Nbseptin2 Expression Pattern and Its Interaction with NbPTP1 during Microsporidia Nosema bombycis Polar Tube Extrusion.
Germination
localization
membrane-associated protein
polar cap
septin
Journal
The Journal of eukaryotic microbiology
ISSN: 1550-7408
Titre abrégé: J Eukaryot Microbiol
Pays: United States
ID NLM: 9306405
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
23
04
2019
revised:
19
06
2019
accepted:
10
07
2019
pubmed:
25
7
2019
medline:
12
9
2020
entrez:
24
7
2019
Statut:
ppublish
Résumé
Nosema bombycis (Nb) is a deadly species of microsporidia capable of causing pébrine, leading to heavy losses in sericulture. Germination is an important biological event in the invasion process of microsporidia. Septins, a family of membrane-associated proteins, play a critical role in tissue invasion and have been recognized as a virulence factor in numerous pathogens. Previous work in our laboratory has shown that Nosema bombycis septin2 (Nbseptin2) interacts with subtilisin-like protease 2 (NbSLP2). Herein, we found that Nbseptin2 was mainly associated with the plasma membrane in spores. Following spore germination, Nbseptin2 was found to co-localize with polar tube protein 1 (NbPTP1) at the polar cap and proximal zone of the polar tube. Co-immunoprecipitation and yeast two-hybrid analysis further confirmed that Nbseptin2 interacted with NbPTP1. The translocation and interaction of Nbseptin2 in the spores suggest that Nbseptin2 may play a significant role in microsporidia polar tube extrusion process. Our findings improve understanding of the mechanisms underlying microsporidia germination.
Substances chimiques
Carrier Proteins
0
Fungal Proteins
0
Septins
EC 3.6.1.-
Banques de données
GENBANK
['EOB13962']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
45-53Informations de copyright
© 2019 International Society of Protistologists.
Références
Bigliardi, E. & Sacchi, L. 2001. Cell biology and invasion of the microsporidia. Microbes Infect., 3:373-379.
Bouzahzah, B., Nagajyothi, F., Ghosh, K., Takvorian, P. M., Cali, A., Tanowitz, H. B. & Weiss, L. M. 2010. Interactions of Encephalitozoon cuniculi polar tube proteins. Infect. Immun., 78:2745-2753.
Bridges, A. A. & Gladfelter, A. S. 2014. Fungal pathogens are platforms for discovering novel and conserved septin properties. Curr. Opin. Microbiol., 20:42-48.
Cali, A., Kotler, D. P. & Orenstein, J. M. 1993. Septata intestinalis NG, n. sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients. J. Eukaryot. Microbiol., 40:101-112.
Cali, A. & Takvorian, P. M. 1999. Developmental morphology and life cycles of the microsporidia. In: Wittner, M. & Weiss, L. (ed.), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. p. 85-128.
Cali, A., Weiss, L. M. & Takvorian, P. M. 2002. Brachiola algerae spore membrane systems, their activity during extrusion, and a new structural entity, the multilayered interlaced network, associated with the polar tube and the sporoplasm. J. Eukaryot. Microbiol., 49:164-174.
Chen, J., Guo, W., Dang, X., Huang, Y., Liu, F., Meng, X., An, Y., Long, M., Bao, J., Zhou, Z., Xiang, Z. & Pan, G. 2017. Easy labeling of proliferative phase and sporogonic phase of microsporidia Nosema bombycis in host cells. PLoS ONE, 12:e0179618. https://doi.org/10.1371/journal.pone.0179618.
Chen, A. H., Xie, Q. R., Lin, Y. H., Xu, H. J., Shang, W. J., Zhang, J., Zhang, D. M., Zheng, W. H., Li, G. P. & Wang, Z. H. 2016. Septins are involved in nuclear division, morphogenesis and pathogenicity in Fusarium graminearum. Fungal Genet. Biol., 94:79-87.
Dagdas, Y. F., Yoshino, K., Dagdas, G., Ryder, L. S., Bielska, E., Steinberg, G. & Talbot, N. J. 2012. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science, 336:1590-1595.
Douglas, L. M., Alvarez, F. J., McCreary, C. & Konopka, J. B. 2005. Septin function in yeast model systems and pathogenic fungi. Eukaryot. Cell, 4:1503-1512.
Franzen, C. 2004. Microsporidia: how can they invade other cells? Trends Parasitol., 20:275-279.
Frixione, E., Ruiz, L., Santillán, M., de Vargas, L. V., Tejero, J. M. & Undeen, A. H. 1992. Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell Motil. Cytoskeleton, 22:38-50.
Gilden, J. & Krummel, M. F. 2010. Control of cortical rigidity by the cytoskeleton: emerging roles for septins. Cytoskeleton, 67:477-486.
Han, B., Polonais, V., Sugi, T., Yakubu, R., Takvorian, P. M., Cali, A., Maier, K., Long, M., Levy, M., Tanowitz, H. B., Pan, G., Delbac, F., Zhou, Z. & Weiss, L. M. 2017. The role of microsporidian polar tube protein 4 (PTP4) in host cell infection. PLoS Pathog., 13:e1006341. https://doi.org/10.1371/journal.ppat.1006341.
Han, B. & Weiss, L. M. 2017. Microsporidia: obligate intracellular pathogens within the fungal kingdom. Microbiol. Spectr., 5:17.
Hernández-Rodríguez, Y. & Momany, M. 2012. Posttranslational modifications and assembly of septin heteropolymers and higher-order structures. Curr. Opin. Microbiol., 15:660-668.
Keohane, E. M., Orr, G. A., Takvorian, P. M., Cali, A., Tanowitz, H. B., Wittner, M. & Weiss, L. M. 1999. Polar tube proteins of microsporidia of the family Encephalitozoonidae. J. Eukaryot. Microbiol., 46:1-5.
Keohane, E. M. & Weiss, L. M. 1999. The structure, function, and composition of the microsporidian polar tube. In: Wittner, M. & Weiss, L. (ed.), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. p. 196-224.
Lee, S. C., Corradi, N., Byrnes, E. J., Torres-Martinez, S., Dietrich, F. S., Keeling, P. J. & Heitman, J. 2008. Microsporidia evolved from ancestral sexual fungi. Curr. Biol., 18:1675-1679.
Leipe, D. D., Wolf, Y. I., Koonin, E. V. & Aravind, L. 2002. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol., 317:41-72.
Li, Z., Pan, G. Q., Li, T., Huang, W., Chen, J., Geng, L. N., Yang, D. L., Wang, L. L. & Zhou, Z. Y. 2012. SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryot. Cell, 11:229-237.
Liu, F. Y., Ma, Q., Dang, X. Q., Wang, Y., Song, Y., Meng, X. Z., Bao, J. L., Chen, J., Pan, G. Q. & Zhou, Z. Y. 2017. Identification of a new subtilisin-like protease NbSLP2 interacting with cytoskeletal protein septin in microsporidia Nosema bombycis. J. Invertebr. Pathol., 148:110-117.
Mathis, A., Weber, R. & Deplazes, P. 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev., 18:423-445.
Meseroll, R. A., Occhipinti, P. & Gladfelter, A. S. 2013. Septin phosphorylation and coiled-coil domains function in cell and septin ring morphology in the filamentous fungus Ashbya gossypii. Eukaryot. Cell, 12:182-193.
Momany, M. & Talbot, N. J. 2017. Septins focus cellular growth for host infection by pathogenic fungi. Front. Cell Dev. Biol., 5:33.
Mostowy, S. & Cossart, P. 2012. Septins: the fourth component of the cytoskeleton. Nat. Rev. Mol. Cell Biol., 13:183.
Oh, Y. & Bi, E. 2011. Septin structure and function in yeast and beyond. Trends Cell Biol., 21:141-148.
Pan, G. Q., Bao, J. L., Ma, Z. G., Song, Y., Han, B., Ran, M. S., Li, C. F. & Zhou, Z. Y. 2018. Invertebrate host responses to microsporidia infections. Dev. Comp. Immunol., 83:104-113.
Pan, F., Malmberg, R. L. & Momany, M. 2007. Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol. Biol., 7:103.
Polonais, V., Prensier, G., Metenier, G., Vivares, C. P. & Delbac, F. 2005. Microsporidian polar tube proteins: highly divergent but closely linked genes encode PTP1 and PTP2 in members of the evolutionarily distant Antonospora and Encephalitozoon groups. Fungal Genet. Biol., 42:791-803.
Qian, Y., Lu, X., Jin, W. & Wang, J. 2003. Observation on the inoculation and propagation of the Nosema bombycis in BmN cell. Sci. Seric., 29:260-263.
Shioya, T., Nakamura, H., Ishii, N., Takahashi, N., Sakamoto, Y., Ozaki, N., Kobayashi, M., Okano, K., Kamada, T. & Muraguchi, H. 2013. The Coprinopsis cinerea septin Cc.Cdc3 is involved in stipe cell elongation. Fungal Genet. Biol., 58-59:80-90.
Spiliotis, E. T. & Nelson, W. J. 2006. Here come the septins: novel polymers that coordinate intracellular functions and organization. J. Cell Sci., 119:4-10.
Undeen, A. H. & Frixione, E. 1990. The role of osmotic pressure in the germination of Nosema algerae spores. J. Protozool., 37:561-567.
Vávra, J. 1976. Structure of the microsporidia. In: Bulla, L. A. & Cheng, T. C. (ed.), Biology of the Microsporidia. Springer, Boston, MA. p. 1-84.
Vavra, J. & Lukes, J. 2013. Microsporidia and ‘the art of living together’. In: Rollinson, D. (ed.), Advances in Parasitology. Academic Press, New York, NY. 82:253-319.
Warenda, A. J., Kauffman, S., Sherrill, T. P., Becker, J. A. & Konopka, J. B. 2003. Candida albicans septin mutants are defective for invasive growth and virulence. Infect. Immun., 71:4045-4051.
Weidner, E. 1972. Ultrastructural study of microsporidian invasion into cells. Z. Parasitenkd., 40:227-242.
Weiss, L. M. 2001. Microsporidia: emerging pathogenic protists. Acta Trop., 78:89-102.
Weiss, L. M., Delbac, F., Hayman, J. R., Pan, G., Dang, X. & Zhou, Z. 2014. The microsporidian polar tube and spore wall. In: Weiss, L. M. & Becnel, J. J. (ed.), Microsporidia: Pathogens of Opportunity. Ackwell Science Publ, Oxford. p. 261-306.
Wu, Z. L., Li, Y. H., Pan, G. Q., Tan, X. H., Hu, J. H., Zhou, Z. Y. & 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.
Wu, Z., Li, Y., Pan, G., Zhou, Z. & Xiang, Z. 2009. SWP25, A novel protein associated with the Nosema bombycis endospore. J. Eukaryot. Microbiol., 56:113-118.
Wu, Y. J., Long, M. X., Chen, J., Li, Z., Li, Z. H., Pan, G. Q., Li, T. & Zhou, Z. Y. 2014. Cloning and prokaryotic expression of Nosema bombycis polar tube protein 1 (NbPTP1). Sci. Seric., 2:258-264.
Xu, H., Yang, G., Zhang, J., Wang, Y., Zhang, T., Wang, N., Jiang, S., Zhang, Z. & Chen, X. 2018. Overexpression of a repressor MdMYB15L negatively regulates anthocyanin and cold tolerance in red-fleshed callus. Biochem. Biophys. Res. Commun., 500:405-410.
Yang, D., Pan, L., Peng, P., Dang, X., Li, C., Li, T., Long, M., Chen, J., Wu, Y., Du, H., Luo, B., Song, Y., Tian, R., Luo, J., Zhou, Z. & Pan, G. 2017. Interaction between SWP9 and polar tube proteins of the microsporidian Nosema bombycis and function of SWP9 as a scaffolding protein contribute to polar tube tethering to the spore wall. Infect. Immun., 85(3):e00872-16.
Yue, Y. J., Tang, X. D., Xu, L., Yan, W., Li, Q. L., Xiao, S. Y., Fu, X. L., Wang, W., Li, N. & Shen, Z. Y. 2015. Early responses of silkworm midgut to microsporidium infection - a digital gene expression analysis. J. Invertebr. Pathol., 124:6-14.