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Identification of a novel chitin-binding spore wall protein (NbSWP12) with a BAR-2 domain from Nosema bombycis (microsporidia)

Published online by Cambridge University Press:  07 August 2013

JIE CHEN ,
LINA GENG ,
MENGXIAN LONG ,
TIAN LI ,
ZHI LI ,
DONGLIN YANG ,
CHAO MA ,
HAIJING WU ,
ZHENGANG MA  and
CHUNFENG LI
...Show all authors
JIE CHEN
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
LINA GENG
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
MENGXIAN LONG
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
TIAN LI
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
ZHI LI
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China College of Life Sciences, Chongqing Normal University, Chongqing 400047, China
DONGLIN YANG
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
CHAO MA
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
HAIJING WU
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
ZHENGANG MA
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
CHUNFENG LI
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
GUOQING PAN
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
ZEYANG ZHOU*
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China College of Life Sciences, Chongqing Normal University, Chongqing 400047, China
*
*Corresponding author: State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China. E-mail: [email protected]
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Summary

The spore wall of Nosema bombycis plays an important role in microsporidian pathogenesis. Protein fractions from germinated spore coats were analysed by two-dimensional polyacrylamide gel electrophoresis and MALDI-TOF/TOF mass spectrometry. Three protein spots were identified as the hypothetical spore wall protein NbHSWP12. A BAR-2 domain (e-value: 1.35e-03) was identified in the protein, and an N-terminal protein-heparin interaction motif, a potential N-glycosylation site, and 16 phosphorylation sites primarily activated by protein kinase C were also predicted. The sequence analysis suggested that Nbhswp12 and its homologous genes are widely distributed among microsporidia. Additionally, Nbhswp12 gene homologues share similar sequence features. An indirect immunofluorescence analysis showed that NbHSWP12 localized to the spore wall, and thus we renamed it spore wall protein 12 (NbSWP12). Moreover, NbSWP12 could adhere to deproteinized N. bombycis chitin coats that were obtained by hot alkaline treatment. This novel N. bombycis spore wall protein may function in a structural capacity to facilitate microsporidial spore maintenance.

Keywords

MicrosporidiaNosema bombycisspore wall proteinBAR domaindeproteinized spore coat
Type
Research Article
Information
Parasitology , Volume 140 , Issue 11 , September 2013 , pp. 1394 - 1402
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Balguerie, A., Sivadon, P., Bonneu, M. and Aigle, M. (1999). Rvs167p, the budding yeast homolog of amphiphysin, colocalizes with actin patches. Journal of Cell Science 112, 2529–2537.CrossRefGoogle ScholarPubMed
Bigliaedi, E., Selmi, M. G., Lupetti, P., Corona, S., Gatti, S., Scaglia, M. and Sacchi, L. (1996). Microsporidian spore wall: ultrastructural findings on Encephalitozoon hellem exospore. Journal of Eukaryotic Microbiology 43, 181–186.CrossRefGoogle 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
Briza, P., Winkler, G., Kalchhauser, H. and Breitenbach, M. (1986). Dityrosine is a prominent component of the yeast ascospore wall. A proof of its structure. Journal of Biological Chemistry 261, 4288–4294.CrossRefGoogle Scholar
Briza, P., Ellinger, A., Winkler, G. and Breitenbach, M. (1988). Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan. Journal of Biological Chemistry 263, 11569–11574.CrossRefGoogle ScholarPubMed
Brosson, D., Kuhn, L., Prensier, G., Vivarès, 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
Cai, S., Lu, X., Qiu, H., Li, M. and Feng, Z. (2011). Identification of a Nosema bombycis (microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology 138, 1102–1109.CrossRefGoogle ScholarPubMed
Coluccio, A. E., Rodriguez, R. K., Kernan, M. J. and Neiman, A. M. (2008). The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS ONE 3, e2873.CrossRefGoogle ScholarPubMed
De Groot, P. W., Ram, A. F. and Klis, F. M. (2005). Features and functions of covalently linked proteins in fungal cell walls. Fungal Genetics and Biology 42, 657–675.CrossRefGoogle ScholarPubMed
Desportes, I., Charpentier, Y. L., Galian, A., Bernard, F., Cochand-Priollet, B., Lavergne, A., Ravisse, P. and Modigliani, R. (1985). Occurrence of a new microsporidan: Enterocytozoon bieneusi ng, n. sp., in the enterocytes of a human patient with AIDS. Journal of Eukaryotic Microbiology 32, 250–254.Google Scholar
Didier, E. S., Snowden, K. F. and Shadduck, J. A. (1998). Biology of microsporidian species infecting mammals. Advances in Parasitology 40, 283–320.CrossRefGoogle ScholarPubMed
Frixione, E., Ruiz, L., Santillán, M., de Vargas, L. V., Tejero, J. M. and Undeen, A. H. (1992). Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell Motility and the Cytoskeleton 22, 38–50.CrossRefGoogle Scholar
Harada, A., Furuta, B., Takeuchi, K.-I., Itakura, M., Takahashi, M. and Umeda, M. (2000). Nadrin, a novel neuron-specific GTPase-activating protein involved in regulated exocytosis. Journal of Biological Chemistry 275, 36885–36891.CrossRefGoogle Scholar
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
Lee, E., Marcucci, M., Daniell, L., Pypaert, M., Weisz, O. A., Ochoa, G.-C., Farsad, K., Wenk, M. R. and De Camilli, P. (2002). Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193–1196.CrossRefGoogle ScholarPubMed
Lesage, G. and Bussey, H. (2006). Cell wall assembly in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 70, 317–343.CrossRefGoogle ScholarPubMed
Li, Y., Wu, Z., Pan, G., He, W., Zhang, R., Hu, J. and Zhou, Z. (2009). Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. International Journal for Parasitology 39, 391–398.CrossRefGoogle ScholarPubMed
Li, Z., Pan, G., Li, T., Huang, W., Chen, J., Geng, L., Yang, D., Wang, L. and Zhou, Z. (2012). SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryotic Cell 11, 229–237.CrossRefGoogle ScholarPubMed
Manners, D. J., Masson, A. J. and Patterson, J. C. (1973). The structure of a β-(1→3)-d-glucan from yeast cell walls. Biochemical Journal 135, 19.CrossRefGoogle Scholar
Nägeli, K. (1857). Uber die neue krankheit der seidenraupe und verwandte organismen. Botanischer Zeitschrift 15, 760–761.Google Scholar
Orlean, P. (1997). Biogenesis of yeast wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Cell Cycle and Cell Biology (ed. Pringle, J. R., Broach, J. R. and Jones, E. W.), pp. 229–362. Cold Spring Harbor Monograph Series 21. Cold Spring Harbour, NY: Cold Spring Harbor Laboratory.Google Scholar
Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J. G., Evans, P. R. and McMahon, H. T. (2004). Bar domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499.CrossRefGoogle ScholarPubMed
Peuvel-Fanget, I., Polonais, V., Brosson, D., Texier, C., Kuhn, L., Peyret, P., Vivarès, 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
Polonais, V., Mazet, M., Wawrzyniak, I., Texier, C., Blot, N., El Alaoui, H. and Delbac, F. (2010). The human microsporidian Encephalitozoon hellem synthesizes two spore wall polymorphic proteins useful for epidemiological studies. Infection and Immunity 78, 2221–2230.CrossRefGoogle ScholarPubMed
Shadduck, J. A. and Polley, M. B. (1978). Some factors influencing the in vitro infectivity and replication of Encephalitozoon cuniculi. Journal of Eukaryotic Microbiology 25, 491–496.Google ScholarPubMed
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
Takei, K., Slepnev, V. I., Haucke, V. and De Camilli, P. (1999). Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nature Cell Biology 1, 33–39.CrossRefGoogle ScholarPubMed
Vavra, J. and Larsson, J. (1999). Structure of the Microsporidia (ed. Wittner, M. and Weiss, L. M.), pp. 7–84. ASM Press, Washington, DC, USA.Google Scholar
Weber, R. and Bryan, R. T. (1994). Microsporidial infections in immunodeficient and immunocompetent patients. Clinical Infectious Diseases 19, 517–521.CrossRefGoogle ScholarPubMed
Wu, Z., Li, Y., Pan, G., Tan, X., Hu, J., Zhou, Z. and Xiang, Z. (2008). Proteomic analysis of spore wall proteins and identification of two spore wall proteins from Nosema bombycis (microsporidia). Proteomics 8, 2447–2461.CrossRefGoogle ScholarPubMed
Wu, Z., Li, Y., Pan, G., Zhou, Z. and Xiang, Z. (2009). SWP25, a novel protein associated with the Nosema bombycis endospore. Journal of Eukaryotic Microbiology 56, 113–118.CrossRefGoogle ScholarPubMed
Xu, J., Pan, G., Fang, L., Li, J., Tian, X., Li, T., Zhou, Z. and Xiang, Z. (2006 a). The varying microsporidian genome: existence of long-terminal repeat retrotransposon in domesticated silkworm parasite Nosema bombycis. International Journal for Parasitology 36, 1049–1056.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
Zhu, F., Shen, Z., Hou, J., Zhang, J., Geng, T., Tang, X., Xu, L. and Guo, X. (2013). Identification of a protein interacting with the spore wall protein SWP26 of Nosema bombycis in a cultured BmN cell line of silkworm. Infection, Genetics and Evolution 17, 38–45.CrossRefGoogle Scholar