Fasciola hepatica Gastrodermal Cells Selectively Release Extracellular Vesicles via a Novel Atypical Secretory Mechanism
Date
2022-05-15
Journal Title
Journal ISSN
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Publisher
MDPI
Abstract
The liver fluke, Fasciola hepatica, is an obligate blood-feeder, and the gastrodermal cells of
the parasite form the interface with the host’s blood. Despite their importance in the host–parasite
interaction, in-depth proteomic analysis of the gastrodermal cells is lacking. Here, we used laser
microdissection of F. hepatica tissue sections to generate unique and biologically exclusive tissue
fractions of the gastrodermal cells and tegument for analysis by mass spectrometry. A total of
226 gastrodermal cell proteins were identified, with proteases that degrade haemoglobin being the
most abundant. Other detected proteins included those such as proton pumps and anticoagulants
which maintain a microenvironment that facilitates digestion. By comparing the gastrodermal cell
proteome and the 102 proteins identified in the laser microdissected tegument with previously
published tegument proteomic datasets, we showed that one-quarter of proteins (removed by freeze–
thaw extraction) or one-third of proteins (removed by detergent extraction) previously identified
as tegumental were instead derived from the gastrodermal cells. Comparative analysis of the laser
microdissected gastrodermal cells, tegument, and F. hepatica secretome revealed that the gastrodermal
cells are the principal source of secreted proteins, as well as showed that both the gastrodermal cells
and the tegument are likely to release subpopulations of extracellular vesicles (EVs). Microscopical
examination of the gut caeca from flukes fixed immediately after their removal from the host bile
ducts showed that selected gastrodermal cells underwent a progressive thinning of the apical plasma
membrane which ruptured to release secretory vesicles en masse into the gut lumen. Our findings
suggest that gut-derived EVs are released via a novel atypical secretory route and highlight the
importance of the gastrodermal cells in nutrient acquisition and possible immunomodulation by
the parasite.
Description
Publication history: Accepted - 12 May, 2022; Published - 15 may 2022.
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Article
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Keywords
Fasciola hepatica, trematode, helminth, extracellular vesicle, secretion, proteome
Citation
Bennett, A., De la Torre-Escudero, E., Dermott, S., Threadgold, L., Hanna, R. and Robinson, M. (2022) ‘Fasciola hepatica Gastrodermal Cells Selectively Release Extracellular Vesicles via a Novel Atypical Secretory Mechanism’, International Journal of Molecular Sciences. MDPI AG. doi:10.3390/ijms23105525.