Cargando…

Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria

Malaria remains one of the greatest public health challenges worldwide, particularly in sub-Saharan Africa. The clinical outcome of individuals infected with Plasmodium falciparum parasites depends on many factors including host systemic inflammatory responses, parasite sequestration in tissues and...

Descripción completa

Detalles Bibliográficos
Autores principales: Mantel, Pierre-Yves, Hjelmqvist, Daisy, Walch, Michael, Kharoubi-Hess, Solange, Nilsson, Sandra, Ravel, Deepali, Ribeiro, Marina, Grüring, Christof, Ma, Siyuan, Padmanabhan, Prasad, Trachtenberg, Alexander, Ankarklev, Johan, Brancucci, Nicolas M., Huttenhower, Curtis, Duraisingh, Manoj T., Ghiran, Ionita, Kuo, Winston P., Filgueira, Luis, Martinelli, Roberta, Marti, Matthias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5062468/
https://www.ncbi.nlm.nih.gov/pubmed/27721445
http://dx.doi.org/10.1038/ncomms12727
_version_ 1782459784963817472
author Mantel, Pierre-Yves
Hjelmqvist, Daisy
Walch, Michael
Kharoubi-Hess, Solange
Nilsson, Sandra
Ravel, Deepali
Ribeiro, Marina
Grüring, Christof
Ma, Siyuan
Padmanabhan, Prasad
Trachtenberg, Alexander
Ankarklev, Johan
Brancucci, Nicolas M.
Huttenhower, Curtis
Duraisingh, Manoj T.
Ghiran, Ionita
Kuo, Winston P.
Filgueira, Luis
Martinelli, Roberta
Marti, Matthias
author_facet Mantel, Pierre-Yves
Hjelmqvist, Daisy
Walch, Michael
Kharoubi-Hess, Solange
Nilsson, Sandra
Ravel, Deepali
Ribeiro, Marina
Grüring, Christof
Ma, Siyuan
Padmanabhan, Prasad
Trachtenberg, Alexander
Ankarklev, Johan
Brancucci, Nicolas M.
Huttenhower, Curtis
Duraisingh, Manoj T.
Ghiran, Ionita
Kuo, Winston P.
Filgueira, Luis
Martinelli, Roberta
Marti, Matthias
author_sort Mantel, Pierre-Yves
collection PubMed
description Malaria remains one of the greatest public health challenges worldwide, particularly in sub-Saharan Africa. The clinical outcome of individuals infected with Plasmodium falciparum parasites depends on many factors including host systemic inflammatory responses, parasite sequestration in tissues and vascular dysfunction. Production of pro-inflammatory cytokines and chemokines promotes endothelial activation as well as recruitment and infiltration of inflammatory cells, which in turn triggers further endothelial cell activation and parasite sequestration. Inflammatory responses are triggered in part by bioactive parasite products such as hemozoin and infected red blood cell-derived extracellular vesicles (iRBC-derived EVs). Here we demonstrate that such EVs contain functional miRNA-Argonaute 2 complexes that are derived from the host RBC. Moreover, we show that EVs are efficiently internalized by endothelial cells, where the miRNA-Argonaute 2 complexes modulate target gene expression and barrier properties. Altogether, these findings provide a mechanistic link between EVs and vascular dysfunction during malaria infection.
format Online
Article
Text
id pubmed-5062468
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-50624682016-10-27 Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria Mantel, Pierre-Yves Hjelmqvist, Daisy Walch, Michael Kharoubi-Hess, Solange Nilsson, Sandra Ravel, Deepali Ribeiro, Marina Grüring, Christof Ma, Siyuan Padmanabhan, Prasad Trachtenberg, Alexander Ankarklev, Johan Brancucci, Nicolas M. Huttenhower, Curtis Duraisingh, Manoj T. Ghiran, Ionita Kuo, Winston P. Filgueira, Luis Martinelli, Roberta Marti, Matthias Nat Commun Article Malaria remains one of the greatest public health challenges worldwide, particularly in sub-Saharan Africa. The clinical outcome of individuals infected with Plasmodium falciparum parasites depends on many factors including host systemic inflammatory responses, parasite sequestration in tissues and vascular dysfunction. Production of pro-inflammatory cytokines and chemokines promotes endothelial activation as well as recruitment and infiltration of inflammatory cells, which in turn triggers further endothelial cell activation and parasite sequestration. Inflammatory responses are triggered in part by bioactive parasite products such as hemozoin and infected red blood cell-derived extracellular vesicles (iRBC-derived EVs). Here we demonstrate that such EVs contain functional miRNA-Argonaute 2 complexes that are derived from the host RBC. Moreover, we show that EVs are efficiently internalized by endothelial cells, where the miRNA-Argonaute 2 complexes modulate target gene expression and barrier properties. Altogether, these findings provide a mechanistic link between EVs and vascular dysfunction during malaria infection. Nature Publishing Group 2016-10-10 /pmc/articles/PMC5062468/ /pubmed/27721445 http://dx.doi.org/10.1038/ncomms12727 Text en Copyright © 2016, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Mantel, Pierre-Yves
Hjelmqvist, Daisy
Walch, Michael
Kharoubi-Hess, Solange
Nilsson, Sandra
Ravel, Deepali
Ribeiro, Marina
Grüring, Christof
Ma, Siyuan
Padmanabhan, Prasad
Trachtenberg, Alexander
Ankarklev, Johan
Brancucci, Nicolas M.
Huttenhower, Curtis
Duraisingh, Manoj T.
Ghiran, Ionita
Kuo, Winston P.
Filgueira, Luis
Martinelli, Roberta
Marti, Matthias
Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title_full Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title_fullStr Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title_full_unstemmed Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title_short Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria
title_sort infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory ago2-mirna complexes in malaria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5062468/
https://www.ncbi.nlm.nih.gov/pubmed/27721445
http://dx.doi.org/10.1038/ncomms12727
work_keys_str_mv AT mantelpierreyves infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT hjelmqvistdaisy infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT walchmichael infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT kharoubihesssolange infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT nilssonsandra infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT raveldeepali infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT ribeiromarina infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT gruringchristof infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT masiyuan infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT padmanabhanprasad infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT trachtenbergalexander infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT ankarklevjohan infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT brancuccinicolasm infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT huttenhowercurtis infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT duraisinghmanojt infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT ghiranionita infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT kuowinstonp infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT filgueiraluis infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT martinelliroberta infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria
AT martimatthias infectederythrocytederivedextracellularvesiclesaltervascularfunctionviaregulatoryago2mirnacomplexesinmalaria