to modulate the cytoskeleton to their own advantage is clearly beneficial. We here review different aspects of the interactions of apicomplexans with the three main cytoskeletal filament types, provide information on the currently known parasite effector proteins and respective host cell targets involved, and how these interactions modulate the host cell physiology. Some of these findings could provide novel targets that could be exploited for the development of preventive and/or therapeutic strategies.

Keywords

Apicomplexahost–parasite interactionactinmicrotubulesintermediate filaments
Type
Review Article
Information
Parasitology , Volume 143 , Issue 8 , July 2016 , pp. 957 - 970
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Adjogble, K. D., Mercier, C., Dubremetz, J. F., Hucke, C., Mackenzie, C. R., Cesbron-Delauw, M. F. and Däubener, W. (2004). GRA9, a new Toxoplasma gondii dense granule protein associated with the intravacuolar network of tubular membranes. International Journal for Parasitology 34, 1255–1264.Google Scholar
Alexander, D. L., Mital, J., Ward, G. E., Bradley, P. and Boothroyd, J. C. (2005). Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathogens 1, e17.Google Scholar
Azimzadeh, J. and Bornens, M. (2007). Structure and duplication of the centrosome. Journal of Cell Science 120, 2139–2142.Google Scholar
Baumgartner, M. (2011). Theileria annulata promotes Src kinase-dependent host cell polarization by manipulating actin dynamics in podosomes and lamellipodia. Cellular Microbiology 13, 538–553.Google Scholar
Besteiro, S., Michelin, A., Poncet, J., Dubremetz, J. F. and Lebrun, M. (2009). Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathogens 5, e1000309.Google Scholar
Bichet, M., Joly, C., Hadj Henni, A., Guilbert, T., Xémard, M., Tafani, V., Lagal, V., Charras, G. and Tardieux, I. (2014). The toxoplasma-host cell junction is anchored to the cell cortex to sustain parasite invasive force. BMC Biology 12, 773.Google Scholar
Blader, I. J. and Saeij, J. P. (2009). Communication between Toxoplasma gondii and its host: impact on parasite growth, development, immune evasion, and virulence. APMIS: Acta Pathologica, Microbiologica, et Immunologica Scandinavica 117, 458–476.Google Scholar
Bradley, P. J., Ward, C., Cheng, S. J., Alexander, D. L., Coller, S., Coombs, G. H., Dunn, J. D., Ferguson, D. J., Sanderson, S. J., Wastling, J. M. and Boothroyd, J. C. (2005). Proteomic analysis of rhoptry organelles reveals many novel constituents for host–parasite interactions in Toxoplasma gondii. Journal of Biological Chemistry 280, 34245–34258.Google Scholar
Brunet, J., Pfaff, A. W., Abidi, A., Unoki, M., Nakamura, Y., Guinard, M., Klein, J. P., Candolfi, E. and Mousli, M. (2008). Toxoplasma gondii exploits UHRF1 and induces host cell cycle arrest at G2 to enable its proliferation. Cellular Microbiology 10, 908–920.Google Scholar
Cardoso, R., Nolasco, S., Gonçalves, J., Cortes, H. C., Leitão, A. and Soares, H. (2014). Besnoitia besnoiti and Toxoplasma gondii: two apicomplexan strategies to manipulate the host cell centrosome and Golgi apparatus. Parasitology 3, 1–19.Google Scholar
Collantes-Fernandez, E., Arrighi, R. B. G., Álvarez-Garcıa, G., Weidner, J. M., Regidor-Cerrillo, J., Boothroyd, J. C., Ortega-Mora, L. M. and Barragan, A. (2012). Infected dendritic cells facilitate systemic dissemination and transplacental passage of the obligate intracellular parasite Neospora caninum in mice. PLoS ONE 7, e32123.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, 261–274.Google Scholar
da Silva, C. V., da Silva, E. A., Cruz, M. C., Chavrier, P. and Mortara, R. A. (2009). ARF6, PI3-kinase and host cell actin cytoskeleton in Toxoplasma gondii cell invasion. Biochemical and Biophysical Research Communications 378, 656–661.Google Scholar
de Forges, H., Bouissou, A. and Perez, F. (2012). Interplay between microtubule dynamics and intracellular organization. International Journal of Biochemistry & Cell Biology 44, 266–274.Google Scholar
Delorme-Walker, V., Abrivard, M., Lagal, V., Anderson, K., Perazzi, A., Gonzalez, V., Page, C., Chauvet, J., Ochoa, W., Volkmann, N., Hanein, D. and Tardieux, I. (2012). Toxofilin upregulates the host cortical actin cytoskeleton dynamics, facilitating Toxoplasma invasion. Journal of Cell Science 125, 4333–4342.Google Scholar
Dobbelaere, D. A. and Kuenzi, P. (2004). The strategies of the Theileria parasite: a new twist in host–pathogen interactions. Current Opinion in Immunology 16, 524–530.Google Scholar
Elliott, D. A., Coleman, D. J., Lane, M. A., May, R. C., Machesky, L. M. and Clark, D. P. (2001). Cryptosporidium parvum infection requires host cell actin polymerization. Infection and Immunity 69, 5940–5942.Google Scholar
Feng, H., Nie, W., Bonilla, R., Widmer, G., Sheoran, A. and Tzipori, S. (2006). Quantitative tracking of Cryptosporidium infection in cell culture with CFSE. Journal of Parasitology 92, 1350–1354.Google Scholar
Fernandez, J., Portilho, D. M., Danckaert, A., Munier, S., Becker, A., Roux, P., Zambo, A., Shorte, S., Jacob, Y., Vidalain, P. O., Charneau, P., Clavel, F. and Arhel, N. J. (2015). Microtubule-associated proteins 1 (MAP1) promote human immunodeficiency virus type I (HIV-1) intracytoplasmic routing to the nucleus. Journal of Biological Chemistry 290, 4631–4646.Google Scholar
Foley, M., Tilley, L., Sawyer, W. H. and Anders, R. F. (1991). The ring-infected erythrocyte surface antigen of Plasmodium falciparum associates with spectrin in the erythrocyte membrane. Molecular and Biochemical Parasitology 46, 137–147.Google Scholar
Foo, K. Y. and Chee, H. Y. (2015). Interaction between Flavivirus and cytoskeleton during virus replication. Biomed Research International 2015, 427814.Google Scholar
Franke, T. F. (2008). PI3K/Akt: getting it right matters. Oncogene 27, 6473–6488.CrossRefGoogle ScholarPubMed
Frénal, K. and Soldati-Favre, D. (2009). Role of the parasite and host cytoskeleton in apicomplexa parasitism. Cell Host & Microbe 5, 602–611.Google Scholar
Gaji, R. Y., Huynh, M. H. and Carruthers, V. B. (2013). A novel high throughput invasion screen identifies host actin regulators required for efficient cell entry by Toxoplasma gondii. PLoS ONE 8, e64693.Google Scholar
Ganguly, A. K., Ranjan, P., Kumar, A. and Bhavesh, N. S. (2015). Dynamic association of PfEMP1 and KAHRP in knobs mediates cytoadherence during Plasmodium invasion. Scientific Reports 5, 8617.Google Scholar
Glenister, F. K., Coppel, R. L., Cowman, A. F., Mohandas, N. and Cooke, B. M. (2002). Contribution of parasite proteins to altered mechanical properties of malaria infected red blood cells. Blood 99, 1060–1063.Google Scholar
Gonçalves, J., Nolasco, S., Nascimento, R., Fanarraga, M. L., Zabala, J. C. and Soares, H. (2010). TBCCD1, a new centrosomal protein, is required for centrosome and Golgi apparatus positioning. EMBO Reports 11, 194–200.Google Scholar
Gonzalez, V., Combe, A., David, V., Malmquist, N. A., Delorme, V., Leroy, C., Blazquez, S., Ménard, R. and Tardieux, I. (2009). Host cell entry by apicomplexa parasites requires actin polymerization in the host cell. Cell Host & Microbe 5, 259–272.Google Scholar
Guionaud, C., Hemphill, A., Mevissen, M. and Alaeddine, F. (2010). Molecular characterization of Neospora caninum MAG1, a dense granule protein secreted into the parasitophorous vacuole, and associated with the cyst wall and the cyst matrix. Parasitology 137, 1605–1619.CrossRefGoogle Scholar
Gundersen, G. G. and Cook, T. A. (1999). Microtubules and signal transduction. Current Opinion in Cell Biology 11, 81–94.CrossRefGoogle ScholarPubMed
Haglund, C. M. and Welch, M. D. (2011). Pathogens and polymers: microbe-host interactions illuminate the cytoskeleton. The Journal of Cell Biology 195, 7–17.Google Scholar
Haldar, K., Samuel, B. U., Mohandas, N., Harrison, T. and Hiller, N. L. (2001). Transport mechanisms in Plasmodium-infected erythrocytes: lipid rafts and a tubovesicular network. International Journal for Parasitology 31, 1393–1401.Google Scholar
Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509–514.Google Scholar
Halonen, S. K. and Weidner, E. (1994). Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments. Journal of Eukaryotic Microbiology 41, 65–71.Google Scholar
Halonen, S. K., Weiss, L. M. and Chiu, F. C. (1998). Association of host cell intermediate filaments with Toxoplasma gondii cysts in murine astrocytes in vitro. International Journal for Parasitology 28, 815–823.Google Scholar
Hemphill, A., Vonlaufen, N., Naguleswaran, A., Keller, N., Riesen, M., Guetg, N., Srinivasan, S. and Alaeddine, F. (2004). Tissue culture and explant approaches to studying and visualizing Neospora caninum and its interactions with the host cell. Microscopy and Microanalysis 10, 602–620.Google Scholar
Hermosilla, C., Schröpfer, E., Stowasser, M., Eckstein-Ludwig, U., Behrendt, J. H. and Zahner, H. (2008). Cytoskeletal changes in Eimeria bovis-infected host endothelial cells during first merogony. Veterinary Research Communications 32, 521–531.Google Scholar
Hermosilla, C., Ruiz, A. and Taubert, A. (2012). Eimeria bovis: an update on parasite–host cell interactions. International Journal of Medical Microbiology 302, 210–215.Google Scholar
Kats, L. M., Proellocks, N. I., Buckingham, D. W., Blanc, L., Hale, J., Guo, X., Pei, X., Herrmann, S., Hanssen, E. G., Coppel, R. L., Mohandas, N., An, X. and Cooke, B. M. (2015). Interactions between Plasmodium falciparum skeleton-binding protein 1 and the membrane skeleton of malaria-infected red blood cells. Biochima et Biophysica Acta 1848, 1619–1628.Google Scholar
Kim, J. Y., Ahn, H. J., Ryu, K. J. and Nam, H. W. (2008). Interaction between parasitophorous vacuolar membrane associated GRA3 and calcium modulating ligand of host cell endoplasmic reticulum in the parasitism of Toxoplasma gondii. The Korean Journal of Parasitology 46, 209–216.CrossRefGoogle ScholarPubMed
Lai, C. K., Saxena, V., Tseng, C. H., Jeng, K. S., Kohara, M. and Lai, M. M. (2014). Nonstructural protein 5A is incorporated into hepatitis C virus low-density particle through interaction with core protein and microtubules during intracellular transport. PLoS ONE 9, e99022.Google Scholar
Laliberté, J. and Carruthers, V. B. (2008). Host cell manipulation by the human pathogen Toxoplasma gondii. Cellular and Molecular Life Sciences 65, 1900–1915.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, 1611–1623.Google Scholar
Lambert, H., Dellacasa-Lindberg, I. and Barragan, A. (2010). Migratory responses of leukocytes infected with Toxoplasma gondii. Microbes and Infection 13, 96–102.Google Scholar
Lang, A. E., Schmidt, G., Schlosser, A., Hey, T. D., Larrinua, I. M., Sheets, J. J., Mannherz, H. G. and Aktories, K. (2010). Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 327, 1139–1142.Google Scholar
Lauer, S. A., Rathod, P. K., Ghori, N. and Haldar, K. (1997). A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276, 1122–1125.Google Scholar
Lebrun, M., Michelin, A., El Hajj, H., Poncet, J., Bradley, P. J., Vial, H. and Dubremetz, J. F. (2005). The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cellular Microbiology 7, 1823–1833.Google Scholar
Lendner, M. and Daugschies, A. (2014). Cryptosporidium infections: molecular advances. Parasitology 141, 1511–1532.Google Scholar
Lüders, J. and Stearns, T. (2007). Microtubule-organizing centres: a re-evaluation. Nature Reviews Molecular Cell Biology 8, 161–167.Google Scholar
Lutz, K., Schmitt, S., Linder, M., Hermosilla, C., Zahner, H. and Taubert, A. (2011). Eimeria bovis-induced modulation of the host cell proteome at the meront I stage. Molecular and Biochemical Parasitology 175, 1–9.Google Scholar
Ma, M. and Baumgartner, M. (2013). Filopodia and membrane blebs drive efficient matrix invasion of macrophages transformed by the intracellular parasite Theileria annulata. PLoS ONE 8, e75577.Google ScholarPubMed
Ma, M. and Baumgartner, M. (2014). Intracellular Theileria annulata promote invasive cell motility through kinase regulation of the host actin cytoskeleton. PLoS Pathogens 10, e1004003.CrossRefGoogle ScholarPubMed
Magno, R. C., Lemgruber, L., Vommaro, R. C., Souza, W. and Attias, M. (2005). Intravacuolar network may act as a mechanical support for Toxoplasma gondii inside the parasitophorous vacuole. Microscopy Research and Technique 67, 45–52.Google Scholar
Maier, A. G., Rug, M., O'Neill, M. T., Beeson, J. G., Marti, M., Reeder, J. and Cowman, A. F. (2007). Skeleton-binding protein 1 functions at the parasitophorous vacuole membrane to traffic PfEMP1 to the Plasmodium falciparum-infected erythrocyte surface. Blood 109, 1289–1297.Google Scholar
Mbengue, A., Yam, X. Y. and Braun-Breton, C. (2012). Human erythrocyte remodelling during Plasmodium falciparum malaria parasite growth and egress. British Journal of Haematology 157, 171–179.Google Scholar
Mercier, C., Dubremetz, J. F., Rauscher, B., Lecordier, L., Sibley, L. D. and Cesbron-Delauw, M. F. (2002). Biogenesis of nanotubular network in Toxoplasma parasitophorous vacuole induced by parasite proteins. Molecular Biology of the Cell 13, 2397–2409.Google Scholar
Mundwiler-Pachlatko, E. and Beck, H. P. (2013). Maurer's clefts, the enigma of Plasmodium falciparum. Proceedings of the National Academy of Sciences of the United States of America 110, 19987–19994.Google Scholar
Na, R. H., Zhu, G. H., Luo, J. X., Meng, X. J., Cui, L., Peng, H. J., Chen, X. G. and Gomez-Cambronero, J. (2013). Enzymatically active Rho and Rac small-GTPases are involved in the establishment of the vacuolar membrane after Toxoplasma gondii invasion of host cells. BMC Microbiology 13, 125.Google Scholar
Nolan, S. J., Romano, J. D., Luechtefeld, T. and Coppens, I. (2015). Neospora caninum recruits host cell structures to its parasitophorous vacuole and salvages lipids from organelles. Eukaryotic Cell 14, 454–473.Google Scholar
Oh, S. S., Voigt, S., Fisher, D., Yi, S. J., LeRoy, P. J. and Derick, L. H. (2000). Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Molecular and Biochemical Parasitology 108, 237–247.Google Scholar
Onishi, K., Higuchi, M., Asakura, T., Masuyama, N. and Gotoh, Y. (2007). The PI3K-Akt pathway promotes microtubule stabilization in migrating fibroblasts. Genes to Cells 12, 535–546.Google Scholar
Pernas, L., Adomako-Ankomah, Y., Shastri, A. J., Ewald, S. E., Treeck, M., Boyle, J. P. and Boothroyd, J. C. (2014). Toxoplasma effector MAF1 mediates recruitment of host mitochondria and impacts the host response. PLoS Biology 12, e1001845.Google Scholar
Pollard, T. (2003). The cytoskeleton, cellular motility and the reductionist agenda. Nature 422, 741–745.Google Scholar
Proellocks, N. I., Herrmann, S., Buckingham, D. W., Hanssen, E., Hodges, E. K. and Elsworth, B. (2014). A lysine-rich membrane-associated PHISTb protein involved in alteration of the cytoadhesive properties of Plasmodium falciparum-infected red blood cells. FASEB Journal 28, 3103–3113.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, 4673–4682.Google Scholar
Romano, J. D., Sonda, S., Bergbower, E., Smith, M. E. and Coppens, I. (2013). Toxoplasma gondii salvages sphingolipids from the host Golgi through the rerouting of selected Rab vesicles to the parasitophorous vacuole. Molecular Biology of the Cell 24, 1974–1995.Google Scholar
Rug, M., Cyrklaff, M., Mikkonen, A., Lemgruber, L., Kuelzer, S., Sanchez, C. P., Thompson, J., Hanssen, E., O'Neill, M., Langer, C., Lanzer, M., Frischknecht, F., Maier, A. G. and Cowman, A. F. (2014). Export of virulence proteins by malaria-infected erythrocytes involves remodeling of host actin cytoskeleton. Blood 124, 3459–3468.Google Scholar
Sana, T. G., Baumann, C., Merdes, A., Soscia, C., Rattei, T., Hachani, A., Jones, C., Bennett, K. L., Filloux, A., Superti-Furga, G., Voulhoux, R. and Bleves, S. (2015). Internalization of Pseudomonas aeruginosa Strain PAO1 into epithelial cells is promoted by interaction of aT6SS effector with the microtubule network. MBio 6, e00712.CrossRefGoogle ScholarPubMed
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, 1065–1074.CrossRefGoogle ScholarPubMed
Schneider, I., Haller, D., Kullmann, B., Beyer, D., Ahmed, J. S. and Seitzer, U. (2007). Identification, molecular characterization and subcellular localization of a Theileria annulata parasite protein secreted into the host cell cytoplasm. Parasitology Research 101, 1471–1482.CrossRefGoogle ScholarPubMed
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, 1125–1141.Google Scholar
Seitzer, U., Gerber, S., Beyer, D., Dobschanski, J., Kullmann, B., Haller, D. and Ahmed, J. S. (2010). Schizonts of Theileria annulata interact with the microtubule network of their host cell via the membrane protein TaSP. Parasitology Research 106, 1085–1102.Google Scholar
Shaw, M. K. (2003). Cell invasion by Theileria sporozoites. Trends in Parasitology 19, 2–6.CrossRefGoogle ScholarPubMed
Shi, H., Liu, Z., Li, A., Yin, J., Chong, A. G., Tan, K. S., Zhang, Y. and Lim, C. T. (2013). Life cycle-dependent cytoskeletal modifications in Plasmodium falciparum infected erythrocytes. PLoS ONE 9, e61170.Google Scholar
Silva, M. D., Cooke, B. M., Guillotte, M., Buckingham, D. W., Sauzet, J. P., Le Scanf, C., Contamin, H., David, P., Mercereau-Puijalon, O. and Bonnefoy, S. (2005). A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Molecular Microbiology 56, 990–1003.Google Scholar
Sinai, A. P., Webster, P. and Joiner, K. A. (1997). Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. Journal of Cell Science 110, 2117–2128.Google Scholar
Soares, H., Marinho, H. S., Real, C. and Antunes, F. (2014). Cellular polarity in aging: role of redox regulation and nutrition. Genes & Nutrition 9, 371.Google Scholar
Spycher, C., Rug, M., Pachlatko, E., Hanssen, E., Ferguson, D., Cowman, A. F., Tilley, L. and Beck, H. P. (2008). The Maurer's cleft protein MAHRP1 is essential for trafficking of PfEMP1 to the surface of Plasmodium falciparum-infected erythrocytes. Molecular Microbiology 68, 1300–1314.Google Scholar
Straub, K., Cheng, S., Sohn, C. and Bradley, P. (2009). Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cellular Microbiology 11, 590–603.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, 1680–1689.Google Scholar
Takemae, H., Sugi, T., Kobayashi, K., Gong, H., Ishiwa, A., Recuenco, F. C., Murakoshi, F., Iwanaga, T., Inomata, A., Horimoto, T., Akashi, H. and Kato, K. (2013). Characterization of the interaction between Toxoplasma gondii rhoptry neck protein 4 and host cellular β-tubulin. Scientific Reports 3, 3199.Google Scholar
Tarr, S. J., Moon, R. W., Hardege, I. and Osborne, A. R. (2014). A conserved domain targets exported PHISTb family proteins to the periphery of Plasmodium infected erythrocytes. Molecular and Biochemical Parasitology 196, 29–40.Google Scholar
Taubert, A., Wimmers, K., Ponsuksili, S., Jimenez, C. A., Zahner, H. and Hermosilla, C. (2010). Microarray-based transcriptional profiling of Eimeria bovis-infected bovine endothelial host cells. Veterinary Research 41, 70.Google Scholar
Tyler, J. S., Treeck, M. and Boothroyd, J. C. (2011). Focus on the ringleader: the role of AMA1 in apicomplexan invasion and replication. Trends in Parasitology 27, 410–420.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, 2168–2174.Google Scholar
von Schubert, C., Xue, G., Schmuckli-Maurer, J., Woods, K. L., Nigg, E. A. and Dobbelaere, D. A. (2010). The transforming parasite Theileria co-opts host cell mitotic and central spindles to persist in continuously dividing cells. PLoS Biology 8, e1000499.Google Scholar
Vonlaufen, N., Gianinazzi, C., Müller, N., Simon, F., Björkman, C., Jungi, T. W., Leib, S. L. and Hemphill, A. (2002). Infection of organotypic slice cultures from rat central nervous tissue with Neospora caninum: an alternative approach to study host–parasite interactions. International Journal for Parasitology 32, 533–542.Google Scholar
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, 1440–1449.CrossRefGoogle ScholarPubMed
Wang, Y., Weiss, L. M. and Orlofsky, A. (2009). Intracellular parasitism with Toxoplasma gondii stimulates mammalian-target-of-rapamycin-dependent host cell growth despite impaired signalling to S6K1 and 4E-BP1. Cellular Microbiology 11, 983–1000.Google Scholar
Wang, Y., Weiss, L. M. and Orlofsky, A. (2010). Coordinate control of host centrosome position, organelle distribution, and migratory response by Toxoplasma gondii via host mTORC2. The Journal of Biological Chemistry 285, 15611–15618.Google Scholar
Watermeyer, J. M., Hale, V. L., Hackett, F., Clare, D. K., Cutts, E. E., Vakonakis, I., Fleck, R. A., Blackman, M. J. and Saibil, H. R. (2016). A spiral scaffold underlies cytoadherent knobs in Plasmodium falciparum-infected erythrocytes. Blood 127, 343–351.Google Scholar
Weidner, J. M. and Barragan, A. (2014). Tightly regulated migratory subversion of immune cells promotes the dissemination of Toxoplasma gondii. International Journal for Parasitology 44, 85–90.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, 1735–1752.Google Scholar
Wiens, O., Xia, D., von Schubert, C., Wastling, J. M., Dobbelaere, D. A., Heussler, V. T. and Woods, K. L. (2014). Cell cycle-dependent phosphorylation of Theileria annulata Schizont surface proteins. PLoS ONE 9, e103821.Google Scholar
Woods, K. L., Theiler, R., Mühlemann, M., Segiser, A., Huber, S., Ansari, H. R., Pain, A. and Dobbelaere, D. A. (2013). Recruitment of EB1, a master regulator of microtubule dynamics, to the surface of the Theileria annulata schizont. PLoS Pathogens 9, e1003346.Google Scholar
Yang, Z. Z., Tschopp, O., Baudry, A., Du Mmler, B., Hynx, D. and Hemmings, B. A. (2004). Physiological functions of protein kinase B/Akt. Biochemical Society Transactions 32, 350–354.Google Scholar