Extracellular vesicles from early stage Plasmodium falciparum‐infected red blood cells contain PfEMP1 and induce transcriptional changes in human monocytes

Pathogens can release extracellular vesicles (EVs) for cell–cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria parasite species, can transfer drug resistance genes between parasites. EVs from late‐stage parasite‐infected RBC (iRBC‐EVs) are immunostimulatory...

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Published inCellular microbiology Vol. 20; no. 5; pp. e12822 - n/a
Main Authors Sampaio, Natália G., Emery, Samantha J., Garnham, Alexandra L., Tan, Qiao Y., Sisquella, Xavier, Pimentel, Matthew A., Jex, Aaron R., Regev‐Rudzki, Neta, Schofield, Louis, Eriksson, Emily M.
Format Journal Article
LanguageEnglish
Published England Hindawi Limited 01.05.2018
Subjects
Animals
Cell Adhesion - genetics
Cell Communication - genetics
Cell interactions
Cell permeability
Cellular stress response
Cytokines
diseases
Drug resistance
Endothelial cells
Endothelial Cells - metabolism
Endothelial Cells - pathology
Erythrocytes
Erythrocytes - parasitology
Extracellular vesicles
Extracellular Vesicles - genetics
Extracellular Vesicles - metabolism
Gene expression
Host-Parasite Interactions - genetics
Humans
immunology
Immunostimulation
infection
Inflammation
Malaria
Malaria, Falciparum - blood
Malaria, Falciparum - genetics
Malaria, Falciparum - parasitology
Monocytes
Monocytes - metabolism
Monocytes - parasitology
Parasites
Pathogenesis
Plasmodium falciparum
Plasmodium falciparum - genetics
Plasmodium falciparum - pathogenicity
Proteins
Proteomics
Protozoan Proteins - genetics
Transcription
transcriptomics
Vector-borne diseases
Vesicles
Virulence
Virulence factors
transcriptomics
diseases
infection
extracellular vesicles
proteomics
immunology
Online AccessGet full text

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Abstract Pathogens can release extracellular vesicles (EVs) for cell–cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria parasite species, can transfer drug resistance genes between parasites. EVs from late‐stage parasite‐infected RBC (iRBC‐EVs) are immunostimulatory and affect endothelial cell permeability, but little is known about EVs from early stage iRBC. We detected the parasite virulence factor PfEMP1, which is responsible for iRBC adherence and a major contributor to disease severity, in EVs, only up to 12‐hr post‐RBC invasion. Furthermore, using PfEMP1 transport knockout parasites, we determined that EVs originated from inside the iRBC rather than the iRBC surface. Proteomic analysis detected 101 parasite and 178 human proteins in iRBC‐EVs. Primary human monocytes stimulated with iRBC‐EVs released low levels of inflammatory cytokines and showed transcriptomic changes. Stimulation with iRBC‐EVs from PfEMP1 knockout parasites induced more gene expression changes and affected pathways involved in defence response, stress response, and response to cytokines, suggesting a novel function of PfEMP1 when present in EVs. We show for the first time the presence of PfEMP1 in early stage P. falciparum iRBC‐EVs and the effects of these EVs on primary human monocytes, uncovering a new mechanism of potential parasite pathogenesis and host interaction. Extracellular vesicles from Plasmodium falciparum‐infected red blood cells were found to contain PfEMP1, a key parasite virulence factor. PfEMP1 was only present in vesicles during the first 12 hours of infection. Vesicles induced transcriptional changes in human monocytes, which were partially dependent on PfEMP1, suggesting a novel mechanism of host modulation by the parasite.
AbstractList Pathogens can release extracellular vesicles (EVs) for cell–cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria parasite species, can transfer drug resistance genes between parasites. EVs from late‐stage parasite‐infected RBC (iRBC‐EVs) are immunostimulatory and affect endothelial cell permeability, but little is known about EVs from early stage iRBC. We detected the parasite virulence factor PfEMP1, which is responsible for iRBC adherence and a major contributor to disease severity, in EVs, only up to 12‐hr post‐RBC invasion. Furthermore, using PfEMP1 transport knockout parasites, we determined that EVs originated from inside the iRBC rather than the iRBC surface. Proteomic analysis detected 101 parasite and 178 human proteins in iRBC‐EVs. Primary human monocytes stimulated with iRBC‐EVs released low levels of inflammatory cytokines and showed transcriptomic changes. Stimulation with iRBC‐EVs from PfEMP1 knockout parasites induced more gene expression changes and affected pathways involved in defence response, stress response, and response to cytokines, suggesting a novel function of PfEMP1 when present in EVs. We show for the first time the presence of PfEMP1 in early stage P. falciparum iRBC‐EVs and the effects of these EVs on primary human monocytes, uncovering a new mechanism of potential parasite pathogenesis and host interaction.
Pathogens can release extracellular vesicles (EVs) for cell-cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria parasite species, can transfer drug resistance genes between parasites. EVs from late-stage parasite-infected RBC (iRBC-EVs) are immunostimulatory and affect endothelial cell permeability, but little is known about EVs from early stage iRBC. We detected the parasite virulence factor PfEMP1, which is responsible for iRBC adherence and a major contributor to disease severity, in EVs, only up to 12-hr post-RBC invasion. Furthermore, using PfEMP1 transport knockout parasites, we determined that EVs originated from inside the iRBC rather than the iRBC surface. Proteomic analysis detected 101 parasite and 178 human proteins in iRBC-EVs. Primary human monocytes stimulated with iRBC-EVs released low levels of inflammatory cytokines and showed transcriptomic changes. Stimulation with iRBC-EVs from PfEMP1 knockout parasites induced more gene expression changes and affected pathways involved in defence response, stress response, and response to cytokines, suggesting a novel function of PfEMP1 when present in EVs. We show for the first time the presence of PfEMP1 in early stage P. falciparum iRBC-EVs and the effects of these EVs on primary human monocytes, uncovering a new mechanism of potential parasite pathogenesis and host interaction.
Pathogens can release extracellular vesicles (EVs) for cell–cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria parasite species, can transfer drug resistance genes between parasites. EVs from late‐stage parasite‐infected RBC (iRBC‐EVs) are immunostimulatory and affect endothelial cell permeability, but little is known about EVs from early stage iRBC. We detected the parasite virulence factor PfEMP1, which is responsible for iRBC adherence and a major contributor to disease severity, in EVs, only up to 12‐hr post‐RBC invasion. Furthermore, using PfEMP1 transport knockout parasites, we determined that EVs originated from inside the iRBC rather than the iRBC surface. Proteomic analysis detected 101 parasite and 178 human proteins in iRBC‐EVs. Primary human monocytes stimulated with iRBC‐EVs released low levels of inflammatory cytokines and showed transcriptomic changes. Stimulation with iRBC‐EVs from PfEMP1 knockout parasites induced more gene expression changes and affected pathways involved in defence response, stress response, and response to cytokines, suggesting a novel function of PfEMP1 when present in EVs. We show for the first time the presence of PfEMP1 in early stage P. falciparum iRBC‐EVs and the effects of these EVs on primary human monocytes, uncovering a new mechanism of potential parasite pathogenesis and host interaction. Extracellular vesicles from Plasmodium falciparum‐infected red blood cells were found to contain PfEMP1, a key parasite virulence factor. PfEMP1 was only present in vesicles during the first 12 hours of infection. Vesicles induced transcriptional changes in human monocytes, which were partially dependent on PfEMP1, suggesting a novel mechanism of host modulation by the parasite.
Author Eriksson, Emily M.
Emery, Samantha J.
Tan, Qiao Y.
Sisquella, Xavier
Regev‐Rudzki, Neta
Garnham, Alexandra L.
Schofield, Louis
Jex, Aaron R.
Pimentel, Matthew A.
Sampaio, Natália G.
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Issue 5
Keywords transcriptomics
diseases
infection
extracellular vesicles
proteomics
immunology
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Snippet Pathogens can release extracellular vesicles (EVs) for cell–cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria...
Pathogens can release extracellular vesicles (EVs) for cell-cell communication and host modulation. EVs from Plasmodium falciparum, the deadliest malaria...
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SubjectTerms Animals
Cell Adhesion - genetics
Cell Communication - genetics
Cell interactions
Cell permeability
Cellular stress response
Cytokines
diseases
Drug resistance
Endothelial cells
Endothelial Cells - metabolism
Endothelial Cells - pathology
Erythrocytes
Erythrocytes - parasitology
Extracellular vesicles
Extracellular Vesicles - genetics
Extracellular Vesicles - metabolism
Gene expression
Host-Parasite Interactions - genetics
Humans
immunology
Immunostimulation
infection
Inflammation
Malaria
Malaria, Falciparum - blood
Malaria, Falciparum - genetics
Malaria, Falciparum - parasitology
Monocytes
Monocytes - metabolism
Monocytes - parasitology
Parasites
Pathogenesis
Plasmodium falciparum
Plasmodium falciparum - genetics
Plasmodium falciparum - pathogenicity
Proteins
Proteomics
Protozoan Proteins - genetics
Transcription
transcriptomics
Vector-borne diseases
Vesicles
Virulence
Virulence factors
Title Extracellular vesicles from early stage Plasmodium falciparum‐infected red blood cells contain PfEMP1 and induce transcriptional changes in human monocytes
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcmi.12822
https://www.ncbi.nlm.nih.gov/pubmed/29349926
https://www.proquest.com/docview/2023134793
https://search.proquest.com/docview/1989600876
Volume 20
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