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Membrane-shed vesicles from the parasite Trichomonas vaginalis: characterization and their association with cell interaction

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Abstract

Trichomonas vaginalis is a common sexually transmitted parasite that colonizes the human urogenital tract, where it remains extracellular and adheres to epithelial cells. Infections range from asymptomatic to highly inflammatory, depending on the host and the parasite strain. Despite the serious consequences associated with trichomoniasis disease, little is known about parasite or host factors involved in attachment of the parasite-to-host epithelial cells. Here, we report the identification of microvesicle-like structures (MVs) released by T. vaginalis. MVs are considered universal transport vehicles for intercellular communication as they can incorporate peptides, proteins, lipids, miRNA, and mRNA, all of which can be transferred to target cells through receptor–ligand interactions, fusion with the cell membrane, and delivery of a functional cargo to the cytoplasm of the target cell. In the present study, we demonstrated that T. vaginalis release MVs from the plasma and the flagellar membranes of the parasite. We performed proteomic profiling of these structures demonstrating that they possess physical characteristics similar to mammalian extracellular vesicles and might be selectively charged with specific protein content. In addition, we demonstrated that viable T. vaginalis parasites release large vesicles (LVs), membrane structures larger than 1 µm that are able to interact with other parasites and with the host cell. Finally, we show that both populations of vesicles present on the surface of T vaginalis are induced in the presence of host cells, consistent with a role in modulating cell interactions.

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Abbreviations

MVs:

Microvesicles

miRNA:

Microribonucleic acid

mRNA:

Mature ribonucleic acid

WHO:

World health organization

HIV:

Human immunodeficiency virus

EVs:

Extracellular vesicles

MVB:

Multivesicular body

DNA:

Desoxyribonucleic acid

TYM:

Trypticase, yeast extract, maltose medium

DMEM:

Dulbecco’s modified eagle medium

PBS:

Phosphate-buffered saline

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscopy

NSAF:

Normalized spectral abundance factor

GO:

Gene ontology

BLAST:

Basic local alignment sequence tool

LVs:

Large vesicles

FBS:

Fetal bovine serum

HA:

Hemagglutinin

FITC:

Fluorescein isothiocyanate

PI:

Propidium iodide

CMTPX:

Cell tracker red

SD:

Standard deviation

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

BspA:

Basic surface-exposed protein

ARF:

ADP-ribosylation factor

ESTs:

Expressed sequence tags

GP63:

Glycoprotein 63

VAMP:

Vesicle-associated membrane proteins

LO:

Large oncosome

PM:

Plasma membrane

F:

Flagella

AF:

Anterior flagella

Ax:

Axostyle

TMD:

Transmembrane domain

TrichDB:

Trichomonas genomic resource

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Acknowledgements

We thank our colleagues in the lab for helpful discussions. This research was supported with a Grant from the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) Grant BID PICT 2013–1184 (NdM), a collaborative Grant from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (NdM and MB) and a National Institute of Health Grant (NIH) AI103182 (PJJ). NdM and VMC are researchers from the National Council of Research (CONICET) and UNSAM. YRN is a PhD fellow from CONICET. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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18_2017_2726_MOESM1_ESM.xlsx

Table S1 List of microvesicles’ proteins identified by mass spectrometry. ID: official gene symbol; NSAFe: normalized spectral abundance factor; # TM domain: number of transmembrane domains (XLSX 166 kb)

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Nievas, Y.R., Coceres, V.M., Midlej, V. et al. Membrane-shed vesicles from the parasite Trichomonas vaginalis: characterization and their association with cell interaction. Cell. Mol. Life Sci. 75, 2211–2226 (2018). https://doi.org/10.1007/s00018-017-2726-3

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