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Immunological characterization of Neospora caninum cyclophilin

Published online by Cambridge University Press:  05 January 2012

KYOHKO KAMEYAMA ,
MAKI NISHIMURA ,
MYAGMARSUREN PUNSANTSOGVOO ,
HANY M. IBRAHIM ,
XUENAN XUAN ,
HIDEFUMI FURUOKA  and
YOSHIFUMI NISHIKAWA
KYOHKO KAMEYAMA
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
MAKI NISHIMURA
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
MYAGMARSUREN PUNSANTSOGVOO
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
HANY M. IBRAHIM
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
XUENAN XUAN
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
HIDEFUMI FURUOKA
Affiliation:
Division of Pathobiological Science, Department of Basic Veterinary Medicine, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080-8555, Japan
YOSHIFUMI NISHIKAWA*
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
*
*Corresponding author: National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan. Tel: +81 155 49 5886. Fax: +81 155 49 5643. E-mail: nisikawa@obihiro.ac.jp
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Summary

Neospora caninum is an intracellular parasite that poses a unique ability to infect a variety of cell types by causing host cell migration. Although previous studies demonstrated that parasite-derived proteins could trigger host cell migration, the related molecules have yet to be determined. Our study aimed to investigate the relationship between Neospora-derived molecules and host cell migration using recombinant protein of N. caninum cyclophilin (NcCyp). Indirect fluorescent antibody test revealed that NcCyp was expressed in the tachyzoite cytosol. Furthermore, NcCyp release from extracellular parasites was detected by sandwich enzyme-linked immunosorbent assay in a time-dependent manner. Recombinant NcCyp caused the cysteine–cysteine chemokine receptor 5-dependent migration of murine and bovine cells. Furthermore, immunohistochemistry indicated that NcCyp was consistently detected in tachyzoites distributed within or around the brain lesions. In conclusion, N. caninum-derived cyclophilin appears to contribute to host cell migration, thereby maintaining parasite/host interactions.

Keywords

Neospora caninumcyclophilincell migration
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 294 - 301
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aliberti, J., Valenzuela, J. G., Carruthers, V. B., Hieny, S., Andersen, J., Charest, H., Reis e Sousa, C., Fairlamb, A., Ribeiro, J. M. and Sher, A. (2003). Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nature Immunology 4, 485–490. doi: 10.1038/ni915.CrossRefGoogle ScholarPubMed
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. doi: 10.1016/S0020-7519(99)00141-1.Google Scholar
Bjerkas, I., and Presthus, J. (1989). The neuropathology in toxoplasmosis-like infection caused by a newly recognized cyst-forming sporozoon in dogs. Acta Pathologica, Microbiologica, et Immunologica Scandinavica 97, 459–468.Google Scholar
Boysen, P., Klevar, S., Olsen, I. and Storset, A. K. (2006). The protozoan Neospora caninum directly triggers bovine NK cells to produce gamma interferon and to kill infected fibroblasts. Infection and Immunity 74, 953–960. doi: 10.1128/IAI.74.2.953-960.2006.Google Scholar
Dubey, J. P. and Lindsay, D. S. (1993). Neosporosis. Parasitology Today 9, 452–458. doi: 10.1016/0169-4758(93)90099-2.Google Scholar
Gottstein, B., Hentrich, B., Wyss, R., Thur, B., Busato, A., Stark, K. D. and Muller, N. (1998). Molecular and immunodiagnostic investigations on bovine neosporosis in Switzerland. International Journal for Parasitology 28, 679–691. doi: 10.1016/S0020-7519(98)00006-X.Google Scholar
Hamilton, G. S. and Steiner, J. P. (1998). Immunophilins: beyond immunosuppression. Journal of Medicinal Chemistry 41, 5119–5143. doi: 10.1021/jm980307x.Google Scholar
Handschumacher, R. E., Harding, M. W., Rice, J., Drugge, R. J. and Speicher, D. W. (1984). Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 2, 544–547. doi: 10.1126/science.6238408.CrossRefGoogle Scholar
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. doi: 10.1017/S0031182006000485.Google Scholar
High, K. P., Joiner, K. A. and Handschumacher, R. E. (1994). Isolation, cDNA sequences, and biochemical characterization of the major cyclosporin-binding proteins of Toxoplasma gondii. The Journal of Biological Chemistry 12, 9105–9112.CrossRefGoogle Scholar
Huang, P., Liao, M., Zhang, H., Lee, E. G., Nishikawa, Y. and Xuan, X. (2007). Dense-granule protein NcGRA7, a new marker for the serodiagnosis of Neospora caninum infection in aborting cows. Clinical and Vaccine Immunology 14, 1640–1643. doi: 10.1128/CVI.00251-07.CrossRefGoogle ScholarPubMed
Ibrahim, H. M., Bannai, H., Xuan, X. and Nishikawa, Y. (2009). Toxoplasma gondii cyclophilin 18-mediated production of nitric oxide induces bradyzoite conversion in a CCR5-dependent manner. Infection and Immunity 77, 3686–3695. doi: 10.1128/IAI.00361-09.Google Scholar
Ibrahim, H. M., Xuan, X. and Nishikawa, Y. (2010). Toxoplasma gondii cyclophilin 18 regulates the proliferation and migration of murine macrophages and spleen cells. Clinical and Vaccine Immunology 17, 1322–1329. doi: 10.1128/CVI.00128-10.Google Scholar
Marks, J., Lundén, A., Harkins, D. and Innes, E. (1998). Identification of Neospora antigens recognized by CD4+ T cells and immune sera from experimentally infected cattle. Parasite Immunology 20, 303–309. doi: 10.1046/j.1365-3024.Google Scholar
Mineo, T. W., Oliveira, C. J., Silva, D. A., Oliveira, L. L., Abatepaulo, A. R., Ribeiro, D. P., Ferreira, B. R., Mineo, J. R. and Silva, J. S. (2010). Neospora caninum excreted/secreted antigens trigger CC-chemokine receptor 5-dependent cell migration. International Journal for Parasitology 40, 797–805. doi: 10.1016/j.ijpara.2009.12.003.Google Scholar
Nishikawa, Y., Kousaka, Y., Fukumoto, S., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2000 b). Delivery of Neospora caninum surface protein, NcSRS2 (Nc-p43), to mouse using recombinant vaccinia virus. Parasitology Research 86, 934–939. doi: 10.1007/s004360000267.Google Scholar
Nishikawa, Y., Makala, L., Otsuka, H., Mikami, T. and Nagasawa, H. (2002). Mechanisms of apoptosis in murine fibroblasts by two intracellular protozoan parasites, Toxoplasma gondii and Neospora caninum. Parasite Immunology 24, 347–354. doi: 10.1046/j.1365-3024.2002.00476.x.Google Scholar
Nishikawa, Y., Mishima, M., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2001 a). Interferon-gamma-induced apoptosis in host cells infected with Neospora caninum. Parasitology 123, 25–31.Google Scholar
Nishikawa, Y., Tragoolpua, K., Inoue, N., Makala, L., Nagasawa, H., Otsuka, H. and Mikami, T. (2001 b). In the absence of endogenous gamma interferon, mice acutely infected with Neospora caninum succumb to a lethal immune response characterized by inactivation of peritoneal macrophages. Clinical and Diagnostic Laboratory Immunology 8, 811–817. doi: 10.1128/CDLI.8.4.811-817.2001.Google Scholar
Nishikawa, Y., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2000 a). Monoclonal antibody inhibition of Neospora caninum tachyzoite invasion into host cells. International Journal for Parasitology 30, 51–58. doi: 10.1016/S0020-7519(99)00162-9.CrossRefGoogle ScholarPubMed
Nishikawa, Y., Zhang, H., Ibrahim, H. M., Yamada, K., Nagasawa, H. and Xuan, X. (2010). Roles of CD122+ cells in resistance against Neospora caninum infection in a murine model. Journal of Veterinary Medical Science 72, 1275–1282. doi: 10.1292/jvms.10-0068.Google Scholar
Persson, E. K., Agnarson, A. M., Lambert, H., Hitziger, N., Yagita, H., Chambers, B. J., Barragan, A. and Grandien, A. (2007). Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxoplasma gondii. The Journal of Immunology 179, 8357–8365.Google Scholar
Strohbusch, M., Müller, N., Hemphill, A., Margos, M., Grandgirard, D., Leib, S., Greif, G. and Gottstein, B. (2009). Neospora caninum and bone marrow-derived dendritic cells: parasite survival, proliferation, and induction of cytokine expression. Parasite Immunology 31, 366–372. doi: 10.1111/j.1365-3024.2009.01112.x.Google Scholar
Tuo, W., Fetterer, R. H., Davis, W. C., Jenkins, M. C. and Dubey, J. P. (2005 a). Neospora caninum antigens defined by antigen-dependent bovine CD4+ T cells. The Journal of Parasitology 91, 564–568. doi: 10.1645/GE-386R.Google Scholar
Tuo, W., Fetterer, R., Jenkins, M. and Dubey, J. P. (2005 b). Identification and characterization of Neospora caninum cyclophilin that elicits gamma interferon production. Infection and Immunity 73, 5093–5100. doi: 10.1128/IAI.73.8.5093-5100.2005.Google Scholar
Yarovinsky, F., Andersen, J. F., King, L. R., Caspar, P., Aliberti, J., Golding, H. and Sher, A. (2004). Structural determinants of the anti-HIV activity of a CCR5 antagonist derived from Toxoplasma gondii. The Journal of Biological Chemistry 279, 53635–53642. doi: 10.1074/jbc.M410550200.CrossRefGoogle ScholarPubMed