Specific antibody responses against Neospora caninum recombinant rNcGRA7, rNcSAG4, rNcBSR4 and rNcSRS9 proteins are correlated with virulence in mice

Parasitology

Volumn 140, Issue 5, 2013, Pages 569-579

  Jiménez Ruiz, Elena ^a   Bech Sàbat, Gregori ^a   Álvarez García, Gema ^a   Regidor Cerrillo, Javier ^a   Hinojal Campaña, Laura ^a   Ortega Mora, Luis M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

antibody response; BALB c mice; Neospora caninum; rNcBSR4; rNcGRA7; rNcSAG4; rNcSRS9; virulence

Indexed keywords

IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; RECOMBINANT PROTEIN; RECOMBINANT RNCBSR 4 PROTEIN; RECOMBINANT RNCGRA 7 PROTEIN; RECOMBINANT RNCSAG 4 PROTEIN; RECOMBINANT RNCSRS 9 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BRADYZOITE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; MOUSE; NEOSPORA CANINUM; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; TACHYZOITE;

ANIMALS; ANTIBODIES, PROTOZOAN; CLONING, MOLECULAR; FEMALE; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; NEOSPORA; PREGNANCY; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; VIRULENCE;

EID: 84875134708     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012002041     Document Type: Article

References (41)

1. Aguado-Martínez, A., Álvarez-García, G., Fernández-García, A., Risco-Castillo, V., Arnaiz-Seco, I., Rebordosa-Trigueros, X., Navarro-Lozano, V. and Ortega-Mora, L. M. (2008). Usefulness of rNcGRA7- and rNcSAG4-based ELISA tests for distinguishing primoinfection, recrudescence, and chronic bovine neosporosis. Veterinary Parasitology 157, 182-195. doi: 10.1016/j.vetpar.2008.08.002.
2. Aguado-Martínez, A., Ortega-Mora, L. M., Álvarez- García, G., Rodríguez-Marco, S., Risco-Castillo, V., Marugán-Hernández, V. and Fernández-García, A. (2009a). Stage-specific expression of Nc SAG4 as a marker of chronic Neospora caninum infection in a mouse model. Parasitology 136, 757-764. doi: 10.1017/S0031182009006076.
3. Aguado-Martínez, A., Álvarez-García, G., Fernández-García, A., Risco-Castillo, V., Marugán- Hernández, V. and Ortega-Mora, L. M. (2009b). Failure of a vaccine using immunogenic recombinant proteins rNcSAG4 and rNcGRA7 against neosporosis in mice. Vaccine 27, 7331- 7338. doi: 10.1016/j.vaccine.2009.09.050.
4. Aguado-Martínez, A., Álvarez-García, G., Schares, G., Risco- Castillo, V., Fernández-García, A., Marugán-Hernández, V. and Ortega-Mora, L. M. (2010). Characterisation of NcGRA7 and NcSAG4 proteins: immunolocalisation and their role in the host cell invasion by Neospora caninum tachyzoites. Acta Parasitologica 55, 304-312. doi: 10.2478/s11686-010-0056-9.
5. Al-Qassab, S., Reichel, M. P., Ivens, A. and Ellis, J. T. (2009). Genetic diversity amongst isolates of Neospora caninum, and the development of a multiplex assay for the detection of distinct strains. Molecular and Cellular Probes 23, 132-139. doi: 10.1016/j.mcp.2009.01.006.
6. 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, 41-50. doi: 10.1017/ S0031182006001284.
7. Bartley, P. M., Wright, S., Sales, J., Chianini, F., Buxton, D. and Innes, E. A. (2006). Long-term passage of tachyzoites in tissue culture can attenuate virulence of Neospora caninum in vivo. Parasitology 133, 421-432. doi: 0.1017/S0031182006000539.
8. Basso,W., Schares, S., Barwald, A., Herrmann, D. C., Conraths, F. J., Pantchev, N., Vrhovec, M. G. and Schares, G. (2009). Molecular comparison of Neospora caninum oocyst isolates from naturally infected dogs with cell culture-derived tachyzoites of the same isolates using nested polymerase chain reaction to amplify microsatellite markers. Veterinary Parasitology 160, 43-50. doi: 10.1016/j.vetpar.2008.10.085.
9. Caspe, S. G., Moore, D. P., Leunda, M. R., Cano, D. B., Lischinsky, L., Regidor-Cerrillo, J., Alvarez-Garcia, G., Echaide, I. G., Bacigalupe, D., Ortega Mora, L. M., Odeon, A. C. and Campero, C. M. (2012). The Neospora caninum-Spain 7 isolate induces placental damage, fetal death and abortion in cattle when inoculated in early gestation. Veterinary Parasitology 189(2-4), 171-811. doi: 10.1016/ j.vetpar.2012.04.034.
10. Collantes-Fernandez, E., Arrighi, R. B., Alvarez-Garcia, 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. doi: 10.1371/journal.pone.0032123.
11. Collantes-Fernández, E., López-Pérez, I., Álvarez-García, G. and Ortega-Mora, L. M. (2006). Temporal distribution and parasite load kinetics in blood and tissues during Neospora caninum infection in mice. Infection and Immunity 74, 2491-2494. doi: 10.1128/IAI.74.4.2491- 2494.2006.
12. Dubey, J. P. and Schares, G. (2011). Neosporosis in animals - the last five years. Veterinary Parasitology 180, 90-108. doi: 10.1016/j.vetpar.2011. 05.031.
13. Dubey, J. P., Buxton, D. and Wouda, W. (2006). Pathogenesis of bovine neosporosis. Journal of Comparative Pathology 134, 267-289. doi: 10.1016/ j.jcpa.2005.11.004.
14. Dubey, J. P., Schares, G. and Ortega-Mora, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology Reviews 20, 323-367. doi: 10.1128/CMR.00031-06.
15. Fernández-García, A., Risco-Castillo, V., Zaballos, A., Álvarez- 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, 89-97. doi: 10.1016/j.molbiopara.2005.08.019.
16. Hemphill, A., Felleisen, R., Connolly, B., Gottstein, B., Hentrich, B. and Muller, N. (1997). Characterization of a cDNA-clone encoding Nc-p43, a major Neospora caninum tachyzoite surface protein. Parasitology 115, 581-590. doi: 10.1017/S0031182097001650.
17. Hemphill, A., Gajendran, N., Sonda, S., Fuchs, N., Gottstein, B., Hentrich, B. and Jenkins, M. (1998). Identification and characterisation of a dense granule-associated protein in Neospora caninum tachyzoites. International Journal for Parasitology 28, 429-438. doi: 10.1016/S0020-7519 (97)00193-8.
18. Hill, R. D., Gouffon, J. S., Saxton, A. M. and Su, C. (2012). Differential gene expression in mice infected with distinct Toxoplasma strains. Infection and Immunity 80, 968-974. doi: 10.1128/IAI.05421-11.
19. Jiménez-Ruiz, E., Álvarez-García, G., Aguado-Martínez, A., Salman, H., Irache, J. M., Marugán- Hernández, V. and Ortega- Mora, L. M. (2012). Low efficacy of NcGRA7, NcSAG4, NcBSR4 and NcSRS9 formulated in poly-epsilon-caprolactone against Neospora caninum infection in mice.Vaccine 30, 4983-4992. doi: 10.1016/j.vaccine.2012.05.033.
20. Kim, S. K. and Boothroyd, J. C. (2005). Stage-specific expression of surface antigens by Toxoplasma gondii as a mechanism to facilitate parasite persistence. Journal of Immunology 174, 8038-8048.
21. Kim, S. K., Karasov, A. and Boothroyd, J. C. (2007). Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine. Infection and Immunity 75, 1626-1634. doi: 10.1128/ IAI.01862-06.
22. Miller, C. M., Quinn, H. E., Windsor, P. A. and Ellis, J. T. (2002). Characterisation of the first Australian isolate of Neospora caninum from cattle. Australian Veterinary Journal 80, 620-625. doi: 10.1111/j.1751- 0813.2002.tb10967.x.
23. Pardini, L., Maksimov, P., Herrmann, D. C., Bacigalupe, D., Rambeaud, M., Machuca, M., More, G., Basso, W., Schares, G. and Venturini, M. C. (2012). Evaluation of an in-house TgSAG1 (P30) IgG ELISA for diagnosis of naturally acquired Toxoplasma gondii infection in pigs. Veterinary Parasitology 189, 204-210. doi: 10.1016/j.vetpar.2012.4.014.
24. Pedraza-Díaz, S., Marugán-Hernández, V., Collantes-Fernández, E., Regidor-Cerrillo, J., Rojo-Montejo, S., Gómez-Bautista, M. and Ortega-Mora, L. M. (2009). Microsatellite markers for the molecular characterization of Neospora caninum: application to clinical samples. Veterinary Parasitology 166, 38-46. doi: 10.1016/j.vetpar.2009.07.043.
25. 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, 1057-1068. doi: 10.1017/ S0031182009991855.
26. 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 cellculture changes: an argument in favor of its clonal population structure. Journal of Parasitology 91, 507-510. doi: 10.1645/GE-381R1.
27. Quinn, H. E., Miller, C. M., Ryce, C., Windsor, P. A. and Ellis, J. T. (2002). Characterization of an outbred pregnant mouse model of Neospora caninum infection. Journal of Parasitology 88, 691-696. doi: 10.1645/0022- 3395(2002)088[0691:COAOPM]2.0.CO;2.
28. Rettigner, C., De Meerschman, F., Focant, C., Vanderplasschen, A. and Losson, B. (2004). The vertical transmission following the reactivation of a Neospora caninum chronic infection does not seem to be due to an alteration of the systemic immune response in pregnant CBA/Ca mice. Parasitology 128, 149-160.
29. Regidor-Cerrillo, J., Pedraza-Díaz, S., Gómez-Bautista, M. and Ortega-Mora, L. M. (2006). Multilocus microsatellite analysis reveals extensive genetic diversity in Neospora caninum. Journal of Parasitology 92, 517-524. doi: 10.1645/GE-713R.1.
30. 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. doi: 10.1051/ vetres/2010024.
31. 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. doi: 10.1186/1297-9716-42-41.
32. 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, 2306-2318. doi: 10.1016/j.jprot.2012.01.039.
33. 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, 887-896. doi: 10.1016/j. ijpara.2007.02.003.
34. Risco-Castillo, V., Marugán-Hernández, V., Fernadez-García, A., Aguado-Martínez, A., Jiménez-Ruiz, E., Rodriguez-Marco, S., Álvarez-García, G. and Ortega-Mora, L. M. (2011). Identification of a gene cluster for cell-surface genes of the SRS superfamily in Neospora caninum and characterization of the novel SRS9 gene. Parasitology 138, 1832-1842. doi: 10.1017/S0031182011001351.
35. 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. doi: 10.1051/vetres/2009032.
36. Rojo-Montejo, S., Collantes-Fernandez, E., Rodriguez-Marcos, S., Perez-Zaballos, F., Lopez-Perez, I., Prenafeta, A. and Ortega- Mora, L. M. (2011). Comparative efficacy of immunization with inactivated whole tachyzoites versus a tachyzoite-bradyzoite mixture against neosporosis in mice. Parasitology 138, 1372-1383. doi: 10.1017/S0031182011001156.
37. Saeij, J. P., Boyle, J. P., Coller, S., Taylor, S., Sibley, L. D., Brooke- Powell, E. T., Ajioka, J.W. and Boothroyd, J. C. (2006). Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314, 1780-1783. doi: 10.1126/science.1133690.
38. Schock, A., Innes, E. A., Yamane, I., Latham, S. M. and Wastling, J. M. (2001). Genetic and biological diversity among isolates of Neospora caninum. Parasitology 123, 13-23. doi: 10.1017/ S003118200100796X.
39. Sousa, S., Ajzenberg, D., Vilanova, M., Costa, J. and Darde, M. L. (2008). Use of GRA6-derived synthetic polymorphic peptides in an immunoenzymatic assay to serotype Toxoplasma gondii in human serum samples collected from three continents. Clinical and Vaccine Immunology 15, 1380-1386. doi: 10.1128/CVI.00186-08.
40. Walsh, C. P., Vemulapalli, R., Sriranganathan, N., Zajac, A. M., Jenkins, M. C. and Lindsay, D. S. (2001). Molecular comparison of the dense granule proteins GRA6 and GRA7 of Neospora hughesi and Neospora caninum. International Journal for Parasitology 31, 253-258. doi: 10.1016/ S0020-7519(00)00169-7.
41. Zhao, J. C., Zhao, Z. D., Wang, W. and Gao, X. M. (2005). Prokaryotic expression, refolding, and purification of fragment 450-650 of the spike protein of SARS-coronavirus. Protein Expression and Purification 39, 169- 174. doi: 10.1016/j.pep.2004.10.004.