Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix
Abstract Background The durable oocyst wall formed from the contents of wall-forming bodies (WFBs) protects Eimeria parasites from harsh conditions and enhances parasite transmission. Comprehending the contents of WFBs and proteins involved in oocyst wall formation is pivotal to understanding the me...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-023-06076-6 |
| _version_ | 1797377108453883904 |
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| author | Lele Wang Dandan Liu Yu Zhu Feiyan Wang Weimin Cai Qianqian Feng Shijie Su Zhaofeng Hou Jinjun Xu Junjie Hu Jianping Tao |
| author_facet | Lele Wang Dandan Liu Yu Zhu Feiyan Wang Weimin Cai Qianqian Feng Shijie Su Zhaofeng Hou Jinjun Xu Junjie Hu Jianping Tao |
| author_sort | Lele Wang |
| collection | DOAJ |
| description | Abstract Background The durable oocyst wall formed from the contents of wall-forming bodies (WFBs) protects Eimeria parasites from harsh conditions and enhances parasite transmission. Comprehending the contents of WFBs and proteins involved in oocyst wall formation is pivotal to understanding the mechanism of the oocyst wall formation and the search for novel targets to disrupt parasite transmission. Methods Total proteins extracted from WFBs and the oocyst wall of Eimeria necatrix were subjected to comparative proteomic analysis using tandem mass tag in conjunction with liquid chromatography tandem-mass spectrometry techniques. After functional clustering analysis of the identified proteins, three proteins, including E. necatrix disulfide isomerase (EnPDI), thioredoxin (EnTrx) and phosphoglycerate kinase (EnPGK), were selected for further study to confirm their potential roles in oocyst wall formation. Results A total of 3009 and 2973 proteins were identified from WFBs and the oocyst wall of E. necatrix, respectively. Among these proteins, 1102 were identified as differentially expressed proteins, of which 506 were upregulated and 596 downregulated in the oocyst wall compared to the WFBs. A total of 108 proteins, including compositional proteins of the oocyst wall, proteases, oxidoreductases, proteins involved in glycosylation, proteins involved in synthesis of the acid-fast lipid layer and proteins related to transport, were proposed to be involved in oocyst wall formation. The approximate molecular sizes of native EnPDI, EnTrx and EnPGK proteins were 55, 50 and 45 kDa, respectively. EnPDI was present in both type 1 and type 2 WFBs, EnTrx was present only in type 2 WFB2 and EnPGK was present only in type 1 WFBs, whereas all of them were localized to the outer layer of the oocyst wall, indicating that all of them participate in the formation of the oocyst wall. Conclusions To the best of our knowledge, this is the first report on the proteomes of WFBs and the oocyst wall of E. necatrix. The data obtained from this study form a basis for deciphering the molecular mechanisms underlying oocyst wall formation of Eimeria parasites. They also provide valuable resources for future studies on the development of novel therapeutic agents and vaccines aimed at combating coccidian transmission. Graphical Abstract |
| first_indexed | 2024-03-08T19:49:13Z |
| format | Article |
| id | doaj.art-4c0b6ee2fd9041a888e27ef345e64300 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-03-08T19:49:13Z |
| publishDate | 2023-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-4c0b6ee2fd9041a888e27ef345e643002023-12-24T12:11:02ZengBMCParasites & Vectors1756-33052023-12-0116112310.1186/s13071-023-06076-6Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrixLele Wang0Dandan Liu1Yu Zhu2Feiyan Wang3Weimin Cai4Qianqian Feng5Shijie Su6Zhaofeng Hou7Jinjun Xu8Junjie Hu9Jianping Tao10College of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversityCollege of Veterinary Medicine, Yangzhou UniversitySchool of Ecology and Environmental Sciences and Yunnan Key Laboratory for Plateau Mountain Ecology and Restoration of Degraded Environments, Yunnan UniversityCollege of Veterinary Medicine, Yangzhou UniversityAbstract Background The durable oocyst wall formed from the contents of wall-forming bodies (WFBs) protects Eimeria parasites from harsh conditions and enhances parasite transmission. Comprehending the contents of WFBs and proteins involved in oocyst wall formation is pivotal to understanding the mechanism of the oocyst wall formation and the search for novel targets to disrupt parasite transmission. Methods Total proteins extracted from WFBs and the oocyst wall of Eimeria necatrix were subjected to comparative proteomic analysis using tandem mass tag in conjunction with liquid chromatography tandem-mass spectrometry techniques. After functional clustering analysis of the identified proteins, three proteins, including E. necatrix disulfide isomerase (EnPDI), thioredoxin (EnTrx) and phosphoglycerate kinase (EnPGK), were selected for further study to confirm their potential roles in oocyst wall formation. Results A total of 3009 and 2973 proteins were identified from WFBs and the oocyst wall of E. necatrix, respectively. Among these proteins, 1102 were identified as differentially expressed proteins, of which 506 were upregulated and 596 downregulated in the oocyst wall compared to the WFBs. A total of 108 proteins, including compositional proteins of the oocyst wall, proteases, oxidoreductases, proteins involved in glycosylation, proteins involved in synthesis of the acid-fast lipid layer and proteins related to transport, were proposed to be involved in oocyst wall formation. The approximate molecular sizes of native EnPDI, EnTrx and EnPGK proteins were 55, 50 and 45 kDa, respectively. EnPDI was present in both type 1 and type 2 WFBs, EnTrx was present only in type 2 WFB2 and EnPGK was present only in type 1 WFBs, whereas all of them were localized to the outer layer of the oocyst wall, indicating that all of them participate in the formation of the oocyst wall. Conclusions To the best of our knowledge, this is the first report on the proteomes of WFBs and the oocyst wall of E. necatrix. The data obtained from this study form a basis for deciphering the molecular mechanisms underlying oocyst wall formation of Eimeria parasites. They also provide valuable resources for future studies on the development of novel therapeutic agents and vaccines aimed at combating coccidian transmission. Graphical Abstracthttps://doi.org/10.1186/s13071-023-06076-6Eimeria necatrixWall-forming bodiesOocyst wallTandem mass tagComparative proteomicsDifferentially expressed proteins |
| spellingShingle | Lele Wang Dandan Liu Yu Zhu Feiyan Wang Weimin Cai Qianqian Feng Shijie Su Zhaofeng Hou Jinjun Xu Junjie Hu Jianping Tao Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix Parasites & Vectors Eimeria necatrix Wall-forming bodies Oocyst wall Tandem mass tag Comparative proteomics Differentially expressed proteins |
| title | Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix |
| title_full | Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix |
| title_fullStr | Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix |
| title_full_unstemmed | Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix |
| title_short | Comparative proteomic analysis of wall-forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in Eimeria necatrix |
| title_sort | comparative proteomic analysis of wall forming bodies and oocyst wall reveals the molecular basis underlying oocyst wall formation in eimeria necatrix |
| topic | Eimeria necatrix Wall-forming bodies Oocyst wall Tandem mass tag Comparative proteomics Differentially expressed proteins |
| url | https://doi.org/10.1186/s13071-023-06076-6 |
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