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The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst

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 w...

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Autores principales: Di Maggio, Lucia S., Fischer, Kerstin, Yates, Devyn, Curtis, Kurt C., Rosa, Bruce A., Martin, John, Erdmann-Gilmore, Petra, Sprung, Robert S. W., Mitreva, Makedonka, Townsend, R. Reid, Weil, Gary J., Fischer, Peter U.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10444896/
https://www.ncbi.nlm.nih.gov/pubmed/37608002
http://dx.doi.org/10.1038/s41598-023-39966-x
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author Di Maggio, Lucia S.
Fischer, Kerstin
Yates, Devyn
Curtis, Kurt C.
Rosa, Bruce A.
Martin, John
Erdmann-Gilmore, Petra
Sprung, Robert S. W.
Mitreva, Makedonka
Townsend, R. Reid
Weil, Gary J.
Fischer, Peter U.
author_facet Di Maggio, Lucia S.
Fischer, Kerstin
Yates, Devyn
Curtis, Kurt C.
Rosa, Bruce A.
Martin, John
Erdmann-Gilmore, Petra
Sprung, Robert S. W.
Mitreva, Makedonka
Townsend, R. Reid
Weil, Gary J.
Fischer, Peter U.
author_sort Di Maggio, Lucia S.
collection PubMed
description 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.
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spelling pubmed-104448962023-08-24 The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst Di Maggio, Lucia S. Fischer, Kerstin Yates, Devyn Curtis, Kurt C. Rosa, Bruce A. Martin, John Erdmann-Gilmore, Petra Sprung, Robert S. W. Mitreva, Makedonka Townsend, R. Reid Weil, Gary J. Fischer, Peter U. Sci Rep Article 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. Nature Publishing Group UK 2023-08-22 /pmc/articles/PMC10444896/ /pubmed/37608002 http://dx.doi.org/10.1038/s41598-023-39966-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Di Maggio, Lucia S.
Fischer, Kerstin
Yates, Devyn
Curtis, Kurt C.
Rosa, Bruce A.
Martin, John
Erdmann-Gilmore, Petra
Sprung, Robert S. W.
Mitreva, Makedonka
Townsend, R. Reid
Weil, Gary J.
Fischer, Peter U.
The proteome of extracellular vesicles of the lung fluke Paragonimus kellicotti produced in vitro and in the lung cyst
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
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10444896/
https://www.ncbi.nlm.nih.gov/pubmed/37608002
http://dx.doi.org/10.1038/s41598-023-39966-x
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