Molecular characterization and analysis of drug resistance-associated protein enolase 2 of Eimeria tenella

Yu Yu1, Wenhao Huang1, Qingjie Wang1, Hui Dong1, Qiping Zhao1, Shunhai Zhu1, Bing Huang1, Hongyu Han1
1Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology of Ministry of Agriculture, Minhang, Shanghai, 200241, PR China

Tài liệu tham khảo

Agarwal, 2008, alpha-Enolase binds to human plasminogen on the surface of Bacillus anthracis, Biochim. Biophys. Acta, 1784, 986, 10.1016/j.bbapap.2008.03.017 Andrade, 2005, Antigens from Ascaris suum trigger in vitro macrophage NO production, Parasite Immunol., 27, 235, 10.1111/j.1365-3024.2005.00774.x Avilán, 2011, Enolase: a key player in the metabolism and a probable virulence factor of trypanosomatid parasites-perspectives for its use as a therapeutic target, Enzym. Res., 10.4061/2011/932549 Bernal, 2004, Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica, FEBS Lett., 563, 203, 10.1016/S0014-5793(04)00306-0 Bhowmick, 2009, Plasmodium falciparum enolase: stage-specific expression and sub-cellular localization, Malar. J., 8, 179, 10.1186/1475-2875-8-179 Blake, 2020, Re-calculating the cost of coccidiosis in chickens, Vet. Res., 51, 115, 10.1186/s13567-020-00837-2 Blake, 2021, Spotlight on avian pathology: Eimeria and the disease coccidiosis, Avian Pathol., 50, 209, 10.1080/03079457.2021.1912288 Chapman, 2014, Vaccination of chickens against coccidiosis ameliorates drug resistance in commercial poultry production, Int. J. Parasitol. Drugs Drug Resist., 4, 214, 10.1016/j.ijpddr.2014.10.002 Chen, 2008, Eimeria tenella: analysis of differentially expressed genes in the monensin- and maduramicin-resistant lines using cdna array, Exp. Parasitol., 119, 264, 10.1016/j.exppara.2008.02.010 Daszak, 1999, Zoite migration during infection: parasite adaptation to host defences, Parasitol. Today, 15, 67, 10.1016/S0169-4758(98)01379-9 Ferguson, 2002, Evidence for nuclear localisation of two stage-specific isoenzymes of enolase in Toxoplasma gondii correlates with active parasite replication, Int. J. Parasitol., 32, 1399, 10.1016/S0020-7519(02)00129-7 Gan, 2010, Reverse vaccinology approach identify an Echinococcus granulosus tegumental membrane protein enolase as vaccine candidate, Parasitol. Res., 106, 873, 10.1007/s00436-010-1729-x Han, 2010, Identification of differentially expressed genes in early stages of Eimeria tenella by suppression subtractive hybridization and cDNA microarray, J. Parasitol., 96, 95, 10.1645/GE-2221.1 Han, 2004, Induction of diclazuril resistant strains and madumycin resistant strains of Eimeria tenella in the laboratory, Chin. J. Vet. Sci., 24, 138 Huang, 1993, Study on the identification and pathogenicity of the pure species of Eimeria tenella, Chinese J. Veterinary Parasitol., 1, 18 Huang, 2022, Molecular characterization of glyceraldehyde-3-phosphate dehydrogenase from Eimeria tenella, Parasitol. Res., 121, 1749, 10.1007/s00436-022-07508-5 Jiang, 2012, Identification and partial characterization of a serine protease inhibitor (serpin) of Eimeria tenella, Parasitol. Res., 110, 865, 10.1007/s00436-011-2568-0 Kasturi, 2018, Drug resistance in Plasmodium, Nat. Rev. Microbiol., 16, 156, 10.1038/nrmicro.2017.161 Khalafalla, 2010, Single oocyst infection: a simple method for isolation of Eimeria spp. from the mixed field samples, Parasitol. Res., 107, 187, 10.1007/s00436-010-1840-z Labbé, 2006, Eimeria tenella enolase and pyruvate kinase: a likely role in glycolysis and in others functions, Int. J. Parasitol., 36, 1443, 10.1016/j.ijpara.2006.08.011 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method, Med. Sci., 25, 402 McDonald, 2009, Past and future: vaccination against Eimeria, Parasitology, 136, 1477, 10.1017/S0031182009006349 McDougald, 1990, Anticoccidial efficacy of diclazuril against recent field isolates of Eimeria from commercial poultry farms, Avian Dis., 34, 911, 10.2307/1591382 Mehlhorn, 1983, The action of polyether ionophorous antibiotics (monensin, salinomycin, lasalocid) on developmental stages of Eimeria tenella (Coccidia, Sporozoa) in vivo and in vitro: study by light and electron microscopy, Z. Parasitenkd., 69, 457, 10.1007/BF00927702 Min, 2004, Application of biotechnological tools for coccidia vaccine development, J. Vet. Sci., 5, 279, 10.4142/jvs.2004.5.4.279 Miska, 2004, Analysis of transcripts expressed by Eimeria tenella oocysts using subtractive hybridization methods, J. Parasitol., 90, 1245, 10.1645/GE-309R Nickel, 2003, The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes, Eur. J. Biochem., 270, 2109, 10.1046/j.1432-1033.2003.03577.x Peek, 2011, Coccidiosis in poultry: anticoccidial products, vaccines and other prevention strategies, Vet. Q., 31, 143, 10.1080/01652176.2011.605247 Péroval, 2006, The heat shock protein 90 of Eimeria tenella is essential for invasion of host cell and schizont growth, Int. J. Parasitol., 36, 1205, 10.1016/j.ijpara.2006.04.006 Peshavaria, 1991, Molecular structure of the humanmuscle-specific enolase gene (ENO3), Biochem. J., 275, 427, 10.1042/bj2750427 Richard, 2009, Chapter 32 elution of proteins from gels, Methods Enzymol., 463, 565, 10.1016/S0076-6879(09)63032-9 Shen, 2014, Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion, Proc. Natl. Acad. Sci. U. S. A., 111, 3567, 10.1073/pnas.1315156111 Sidhu, 2006, Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin, J. Infect. Dis., 194, 528, 10.1086/507115 Singh, 2017, Integrating genomics and proteomics permits identification of immunodominant antigens associated with drug resistance in human visceral leishmaniasis in India, Exp. Parasitol., 176, 30, 10.1016/j.exppara.2017.02.019 Song, 2000, Dichroa powder on the control effect of chicken coccidiosis, Chinese Veterinary Sci., 30, 37 Stephen, 1997, Studies of resistance to anticoccidials in Eimeria field isolates and pure Eimeria strains, Vet. Parasitol., 69, 19, 10.1016/S0304-4017(96)01096-5 Thabet, 2017, Quantitative proteomic studies in resistance mechanisms of Eimeria tenella against polyether ionophores, Parasitol. Res., 116, 1553, 10.1007/s00436-017-5432-z Tomley, 1997, Techniques for isolation and characterization of apical organelles from Eimeria tenella sporozoites, Methods, 13, 171, 10.1006/meth.1997.0509 Tomley, 1996, Molecular cloning and characterization of a novel acidic microneme protein (Etmic-2) from the apicomplexan protozoan parasite, Eimeria tenella. Mol Biochem Parasitol, 79, 195, 10.1016/0166-6851(96)02662-X Vanegas, 2007, Enolase as a plasminogen binding protein in Leishmania mexicana, Parasitol. Res., 101, 1511, 10.1007/s00436-007-0668-7 Vanparijs, 1989, Diclazuril, a new broad spectrum anticoccidial drug in chickens. 1. Dose titration studies and pilot floor pen trials, Poultry Sci., 68, 489, 10.3382/ps.0680489 Waletzky, 1954, A field strain of Eimeria tenella resistant to sulfonamides, J. Parasitol., 4, 24 Wang, 2019, Laboratory induction of salamycin resistant strains of Eimeria tenella, Chin. J. Anim. Infect. Dis., 1–9 Wang, 2010, Cloning and differential expression analysis of enolase gene of Moniezia expansa, Chinese Veterinary Sci., 40, 572 Wicht, 2020, Molecular mechanisms of drug resistance in Plasmodium falciparum malaria, Annu. Rev. Microbiol., 74, 431, 10.1146/annurev-micro-020518-115546 Xie, 2020, Comparative transcriptome analyses of drug-sensitive and drug-resistant strains of Eimeria tenella by RNA-sequencing, J. Eukaryot. Microbiol., 67, 1 Yang, 2019, Decreased K13 abundance reduces hemoglobin catabolism and proteotoxic stress, underpinning artemisinin resistance, Cell Rep., 29, 2917, 10.1016/j.celrep.2019.10.095 Yoshimura, 2021, Small-scale hypoxic cultures for monitoring the spatial reorganization of glycolytic enzymes in Saccharomyces cerevisiae, Cell Biol. Int., 45, 1776, 10.1002/cbin.11617 Zhang, 2014, Enolase of Angiostrongylus cantonensis: more likely a structural component?, Parasitol. Res., 113, 3927, 10.1007/s00436-014-4056-9 Zhou, 2010, Eimeria tenella: effects of diclazuril treatment on microneme genes expression in second-generation merozoites and pathological changes of caeca in parasitized chickens, Exp. Parasitol., 125, 264, 10.1016/j.exppara.2010.01.022