Nosema bombycis: A remarkable unicellular parasite infecting insects.
Nosema bombycis
host–pathogen interactions
microsporidia
pathobiology
silkworm
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:
02 Aug 2024
02 Aug 2024
Historique:
revised:
12
06
2024
received:
10
05
2024
accepted:
17
06
2024
medline:
3
8
2024
pubmed:
3
8
2024
entrez:
2
8
2024
Statut:
aheadofprint
Résumé
Microsporidia are opportunistic fungal-like pathogens that cause microsporidiosis, which results in significant economic losses and threatens public health. Infection of domesticated silkworms by the microsporidium Nosema bombycis causes pébrine disease, for which this species of microsporidia has received much attention. Research has been conducted extensively on this microsporidium over the past few decades to better understand its infection, transmission, host-parasite interaction, and detection. Several tools exist to study this species including the complete genome sequence of N. bombycis. In addition to the understanding of N. bombycis being important for the silkworm industry, this species has become a model organism for studying microsporidia. Research on biology of N. bombycis will contribute to the development of knowledge regarding microsporidia and potential antimicrosporidia drugs. Furthermore, this will provide insight into the molecular evolution and functioning of other fungal pathogens.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13045Subventions
Organisme : Natural Science Foundation of Chongqing, China
ID : 2022YSZX-JCX0010CSTB
Organisme : Natural Science Foundation of Chongqing, China
ID : cstc2021jcyj-msxmX1003
Organisme : Fundamental Research Funds for the Central Universities
ID : SWU-KT22033
Organisme : National Natural Science Foundation of China
ID : 32272942
Informations de copyright
© 2024 International Society of Protistologists.
Références
Baig, M., Datta, R.K., Nataraju, B., Samson, M.V. & Sivaprasad, V. (1992) Protein A‐linked latex antisera test for the detection of Nosema bombycis Naegeli spores. Journal of Invertebrate Pathology, 60, 312–313.
Bao, J., Liu, L., An, Y., Ran, M., Ni, W., Chen, J. et al. (2019) Nosema bombycis suppresses host hemolymph melanization through secreted serpin 6 inhibiting the prophenoloxidase activation cascade. Journal of Invertebrate Pathology, 168, 107260.
Caccia, S., Casartelli, M. & Tettamanti, G. (2019) The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell and Tissue Research, 377, 505–525.
Cai, S., Lu, X., Qiu, H., Li, M. & Feng, Z. (2011) Identification of a Nosema bombycis (microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology, 138, 1102–1109.
Cali, A. (1971) Morphogenesis in the genus Nosema. In: Proc. IVth Int. Colloq. Insect Pathology, Vol. 4, Japan, pp. 104–112.
Chakrabarti, S. & Manna, B. (2008) Effect of microsporidian infection on reproductive potentiality on mulberry silkworm, Bombyx mori L. (Lepidoptera: Bombycidae) in different seasons. International Journal of Industrial Entomology, 17, 157–163.
Chandrakanth, N., Makwana, P., Satish, L., Rabha, M. & Sivaprasad, V. (2021) Chapter 3—molecular approaches for detection of pebrine disease in sericulture. In: Gurtler, V. & Subrahmanyam, G. (Eds.) Methods in microbiology. Vol. 49. Methods in silkworm microbiology. San Diego: Academic Press, pp. 47–77.
Chen, G., Wang, W., Chen, H., Dai, W., Peng, X., Li, X. et al. (2017) Functional characterization of an aquaporin from a microsporidium, Nosema bombycis. PLoS One, 12, e0181703.
Chen, J., Hu, C. & Jin, W. (1988) Production of monoclonal antibodies to Pebrine protozoa of domestic silkworm and their application. Acta Sericologica Sin. China, 14(3).
Chen, J., Geng, L., Long, M., Li, T., Li, Z., Yang, D. et al. (2013) Identification of a novel chitin‐binding spore wall protein (NbSWP12) with a BAR‐2 domain from Nosema bombycis (microsporidia). Parasitology, 140, 1394–1402.
Chen, J., Li, Z., Sheng, X., Huang, J., Sun, Q., Huang, Y. et al. (2022) Heterologous expressed NbSWP12 from microsporidia Nosema bombycis can bind with phosphatidylinositol 3‐phosphate and affect vesicle genesis. Journal of Fungi, 8, 764.
Chen, P., Feng, L., Pan, M., Wan, Y., Zhu, R., Zhou, K. et al. (1996) A study on serologic testing techniques for microparticle disease in the silkworm, Bombyx mori III‐N.b carbon agglutination reaction for the detection of microparticles in the original female moths. Newsletter Sericultural Science, 2, 12–16.
Chen, Y., Wei, E., Chen, Y., He, P., Wang, R., Wang, Q. et al. (2022) Identification and subcellular localization analysis of membrane protein Ycf 1 in the microsporidian Nosema bombycis. PeerJ, 10, e13530.
Cheng, T., Zhang, Y., Liu, C., Xu, P., Gao, Z., Xia, Q. et al. (2008) Identification and analysis of toll‐related genes in the domesticated silkworm, Bombyx mori. Developmental and Comparative Immunology, 32, 464–475.
Corradi, N. (2015) Microsporidia: eukaryotic intracellular parasites shaped by gene loss and horizontal gene transfers. Annual Review of Microbiology, 69, 167–183.
Dai, W.J., Chen, G., Peng, X.R., Li, X.L., Ma, L., Tang, X.D. et al. (2017) Staining and discrimination of Nosema bombycis spores with fluorescent brightener 28 and propidium iodide. Science Sericulture, 43, 62–67.
dan Ulat, R.R.B.I., dalam Makmal, R., Ramli, S., Zainal‐Abidin, B.A.H. & Idris, A. (2011) In vivo production of Nosema bombycis spores and their efficacies against diamondback moth and beet armyworm larvae in laboratory conditions. Sains Malaysiana, 40(4), 311–316.
Dang, X., Pan, G., Li, T., Lin, L., Ma, Q., Geng, L. et al. (2013) Characterization of a subtilisin‐like protease with apical localization from microsporidian Nosema bombycis. Journal of Invertebrate Pathology, 112, 166–174.
Dang, X. & Zhou, Z. (2014) Prokaryotic expression and subcellular localization of ADP/ATP carrier protein in microsporidian Nosema bombycis. Acta Entomologica Sinica, 57, 300–307.
de Albuquerque, N., Ebert, D. & Haag, K.L. (2020) Transposable element abundance correlates with mode of transmission in microsporidian parasites. Mobile DNA, 11, 19.
Dolgikh, V.V., Senderskiy, I.V., Timofeev, S.A., Zhuravlyov, V.S., Dolgikh, A.V., Seliverstova, E.V. et al. (2022) Construction of scFv antibodies against the outer loops of the microsporidium Nosema bombycis ATP/ADP‐transporters and selection of the fragment efficiently inhibiting parasite growth. International Journal of Molecular Sciences, 23, 15307.
Dolgikh, V.V., Senderskiy, I.V., Zhuravlyov, V.S., Ignatieva, A.N., Timofeev, S.A., Ismatullaeva, D.A. et al. (2022) Molecular detection of microsporidia Vairimorpha ceranae and Nosema bombycis growth in the lepidopteran Sf9 cell line. Protistology, 16, 21–29.
Dolgikh, V.V., Tsarev, A.A., Timofeev, S.A. & Zhuravlyov, V.S. (2019) Heterologous overexpression of active hexokinases from microsporidia Nosema bombycis and Nosema ceranae confirms their ability to phosphorylate host glucose. Parasitology Research, 118, 1511–1518.
Dong, Z., Gao, N., Deng, B., Huang, X., Hu, C., Chen, P. et al. (2022) Stable transformation of fluorescent proteins into Nosema bombycis by electroporation. Parasites & Vectors, 15, 141.
Dong, Z., Zheng, N., Hu, C., Deng, B., Fang, W., Wu, Q. et al. (2021) Nosema bombycis microRNA‐like RNA 8 (Nb‐milR8) increases fungal pathogenicity by modulating BmPEX16 gene expression in its host, Bombyx mori. Microbiology Spectrum, 9, e01048‐21.
Dong, Z., Zheng, N., Hu, C., Huang, X., Chen, P., Wu, Q. et al. (2021) Genetic bioengineering of overexpressed guanylate binding protein family BmAtlastin‐n enhances silkworm resistance to Nosema bombycis. International Journal of Biological Macromolecules, 172, 223–230.
Eskov, E.K., Eskova, M.D., Rozhenkov, A.S. & Shestakova, E.V. (2022) Damage to the intestinal medium of honey bees with Nosema. Cell and Tissue Biology, 16, 92–96.
Esvaran, V.G., Gupta, T., Nayaka, A.R.N., Sivaprasad, V. & Ponnuvel, K.M. (2018) Molecular characterization of Nosema bombycis methionine aminopeptidase 2 (MetAP2) gene and evaluation of anti‐microsporidian activity of Fumagilin‐B in silkworm Bombyx mori. 3 Biotech, 8, 386.
Ferguson, S. & Lucocq, J. (2019) The invasive cell coat at the microsporidian Trachipleistophora hominis–host cell interface contains secreted hexokinases. MicrobiologyOpen, 8, e00696.
Franzen, C. (2008) Microsporidia: a review of 150 years of research. The Open Parasitology Journal, 2, 1–34.
Frixione, E., Ruiz, L. & Undeen, A.H. (1994) Monovalent cations induce microsporidian spore germination in vitro. The Journal of Eukaryotic Microbiology, 41, 464–468.
Fu, Z., He, X., Cai, S., Liu, H., He, X., Li, M. et al. (2016) Quantitative PCR for detection of Nosema bombycis in single silkworm eggs and newly hatched larvae. Journal of Microbiological Methods, 120, 72–78.
Ghosh, K. & Weiss, L.M. (2009) Molecular diagnostic tests for microsporidia. Interdisciplinary Perspectives on Infectious Diseases, 2009, e926521.
Guo, R., Cao, G., Lu, Y., Xue, R., Kumar, D., Hu, X. et al. (2016) Exogenous gene can be integrated into Nosema bombycis genome by mediating with a non‐transposon vector. Parasitology Research, 115, 3093–3098.
Han, B., Zhou, K., Li, Z., Sun, B., Ni, Q., Meng, X. et al. (2016) Characterization of the first fungal Glycosyl hydrolase family 19 Chitinase (NbchiA) from Nosema bombycis (Nb). The Journal of Eukaryotic Microbiology, 63, 37–45.
Han, M.‐S. & Watanabe, H. (1988) Transovarial transmission of two microsporidia in the silkworm, Bombyx mori, and disease occurrence in the progeny population. Journal of Invertebrate Pathology, 51, 41–45.
Haque, M.A., Hollister, W.S., Willcox, A. & Canning, E.U. (1993) The Antimicrosporidial activity of Albendazole. Journal of Invertebrate Pathology, 62, 171–177.
Harvey, W.R. & Zerahn, K. (1972) Active transport of potassium and other alkali metals by the isolated Midgut of the silkworm. In: Bronner, F. & Kleinzeller, A. (Eds.) Current topics in membranes and transport, Vol. 3. New York and London: Academic Press, pp. 367–410.
Hayman, J.R., Southern, T.R. & 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.
He, P., Chen, H., Sun, J., Wang, Q., Tang, X., Zhang, Y. et al. (2022) Use of DNA nanosensors based on upconverting nanoparticles for detection of Nosema bombycis by fluorescence resonance energy transfer. Folia Microbiologia, 67, 419–425.
He, Q., Luo, J., Xu, J., Meng, X., Pan, G., Li, T. et al. (2020) In‐vitro cultivation of Nosema bombycis sporoplasms: a method for potential genetic engineering of microsporidia. Journal of Invertebrate Pathology, 174, 107420.
He, Q., Luo, J., Xu, J., Wang, C., Meng, X., Pan, G. et al. (2020) Morphology and transcriptome analysis of Nosema bombycis Sporoplasm and insights into the initial infection of microsporidia. mSphere, 5, e00958‐19. Available from: https://doi.org/10.1128/msphere.00958‐19
He, Z., Ni, Q., Song, Y., Wang, R., Tang, Y., Wu, Y. et al. (2019) Development of a nucleic acid lateral flow strip for rapid, visual detection of Nosema bombycis in silkworm eggs. Journal of Invertebrate Pathology, 164, 59–65.
Heinz, E., Hacker, C., Dean, P., Mifsud, J., Goldberg, A.V., Williams, T.A. et al. (2014) Plasma membrane‐located purine nucleotide transport proteins are key components for host exploitation by microsporidian intracellular parasites. PLoS Pathogens, 10, e1004547.
Hu, C., Dong, Z., Deng, B., Wu, Q., Chen, P., Lu, C. et al. (2021) MicroRNA‐6498‐5p inhibits Nosema bombycis proliferation by downregulating BmPLPP2 in Bombyx mori. Journal of Fungi, 7, 1051.
Hu, N., Dong, Z.‐Q., Long, J.‐Q., Zheng, N., Hu, C.‐W., Wu, Q. et al. (2021) Transcriptome analysis reveals changes in silkworm energy metabolism during Nosema bombycis infection. Pesticide Biochemistry and Physiology, 174, 104809.
Hua, X., Xu, W., Ma, S. & Xia, Q. (2021) STING‐dependent autophagy suppresses Nosema bombycis infection in silkworms, Bombyx mori. Developmental & Comparative Immunology, 115, 103862.
Huang, J., Chen, J., Liu, F., He, Q., Wu, Y., Sun, Q. et al. (2021) Septin homologs cooperating in the proliferative stage of microsporidia Nosema bombycis. Journal of Invertebrate Pathology, 183, 107600.
Huang, Y., Chen, J., Sun, B., Zheng, R., Li, B., Li, Z. et al. (2018) Engineered resistance to Nosema bombycis by in vitro expression of a single‐chain antibody in Sf9‐III cells. PLoS One, 13, e0193065.
Huang, Y., Zheng, S., Mei, X., Yu, B., Sun, B., Li, B. et al. (2018) A secretory hexokinase plays an active role in the proliferation of Nosema bombycis. PeerJ, 6, e5658.
Idris, A., Zainal‐Abidin, B., Sajap, A.S., Noran, A., Hussan, A., Endersby, N. et al. (2004) Some studies on Nosema infecting DBM in Malaysia.
Ishihara, R. (1969) The life cycle of Nosema bombycis as revealed in tissue culture cells of Bombyx mori. Journal of Invertebrate Pathology, 14, 316–320.
Iwano, H. & Ishihara, R. (1991a) Dimorphism of spores of Nosema spp. in cultured cell. Journal of Invertebrate Pathology, 57, 211–219.
Iwano, H. & Ishihara, R. (1991b) Dimorphic development of Nosema bombycis spores in gut epithelium of larvae of the silkworm, Bombyx mori. The Journal of Sericultural Science of Japan, 60, 249–256.
Jyothi, N.B. & Patil, C.S. (2011) Light and electron microscopic study on the development of Nosema Bombyics Naegeli in the Midgut of silkworm Bombyx Mori L. International Journal of Industrial Entomology, 23, 107–113.
Jyothi, N.B. & Patil, C.S. (2024) Chemotherapeutic effect of benzimidazole derivatives on Nosema Bombycis naegeli in silkworm bombyx mori l—an ultrastructural study.
Jyothi, N.B., Patil, C.S. & Dass, C.M.S. (2005) Action of carbendazim on the development of Nosema bombycis Naegeli in silkworm Bombyx mori L. Journal of Applied Entomology, 129, 205–210.
Kaku, O. (1964) Effect of potassium ion on filament Evagination of spores of Nosema bombycis as studied by neutralization method. Annotationes Zoologicae Japonenses, 37, 102–103.
Katinka, M.D., Duprat, S., Cornillot, E., Méténier, G., Thomarat, F., Prensier, G. et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature, 414, 450–453.
Kawakami, Y., Inoue, T., Ito, K., Kitamizu, K., Hanawa, C., Ando, T. et al. (1994) Identification of a chromosome harboring the small subunit ribosomal RNA gene of Nosema bombycis. Journal of Invertebrate Pathology, 64, 147–148.
Kawarabata, T. (2003) Biology of microsporidians infecting the silkworm, Bombyx mori, in Japan. Journal of Insect Biotechnology and Sericology, 72, 1–32.
Ke, Z., Xie, W., Wang, X., Long, Q. & Pu, Z. (1990) A monoclonal antibody to Nosema bombycis and its use for identification of microsporidian spores. Journal of Invertebrate Pathology, 56, 395–400.
Kellen, W.R. & Lindegren, J.E. (1973) Transovarian transmission of Nosema plodiae in the Indian‐meal moth, Plodia interpunctella. Journal of Invertebrate Pathology, 21, 248–254.
Knell, J.D. & Zam, S.G. (1978) A serological comparison of some species of microsporida. Journal of Invertebrate Pathology, 31, 280–288.
Lehane, M. & Billingsley, P. (2012) Biology of the insect midgut. Dordrecht: Springer Science & Business Media.
Li, X., Peng, X. & Shen, Z. (2016) Bioinformatic analysis, prokaryotic expression and polyclonal antibody preparation of Nosema bombycis trehalase gene. Science Sericulture, 42, 1026–1034.
Li, Y., Wu, Z., Pan, G., He, W., Zhang, R., Hu, J. et al. (2009) Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. International Journal for Parasitology, 39, 391–398.
Li, Y., Xie, L., Pan, G., Wu, Z., Pang, M. & Zhou, Z. (2006) Establishment and application of an immunofluorescence method for the detection of antibodies against microsporidia in the silkworm, Bombyx mori. Journal of Southwest Jiaotong University, 28, 990–993.
Li, Z., Pan, G., Li, T., Huang, W., Chen, J., Geng, L. et al. (2012) SWP5, a Spore Wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryotic Cell, 11, 229–237.
Li, Z., Pan, G., Ma, Z., Han, B., Sun, B., Ni, Q. et al. (2017) Comparative proteomic analysis of differentially expressed proteins in the Bombyx mori fat body during the microsporidia Nosema bombycis infection. Journal of Invertebrate Pathology, 149, 36–43.
Liang, X., Jintao, H., Nan, Z., Lu, X. & Shao, Y. (2023) Genome‐wide analysis of Nosema bombycis Zhejiang strain based on PacBio's third‐generation sequencing technology. Science Sericulture, 49, 498–514.
Lin, L., Pan, G., Li, T., Dang, X., Deng, Y., Ma, C. et al. (2012) The protein import pore Tom40 in the microsporidian Nosema bombycis. The Journal of Eukaryotic Microbiology, 59, 251–257.
Liu, F., Chen, J., Dang, X., Meng, X., Wang, R., Bao, J. et al. (2020) Nbseptin2 expression pattern and its interaction with NbPTP1 during microsporidia Nosema bombycis polar tube extrusion. The Journal of Eukaryotic Microbiology, 67, 45–53.
Liu, F., Ma, Q., Dang, X., Wang, Y., Song, Y., Meng, X. et al. (2017) Identification of a new subtilisin‐like protease NbSLP2 interacting with cytoskeletal protein septin in microsporidia Nosema bombycis. Journal of Invertebrate Pathology, 148, 110–117.
Liu, H., Chen, B., Hu, S., Liang, X., Lu, X. & Shao, Y. (2016) Quantitative proteomic analysis of germination of Nosema bombycis spores under extremely alkaline conditions. Frontiers in Microbiology, 7, 1459.
Liu, H., Li, M., Cai, S., He, X., Shao, Y. & Lu, X. (2016) Ricin‐B‐lectin enhances microsporidia Nosema bombycis infection in BmN cells from silkworm Bombyx mori. Acta Biochimica et Biophysica Sinica, 48, 1050–1057.
Liu, H., Li, M., He, X., Cai, S., He, X. & Lu, X. (2016) Transcriptome sequencing and characterization of ungerminated and germinated spores of Nosema bombycis. Acta Biochimica et Biophysica Sinica, 48, 246–256.
Liu, J. & Zeng, L. (2007) Staining and discrimination of Nosema bombycis spores with Calcofluor white M2R. Acta Entomologica Sinica, 50, 1185.
Liu, K. (2019) Identification of polar tube protein 4 (NbPTP4) and 5 (NbPTP5) from Nosema bombycis and the role of NbPTP4 in host cell infection. China: Southwest University Chongqing.
Long, M., Tan, Y., Liu, K., Wu, Y., Lü, Q., Pan, G. et al. (2018) Expression of polar tube protein 1 (NbPTP1) from Nosema bombycis in drosophila S2 cell lines and its glycosylation. Sheng Wu Gong Cheng Xue Bao. Chinese Journal of Biotechnology, 34, 1460–1468.
Lv, Q., Hong, L., Qi, L., Chen, Y., Xie, Z., Liao, H. et al. (2024) Microsporidia dressing up: the spore polaroplast transport through the polar tube and transformation into the sporoplasm membrane. MBio, 15, e02749‐23.
Lv, Q., Wang, L., Fan, Y., Meng, X., Liu, K., Zhou, B. et al. (2020) Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis. Parasites & Vectors, 13, 475.
Lv, Q., Zhou, B., Liao, H., He, X., Chen, Y., Pan, G. et al. (2022) Proteomic profile of polar filament and polar tube from fungal pathogen microsporidium Nosema bombycis provides new insights into its unique invasion organelle. Journal of Proteomics, 263, 104617.
Ma, M., Ling, M., Huang, Q., Xu, Y., Yang, X., Kyei, B. et al. (2023) Functional characterization of Nosema bombycis (microsporidia) trehalase 3. Parasitology Research, 123, 59.
Ma, Z., Li, C., Pan, G., Li, Z., Han, B., Xu, J. et al. (2013) Genome‐wide transcriptional response of silkworm (Bombyx mori) to infection by the microsporidian Nosema bombycis. PLoS One, 8, e84137.
Major, P., Embley, T.M. & Williams, T.A. (2017) Phylogenetic diversity of NTT nucleotide transport proteins in free‐living and parasitic bacteria and eukaryotes. Genome Biology and Evolution, 9, 480–487.
Meng, X., Luo, B., Tang, X., He, Q., Xiong, T., Fang, Z. et al. (2018) Pathological analysis of silkworm infected by two microsporidia Nosema bombycis CQ1 and Vairimorpha necatrix BM. Journal of Invertebrate Pathology, 153, 75–84.
Min, Y., Qing, L., KeKe, L., LiJun, W., YuJiao, W., ZeYang, Z. & MengXian, L. (2019) Expression, purification, and localization analysis of polar tube protein 2 (NbPTP2) from Nosema bombycis. Scientia Agricultura Sinica, 52, 1830–1838.
Nadia, M.K. & Idris, A.B. (2017) Effect of Nosema bombycis on the preference and performance of Plutella xylostella (L.) (Lepidoptera: Plutellidae). Mysore The Journal of Agricultural Science, 51(A), 140–147.
Nageli, C. (1857) uber die neue Krankheit der Seidenraupe und verwandte Organismen. Botanische Zeitung, 15, 760–761.
Nakhleh, J., El Moussawi, L. & Osta, M.A. (2017) Chapter three—the Melanization response in insect immunity. In: Ligoxygakis, P. (Ed.) Advances in insect physiology. Vol. 52. Insect Immunity. London: Academic Press, pp. 83–109.
Nakjang, S., Williams, T.A., Heinz, E., Watson, A.K., Foster, P.G., Sendra, K.M. et al. (2013) Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biology and Evolution, 5, 2285–2303.
Pan, G. (2014) Histopathological observations of the silkworm, Bombyx mori, infected with the microsporidian strain CQ1 of Bombyx mori. Science Sericulture, 2, 100.
Pan, G., Bao, J., Ma, Z., Song, Y., Han, B., Ran, M. et al. (2018) Invertebrate host responses to microsporidia infections. Developmental and Comparative Immunology, 83, 104–113.
Pan, G., Xu, J., Li, T., Xia, Q., Liu, S.‐L., Zhang, G. et al. (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics, 14, 186.
Pei, B., Wang, C., Yu, B., Xia, D., Li, T. & Zhou, Z. (2021) The first report on the Transovarial transmission of microsporidian Nosema bombycis in lepidopteran crop pests Spodoptera litura and Helicoverpa armigera. Microorganisms, 9, 1442.
Peng, X., Li, X., Chen, G., Dai, W., Li, N., Wang, W. et al. (2016) Molecular cloning, sequence analysis and prokaryotic expression of Nosema bombycis enolase gene. Science Sericulture, 42, 1035–1040.
Peng, X., Qi, J., Shang, R., Zhang, Z., Chen, H. & Shen, Z. (2018) Cloning and expression characteristic analysis of Nb6PGDH gene of Nosema bombycis. Science Sericulture, 44, 698–704.
Qi, J., Shang, R., Zhang, Z., Chen, H., Zhang, Y. & Shen, Z. (2018) Cloning and expression profile analysis of G6PDH gene of Nosema bombycis. Science Sericulture, 44, 884–890.
Qui, H., Li, M., He, X. & Lu, X. (2014) Expression and characterization of a novel spore wall protein from Nosema bombycis. African Journal of Biotechnology, 13, 2459–2465.
Ran, M., Shi, Y., Li, B., Xiang, H., Tao, M., Meng, X. et al. (2023) Genome‐wide characterization and comparative genomic analysis of the serpin gene family in microsporidian Nosema bombycis. International Journal of Molecular Sciences, 24, 550.
Rao, S.N., Nath, B.S., Bhuvaneswari, G. & Urs, S.R. (2007) Genetic diversity and phylogenetic relationships among microsporidia infecting the silkworm, Bombyx mori, using random amplification of polymorphic DNA: morphological and ultrastructural characterization. Journal of Invertebrate Pathology, 96, 193–204.
Reinke, A.W., Balla, K.M., Bennett, E.J. & Troemel, E.R. (2017) Identification of microsporidia host‐exposed proteins reveals a repertoire of rapidly evolving proteins. Nature Communications, 8, 14023.
Reinke, A.W. & Troemel, E.R. (2015) The development of genetic modification techniques in intracellular parasites and potential applications to microsporidia. PLoS Pathogens, 11, e1005283.
Sarfraz, M., Keddie, A.B. & Dosdall, L.M. (2005) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Science and Technology, 15, 763–789.
Shabir Ahmad Bhat. (2012) Efficacy of different benzimidazole derivatives on microsporidiosis of lamerin breed of the silkworm, Bombyx mori L. Journal of Entomology and Nematology, 4, 12–14.
Shamim, M., Ghosh, D., Baig, M., Nataraju, B., Datta, R.K. & Gupta, S.K. (1997) Production of monoclonal antibodies against Nosema bombycis and their utility for detection of Pebrine infection in Bombyx mori L. Journal of Immunoassay, 18, 357–370.
Shang, R., Qi, J., Chen, H., Zhang, Z., Zhang, Y. & Shen, Z. (2019) Cloning and expression characteristics of Ribose‐5‐phosphate isomerase a gene of Nosema bombycis. Science Sericulture, 45, 61–66.
Shen, Z., Ke, Z., Yang, Q., Ghebremichael, S.T., Tangxin, L., Tian, L. et al. (2024) Transcriptomic changes in the microsporidia proliferation and host responses in congenitally infected embryos and larvae. BMC Genomics, 25, 321.
Shen, Z., Yang, Q., Luo, L., Tangxin, L., Ke, Z., Tian, L. et al. (2023) Non‐coding RNAs identification and regulatory networks in pathogen‐host interaction in the microsporidia congenital infection. BMC Genomics, 24, 420.
Sin, N., Meng, L., Wang, M.Q.W., Wen, J.J., Bornmann, W.G. & Crews, C.M. (1997) The anti‐angiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP‐2. Proceedings of the National Academy of Sciences, 94, 6099–6103.
Smith, J.E. (2009) The ecology and evolution of microsporidian parasites. Parasitology, 136, 1901–1914.
Sokol, C.L. & Luster, A.D. (2015) The chemokine system in innate immunity. Cold Spring Harbor Perspectives in Biology, 7, a016303.
Sokolova, Y., Sokolov, I. & Fuxa, J.R. (2004) Identification of microsporidia infections in nature: light microscopy or PCR? Protistology, 3, 273–281.
Song, Y., Tang, Y., Yang, Q., Tangxin, L., He, Z., Wu, Y. et al. (2020) Proliferation characteristics of the intracellular microsporidian pathogen Nosema bombycis in congenitally infected embryos. Journal of Invertebrate Pathology, 169, 107310.
Su, Y., Qu, Q., Li, J., Han, Z., Fang, Y., Flavorta, B.L. et al. (2024) Perilipin1 inhibits Nosema bombycis proliferation by promoting Domeless‐ and hop‐mediated JAK‐STAT pathway activation in Bombyx mori. Microbiology Spectrum, 12, e03671‐23.
Sun, F., Wang, R., He, P., Wei, E., Wang, Q., Tang, X. et al. (2022) Sar1 interacts with Sec23/Sec24 and Sec13/Sec31 complexes: insight into its involvement in the assembly of coat protein complex II in the microsporidian Nosema bombycis. Microbiology Spectrum, 10, e00719‐22.
Sun, J., Qin, F., Sun, F., He, P., Wei, E., Wang, R. et al. (2023) Identification and subcellular colocalization of protein transport protein Sec61α and Sec61γ in Nosema bombycis. Gene, 851, 146971.
Sun, X., Yu, B., Zhang, R., Wei, J., Pan, G., Li, C. et al. (2022) Generation of resistance to Nosema bombycis (Dissociodihaplophasida: Nosematidae) by degrading NbSWP12 using the ubiquitin‐proteasome pathway in Sf9‐III cells. Journal of Economic Entomology, 115, 2068–2074.
Tan, X., Pan, G., Wu, Z., Li, Y., Zhang, R., Xu, J. et al. (2008) Relationship between the germination and spore wall proteins in Nosema bombycis. Acta Zoologica Sinica, 54, 1068–1074.
Tang, X., Zhang, Y., Zhou, Y., Liu, R. & Shen, Z. (2020) Quantitative proteomic analysis of ovaries from Nosema bombycis‐infected silkworm (Bombyx mori). Journal of Invertebrate Pathology, 172, 107355.
Tian, L., Guo, E., Diao, Y., Zhou, S., Peng, Q., Cao, Y. et al. (2010) Genome‐wide regulation of innate immunity by juvenile hormone and 20‐hydroxyecdysone in the Bombyx fat body. BMC Genomics, 11, 549.
Tokarev, Y.S., Timofeev, S.A., Malysh, J.M., Tsarev, A.A., Ignatieva, A.N., Tomilova, O.G. et al. (2019) Hexokinase as a versatile molecular genetic marker for microsporidia. Parasitology, 146, 472–478.
Trager, W. (1937) The hatching of spores of Nosema bombycis Nageli and the partial development of the organism in tissue cultures. The Journal of Parasitology, 23, 226.
Tsaousis, A.D., Kunji, E.R.S., Goldberg, A.V., Lucocq, J.M., Hirt, R.P. & Embley, T.M. (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature, 453, 553–556.
Vávra, J. & Ronny Larsson, J.I. (2014) Structure of Microsporidia. In: Weiss, L.M. & Becnel, J.J. (Eds.) Microsporidia, 1st edition. Wiley, pp. 1–70.
Vavra, J. & Undeen, A.H. (1970) Nosema algerae n. sp. (Cnidospora, Microsporida) a pathogen in a laboratory Colony of Anopheles stephensi Liston (Diptera, Culicidae). The Journal of Protozoology, 17, 240–249.
Wang, C., Yu, B., Meng, X., Xia, D., Pei, B., Tang, X. et al. (2023) Microsporidian Nosema bombycis hijacks host vitellogenin and restructures ovariole cells for transovarial transmission. PLoS Pathogens, 19, e1011859.
Wang, F., Hu, C., Hua, X., Song, L. & Xia, Q. (2013) Translationally controlled tumor protein, a dual functional protein involved in the immune response of the silkworm, Bombyx mori. PLoS One, 8, e69284.
Wang, J., Chambon, C., Lu, C., Huang, K., Vivarès, C. & Texier, C. (2007) A proteomic‐based approach for the characterization of some major structural proteins involved in host–parasite relationships from the silkworm parasite Nosema bombycis (microsporidia). Proteomics, 7, 1461–1472.
Wang, L., Chenmin, H., Xiaoqun, D., Jinshan, X. & ZeYang, Z. (2015) Identification, evolutionary and transcriptional activity analyses of a dicer‐like gene in microsporidium Nosema bombycis. Science Sericulture, 41, 64–71.
Wang, Q., Song, Y., Chai, Y., Pan, G., Li, T., Yuan, Y. et al. (2014) Electrochemical immunosensor for detecting the spore wall protein of Nosema bombycis based on the amplification of hemin/G‐quadruplex DNAzyme concatamers functionalized Pt@Pd nanowires. Biosensors & Bioelectronics, 60, 118–123.
Wang, R., Li, Q., Liu, F., Dang, X., Sun, Q., Sheng, X. et al. (2022) Maturation of subtilisin‐like protease NbSLP1 from microsporidia Nosema bombycis. Frontiers in Cellular and Infection Microbiology, 12, 897509.
Wang, Y., Dang, X., Ma, Q., Liu, F., Pan, G., Li, T. et al. (2015) Characterization of a novel spore wall protein NbSWP16 with proline‐rich tandem repeats from Nosema bombycis (microsporidia). Parasitology, 142, 534–542.
Wang, Y., Geng, L., Xu, J., Jiang, P., An, Q., Pu, Y. et al. (2020) Expression and identification of a novel Spore Wall protein in microsporidian Nosema bombycis. The Journal of Eukaryotic Microbiology, 67, 671–677.
Wang, Y., Zhang, R., Barandun, J., Du, H., Chen, D., Jia, Y. et al. (2018) Divergence of a tandem duplication of manganese superoxide dismutase in Nosema bombycis. The Journal of Eukaryotic Microbiology, 65, 93–103.
Wei, J., Fei, Z., Pan, G., Weiss, L.M. & Zhou, Z. (2022) Current therapy and therapeutic targets for Microsporidiosis. Frontiers in Microbiology, 13, 835390.
Weiss, L.M., Delbac, F., Russell, H.J., Pan, G., Dang, X. & Zhou, Z. (2014) The microsporidian polar tube and Spore Wall. In: Weiss, L.M. & Becnel, J.J. (Eds.) Microsporidia, 1st edition. Hoboken, New Jersey: Wiley, pp. 261–306.
Weiss, L.M. & Reinke, A.W. (2022) Microsporidia: current advances in biology. Cham, Switzerland: Springer Nature.
Wen, Y. (2024) Hexokinase of Nosema bombycis modulates gene expression and related pathways in silkworm. Acta Microbiologica Sinica, 64, 1203–1218.
Wu, S., He, T., Lu, X., Zhang, X., Shuai, J., Yu, H. et al. (2017) Early and simultaneous detection of Nosema bombycis (microsporidia: Nosematidae), nucleopolyhedrovirus (Baculoviridae), and densovirus (Parvoviridae) by multiplex real‐time polymerase chain reaction in Bombyx mori (Lepidoptera: Bombycidae). Canadian Entomologist, 149, 265–275.
Wu, Y., Long, M., Chen, J., Zhi, L., Li, Z., Pan, G. et al. (2014) Cloning and prokaryotic expression of Nosema bombycis polar tube protein 1 (PTP1). Science Sericulture, 2, 22.
Wu, Z., Li, Y., Pan, G., Tan, X., Hu, J., Zhou, Z. et al. (2008) Proteomic analysis of spore wall proteins and identification of two spore wall proteins from Nosema bombycis (microsporidia). Proteomics, 8, 2447–2461.
Xie, H., Zhang, Q., Wang, Q., Chai, Y., Yuan, Y. & Yuan, R. (2015) Fe3O4 NPs mediated nonenzymatic electrochemical immunosensor for the total protein of Nosema bombycis detection without addition of substrate. Chemical Communications, 51, 7132–7135.
Xing, D., Liao, S., Huang, W., Li, Q., Xiao, Y., Yan, S. et al. (2022) Mechanism of carbendazim in treating pebrine disease of Bombyx mori based on GC/MS‐based metabonomics. Parasitology Research, 121, 453–460.
Xu, J., He, Q., Ma, Z., Li, T., Zhang, X., Debrunner‐Vossbrinck, B.A. et al. (2016) The genome of Nosema sp. isolate YNPr: a comparative analysis of genome evolution within the Nosema/Vairimorpha clade. PLoS One, 11, e0162336.
Xu, J., Luo, J., Chen, J., Vossbrinck, C.R., Li, T. & Zhou, Z. (2022) Characterization of the largest secretory protein family, ricin B lectin‐like protein, in Nosema bombycis: insights into microsporidian adaptation to host. Journal of Fungi, 8, 551.
Xu, Y., Takvorian, P.M., Cali, A., Orr, G. & Weiss, L.M. (2004) Glycosylation of the Major polar tube protein of Encephalitozoon hellem, a microsporidian parasite that infects humans. Infection and Immunity, 72, 6341–6350.
Yan, W., Shen, Z., Tang, X., Xu, L., Li, Q., Yue, Y. et al. (2014) Detection of Nosema bombycis by FTA cards and loop‐mediated isothermal amplification (LAMP). Current Microbiology, 69, 532–540.
Yang, D., Dang, X., Peng, P., Long, M., Ma, C., Qin, J.J.G. et al. (2014) NbHSWP11, a microsporidia Nosema bombycis protein, localizing in the spore wall and membranes, reduces spore adherence to host cell BME. The Journal of Parasitology, 100, 623–632.
Yang, D., Dang, X., Tian, R., Long, M., Li, C., Li, T. et al. (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.
Yang, D., Pan, G., Dang, X., Shi, Y., Li, C., Peng, P. et al. (2015) Interaction and assembly of two novel proteins in the Spore Wall of the microsporidian species Nosema bombycis and their roles in adherence to and infection of host cells. Infection and Immunity, 83, 1715–1731.
Yang, D., Pan, L., Peng, P., Dang, X., Li, C., Li, T. et al. (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. Infection and Immunity, 85, 10–1128. Available from: https://doi.org/10.1128/iai.00872‐16
Yi, M., Lv, Q., Liu, K., Wang, L., Wu, Y., Zhou, Z. et al. (2019) Expression, purification and localization analysis of polar tube protein 2 (NbPTP2) from Nosema bombycis. Scientia Agricultura Sinica, 52, 1830–1838.
Yu, B., Yang, Q., Wei, J., Pan, G., Li, C. & Zhou, Z. (2021) UDP‐glucosyltransferases induced by Nosema bombycis provide resistance to microsporidia in silkworm (Bombyx mori). Insects, 12, 799.
Yu, B., Zheng, R., Bian, M., Liu, T., Lu, K., Bao, J. et al. (2023) A monoclonal antibody targeting spore wall protein 1 inhibits the proliferation of Nosema bombycis in Bombyx mori. Microbiology Spectrum, 11, e00681‐23.
Yue, Y., Tang, X., Xu, L., Yan, W., Li, Q., Xiao, S. et al. (2015) Early responses of silkworm midgut to microsporidium infection—a digital gene expression analysis. Journal of Invertebrate Pathology, 124, 6–14.
Zhang, L. & Lecoq, M. (2021) Nosema locustae (protozoa, microsporidia), a biological agent for locust and grasshopper control. Agronomy, 11, 711.
Zhang, X., Feng, H., He, J., Liang, X., Zhang, N., Shao, Y. et al. (2022) The gut commensal bacterium Enterococcus faecalis LX10 contributes to defending against Nosema bombycis infection in Bombyx mori. Pest Management Science, 78, 2215–2227.
Zhang, Z., Qi, J., Shang, R., Chen, H., Zhang, Y. & Shen, Z. (2019) Cloning and expression analysis of the pyruvate kinase gene of Nosema bombycis. Shen Zhongyuan, 45, 212–217.
Zhao, Z., Zhou, X., Wu, Y., Shen, Z., Lin, S., Chen, Z. et al. (2023) Development of rapid visual detection technology for Nosema bombycis based on CRISPR/Cas12a system. Entomologia Generalis, 43, 4.
Zheng, S., Huang, Y., Huang, H., Yu, B., Zhou, N., Wei, J. et al. (2021) The role of NbTMP1, a surface protein of sporoplasm, in Nosema bombycis infection. Parasites & Vectors, 14, 81.
Zheng, S., Huang, Y., Yu, B., Huang, H., Wei, J., Pan, G. et al. (2020) Cloning and expression analysis of hypothetical membrane protein gene NBO_32g0046 of Nosema bombycis.
Zhu, F., Li, X., Tang, X., Xu, L., Bai, X. & Shen, Z. (2017) Cloning and prokaryotic expression of Nosema bombycis Trehalose‐phosphate synthase gene. Science Sericulture.
Zhu, F., Shen, Z., Hou, J., Zhang, J., Geng, T., Tang, X. et al. (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.
Zhu, F., Tang, X., Xiao, S., Wang, H., Zhang, Y., Shao, Y. et al. (2019) The role of Bombyx mori Bmtutl‐519 protein in the infection of BmN cells by Nosema bombycis. Developmental and Comparative Immunology, 92, 283–290.
Zhu, F., Xiao, S., Qin, X., Liu, Q., Li, H., Ming, D. et al. (2022) Identification and subcellular localization of NbIAP in the microsporidian Nosema bombycis. Journal of Invertebrate Pathology, 195, 107846.