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Characterization of a novel spore wall protein NbSWP16 with proline-rich tandem repeats from Nosema bombycis (microsporidia)

Published online by Cambridge University Press:  03 November 2014

YING WANG ,
XIAOQUN DANG ,
QIANG MA ,
FANGYAN LIU ,
GUOQING PAN ,
TIAN LI  and
ZEYANG ZHOU
YING WANG
Affiliation:
State Key Laboratory of Silkworm genome Biology, Southwest University, Chongqing 400716, China
XIAOQUN DANG
Affiliation:
State Key Laboratory of Silkworm genome Biology, Southwest University, Chongqing 400716, China Laboratory of Animal Biology, Chongqing Normal University, Chongqing 400047, China
QIANG MA
Affiliation:
State Key Laboratory of Silkworm genome Biology, Southwest University, Chongqing 400716, China
FANGYAN LIU
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
TIAN LI
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 Laboratory of Animal Biology, 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

Nosema bombycis, a pathogen of silkworm pebrine, is an obligate unicellular eukaryotic parasite. It is reported that the spore wall proteins have essential functions in the adherence and infection process of microsporidia. To date, the information related to spore wall proteins from microsporidia is still limited. Here, a 44 kDa spore wall protein NbSWP16 was characterized in N. bombycis. In NbSWP16, a 25 amino acids signal peptide and 3 heparin binding motifs were predicted. Interestingly, a region that contains 3 proline-rich tandem repeats lacking homology to any known protein was also present in this protein. The immunofluorescence analysis (IFA) demonstrated that distinct fluorescent signals were detected both on the surface of mature spores and the germinated spore coats. Immunolocation by electron microscopy revealed that NbSWP16 localized on the exospore regions. Finally, spore adherence analysis indicated that spore adherence to host cell was decreased more than 20% by anti-NbSWP16 blocking compared with the negative control in vitro. In contrast with anti-NbSWP16, no remarkable decrement inhibition was detected when antibodies of NbSWP16 and NbSWP5 were used simultaneously. Collectively, these results suggest that NbSWP16 is a new exospore protein and probably be involved in spore adherence of N. bombycis.

Keywords

spore wall proteinNbSWP16tandem repeatNosema bombycis
Type
Research Article
Information
Parasitology , Volume 142 , Issue 4 , April 2015 , pp. 534 - 542
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Becnel, J. and Andreadis, T. G. (1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 447–501. ASM Press, Washington, DC, 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.Google Scholar
Cai, S. F., Lu, X. M., Qiu, H. H., Li, M. Q. and Feng, Z. Z. (2011). Identification of a Nosema bombycis (Microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology 138, 1102–1109.Google Scholar
Chen, J., Long, M. X., Li, T., Geng, L. N., Li, Z., Yang, D. L., Ma, C., Wu, H. J., Ma, Z. G., Li, C. F., Pan, G. Q. and Zhou, Z. Y. (2013). Identification of a novel chitin-binding spore wall protein (NbSWP12) with a BAR-2 domain from Nosema bombycis (microsporidia). Parasitology 140, 1394–1402.Google Scholar
Corradi, N., Gangaeva, A. and Keeling, P. J. (2008). Comparative profiling of overlapping transcription in the compacted genomes of microsporidia Antonospora locustae and Encephalitozoon cuniculi . Genomics 91, 388–393.Google Scholar
Didier, E., Snowden, K. and Shadduck, J. (1998). Biology of microsporidian species infecting mammals. Advances in Parasitology 40, 283–320.Google Scholar
Gemayel, R., Cho, J., Boeynaems, S. and Verstrepen, K. J. (2012). Beyond junk-variable tandem repeats as facilitators of rapid evolution of regulatory and coding sequences. Genes 3, 461–480.Google 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.Google Scholar
Hayman, J. R., Southern, T. R. and Nash, T. E. (2005). Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro . Infection and Immunity 73, 841–848.Google Scholar
Julenius, K., Mølgaard, A., Gupta, R. and Brunak, S. (2005). Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15, 153–164.CrossRefGoogle ScholarPubMed
Katinka, M. D. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi . Nature 414, 450–453.Google Scholar
Katti, M. V., Sami-Subbu, R., Ranjekar, P. K. and Gupta, V. S. (2000). Amino acid repeat patterns in protein sequences: their diversity and structural-functional implications. Protein Science 9, 1203–1209.Google Scholar
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.Google Scholar
Li, Z., Pan, G. Q., Li, T., Huang, W., Chen, J., Geng, L. N., Yang, D. L., Wang, L. L. and Zhou, Z. Y. (2012). SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis . Eukaryotic cell 11, 229–237.Google Scholar
Nageli, K. (1857). Uber die neue Krankheit der Seidenraupe und verwandte Organismen. Bot Z 15, 760–761.Google Scholar
Pan, G. Q., Xu, J. S., Li, T., Xia, Q. Y., Liu, S. L., Zhang, G. J., Li, S. G., Li, C. F., Liu, H. D., Yang, L., Liu, T., Zhang, X., Wu, Z. L., Fan, W., Dang, X. Q., Xiang, H., Tao, M. L., Li, Y. H., Hu, J. H., Li, Z., Lin, L. P., Luo, J., Geng, L. N., Wang, L. L., Long, M. X., Wan, Y. J., He, N. J., Zhang, Z., Lu, C., Patrick, J. K. et al. (2013). Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC genomics 14, 186.Google Scholar
Peuvel-Fanget, I., Polonais, V., Brosson, D., Texier, C., Kuhn, L., Peyret, P., Vivarè, C., 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.Google Scholar
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 Scholar
Smith, G. A., Theriot, J. A. and Portnoy, D. A. (1996). The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. Journal of Cell Biology 135, 647–660.Google Scholar
Southern, T. R., Jolly, C. E. and Russell Hayman, J. (2006). Augmentation of microsporidia adherence and host cell infection by divalent cations. FEMS Microbiology Letters 260, 143–149.Google 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
Verstrepen, K. J., Jansen, A., Lewitter, F. and Fink, G. R. (2005). Intragenic tandem repeats generate functional variability. Nature Genetics 37, 986–990.Google Scholar
Weidner, E. and Halonen, S. K. (1993). Microsporidian spore envelope keratins phosphorylate and disassemble during spore activation. Journal of Eukaryotic Microbiology 40, 783–788.CrossRefGoogle Scholar
Weidner, E., Avila, J. and Harris, J. (1992). Cytoskeletal proteins expressed by microsporidian parasites. Subcellular biochemistry. Intracellular Parasites 18, 385–399.Google Scholar
Wu, Z. L., Li, Y. H., Pan, G. Q., Tan, X. H., Hu, J. H., Zhou, Z. Y. 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.Google Scholar
Xu, Y. J., Peter, T., Ann, C., Wang, F., Zhang, H., George, O., Louis, M. W. (2006). Identification of a new spore wall protein from Encephalitozoon cuniculi . Infection and Immunity 74, 239–247.Google Scholar
Yang, D. L., Dang, X. Q., Tian, R., Long, M. X., Li, C. F., Li, T., Chen, J., Li, Z., Pan, G. Q. and Zhou, Z. Y. (2014). Development of an approach to analyze the interaction between Nosema bombycis (microsporidia) deproteinated chitin spore coats and spore wall proteins. Journal of Invertebrate Pathology 115, 1–7.Google Scholar
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