Isolation of protein-free chitin spore coats of Nosema ceranae and its application to screen the interactive spore wall proteins.
Chitin spore coats
Honeybee
Interaction
Nosema ceranae
Spore wall protein
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
22
10
2020
accepted:
09
02
2021
revised:
28
12
2020
pubmed:
2
3
2021
medline:
7
7
2021
entrez:
1
3
2021
Statut:
ppublish
Résumé
Nosema ceranae is the pathogen of nosemosis in the honey bee, which can bring great economic loss to apiculture. Chitin acts as a major component of the endospore of microsporidia and plays an essential role to form the bridges across the endospore. Here, Chitin Spore Coats (CSCs) of N. ceranae were successfully extracted by optimized hot alkaline treatment. SDS-PAGE and Calcofluor White Stain (CWS) staining indicated that the obtained CSCs were protein-free and the transmission electron microscopy analysis showed that CSCs performed the intact and loose chitin spore coats. Western blotting and indirect immunofluorescence analysis (IFA) demonstrated that CSCs could interact with three spore wall proteins (rNcSWP7, rNcSWP8, and rNcSWP12). Our method was effective to extract CSCs of N. ceranae and this could be very useful for screening spore wall proteins involved in endospore composition, which could be helpful to uncover the biological structure and pathogenesis of microsporidia.
Identifiants
pubmed: 33646339
doi: 10.1007/s00203-021-02214-9
pii: 10.1007/s00203-021-02214-9
doi:
Substances chimiques
Fungal Proteins
0
Chitin
1398-61-4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2727-2733Subventions
Organisme : National Natural Science Foundation of China
ID : 31770160
Organisme : the Science and Technology Research Program of Chongqing Municipal Education Commission
ID : KJQN201800524
Organisme : Agriculture Research System of China
ID : CARS-44-KXJ21
Organisme : Chongqing Basic Science and Advanced Technology Research Program
ID : No.cstc2018jcyjAX0832
Références
Ajibola A, Chamunorwa JP, Erlwanger KH (2012) Nutraceutical values of natural honey and its contribution to human health and wealth. Nutr Metab 9:61–61
doi: 10.1186/1743-7075-9-61
Bigliardi E, Selmi MG, Lupetti P, Corona S, Gatti S, Scaglia M, Sacchi L (1996) Microsporidian spore wall: ultrastructural findings on encephalitozoon hellem exospore. J Eukaryot Microbiol 43:181–186
doi: 10.1111/j.1550-7408.1996.tb01388.x
Bohne W, Ferguson DJP, Kohler K, Gross U (2000) Developmental expression of a tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infect Immun 68(4):2268–2275
doi: 10.1128/IAI.68.4.2268-2275.2000
Chatterjee A, Carpentieri A, Ratner DM, Bullitt E, Costello CE, Robbins PW, Samuelson J (2010) Giardia cyst wall protein 1 is a lectin that binds to curled fibrils of the GalNAc homopolymer. PLoS Pathog 6:e1001059
doi: 10.1371/journal.ppat.1001059
Cai SF, Lu XM, Qiu HH, Li MQ, Feng ZZ (2011) Identification of a Nosema bombycis (Microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology 138(9):1102–1109
doi: 10.1017/S0031182011000801
Chen J, Geng LN, Long MX, Li T, Li Z, Yang DL, Ma C, Wu HJ, Ma ZG, Li CF, Pan GQ, Zhou ZY (2013) Identification of a novel chitin-binding spore wall protein (Nbswp12) with a bar-2 domain from Nosema bombycis (microsporidia). Parasitology 140:1394–1402
doi: 10.1017/S0031182013000875
Chen J, Guo W, Dang XQ, Huang YK, Liu FY, Meng XZ, An YY, Long MX, Bao JL, Zhou ZY, Xiang ZH, Pan GQ (2017a) Easy labeling of proliferative phase and sporogonic phase of microsporidia Nosema bombycis in host cells. PLoS ONE 12:e0179618
doi: 10.1371/journal.pone.0179618
Chen LX, Li RT, You YW, Zhang K, Zhang L (2017b) A novel spore wall protein from antonospora locustae (Microsporidia: Nosematidae) contributes to sporulation. J Eukaryot Microbiol 64(6):779–791
doi: 10.1111/jeu.12410
Davids B, Mehta K, Fesus L, McCaffery J, Gillin F (2004) Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol Biochem Parasit 136:173–180
doi: 10.1016/j.molbiopara.2004.03.011
Dussaubat C, Brunet JL, Higes M, Colbourne JK, Lopez J, Choi JH, Martin-Hernandez R, Botias C, Cousin M, McDonnell C, Bonnet M, Belzunces LP, Moritz RFA, Le Conte Y, Alaux C (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS ONE 7:e37017
doi: 10.1371/journal.pone.0037017
Han B, Weiss LM (2018) Therapeutic targets for the treatment of microsporidiosis in humans. Expert Opin Ther Targets 22:903–915
doi: 10.1080/14728222.2018.1538360
Hayman JR, Hayes SF, Amon J, Nash TE (2001) Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis. Infect Immun 69(11):7057–7066
doi: 10.1128/IAI.69.11.7057-7066.2001
Higes M, Martin-Hernandez R, Garrido-Bailon E, Botias C, Meana A (2009) The presence of Nosema ceranae (microsporidia) in north african honey bees (Apis mellifera intermissa). J Apicult Res 48:217–219
doi: 10.3896/IBRA.1.48.3.12
Jaroenlak P, Boakye DW, Vanichviriyakit R, Williams BAP, Sritunyalucksana K, Itsathitphaisarn O (2018) Identification, characterization and heparin binding capacity of a spore-wall, virulence protein from the shrimp microsporidian, Enterocytozoon hepatopenaei (EHP). Parasite Vector 11:177
doi: 10.1186/s13071-018-2758-z
Lauwaet T, Davids BJ, Torres-Escobar A, Birkeland SR, Cipriano MJ, Preheim SP, Palm D, Svard SG, McArthur AG, Gillin FD (2007) Protein phosphatase 2A plays a crucial role in giardia lamblia differentiation. Mol Biochem Parasit 152:80–89
doi: 10.1016/j.molbiopara.2006.12.001
Li YH, Wu ZL, PanZ GQ, He WW, Zhang RZ, Hu JH, Zhou ZY (2009) Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. Int J Parasitol 39(4):391–398
doi: 10.1016/j.ijpara.2008.08.011
Li Z, Pan GQ, Li T, Huang W, Chen J, Geng LN, Yang DL, Wang LL, Zhou ZY (2012) SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryot Cell 11(2):229–237
doi: 10.1128/EC.05127-11
Malhotra C, Jain AK, Kaur S, Dhingra D, Hemanth V, Sharma SP (2017) In vivo confocal microscopic characteristics of microsporidial keratoconjunctivitis in immunocompetent adults. Br J Ophthalmol 101:1217–1222
doi: 10.1136/bjophthalmol-2016-309794
Martin-Hernandez R, Botias C, Barrios L, Martinez-Salvador A, Meana A, Mayack C, Higes M (2011) Comparison of the energetic stress associated with experimental nosema ceranae and nosema apis infection of honeybees (Apis mellifera). Parasitol Res 109:605–612
doi: 10.1007/s00436-011-2292-9
Meng XC, Zheng J, Gao Y, Zhang YL, Jia HL (2014) Evaluation of spore wall protein 1 as an alternative antigen for the diagnosis of Encephalitozoon cuniculi infection of farmed foxes using an enzyme-linked immunosorbent assay. Vet Parasitol 203(3–4):331–334
doi: 10.1016/j.vetpar.2014.03.011
Pacini A, Mira A, Molineri A, Giacobino A, Cagnolo NB, Aignasse A, Zago L, Izaguirre M, Merke J, Orellano E, Bertozzi E, Pietronave H, Russo R, Scannapieco A, Lanzavecchia S, Schnittger L, Signorini M (2016) Distribution and prevalence of nosema apis and n-ceranae in temperate and subtropical eco-regions of argentina. J Invertebr Pathol 141:34–37
doi: 10.1016/j.jip.2016.11.002
Peuvel-Fanget I, Polonais V, Brosson D, Texier C, Kuhn L, Peyret P, Vivares 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. Int J Parasit 36:309–318
doi: 10.1016/j.ijpara.2005.10.005
Shravan UM, KarunakarKrishnamurthy PV (2020) Homology modeling, virtual screening and dynamics study of proteins involved in Pebrine-Serine Protease Inhibitor 106 and Spore Wall Protein 26. J Biomol Struct Dyn 38(17):5148–5158
doi: 10.1080/07391102.2019.1696704
Slavin I, Saura A, Carranza PG, Touz MC, Nores MJ, Luján HD (2002) Dephosphorylation of cyst wall proteins by a secreted lysosomal acid phosphatase is essential for excystation of giardia lamblia. Mol Biochem Parasit 122:95
doi: 10.1016/S0166-6851(02)00065-8
Southern TR, Jolly CE, Lester ME, Hayman JR (2007) Enp1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro. Eukaryot Cell 6:1354–1362
doi: 10.1128/EC.00113-07
Tokarev YS, Zinatullina ZY, Ignatieva AN, Zhigileva ON, Malysh JM, Sokolova YY (2018) Detection of two microsporidia pathogens of the european honey bee Apis mellifera (insecta: Apidae) in western Siberia. Acta Parasitolog 63:728–732
doi: 10.1515/ap-2018-0086
Vávra J (1976) Structure of the microsporidia. Biology of the microsporidia. Springer, Berlin
Wang Y, Dang XQ, Ma Q, Liu FY, Pan GQ, Li T, Zhou ZY (2015) Characterization of a novel spore wall protein nbswp16 with proline-rich tandem repeats from Nosema bombycis (microsporidia). Parasitology 142:534–542
doi: 10.1017/S0031182014001565
Weiss LM, Becnel JJ (2014) Microsporidia: pathogens of opportunity. Wiley Hoboken, New Jersey
doi: 10.1002/9781118395264
Xu YJ, Takvorian P, Cali A, Wang F, Zhang H, Orr G, Weiss LM (2006) Identification of a new spore wall protein from Encephalitozoon cuniculi. Infect Immun 74:239–247
doi: 10.1128/IAI.74.1.239-247.2006
Yang DL, Dang XQ, Tian R, Long MX, Li CF, Li T, Chen J, Li Z, Pan GQ, Zhou ZY (2014) Development of an approach to analyze the interaction between Nnosema bombycis (microsporidia) deproteinated chitin spore coats and spore wall proteins. J Invertebr Pathol 115:1–7
doi: 10.1016/j.jip.2013.10.004
Yang DL, Pan GQ, Dang XQ, Shi YW, Li CF, Peng P, Luo B, Bian MF, Song Y, Ma C, Chen J, Ma ZG, Geng LN, Li Z, Tian R, Wei CF, Zhou ZY (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. Infect Immun 83:1715–1731
doi: 10.1128/IAI.03155-14
Yang DL, Pan LX, Chen ZZ, Du HH, Luo B, Luo J, Pan GQ (2018) The roles of microsporidia spore wall proteins in the spore wall formation and polar tube anchorage to spore wall during development and infection processes. Exp Parasitol 187:93–100
doi: 10.1016/j.exppara.2018.03.007
Zaku S, Emmanuel S, Aguzue O, Thomas S (2011) Extraction and characterization of chitin; a functional biopolymer obtained from scales of common carp fish (cyprinus carpiol.): a lesser known source. Afr J Food Sci 5:478–483
Zhu F, Shen ZY, Hou JG, Zhang J, Geng T, Tang XD, Xu L, Guo XJ (2013) Identification of a protein interacting with the spore wall protein SWP26 of Nosema bombycis in a cultured BmN cell line of silkworm. Infect Genet Evol 17:38–45
doi: 10.1016/j.meegid.2013.03.029