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

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.

The Role of Small Extracellular Vesicles in Viral-Protozoan Symbiosis: Lessons From Trichomonasvirus in an Isogenic Host Parasite Model

“…Briefly, sEV preparations were diluted 1000× and 50,000× in PBS and quantified using the ZetaView ® (Particle Metrix, Meerbusch, Germany) by translational diffusion size distribution. Nanotracking analysis confirmed presence of sEVs from TV cultures in the peak size range of 76.6-106.9 nm similar to those previously reported for T. vaginalis (Twu et al, 2013;Olmos-Ortiz et al, 2017;Nievas et al, 2018) and at peak concentrations ranging from 1.1E9-1.65E11 particles/ml (Supplementary Figure S2A). Transmission electron microscopy with immunogold labelling of CD63 confirmed the presence of exosomes in the sEV samples (Supplementary Figure S2B).…”

Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: a critical review

“…Attachment of one trichomonad is shown to facilitate the enrolment of others, through the secretion of chemo-attractant [136]. A recent study reported the release of membrane vesicles from T. vaginalis surface that interact with target host cells through receptor or through fusion with target cell membrane to deliver certain signals important for this parasite pathogenesis [137].…”

Investigation of the Secretory Pathway in Trichomonas vaginalis Argues against a Moonlighting Function of Hydrogenosomal Enzymes

“…Proteomic analysis of exosomes and ectosomes revealed large numbers of proteins as their possible cargoes (215 and 592, respectively), including three paralogs of α‐SCS in exosomes and four paralogs of hydrogenosomal malic enzyme in ectosomes (Nievas et al. ; Twu et al. ).…”

“…(iii) T. vaginalis has been reported to release microvesicles that are derived from endocytic compartments (exosomes) or the plasma membrane (ectosomes). Proteomic analysis of exosomes and ectosomes revealed large numbers of proteins as their possible cargoes (215 and 592, respectively), including three paralogs of a-SCS in exosomes and four paralogs of hydrogenosomal malic enzyme in ectosomes (Nievas et al 2018;Twu et al 2013). These findings provide new potential modes of protein export and delivery to target cells; however, whether the two hydrogenosomal proteins represent specific cargoes in microvesicles needs to be experimentally verified.…”