Skip to main content Accessibility help
×
Home
Hostname: page-component-564cf476b6-s5ssh Total loading time: 0.392 Render date: 2021-06-19T15:44:27.823Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

Article contents

Characterization of the Neospora caninum NcROP40 and NcROP2Fam-1 rhoptry proteins during the tachyzoite lytic cycle

Published online by Cambridge University Press:  02 November 2015

IVÁN PASTOR-FERNÁNDEZ
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
JAVIER REGIDOR-CERRILLO
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
ELENA JIMÉNEZ-RUIZ
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
GEMA ÁLVAREZ-GARCÍA
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
VIRGINIA MARUGÁN-HERNÁNDEZ
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
ANDREW HEMPHILL
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, Länggass-Strasse 122, CH-3012 Berne, Switzerland
LUIS M. ORTEGA-MORA
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
Corresponding
E-mail address:

Summary

Virulence factors from the ROP2-family have been extensively studied in Toxoplasma gondii, but in the closely related Neospora caninum only NcROP2Fam-1 has been partially characterized to date. NcROP40 is a member of this family and was found to be more abundantly expressed in virulent isolates. Both NcROP2Fam-1 and NcROP40 were evaluated as vaccine candidates and exerted a synergistic effect in terms of protection against vertical transmission in mouse models, which suggests that they may be relevant for parasite pathogenicity. NcROP40 is localized in the rhoptry bulbs of tachyzoites and bradyzoites, but in contrast to NcROP2Fam-1, the protein does not associate with the parasitophorous vacuole membrane due to the lack of arginine-rich amphipathic helix in its sequence. Similarly to NcROP2Fam-1, NcROP40 mRNA levels are highly increased during tachyzoite egress and invasion. However, NcROP40 up-regulation does not appear to be linked to the mechanisms triggering egress. In contrast to NcROP2Fam-1, phosphorylation of NcROP40 was not observed during egress. Besides, NcROP40 secretion into the host cell was not successfully detected by immunofluorescence techniques. These findings indicate that NcROP40 and NcROP2Fam-1 carry out different functions, and highlight the need to elucidate the role of NcROP40 within the lytic cycle and to explain its relative abundance in tachyzoites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below.

References

Alaeddine, F., Hemphill, A., Debache, K. and Guionaud, C. (2013). Molecular cloning and characterization of NcROP2Fam-1, a member of the ROP2 family of rhoptry proteins in Neospora caninum that is targeted by antibodies neutralizing host cell invasion in vitro . Parasitology 140, 10331050.CrossRefGoogle ScholarPubMed
Álvarez-García, G., Pitarch, A., Zaballos, A., Fernández-García, A., Gil, C., Gómez-Bautista, M., Aguado-Martínez, A. and Ortega-Mora, L. M. (2007). The NcGRA7 gene encodes the immunodominant 17 kDa antigen of Neospora caninum . Parasitology 134, 4150.CrossRefGoogle ScholarPubMed
Barber, J., Trees, A. J., Owen, M. and Tennant, B. (1993). Isolation of Neospora caninum from a British dog. The Veterinary Record 133, 531532.CrossRefGoogle ScholarPubMed
Beck, J. R., Chen, A. L., Kim, E. W. and Bradley, P. J. (2014). RON5 is critical for organization and function of the Toxoplasma moving junction complex. PLoS Pathogens 10, e1004025.CrossRefGoogle ScholarPubMed
Beckers, C. J., Dubremetz, J. F., Mercereau-Puijalon, O. and Joiner, K. A. (1994). The Toxoplasma gondii rhoptry protein ROP2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. The Journal of Cell Biology 127, 947961.CrossRefGoogle Scholar
Behnke, M. S., Wootton, J. C., Lehmann, M. M., Radke, J. B., Lucas, O., Nawas, J., Sibley, L. D. and White, M. W. (2010). Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii . PLoS ONE 5, e12354.CrossRefGoogle ScholarPubMed
Björkman, C. and Hemphill, A. (1998). Characterization of Neospora caninum iscom antigens using monoclonal antibodies. Parasite Immunology 20, 7380.CrossRefGoogle ScholarPubMed
Blackman, M. J. and Carruthers, V. B. (2013). Recent insights into apicomplexan parasite egress provide new views to a kill. Current Opinion in Microbiology 16, 459464.CrossRefGoogle ScholarPubMed
Boothroyd, J. C. and Dubremetz, J. F. (2008). Kiss and spit: the dual roles of Toxoplasma rhoptries. Nature Reviews Microbiology 6, 7988.CrossRefGoogle ScholarPubMed
Bradley, P. J. and Sibley, L. D. (2007). Rhoptries: an arsenal of secreted virulence factors. Current Opinion in Microbiology 10, 582587.CrossRefGoogle ScholarPubMed
Carey, K. L., Jongco, A. M., Kim, K. and Ward, G. E. (2004). The Toxoplasma gondii rhoptry protein ROP4 is secreted into the parasitophorous vacuole and becomes phosphorylated in infected cells. Eukaryotic Cell 3, 13201330.CrossRefGoogle ScholarPubMed
Carruthers, V. B. and Sibley, L. D. (1997). Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. European Journal of Cell Biology 73, 114123.Google ScholarPubMed
Carruthers, V. B. and Sibley, L. D. (1999). Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii . Molecular Microbiology 31, 421428.CrossRefGoogle ScholarPubMed
Cowman, A. F., Berry, D. and Baum, J. (2012). The cellular and molecular basis for malaria parasite invasion of the human red blood cell. The Journal of Cell Biology 198, 961971.CrossRefGoogle ScholarPubMed
Debache, K., Guionaud, C., Alaeddine, F., Mevissen, M. and Hemphill, A. (2008). Vaccination of mice with recombinant NcROP2 antigen reduces mortality and cerebral infection in mice infected with Neospora caninum tachyzoites. International Journal for Parasitology 38, 14551463.CrossRefGoogle ScholarPubMed
Debache, K., Alaeddine, F., Guionaud, C., Monney, T., Muller, J., Strohbusch, M., Leib, S. L., Grandgirard, D. and Hemphill, A. (2009). Vaccination with recombinant NcROP2 combined with recombinant NcMIC1 and NcMIC3 reduces cerebral infection and vertical transmission in mice experimentally infected with Neospora caninum tachyzoites. International Journal for Parasitology 39, 13731384.CrossRefGoogle ScholarPubMed
Debache, K., Guionaud, C., Alaeddine, F. and Hemphill, A. (2010). Intraperitoneal and intra-nasal vaccination of mice with three distinct recombinant Neospora caninum antigens results in differential effects with regard to protection against experimental challenge with Neospora caninum tachyzoites. Parasitology 137, 229240.CrossRefGoogle ScholarPubMed
Dixon, S. E., Stilger, K. L., Elias, E. V., Naguleswaran, A. and Sullivan, W. J. Jr. (2010). A decade of epigenetic research in Toxoplasma gondii . Molecular and Biochemical Parasitology 173, 19.CrossRefGoogle ScholarPubMed
Du, J., An, R., Chen, L., Shen, Y., Chen, Y., Cheng, L., Jiang, Z., Zhang, A., Yu, L., Chu, D., Shen, Y., Luo, Q., Chen, H., Wan, L., Li, M., Xu, X. and Shen, J. (2014). Toxoplasma gondii virulence factor ROP18 inhibits the host NF-kappaB pathway by promoting p65 degradation. The Journal of Biological Chemistry 289, 1257812592.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Schares, G. (2011). Neosporosis in animals-The last five years. Veterinary Parasitology 180, 90108.CrossRefGoogle ScholarPubMed
Dunn, J. D., Ravindran, S., Kim, S. K. and Boothroyd, J. C. (2008). The Toxoplasma gondii dense granule protein GRA7 is phosphorylated upon invasion and forms an unexpected association with the rhoptry proteins ROP2 and ROP4. Infection and Immunity 76, 58535861.CrossRefGoogle ScholarPubMed
El Hajj, H., Demey, E., Poncet, J., Lebrun, M., Wu, B., Galeotti, N., Fourmaux, M. N., Mercereau-Puijalon, O., Vial, H., Labesse, G. and Dubremetz, J. F. (2006). The ROP2 family of Toxoplasma gondii rhoptry proteins: proteomic and genomic characterization and molecular modeling. Proteomics 6, 57735784.CrossRefGoogle ScholarPubMed
El Hajj, H., Lebrun, M., Fourmaux, M. N., Vial, H. and Dubremetz, J. F. (2007). Inverted topology of the Toxoplasma gondii ROP5 rhoptry protein provides new insights into the association of the ROP2 protein family with the parasitophorous vacuole membrane. Cellular Microbiology 9, 5464.CrossRefGoogle ScholarPubMed
Esposito, M., Moores, S., Naguleswaran, A., Muller, J. and Hemphill, A. (2007). Induction of tachyzoite egress from cells infected with the protozoan Neospora caninum by nitro- and bromo-thiazolides, a class of broad-spectrum anti-parasitic drugs 9. International Journal for Parasitology 37, 11431152.CrossRefGoogle Scholar
Etheridge, R. D., Alaganan, A., Tang, K., Lou, H. J., Turk, B. E. and Sibley, L. D. (2014). The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice. Cell Host & Microbe 15, 537550.CrossRefGoogle ScholarPubMed
Fernández-García, A., Risco-Castillo, V., Zaballos, A., Alvarez-García, G. and Ortega-Mora, L. M. (2006). Identification and molecular cloning of the Neospora caninum SAG4 gene specifically expressed at bradyzoite stage. Molecular and Biochemical Parasitology 146, 8997.CrossRefGoogle ScholarPubMed
Gaji, R. Y., Behnke, M. S., Lehmann, M. M., White, M. W. and Carruthers, V. B. (2011). Cell cycle-dependent, intercellular transmission of Toxoplasma gondii is accompanied by marked changes in parasite gene expression. Molecular Microbiology 79, 192204.CrossRefGoogle ScholarPubMed
Hajagos, B. E., Turetzky, J. M., Peng, E. D., Cheng, S. J., Ryan, C. M., Souda, P., Whitelegge, J. P., Lebrun, M., Dubremetz, J. F. and Bradley, P. J. (2012). Molecular dissection of novel trafficking and processing of the Toxoplasma gondii rhoptry metalloprotease toxolysin-1. Traffic 13, 292304.CrossRefGoogle ScholarPubMed
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, 602620.CrossRefGoogle ScholarPubMed
Hemphill, A., Debache, K., Monney, T., Schorer, M., Guionaud, C., Alaeddine, F., Mueller, N. and Mueller, J. (2013). Proteins mediating the Neospora caninum-host cell interaction as targets for vaccination. Frontiers in Bioscience (Elite edition) 5, 2336.CrossRefGoogle ScholarPubMed
Jacot, D. and Soldati-Favre, D. (2012). Does protein phosphorylation govern host cell entry and egress by the Apicomplexa? International Journal of Medical Microbiology 302, 195202.CrossRefGoogle ScholarPubMed
Jensen, K. D., Hu, K., Whitmarsh, R. J., Hassan, M. A., Julien, L., Lu, D., Chen, L., Hunter, C. A. and Saeij, J. P. (2013). Toxoplasma gondii rhoptry 16 kinase promotes host resistance to oral infection and intestinal inflammation only in the context of the dense granule protein GRA15. Infection and Immunity 81, 21562167.CrossRefGoogle ScholarPubMed
Kemp, L. E., Yamamoto, M. and Soldati-Favre, D. (2013). Subversion of host cellular functions by the apicomplexan parasites. FEMS Microbiology Reviews 37, 607631.CrossRefGoogle ScholarPubMed
Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. and Koike, T. (2006). Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Molecular & Cellular Proteomics 5, 749757.CrossRefGoogle ScholarPubMed
Labruyere, E., Lingnau, M., Mercier, C. and Sibley, L. D. (1999). Differential membrane targeting of the secretory proteins GRA4 and GRA6 within the parasitophorous vacuole formed by Toxoplasma gondii . Molecular and Biochemical Parasitology 102, 311324.CrossRefGoogle ScholarPubMed
Le Roch, K. G., Johnson, J. R., Florens, L., Zhou, Y., Santrosyan, A., Grainger, M., Yan, S. F., Williamson, K. C., Holder, A. A., Carucci, D. J., Yates, J. R. and Winzeler, E. A. (2004). Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Research 14, 23082318.CrossRefGoogle ScholarPubMed
Lei, T., Wang, H., Liu, J., Nan, H. and Liu, Q. (2014). ROP18 is a key factor responsible for virulence difference between Toxoplasma gondii and Neospora caninum . PLoS ONE 9, e99744.CrossRefGoogle ScholarPubMed
Lescault, P. J., Thompson, A. B., Patil, V., Lirussi, D., Burton, A., Margarit, J., Bond, J. and Matrajt, M. (2010). Genomic data reveal Toxoplasma gondii differentiation mutants are also impaired with respect to switching into a novel extracellular tachyzoite state. PLoS ONE 12, e14463.Google Scholar
Lim, D. C., Cooke, B. M., Doerig, C. and Saeij, J. P. (2012). Toxoplasma and Plasmodium protein kinases: roles in invasion and host cell remodelling. International Journal for Parasitology 42, 2132.CrossRefGoogle ScholarPubMed
Llinas, M. and DeRisi, J. L. (2004). Pernicious plans revealed: Plasmodium falciparum genome wide expression analysis. Current Opinion in Microbiology 7, 382387.CrossRefGoogle ScholarPubMed
Lodoen, M. B., Gerke, C. and Boothroyd, J. C. (2009). A highly sensitive FRET-based approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cellular Microbiology 12, 5566.CrossRefGoogle ScholarPubMed
Lovett, J. L., Howe, D. K. and Sibley, L. D. (2000). Molecular characterization of a thrombospondin-related anonymous protein homologue in Neospora caninum . Molecular and Biochemical Parasitology 107, 3343.CrossRefGoogle ScholarPubMed
Marugán-Hernández, V., Álvarez-García, G., Tomley, F., Hemphill, A., Regidor-Cerrillo, J. and Ortega-Mora, L. M. (2011). Identification of novel rhoptry proteins in Neospora caninum by LC/MS–MS analysis of subcellular fractions. Journal of Proteomics 74, 629642.CrossRefGoogle ScholarPubMed
Mercier, C., Adjogble, K. D., Daubener, W. and Delauw, M. F. (2005). Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? International Journal for Parasitology 35, 829849.CrossRefGoogle ScholarPubMed
Naguleswaran, A., Cannas, A., Keller, N., Vonlaufen, N., Schares, G., Conraths, F. J., Bjorkman, C. and Hemphill, A. (2001). Neospora caninum microneme protein NcMIC3: secretion, subcellular localization, and functional involvement in host cell interaction. Infection and Immunity 69, 64836494.CrossRefGoogle ScholarPubMed
Nakaar, V., Ngô, H. M., Aaronson, E. P., Coppens, I., Stedman, T. T. and Joiner, K. A. (2003). Pleiotropic effect due to targeted depletion of secretory rhoptry protein ROP2 in Toxoplasma gondii . Journal of Cell Science 116, 23112320.CrossRefGoogle ScholarPubMed
Pastor-Fernández, I., Arranz-Solís, D., Regidor-Cerrillo, J., Álvarez-García, G., Hemphill, A., García-Culebras, A., Cuevas-Martín, C. and Ortega-Mora, L. M. (2015). A vaccine formulation combining rhoptry proteins NcROP40 and NcROP2 improves pup survival in a pregnant mouse model of neosporosis. Veterinary Parasitology 207, 203215.CrossRefGoogle Scholar
Peixoto, L., Chen, F., Harb, O. S., Davis, P. H., Beiting, D. P., Brownback, C. S., Ouloguem, D. and Roos, D. S. (2010). Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses. Cell Host & Microbe 8, 208218.CrossRefGoogle ScholarPubMed
Pereira García-Melo, D., Regidor-Cerrillo, J., Collantes-Fernández, E., Aguado-Martínez, A., Del Pozo, I., Minguijon, E., Gómez-Bautista, M., Aduriz, G. and Ortega-Mora, L. M. (2010). Pathogenic characterization in mice of Neospora caninum isolates obtained from asymptomatic calves. Parasitology 137, 10571068.CrossRefGoogle ScholarPubMed
Pérez-Zaballos, F. J., Ortega-Mora, L. M., Álvarez-García, G., Collantes-Fernández, E., Navarro-Lozano, V., García-Villada, L. and Costas, E. (2005). Adaptation of Neospora caninum isolates to cell-culture changes: an argument in favor of its clonal population structure. The Journal of Parasitology 91, 507510.CrossRefGoogle ScholarPubMed
Pittman, K. J., Aliota, M. T. and Knoll, L. J. (2014). Dual transcriptional profiling of mice and Toxoplasma gondii during acute and chronic infection. BMC Genomics 15, 806.CrossRefGoogle ScholarPubMed
Pollo-Oliveira, L., Post, H., Acencio, M. L., Lemke, N., van den Toorn, H., Tragante, V., Heck, A. J., Altelaar, A. F. and Yatsuda, A. P. (2013). Unravelling the Neospora caninum secretome through the secreted fraction (ESA) and quantification of the discharged tachyzoite using high-resolution mass spectrometry-based proteomics. Parasites & Vectors 6, 335.CrossRefGoogle ScholarPubMed
Radke, J. R., Behnke, M. S., Mackey, A. J., Radke, J. B., Roos, D. S. and White, M. W. (2005). The transcriptome of Toxoplasma gondii . BMC Biology 3, 26.CrossRefGoogle ScholarPubMed
Ramaprasad, A., Mourier, T., Naeem, R., Malas, T. B., Moussa, E., Panigrahi, A., Vermont, S. J., Otto, T. D., Wastling, J. and Pain, A. (2015). Comprehensive evaluation of Toxoplasma gondii VEG and Neospora caninum LIV genomes with tachyzoite stage transcriptome and proteome defines novel transcript features. PLoS ONE 10, e0124473.CrossRefGoogle ScholarPubMed
Reese, M. L. and Boothroyd, J. C. (2009). A helical membrane-binding domain targets the Toxoplasma ROP2 family to the parasitophorous vacuole. Traffic 10, 14581470.CrossRefGoogle ScholarPubMed
Reese, M. L. and Boothroyd, J. C. (2011). A conserved non-canonical motif in the pseudoactive site of the ROP5 pseudokinase domain mediates its effect on Toxoplasma virulence. The Journal of Biological Chemistry 286, 2936629375.CrossRefGoogle ScholarPubMed
Reese, M. L., Shah, N. and Boothroyd, J. C. (2014). The Toxoplasma pseudokinase ROP5 is an allosteric inhibitor of the immunity-related GTPases. The Journal of Biological Chemistry 289, 2784927858.CrossRefGoogle ScholarPubMed
Regidor-Cerrillo, J., Gómez-Bautista, M., Pereira-Bueno, J., Adúriz, G., Navarro-Lozano, V., Risco-Castillo, V., Fernández-García, A., Pedraza-Díaz, S. and Ortega-Mora, L. M. (2008). Isolation and genetic characterization of Neospora caninum from asymptomatic calves in Spain. Parasitology 135, 16511659.CrossRefGoogle ScholarPubMed
Regidor-Cerrillo, J., Gómez-Bautista, M., Del Pozo, I., Jiménez-Ruiz, E., Aduriz, G. and Ortega-Mora, L. M. (2010). Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Veterinary Research 41, 52.CrossRefGoogle Scholar
Regidor-Cerrillo, J., Gómez-Bautista, M., Sodupe, I., Aduriz, G., Álvarez-García, G., Del Pozo, I. and Ortega-Mora, L. M. (2011). In vitro invasion efficiency and intracellular proliferation rate comprise virulence-related phenotypic traits of Neospora caninum . Veterinary Research 42, 41.CrossRefGoogle ScholarPubMed
Regidor-Cerrillo, J., Álvarez-García, G., Pastor-Fernández, I., Marugán-Hernández, V., Gómez-Bautista, M. and Ortega-Mora, L. M. (2012). Proteome expression changes among virulent and attenuated Neospora caninum isolates. Journal of Proteomics 75, 23062318.CrossRefGoogle ScholarPubMed
Reid, A. J., Vermont, S. J., Cotton, J. A., Harris, D., Hill-Cawthorne, G. A., Konen-Waisman, S., Latham, S. M., Mourier, T., Norton, R., Quail, M. A., Sanders, M., Shanmugam, D., Sohal, A., Wasmuth, J. D., Brunk, B., Grigg, M. E., Howard, J. C., Parkinson, J., Roos, D. S., Trees, A. J., Berriman, M., Pain, A. and Wastling, J. M. (2012). Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Pathogens 8, e1002567.CrossRefGoogle ScholarPubMed
Risco-Castillo, V., Fernández-García, A., Zaballos, A., Aguado-Martínez, A., Hemphill, A., Rodríguez-Bertos, A., Álvarez-García, G. and Ortega-Mora, L. M. (2007). Molecular characterisation of BSR4, a novel bradyzoite-specific gene from Neospora caninum . International Journal for Parasitology 37, 887896.CrossRefGoogle ScholarPubMed
Rojo-Montejo, S., Collantes-Fernández, E., Blanco-Murcia, J., Rodríguez-Bertos, A., Risco-Castillo, V. and Ortega-Mora, L. M. (2009). Experimental infection with a low virulence isolate of Neospora caninum at 70 days gestation in cattle did not result in foetopathy. Veterinary Research 40, 49.CrossRefGoogle Scholar
Schmittgen, T. D. and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 3, 11011108.CrossRefGoogle Scholar
Schneider, A. G., Abi Abdallah, D. S., Butcher, B. A. and Denkers, E. Y. (2013). Toxoplasma gondii triggers phosphorylation and nuclear translocation of dendritic cell STAT1 while simultaneously blocking IFNgamma-induced STAT1 transcriptional activity. PLoS ONE 8, e60215.CrossRefGoogle ScholarPubMed
Sinai, A. P. and Joiner, K. A. (2001). The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. The Journal of Cell Biology 154, 95108.CrossRefGoogle ScholarPubMed
Sohn, C. S., Cheng, T. T., Drummond, M. L., Peng, E. D., Vermont, S. J., Xia, D., Cheng, S. J., Wastling, J. M. and Bradley, P. J. (2011). Identification of novel proteins in Neospora caninum using an organelle purification and monoclonal antibody approach. PLoS ONE 6, e18383.CrossRefGoogle ScholarPubMed
Steinfeldt, T., Konen-Waisman, S., Tong, L., Pawlowski, N., Lamkemeyer, T., Sibley, L. D., Hunn, J. P. and Howard, J. C. (2010). Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii . PLoS Biology 8, e1000576.CrossRefGoogle ScholarPubMed
Straub, K. W., Cheng, S. J., Sohn, C. S. and Bradley, P. J. (2009). Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cellular Microbiology 11, 590603.CrossRefGoogle ScholarPubMed
Talevich, E. and Kannan, N. (2013). Structural and evolutionary adaptation of rhoptry kinases and pseudokinases, a family of coccidian virulence factors. BMC Evolutionary Biology 13, 117.CrossRefGoogle ScholarPubMed
Vonlaufen, N., Muller, N., Keller, N., Naguleswaran, A., Bohne, W., McAllister, M. M., Bjorkman, C., Muller, E., Caldelari, R. and Hemphill, A. (2002). Exogenous nitric oxide triggers Neospora caninum tachyzoite-to-bradyzoite stage conversion in murine epidermal keratinocyte cell cultures. International Journal for Parasitology 32, 12531265.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Pastor-Fernandez supplementary material

Pastor-Fernandez supplementary material 1

Download Pastor-Fernandez supplementary material(PDF)
PDF 124 KB
Supplementary material: File

Pastor-Fernandez supplementary material

Pastor-Fernandez supplementary material 2

Download Pastor-Fernandez supplementary material(File)
File 8 MB
8
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Characterization of the Neospora caninum NcROP40 and NcROP2Fam-1 rhoptry proteins during the tachyzoite lytic cycle
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Characterization of the Neospora caninum NcROP40 and NcROP2Fam-1 rhoptry proteins during the tachyzoite lytic cycle
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Characterization of the Neospora caninum NcROP40 and NcROP2Fam-1 rhoptry proteins during the tachyzoite lytic cycle
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *