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Phenotypic characterization of acoustically enriched extracellular vesicles from pathogen-activated platelets

Palm, Frida LU ; Broman, Axel LU ; Marcoux, Genevieve LU ; Semple, John W LU ; Laurell, Thomas L LU ; Malmström, Johan LU orcid and Shannon, Oonagh LU (2023) In Journal of Innate Immunity 15(1). p.599-613
Abstract

Extracellular vesicles (EVs) are derived from the membrane of platelets and released in the circulation upon activation or injury. Analogous to the parent cell, platelet derived EVs play an important role in hemostasis and immune responses by transfer of bioactive cargo from the parent cells. Platelet activation and release of EVs increases in several pathological inflammatory diseases, such as sepsis. We have previously reported that the M1 protein released from the bacterial pathogen Streptococcus pyogenes directly mediates platelet activation. In this study, EVs were isolated from these pathogen-activated platelets using acoustic trapping and their inflammation phenotype was characterized using quantitative mass spectrometry-based... (More)

Extracellular vesicles (EVs) are derived from the membrane of platelets and released in the circulation upon activation or injury. Analogous to the parent cell, platelet derived EVs play an important role in hemostasis and immune responses by transfer of bioactive cargo from the parent cells. Platelet activation and release of EVs increases in several pathological inflammatory diseases, such as sepsis. We have previously reported that the M1 protein released from the bacterial pathogen Streptococcus pyogenes directly mediates platelet activation. In this study, EVs were isolated from these pathogen-activated platelets using acoustic trapping and their inflammation phenotype was characterized using quantitative mass spectrometry-based proteomics and cell-based models of inflammation. We determined that M1 protein mediated release of platelet derived EVs that contained the M1 protein. The isolated EVs derived from pathogen-activated platelets contained a similar protein cargo to those from physiologically activated platelets (thrombin), and included platelet membrane proteins, granule proteins and cytoskeletal proteins, coagulation factors and immune mediators. Immunomodulatory cargo, complement proteins and IgG3, were significantly enriched in EVs isolated from M1 protein-stimulated platelets. Acoustically enriched EVs were functionally intact and exhibited proinflammatory effects on addition to blood, including platelet-neutrophil complex formation, neutrophil activation, and cytokine release. Collectively, our findings reveal novel aspects of pathogen-mediated platelet activation during invasive streptococcal infection.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Journal of Innate Immunity
volume
15
issue
1
pages
15 pages
publisher
Karger
external identifiers
  • scopus:85181177709
  • pmid:37245510
ISSN
1662-811X
DOI
10.1159/000531266
language
English
LU publication?
yes
additional info
The Author(s). Published by S. Karger AG, Basel.
id
de3d78ff-9b26-4242-9249-bdf2537350ee
date added to LUP
2023-06-05 13:25:49
date last changed
2024-04-17 01:19:27
@article{de3d78ff-9b26-4242-9249-bdf2537350ee,
  abstract     = {{<p>Extracellular vesicles (EVs) are derived from the membrane of platelets and released in the circulation upon activation or injury. Analogous to the parent cell, platelet derived EVs play an important role in hemostasis and immune responses by transfer of bioactive cargo from the parent cells. Platelet activation and release of EVs increases in several pathological inflammatory diseases, such as sepsis. We have previously reported that the M1 protein released from the bacterial pathogen Streptococcus pyogenes directly mediates platelet activation. In this study, EVs were isolated from these pathogen-activated platelets using acoustic trapping and their inflammation phenotype was characterized using quantitative mass spectrometry-based proteomics and cell-based models of inflammation. We determined that M1 protein mediated release of platelet derived EVs that contained the M1 protein. The isolated EVs derived from pathogen-activated platelets contained a similar protein cargo to those from physiologically activated platelets (thrombin), and included platelet membrane proteins, granule proteins and cytoskeletal proteins, coagulation factors and immune mediators. Immunomodulatory cargo, complement proteins and IgG3, were significantly enriched in EVs isolated from M1 protein-stimulated platelets. Acoustically enriched EVs were functionally intact and exhibited proinflammatory effects on addition to blood, including platelet-neutrophil complex formation, neutrophil activation, and cytokine release. Collectively, our findings reveal novel aspects of pathogen-mediated platelet activation during invasive streptococcal infection.</p>}},
  author       = {{Palm, Frida and Broman, Axel and Marcoux, Genevieve and Semple, John W and Laurell, Thomas L and Malmström, Johan and Shannon, Oonagh}},
  issn         = {{1662-811X}},
  language     = {{eng}},
  month        = {{05}},
  number       = {{1}},
  pages        = {{599--613}},
  publisher    = {{Karger}},
  series       = {{Journal of Innate Immunity}},
  title        = {{Phenotypic characterization of acoustically enriched extracellular vesicles from pathogen-activated platelets}},
  url          = {{http://dx.doi.org/10.1159/000531266}},
  doi          = {{10.1159/000531266}},
  volume       = {{15}},
  year         = {{2023}},
}