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Identification of a Nosema bombycis (Microsporidia) spore wall protein corresponding to spore phagocytosis

Published online by Cambridge University Press:  15 July 2011

SHUNFENG CAI ,
XINGMENG LU ,
HAIHONG QIU ,
MINGQIAN LI  and
ZHENZHEN FENG
SHUNFENG CAI
Affiliation:
Laboratory of Invertebrate Pathology, Zhejiang University, Hangzhou 310029, China
XINGMENG LU*
Affiliation:
Laboratory of Invertebrate Pathology, Zhejiang University, Hangzhou 310029, China
HAIHONG QIU
Affiliation:
Laboratory of Invertebrate Pathology, Zhejiang University, Hangzhou 310029, China
MINGQIAN LI
Affiliation:
Laboratory of Invertebrate Pathology, Zhejiang University, Hangzhou 310029, China
ZHENZHEN FENG
Affiliation:
Laboratory of Invertebrate Pathology, Zhejiang University, Hangzhou 310029, China
*
*Corresponding author: Fax: +86 571 86971697. E-mail: [email protected]
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Summary

Life-cycle stages of the microsporidia Nosema bombycis, the pathogen causing silkworm pebrine, were separated and purified by an improved method of Percoll-gradient centrifugation. Soluble protein fractions of late sporoblasts (spore precursor cells) and mature spores were analysed by two-dimensional polyacrylamide gel electrophoresis (2D-PAGE). Protein spots were recovered from gels and analysed by mass spectrometry. The most abundant differential protein spot was identified by database search to be a hypothetical spore wall protein. Using immunoelectron microscopy, we demonstrated that HSWP5 is localized to the exospore of mature spores and renamed it as spore wall protein 5 (NbSWP5). Further spore phagocytosis assays indicated that NbSWP5 can protect spores from phagocytic uptake by cultured insect cells. This spore wall protein may function both for structural integrity and in modulating host cell invasion.

Keywords

MicrosporidiaNosema bombycis2D-PAGEspore wall proteinsporoblastphagocytosis
Type
Research Article
Information
Parasitology , Volume 138 , Issue 9 , August 2011 , pp. 1102 - 1109
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Aimanianda, V., Bayry, J., Bozza, S., Kniemeyer, O., Perruccio, K., Elluru, S. R., Clavaud, C., Paris, S., Brakhage, A. A., Kaveri, S. V., Romani, L. and Latge, J. P. (2009). Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature, London 460, 1117–1121.CrossRefGoogle ScholarPubMed
Becnel, J. J. and Andreadis, T. G. (1999). Microsporidia in insect. In The Microsporidia and Microsporidiosis (ed. Wittner, M and Weiss, L. M.), pp. 447–501. ASM Press, Washington, D. C., USA.Google Scholar
Bohne, W., Ferguson, D. J., Kohler, K. and Gross, U. (2000). Developmental expression of a tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infection and Immunity 68, 2268–2275.CrossRefGoogle ScholarPubMed
Brosson, D., Kuhn, L., Delbac, F., Garin, J., Vivares, C. P. and Texier, C. (2006). Proteomic analysis of the eukaryotic parasite Encephalitozoon cuniculi (microsporidia): a reference map for proteins expressed in late sporogonial stages. Proteomics 6, 3625–3635.CrossRefGoogle ScholarPubMed
Brosson, D., Kuhn, L., Prensier, G., Vivares, C. P. and Texier, C. (2005). The putative chitin deacetylase of Encephalitozoon cuniculi: a surface protein implicated in microsporidian spore-wall formation. FEMS Microbiology Letters 247, 81–90.CrossRefGoogle ScholarPubMed
Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M., Grainger, M., Haynes, J. D., Moch, J. K., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y. M., Gardner, M. J., Holder, A. A., Sinden, R. E., Yates, J. R. and Carucci, D. J. (2002). A proteomic view of the Plasmodium falciparum life cycle. Nature, London 419, 520–526.Google ScholarPubMed
Hayman, J. R., Hayes, S. F., Amon, J. and Nash, T. E. (2001). Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis. Infection and Immunity 69, 7057–7066.CrossRefGoogle ScholarPubMed
Katinka, M. D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., Barbe, V., Peyretaillade, E., Brottier, P., Wincker, P., Delbac, F., El Alaoui, H., Peyret, P., Saurin, W., Gouy, M., Weissenbach, J. and Vivares, C. P. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature, London 414, 450–453.CrossRefGoogle ScholarPubMed
Keeling, P. J. (2003). Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genetics and Biology 38, 298–309.CrossRefGoogle ScholarPubMed
Li, Y. H., Wu, Z. L., Pan, G. Q., He, W. W., Zhang, R. Z., Hu, J. H. and Zhou, Z. Y. (2009). Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. International Journal for Parasitology 39, 391–398.CrossRefGoogle ScholarPubMed
Mei, L. L. and Jin, W. (1989). Studies on Nosema bombycis and Nosema hemerophila. Acta Sericologica Sinica 15, 135–138.Google Scholar
Naegli, C. (1857). Ueber die neue Krankheit der Seidenraupe und verwandte Organismen. Botanischer Zeitschrift 15, 760–761.Google Scholar
Peuvel-Fanget, I., Polonais, V., Brosson, D., Texier, C., Kuhn, L., Peyret, P., Vivares, C. and Delbac, F. (2006). EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. International Journal for Parasitology 36, 309–318.CrossRefGoogle ScholarPubMed
Seider, K., Heyken, A., Luttich, A., Miramon, P. and Hube, B. (2010). Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Current Opinion in Microbiology 13, 392–400.CrossRefGoogle ScholarPubMed
Seleznev, K. V., Issi, I. V., Dolgikh, V. V., Belostotskaya, G. B., Antonova, O. A. and Sokolova, J. J. (1995). Fractionation of different life-cycle stages of microsporidia Nosema-grylli from cruckets gryllus-bimaculatus by centrifugation in percoll density gradent for biochemical-research. Journal of Eukaryotic Microbiology 42, 288–292.CrossRefGoogle Scholar
Southern, T. R., Jolly, C. E., Lester, M. E. and Hayman, J. R. (2007). EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro. Eukaryotic Cell 6, 1354–1362.CrossRefGoogle ScholarPubMed
Sprague, V., Becnel, J. J. and Hazard, E. I. (1992). Taxonomy of phylum microspora. Critical Reviews in Microbiology 18, 285–395.CrossRefGoogle ScholarPubMed
Taupin, V., Metenier, G., Vivares, C. P. and Prensier, G. (2006). An improved procedure for Percoll gradient separation of sporogonial stages in Encephalitozoon cuniculi (Microsporidia). Parasitology Research 99, 708–714.CrossRefGoogle ScholarPubMed
Wu, Z., Li, Y., Pan, G., Zhou, Z. and Xiang, Z. (2009). SWP25, A novel protein associated with the Nosema bombycis endospore. The Journal of Eukaryotic Microbiology 56, 113–118.CrossRefGoogle ScholarPubMed
Wu, Z. L., Li, Y. H., Pan, G. Q., Tan, X. H., Hu, J. H., Zhou, Z. Y. and Xiang, Z. H. (2008). Proteomic analysis of spore wall proteins and identification of two spore wall proteins from Nosema bombycis (Microsporidia). Proteomics 8, 2447–2461.CrossRefGoogle ScholarPubMed
Xiang, H., Pan, G., Zhang, R., Xu, J., Li, T., Li, W., Zhou, Z. and Xiang, Z. (2010). Natural selection maintains the transcribed LTR retrotransposons in Nosema bombycis. Journal of Genetics and Genomics 37, 305–314.CrossRefGoogle ScholarPubMed
Xu, J. S., Pan, G. Q., Fang, L., Li, J., Tian, X. J., Li, T., Zhou, Z. Y. and Xiang, Z. H. (2006 a). The varying microsporidian genome: Existence of long-terminal repeat retrotransposon in domesticated silkworm parasite Nosema bombycis. International Journal for Parasitology 36, 1543–1544.CrossRefGoogle ScholarPubMed
Xu, Y., Takvorian, P., Cali, A., Wang, F., Zhang, H., Orr, G. and Weiss, L. M. (2006 b). Identification of a new spore wall protein from Encephalitozoon cuniculi. Infection and Immunity 74, 239–247.CrossRefGoogle ScholarPubMed
Zhang, F., Lu, X. M., Kumar, V. S., Zhu, H., Chen, H., Chen, Z. and Hong, J. (2007). Effects of a novel anti-exospore monoclonal antibody on microsporidial Nosema bombycis germination and reproduction in vitro. Parasitology 134, 1551–1558.CrossRefGoogle ScholarPubMed