The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst
Abstract Paragonimiasis is a zoonotic, food-borne trematode infection that affects 21 million people globally. Trematodes interact with their hosts via extracellular vesicles (EV) that carry protein and RNA cargo. We analyzed EV in excretory-secretory products (ESP) released by Paragonimus kellicott...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
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Nature Portfolio
2023-08-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-39966-x |
| _version_ | 1797453020892495872 |
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| author | Lucia S. Di Maggio Kerstin Fischer Devyn Yates Kurt C. Curtis Bruce A. Rosa John Martin Petra Erdmann-Gilmore Robert S. W. Sprung Makedonka Mitreva R. Reid Townsend Gary J. Weil Peter U. Fischer |
| author_facet | Lucia S. Di Maggio Kerstin Fischer Devyn Yates Kurt C. Curtis Bruce A. Rosa John Martin Petra Erdmann-Gilmore Robert S. W. Sprung Makedonka Mitreva R. Reid Townsend Gary J. Weil Peter U. Fischer |
| author_sort | Lucia S. Di Maggio |
| collection | DOAJ |
| description | Abstract Paragonimiasis is a zoonotic, food-borne trematode infection that affects 21 million people globally. Trematodes interact with their hosts via extracellular vesicles (EV) that carry protein and RNA cargo. We analyzed EV in excretory-secretory products (ESP) released by Paragonimus kellicotti adult worms cultured in vitro (EV ESP) and EV isolated from lung cyst fluid (EV CFP) recovered from infected gerbils. The majority of EV were approximately 30–50 nm in diameter. We identified 548 P. kellicotti-derived proteins in EV ESP by mass spectrometry and 8 proteins in EV CFP of which 7 were also present in EV ESP. No parasite-derived proteins were reliably detected in EV isolated from plasma samples. A cysteine protease (MK050848, CP-6) was the most abundant protein found in EV CFP in all technical and biological replicates. Immunolocalization of CP-6 showed strong labeling in the tegument of P. kellicotti and in the adjacent cyst and lung tissue that contained worm eggs. It is likely that CP-6 present in EV is involved in parasite-host interactions. These results provide new insights into interactions between Paragonimus and their mammalian hosts, and they provide potential clues for development of novel diagnostic tools and treatments. |
| first_indexed | 2024-03-09T15:16:50Z |
| format | Article |
| id | doaj.art-ad1736ee439c48df8c879adcd35181d2 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-09T15:16:50Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-ad1736ee439c48df8c879adcd35181d22023-11-26T13:04:00ZengNature PortfolioScientific Reports2045-23222023-08-0113111110.1038/s41598-023-39966-xThe proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cystLucia S. Di Maggio0Kerstin Fischer1Devyn Yates2Kurt C. Curtis3Bruce A. Rosa4John Martin5Petra Erdmann-Gilmore6Robert S. W. Sprung7Makedonka Mitreva8R. Reid Townsend9Gary J. Weil10Peter U. Fischer11Division of Infectious Diseases, Department of Medicine, Washington University School of MedicineDivision of Infectious Diseases, Department of Medicine, Washington University School of MedicineDivision of Infectious Diseases, Department of Medicine, Washington University School of MedicineDivision of Infectious Diseases, Department of Medicine, Washington University School of MedicineDepartment of Internal Medicine, Washington University of St. Louis School of MedicineDepartment of Internal Medicine, Washington University of St. Louis School of MedicineDivision of Endocrinology, Metabolism and Lipid Research, Department of Medicine, Washington University School of MedicineDivision of Endocrinology, Metabolism and Lipid Research, Department of Medicine, Washington University School of MedicineDepartment of Internal Medicine, Washington University of St. Louis School of MedicineDivision of Endocrinology, Metabolism and Lipid Research, Department of Medicine, Washington University School of MedicineDivision of Infectious Diseases, Department of Medicine, Washington University School of MedicineDivision of Infectious Diseases, Department of Medicine, Washington University School of MedicineAbstract Paragonimiasis is a zoonotic, food-borne trematode infection that affects 21 million people globally. Trematodes interact with their hosts via extracellular vesicles (EV) that carry protein and RNA cargo. We analyzed EV in excretory-secretory products (ESP) released by Paragonimus kellicotti adult worms cultured in vitro (EV ESP) and EV isolated from lung cyst fluid (EV CFP) recovered from infected gerbils. The majority of EV were approximately 30–50 nm in diameter. We identified 548 P. kellicotti-derived proteins in EV ESP by mass spectrometry and 8 proteins in EV CFP of which 7 were also present in EV ESP. No parasite-derived proteins were reliably detected in EV isolated from plasma samples. A cysteine protease (MK050848, CP-6) was the most abundant protein found in EV CFP in all technical and biological replicates. Immunolocalization of CP-6 showed strong labeling in the tegument of P. kellicotti and in the adjacent cyst and lung tissue that contained worm eggs. It is likely that CP-6 present in EV is involved in parasite-host interactions. These results provide new insights into interactions between Paragonimus and their mammalian hosts, and they provide potential clues for development of novel diagnostic tools and treatments.https://doi.org/10.1038/s41598-023-39966-x |
| spellingShingle | Lucia S. Di Maggio Kerstin Fischer Devyn Yates Kurt C. Curtis Bruce A. Rosa John Martin Petra Erdmann-Gilmore Robert S. W. Sprung Makedonka Mitreva R. Reid Townsend Gary J. Weil Peter U. Fischer The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst Scientific Reports |
| title | The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst |
| title_full | The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst |
| title_fullStr | The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst |
| title_full_unstemmed | The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst |
| title_short | The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst |
| title_sort | proteome of extracellular vesicles of the lung fluke paragonimus kellicotti produced in vitro and in the lung cyst |
| url | https://doi.org/10.1038/s41598-023-39966-x |
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