Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host
Abstract Background Extracellular vesicles (EVs) are membranous structures that are formed during pathophysiology, host-parasite interactions and parasite motility. Typically, apicomplexan-infected host cells secrete EVs which traverse local and systemic strata of the host as the parasites develop....
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | Parasites & Vectors |
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| Online Access: | https://doi.org/10.1186/s13071-023-05906-x |
| _version_ | 1797453712449339392 |
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| author | Joshua Seun Olajide Zigang Qu Shunli Yang Bin Yang Xiao Xu Jing Wang Jianping Cai |
| author_facet | Joshua Seun Olajide Zigang Qu Shunli Yang Bin Yang Xiao Xu Jing Wang Jianping Cai |
| author_sort | Joshua Seun Olajide |
| collection | DOAJ |
| description | Abstract Background Extracellular vesicles (EVs) are membranous structures that are formed during pathophysiology, host-parasite interactions and parasite motility. Typically, apicomplexan-infected host cells secrete EVs which traverse local and systemic strata of the host as the parasites develop. Methods Extracellular vesicles were isolated from the caecum and serum of Eimeria falciformis-infected mice during oocyst ingestion (0 h post-infection [0 hpi]), merozont stages 1 and 2 (68 and 116 hpi), oocyst shedding (7 days post-infection [7 dpi]) and host recovery (10 dpi) and subsequently characterized and profiled by tandem mass tag (TMT). Results With the progression of E. falciformis life stages, subpopulation of EVs bearing EV biomarkers, including CD9, CD82, heat shock protein 70 (HSP70) and major histocompatibility complex (MHC) molecules, increased. A total of 860 and 1024 differentially expressed proteins were identified in serum EVs (sEVs) and caecum EVs (cEVs), respectively. Identified immune-related molecules (such as cytokines, receptors, immunoglobins, complements, hormones, inflammasomes), ion exchange and cell death-associated proteins were significantly expressed, at least during the E. falciformis first and second merozont stages. Bioinformatics assessment indicated that sEV proteins were at all time points implicated in antigen processing and presentation as well as natural killer cell-mediated cytotoxicity (68 hpi), complement activation/blood coagulation (116 hpi/10 dpi) and catabolic activities (7 dpi). In contrast, cEV proteins were involved in catabolic process, ion transport and antigen presentation (68 and 116 hpi). Host response to E. falciformis infection was similar to intestinal bacterium at 7 dpi and cell adhesion and intercellular protein transport at 10 dpi. In both systems, ferroptosis and necroptosis were common across the parasite’s infectious cycle while apoptosis occurred at 68 hpi. Conclusion The proteomic data indicate that E. falciformis infection co-opts cellular and humoral responses through EV secretions, and that, host cell death and ionic imbalance are associated with E. falciformis infection. This study offers additional insight into host-parasite interactions and host regulatory EV proteins as potential disease indicators or diagnostic molecules. Graphical Abstract |
| first_indexed | 2024-03-09T15:26:45Z |
| format | Article |
| id | doaj.art-e0098f78f7e847eca3247226225c8cc2 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-03-09T15:26:45Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
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| series | Parasites & Vectors |
| spelling | doaj.art-e0098f78f7e847eca3247226225c8cc22023-11-26T12:29:48ZengBMCParasites & Vectors1756-33052023-09-0116111710.1186/s13071-023-05906-xQuantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the hostJoshua Seun Olajide0Zigang Qu1Shunli Yang2Bin Yang3Xiao Xu4Jing Wang5Jianping Cai6State Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesAbstract Background Extracellular vesicles (EVs) are membranous structures that are formed during pathophysiology, host-parasite interactions and parasite motility. Typically, apicomplexan-infected host cells secrete EVs which traverse local and systemic strata of the host as the parasites develop. Methods Extracellular vesicles were isolated from the caecum and serum of Eimeria falciformis-infected mice during oocyst ingestion (0 h post-infection [0 hpi]), merozont stages 1 and 2 (68 and 116 hpi), oocyst shedding (7 days post-infection [7 dpi]) and host recovery (10 dpi) and subsequently characterized and profiled by tandem mass tag (TMT). Results With the progression of E. falciformis life stages, subpopulation of EVs bearing EV biomarkers, including CD9, CD82, heat shock protein 70 (HSP70) and major histocompatibility complex (MHC) molecules, increased. A total of 860 and 1024 differentially expressed proteins were identified in serum EVs (sEVs) and caecum EVs (cEVs), respectively. Identified immune-related molecules (such as cytokines, receptors, immunoglobins, complements, hormones, inflammasomes), ion exchange and cell death-associated proteins were significantly expressed, at least during the E. falciformis first and second merozont stages. Bioinformatics assessment indicated that sEV proteins were at all time points implicated in antigen processing and presentation as well as natural killer cell-mediated cytotoxicity (68 hpi), complement activation/blood coagulation (116 hpi/10 dpi) and catabolic activities (7 dpi). In contrast, cEV proteins were involved in catabolic process, ion transport and antigen presentation (68 and 116 hpi). Host response to E. falciformis infection was similar to intestinal bacterium at 7 dpi and cell adhesion and intercellular protein transport at 10 dpi. In both systems, ferroptosis and necroptosis were common across the parasite’s infectious cycle while apoptosis occurred at 68 hpi. Conclusion The proteomic data indicate that E. falciformis infection co-opts cellular and humoral responses through EV secretions, and that, host cell death and ionic imbalance are associated with E. falciformis infection. This study offers additional insight into host-parasite interactions and host regulatory EV proteins as potential disease indicators or diagnostic molecules. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05906-xExtracellular vesiclesProteinsEimeria falciformisTandem mass tagCoccidiosis |
| spellingShingle | Joshua Seun Olajide Zigang Qu Shunli Yang Bin Yang Xiao Xu Jing Wang Jianping Cai Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host Parasites & Vectors Extracellular vesicles Proteins Eimeria falciformis Tandem mass tag Coccidiosis |
| title | Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host |
| title_full | Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host |
| title_fullStr | Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host |
| title_full_unstemmed | Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host |
| title_short | Quantitative proteomic analysis of local and systemic extracellular vesicles during Eimeria falciformis infectious cycle in the host |
| title_sort | quantitative proteomic analysis of local and systemic extracellular vesicles during eimeria falciformis infectious cycle in the host |
| topic | Extracellular vesicles Proteins Eimeria falciformis Tandem mass tag Coccidiosis |
| url | https://doi.org/10.1186/s13071-023-05906-x |
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