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

Volumn 137, Issue 2, 2010, Pages 229-240

  Debache, K ^a   Guionaud, C ^a   Alaeddine, F ^a   Hemphill, A ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Intra nasal; Intraperitoneal; Mice; Recombinant Neospora caninum antigen; Tachyzoites; Vaccination

Indexed keywords

CHOLERA TOXIN; GENOMIC DNA; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOLOGICAL ADJUVANT; PROTOZOAL DNA; PROTOZOAL RNA; PROTOZOAL VACCINE; RECOMBINANT ANTIGEN; RECOMBINANT NEOSPORA CANINUM ANTIGEN NCMAG 1; RECOMBINANT NEOSPORA CANINUM ANTIGEN NCPD 1; RECOMBINANT NEOSPORA CANINUM ANTIGEN NCROP 2; RNA; SAPONIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; BRAIN INFECTION; C57BL 6 MOUSE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL INFECTION; FEMALE; HUMAN; HUMAN CELL; INFECTION PREVENTION; MOLECULAR CLONING; MOUSE; NEOSPORA CANINUM; NEOSPOROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE LOCALIZATION; PARASITE VIABILITY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TACHYZOITE; VACCINATION;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; BRAIN; BRAIN DISEASES; COCCIDIOSIS; DISEASE MODELS, ANIMAL; FEMALE; INJECTIONS, INTRAPERITONEAL; MICE; MICE, INBRED C57BL; NEOSPORA; PROTOZOAN VACCINES; RECOMBINANT PROTEINS; VACCINATION;

ANIMALIA; ESCHERICHIA COLI; MUS; NEOSPORA CANINUM;

EID: 77949653962     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009991259     Document Type: Article

References (52)

1. Aguado-Martinez, A., Ortege-Mora, L. M., Alvarez-Garcia, G., Rodriguez-Marco, S., Risco-Castillo, V., Marugan-Hernandez, V. and Fernandez-Garcia, A. (2009). Stage-specific expression of NcSAG4 as a marker of chronic Neospora caninum infection in a mouse model. Parasitology 136, 757-764.
2. Alaeddine, F., Keller, N., Leepin, A. and Hemphill, A. (2005). Reduced infection and protection from clinical signs of cerebral neosporosis in C57BL/6 mice vaccinated with recombinant microneme antigen NcMIC1. Journal of Parasitology 91, 657-665.
3. Arakawa, T., Tsuboi, T., Kishimoto, A., Sattabongkot, J., Suwanabun, N., Rungruang, T., Matsumoto, Y., Tsuji, N., Hisaeda, H., Stowers, A., Shimabukuro, I., Sato, Y. and Torii, M. (2003). Serum antibodies induced by intranasal immunization of mice with Plasmodium vivax Pvs25 coadministred with cholera toxin completely block parasite transmission to mosquitoes. Vaccine 21, 3143-3148.
4. Arakawa, T., Komesu, A., Otsuki, H., Sattanbongkot, J., Udomsangpetch, R., Matsumoto, Y., Tsuji, N., Wu, Y., Torii, M. and Tsuboi, T. (2005). Nasal immunization with a malaria transmission-blocking vaccine candidate; Pfs25 induces complete protective immunity in mice against field isolates of Plasmodium falciparum. Infection and Immunity 73, 7375-7380.
5. Baszler, T. V., Long, M. T., McElwain, T. F. and Mathison, B. A. (1999). Interferon-gamma and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. International Journal for Parasitology 29, 1635-1646.
6. Baszler, T. V., McElwain, T. F. and Mathison, B. A. (2000). Immunization of BALB/c mice with killed Neospora caninum tachyzoite antigen induces a type 2 immune response and exacerbates encephalitis and neurological disease. Clinical and Diagnostic Laboroatory Immunology 7, 893-898.
7. Bonenfant, C., Dimier-Poisson, I., Velge-Roussel, F., Buzoni-Gatel, D., Del Giudice, G., Rappuoli, R. and Bout, D. (2001). Intranasal immunization with SAG1 and non-toxic mutant heat-labile enterotoxins protects mice against Toxoplasma gondii. Infection and Immunity 69, 1605-1612.
8. Byun, Y., Ohmura, M., Fijihashi, K., Yamamota, S., McGhee, J. R., Udaka, S., Kiyono, H., Takeda, Y., Kohsaka, T. and Yuki, Y. (2001). Nasal immunization with E. coli verotoxin 1 (VT1)-B subunit and a non-toxic mutant of cholera toxin elicits serum neutralizing antibodies. Vaccine 19, 2061-2070.
9. Cannas, A., Naguleswaran, A., Müller, N., Gottstein, B., Eperon, S. and Hemphill, A. (2003a). Vaccination of mice against experimental N. caninum infection using NcSAG1- and NcSRS2-based recombinant antigens and DNA-vaccines. Parasitology 126, 303-312.
10. Cannas, A., Naguleswaran, A., Muller, N., Gottstein, B. and Hemphill, A. (2003b). Reduced cerebral infection of Neospora caninum-infected mice after vaccination with recombinant microneme protein NcMIC3 and ribi adjuvant. Journal of Parasitology 89, 44-50.
11. Cho, J., Chung, W., Song, K., Na, B., Kang, S., Song, C. and Kim, T. (2005). Protective efficacy of vaccination with Neospora caninum multiple recombinant antigens against experimental Neospora caninum infection. Korean Journal for Parasitology 1, 19-25.
12. Debache, K., Alaeddine, F., Guionaud, C., Monney, T., Müller, 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 May 15: Epub ahead of print
13. 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, 1455-1463.
14. Dimier-Poisson, I., Aline, F., Bout, D. and Mevelec, M. N. (2006). Induction of protective immunity against toxoplasmosis in mice by immunization with Toxoplasma RNA. Vaccine 24, 1705-1709.
15. Dubey, J. P., Hattel, A. L., Lindsay, D. S. and Topper, M. J. (1988). Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. Journal of the American Veterinary Medical Association 193, 1259-1263.
16. Dubey, J. P. and Lindsay, D. S. (1996). A review of Neospora caninum and neosporosis. Veterinary Parasitology 67, 1-59.
17. Dubey, J. P., Schares, G. and Ortega, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology. Microbiology Reviews 20, 323-367.
18. Ellis, J. T., Miller, C., Quinn, H., Ryce, C. and Reichel, M. P. (2008). Evaluation of recombinant proteins of Neospora caninum as vaccine candidates (in a mouse model). Vaccine 26, 5989-5996.
19. Garcia, J. L., Navarro, I. T., Biazzono, L., Freire, R. L., da Silva Guimaraes, J., Cryssafidis, A. L., Bugni, F. M., Leme da Cunha, I. A., Hamada, F. N. and Ferriera Dias, R. C. (2007). Protective activity against oocyst shedding in cats vaccinated with crude rhoptry proteins of the Toxoplasma gondii by the intranasal route. Veterinary Parasitology 145, 197-206.
20. Gondim, L. F., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. (2004). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159-161.
21. Haldorson, G. J., Mathison, B. A., Wenberg, K., Conrad, P. A., Dubey, J. P., Trees, A. J., Yamane, I. and Baszler, T. V. (2005). Immunization with native surface protein NcSRS2 induces a Th2 immune response and reduces congenital Neospora caninum transmission in mice. International Journal for Parasitology 35, 1407-1415.
22. Hemphill, A., Gottstein, B. and Kaufmann, H. (1996). Adhesion and invasion of bovine endothelial cells by Neospora caninum. Parasitology 112, 183-197.
23. Hemphill, A., Vonlaufen, N. and Naguleswaran, A. (2006). Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum. Parasitology 133, 261-278.
24. Hirunpetcharat, C., Stanisic, D., Liu, X. Q., Vadolas, J., Strugnell, R. A., Lee, R., Miller, L. H., Kaslow, D. C. and Good, M. F. (1998). Intranasal immunization with yeast-expressed 19 kDa carboxyl-terminal fragment of Plasmodium yoelii merozoite surface protein-1 (yMSP119) induces protective immunity to blood stage malaria infection in mice. Parasite Immunology 20, 413-420.
25. Hiroi, T., Iwatani, K., Iijima, H., Kodama, S., Yanagita, M. and Kiyono, H. (1998). Nasal immune system: distinctive Th0 and Th1/Th2 type environments in murine nasal-associated lymphoid tissues and nasal passage, respectively. European Journal of Immunology 28, 3346-3353.
26. Igarashi, M., Kano, F., Tamekun, i K., Machado, R. Z., Navarro, I. T., Vidotto, O., Vidotto, M. C. and Garcia, J. L. (2007). Toxoplasma gondii: Evaluation of an intranasal vaccine using recombinant proteins against brain cyst formation in BALB/c mice. Experimental Parasitology 118, 386-392
27. Innes, E. A. (2007). The host-parasite relationship in pregnant cattle infected with Neospora caninum. Parasitology 134, 1903-1910.
28. Innes, E. A. and Mattsson, J. G. (2007). Neospora caninum emerges from the shadow of Toxoplasma gondii. Trends in Parasitology 23, 43-44.
29. Innes, E. A. and Vermeulen, A. N. (2006). Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora. Parasitology 133, S145-S168.
30. Khan, I. A., Schwartzman, J. D., Fonseka, S. and Kasper, L. H. (1997). Neospora caninum: role of immune cytokines in host immunity. Experimental Parasitology 85, 23-34.
31. Klevar, S., Kulberg, S., Boysen, P., Storset, A. K., Moldal, T., Bjorkman, C. and Olsen, I. (2007). Natural killer cells act as early responders in an experimental infection with Neospora caninum in calves. International Journal for Parasitology 37, 329-339.
32. Liao, M., Ma, L., Bannai, H., Lee, E. G., Xie, Z., Tang, X., Zhang, H., Xuan, X. and Fujisaki, K. (2006). Identification of a protein disulfide isomerase of Neospora caninum in excretory-secretory products and its IgA binding and enzymatic activities. Veterinary Parasitology 139, 47-56.
33. Liddell, S., Jenkins, M. C., Collica, C. M. and Dubey, J. P. (1999). Prevention of vertical transfer of Neospora caninum in BALB/c mice by vaccination. Journal of Parasitology 85, 1072-1075.
34. McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A. and McGuire, A. M. (1998). Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 1473-1478.
35. Meek, B., Back, J. W., Klaren, V. N., Speijer, D. and Peek, R. (2002). Protein disulfide isomerase of Toxoplasma gondii is targeted by mucosal IgA antibodies in humans. FEBS Letters 522, 104-108.
36. Müller, J., Naguleswaran, A., Nüller, N. and Hemphill, A. (2008). Neospora caninum: functional inhibition of protein disulfide isomerase by the broad-spectrum anti-parasitic drug nitazoxanide and other thiazolides. Experminental Parasitology 118, 80-88.
37. Müller, N., Vonlaufen, N., Gianinazzi, C., Leib, S. L. and Hemphill, A. (2002). Application of real time fluorescent PCR for quantitative assessment of Neospora caninum infections in organotypic slice cultures of rat central nervous tissue. Journal of Clinical Microbiology 40, 252-255.
38. Naguleswaran, A., Alaeddine, F., Guionaud, C., Vonlaufen, N., Sonda, S., Jenoe, P., Mevissen, M. and Hemphill, A. (2005). Neospora caninum protein disulfide isomerase is involved in tachyzoite-host cell interaction. International Journal for Parasitology 35, 1459-1472.
39. Parmley, S. F., Yang, S., Harth, G., Sibley, L. D., Sucharczuk, A. and Remington, J. S. (1994). Molecular characterization of a 65 kilodalton Toxoplasma gondii antigen expressed abundantly in the matrix of tissue cysts. Molecular and Biochemical Parasitology 66, 283-296.
40. Partidos, C. D., Beignon, A.-S., Semetey, V., Briand, J.-P. and Muller, S. (2001). The bare skin and the nose as non-invasive routes for administering peptide vaccines. Vaccine 19, 2708-2715.
41. Porgador, A., Staats, H. F., Faiola, B., Gilboa, E. and Palker, T. J. (1997). Intranasal immunization with CTL epitope peptides from HIV-1 or ovalbumin and the mucosal adjuvant cholera toxin induces peptide-specific CTLs and protection against tumor development in vivo. Journal of Immunology 158, 834-841.
42. Pinto, E. F., Pinheiro, R. O., Rayol, A., Larraga, V. and Rossi-Bergmann, B. (2004). Intranasal vaccination against cutaneous leishmaniasis with a particulated leishmanial antigen or DNA encoding LACK. Infection and Immunity 72, 4521-4527.
43. Ramamoorthy, S., Sanakkayala, N., Vemulapalli, R., Duncan, R. B., Lindsay, D. S., Schurig, G. S., Boyle, S. M., Kasimanickam, R. and Sriranganathan, N. (2007b). Prevention of lethal experimental infection of C57BL/6 mice by vaccination with Brucella abortus strain RB51 expressing Neospora caninum antigens. International Journal for Parasitology 37, 1521-1529.
44. Ramamoorthy, S., Sanakkayala, N., Vemulapalli, R., Jain, N., Lindsay, D. S., Schurig, G. S., Boyle, S. M. and Sriranganathan, N. (2007a). Prevention of vertical transmission of Neospora caninum in C57BL/6 mice vaccinated with Brucella abortus strain RB51 expressing N. caninum protective antigens. International Journal for Parasitology 37, 1531-1538.
45. Risco-Castillo, V., Fernández-Garcia, A. and Ortega-Mora, L. M. (2004). Comparative analysis of stress agents in a simplified in vitro system of Neospora caninum bradyzoite production. Journal of Parasitology 90, 466-470.
46. Srinivasan, S., Müller, J., Suana, A. and Hemphill, A. (2007). Vaccination with microneme protein NcMIC4 increases mortality in mice inoculated with Neospora caninum. Parasitology 92, 1235-1243.
47. Stanley, A. C., Buxton, D., Innes, E. A. and Huntley, J. F. (2004). Intranasal immunisation with Toxoplasma gondii tachyzoite antigen encapsulated into PLG microspheres induces humoral and cell mediated immunity in sheep. Vaccine 22, 3929-3941.
48. Strohbusch, M., Müller, N., Hemphill, A., Greif, G. and Gottstein, B. (2008a). NcGRA2 as a molecular target to assess the parasiticidal activity of toltrazuril against Neospora caninum. Parasitology 135, 1065-1073.
49. Strohbusch, M., Müller, N., Hemphill, A., Greif, G. and Gottstein, B. (2008b). NcGRA2-RT-PCR to detect live versus dead parasites in Neospora caninum infected mice. The Open Parasitology Journal 2, 64-68.
50. Vonlaufen, N., Guetg, N., Naguleswaran, A., Müller, N., Björkman, C., Schares, G., von Blumröder, D., Ellis, J. and Hemphill, A. (2004). In vitro induction of Neospora caninum bradyzoites in Vero cells reveals differential antigen expression, localization, and host cell recognition of tachyzoites and bradyzoites. Infection and Immunity 72, 576-583.
51. Williams, D. J. L. and Trees, A. J. (2006). Protecting babies: vaccine strategies to prevent foetal infection in Neospora caninum infected cattle. Parasite Immunology 28, 61-67.
52. Williams, D. J., Guy, C. S., Smith, R. F., Ellis, J. T., Björkman, C., Reichel, M. P. and Trees, A. J. (2007). Immunization of cattle with live tachyzoites of Neospora caninum confers protection against fetal death. Infection and Immunity 75, 1343-1348.