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Cestode parasites release extracellular vesicles with microRNAs and immunodiagnostic protein cargo

María Eugenia Ancarola¹, Antonio Marcilla², Michaela Herz³

¹Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM, UBA-CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Paraguay 2155, Piso 13, Buenos Aires, Argentina.

International Journal for Parasitology

|July 3, 2017

Abstract:

Intercellular communication is crucial in multiple aspects of cell biology. This interaction can be mediated by several mechanisms including extracellular vesicle (EV) transfer. EV secretion by parasites has been reported in protozoans, trematodes and nematodes. Here we report that this mechanism is present in three different species of cestodes, Taenia crassiceps, Mesocestoides corti and Echinococcus multilocularis. To confirm this we determined, in vitro, the presence of EVs in culture supernatants by transmission electron microscopy. Interestingly, while T. crassiceps and M. corti metacestodes secrete membranous structures into the culture media, similar vesicles were observed in the interface of the germinal and laminated layers of E. multilocularis metacestodes and were hardly detected in culture supernatants. We then determined the protein cargo in the EV-enriched secreted fractions of T. crassiceps and M. corti conditioned media by LC-MS/MS. Among the identified proteins, eukaryotic vesicle-enriched proteins were identified as expected, but also proteins used for cestode disease diagnosis, proteins related to neurotransmission, lipid binding proteins as well as host immunoglobulins and complement factors. Finally, we confirmed by capillary electrophoresis the presence of intravesicular RNA for both parasites and detected microRNAs by reverse transcription-PCR. This is the first report of EV secretion in cestode parasites and of an RNA secretion mechanism. These findings will provide valuable data not only for basic cestode biology but also for the rational search for new diagnostic targets.

Insights

Cestode parasites, including Taenia crassiceps and Echinococcus multilocularis, secrete extracellular vesicles (EVs) containing RNA. This discovery reveals a novel RNA secretion mechanism in cestodes, offering potential new diagnostic targets.

Area of Science:

Parasitology
Cell Biology
Molecular Biology

Background:

Intercellular communication is vital for cell biology, often mediated by extracellular vesicles (EVs).
EV secretion has been documented in various parasitic organisms, including protozoans, trematodes, and nematodes.
However, the presence and function of EVs in cestode parasites remained largely unexplored.

Purpose of the Study:

To investigate the presence and characteristics of extracellular vesicle (EV) secretion in three distinct cestode species: Taenia crassiceps, Mesocestoides corti, and Echinococcus multilocularis.
To identify the molecular cargo, including proteins and RNA, within the secreted EVs.
To establish a novel RNA secretion mechanism in cestode parasites.

Main Methods:

In vitro culture of cestode metacestodes.
Transmission electron microscopy (TEM) for visualizing EVs.
Liquid chromatography-tandem mass spectrometry (LC-MS/MS) for protein cargo analysis.
Capillary electrophoresis and reverse transcription-polymerase chain reaction (RT-PCR) for RNA analysis.

Main Results:

EVs were detected in culture supernatants of Taenia crassiceps and Mesocestoides corti, and at the interface of germinal and laminated layers in Echinococcus multilocularis.
LC-MS/MS identified EV-enriched proteins, diagnostic proteins, neurotransmission-related proteins, lipid-binding proteins, host immunoglobulins, and complement factors in secreted fractions.
Capillary electrophoresis confirmed intravesicular RNA, and RT-PCR detected specific microRNAs in EVs from both parasites.

Conclusions:

This study provides the first evidence of extracellular vesicle (EV) secretion in cestode parasites.
A novel mechanism for RNA secretion via EVs in cestodes has been identified.
These findings offer valuable insights into basic cestode biology and highlight potential new targets for diagnostic strategies.

Read full analysis

Keywords:

Cestode Echinococcus Extracellular vesicle Mesocestoides corti Platyhelminth Secretion Taenia microRNA

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