Abstract
Recent body of evidence demonstrates that extracellular vesicles (EVs) represent the first language of cell-cell communication emerged during evolution. In aquatic environments, transferring signals between cells by EVs offers protection against degradation, allowing delivering of chemical information in high local concentrations to the target cells. The packaging of multiple signals, including those of hydrophobic nature, ensures target cells to receive the same EV-conveyed messages, and the coordination of a variety of physiological processes across cells of a single organisms, or at the population level, i.e., mediating the population’s response to changing environmental conditions. Here, we purified EVs from the medium of the freshwater invertebrate Hydra vulgaris, and the molecular profiling by proteomic and transcriptomic analyses revealed multiple markers of the exosome EV subtype, from structural proteins to stress induced messages promoting cell survival. Moreover, positive and negative regulators of the Wnt/β-catenin signaling pathway, the major developmental pathway acting in body axial patterning, were identified. Functional analysis on amputated polyps revealed EV ability to modulate both head and foot regeneration, suggesting bioactivity of the EV cargo and opening new perspectives on the mechanisms of developmental signalling. Our results open the path to unravel EV biogenesis and function in all cnidarian species, tracing back the origin of the cell-cell, cross-species or cross-kingdom communication in aquatic ecosystems.
Highlights
Cell-cell communication is a mandatory condition for all the multicellular organisms as we know them; the possibility to exchange multiple and different signals between cells, at great distances or even between different organisms, supports the organism homeostasis and allows interacting with the surrounding environment
Pelleted extracellular vesicles (EVs) suspended in Phosphate buffered saline (PBS) where characterized by Transmission Electron Microscopy (TEM)
A good correlation with these measurements was obtained through other approaches, such as Dynamic Light Scattering (DLS) analysis and TEM (Supplementary Figure S1), both confirming the average size of 66 nm, and suggesting an enrichment in exosomelike vesicles
Summary
Cell-cell communication is a mandatory condition for all the multicellular organisms as we know them; the possibility to exchange multiple and different signals between cells, at great distances or even between different organisms, supports the organism homeostasis and allows interacting with the surrounding environment. One fascinating feature of this type of EVs is that their content, comprising proteins, lipids and nucleic acids, is determined by the cell type they originate from, and by the physiological state of the organism, resulting in major differences of these vesicles and their cargo in terms of quantity and quality (Ludwig et al, 2019). Such diversity is in agreement with the many processes exosomes have been implicated into, such as parasitic host-pathogen interaction (Coakley et al, 2015), viral infection, immune response, cardiovascular diseases, central nervous system disease, and cancer progression, shuttling into the receiving cells nucleic acids, metabolites, lipid and proteins (Kalluri and Lebleu, 2020). The intrinsic properties of exosomes in regulating complex intracellular pathways offer a new paradigm for their application as disease biomarkers, or as nanocarriers of therapeutic agents in cell-free therapies (Lu and Huang, 2020)
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