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Extracellular Vesicles in Modifying the Effects of Ionizing Radiation

Szatmári, Tünde, Hargitai, Rita, Sáfrány, Géza, Lumniczky, Katalin·2019·International Journal of Molecular Sciences
DOI 10.3390/ijms20225527PMC PMC6888126
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Abstract

Extracellular vesicles (EVs) are membrane-coated nanovesicles actively secreted by almost all cell types. EVs can travel long distances within the body, being finally taken up by the target cells, transferring information from one cell to another, thus influencing their behavior. The cargo of EVs comprises of nucleic acids, lipids, and proteins derived from the cell of origin, thereby it is cell-type specific; moreover, it differs between diseased and normal cells. Several studies have shown that EVs have a role in tumor formation and prognosis. It was also demonstrated that ionizing radiation can alter the cargo of EVs. EVs, in turn can modulate radiation responses and they play a role in radiation-induced bystander effects. Due to their biocompatibility and selective targeting, EVs are suitable nanocarrier candidates of drugs in various diseases, including cancer. Furthermore, the cargo of EVs can be engineered, and in this way they can be designed to carry certain genes or even drugs, similar to synthetic nanoparticles. In this review, we describe the biological characteristics of EVs, focusing on the recent efforts to use EVs as nanocarriers in oncology, the effects of EVs in radiation therapy, highlighting the possibilities to use EVs as nanocarriers to modulate radiation effects in clinical applications.

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Figure 1 Types, release, and composition of extracellular vesicles. Based on their generation and size distribution EVs can be divided into exosomes, microvesicles, and apoptotic bodies. Exosomes are formed inside endosomes by inward budding of the membrane, generating multivesicular bodies (MVB). Exosomes are released by fusion of MVB with the plasma membrane. Microvesicles (MV) arise as a result of direct budding and fission of the plasma membrane from the cells. Apoptotic bodies are formed during apoptosis, from outward blebbing of the cell surface. EVs are composed of a phospholipid bilayer with membrane proteins (immuno-regulatory molecules such as MHCI, MHCII, integrins, tetraspanins, receptors, heparan-sulfate proteoglycans (HSPG), annexins, cholesterol, sphingolipids, ceramides), carrying soluble cytosolic components of the donor cell, such as miRNAs, mRNAs, signaling proteins, cytoskeletal proteins, enzymes, and lipids.
Figure 1 Types, release, and composition of extracellular vesicles. Based on their generation and size distribution EVs can be divided into exosomes, microvesicles, and apoptotic bodies. Exosomes are formed inside endosomes by inward budding of the membrane, generating multivesicular bodies (MVB). Exosomes are released by fusion of MVB with the plasma membrane. Microvesicles (MV) arise as a result of direct budding and fission of the plasma membrane from the cells. Apoptotic bodies are formed during apoptosis, from outward blebbing of the cell surface. EVs are composed of a phospholipid bilayer with membrane proteins (immuno-regulatory molecules such as MHCI, MHCII, integrins, tetraspanins, receptors, heparan-sulfate proteoglycans (HSPG), annexins, cholesterol, sphingolipids, ceramides), carrying soluble cytosolic components of the donor cell, such as miRNAs, mRNAs, signaling proteins, cytoskeletal proteins, enzymes, and lipids.CC BY · PubMed Central
Figure 2 Mechanisms of EV uptake. EVs can be internalized by cells through different endocytic processes. During phagocytosis, the cytoplasm creates invaginations around the EV, which is then internalized creating an endosome. During macropinocytosis, plasma membrane ruffles fold back on themselves around the EVs, forming a lumen of a macropinosome. Clathrin-dependent endocytosis induces membrane curvature around the EV. In caveolin-mediated endocytosis caveolae (small, cave-like invaginations in the cell membrane) with EVs inside are internalized into the cell. Intracellularly, they develop chlatrin- or caveolin-coated vesicles, fuse with endosomes and deliver the cargo. EV uptake can occur by interaction of EVs with lipid rafts. Lipid rafts are involved in both clathrin- and caveolin-mediated endocytosis. Another possible way for EVs to deliver their cargo to recipient cell is by passive fusion with the plasma membrane.
Figure 2 Mechanisms of EV uptake. EVs can be internalized by cells through different endocytic processes. During phagocytosis, the cytoplasm creates invaginations around the EV, which is then internalized creating an endosome. During macropinocytosis, plasma membrane ruffles fold back on themselves around the EVs, forming a lumen of a macropinosome. Clathrin-dependent endocytosis induces membrane curvature around the EV. In caveolin-mediated endocytosis caveolae (small, cave-like invaginations in the cell membrane) with EVs inside are internalized into the cell. Intracellularly, they develop chlatrin- or caveolin-coated vesicles, fuse with endosomes and deliver the cargo. EV uptake can occur by interaction of EVs with lipid rafts. Lipid rafts are involved in both clathrin- and caveolin-mediated endocytosis. Another possible way for EVs to deliver their cargo to recipient cell is by passive fusion with the plasma membrane.CC BY · PubMed Central
Figure 3 Functions of extracellular vesicles with a role in modulating radiation response. EV-extracellular vesicle; CSC-cancer stem cell; EMT-epithelial-mesenchymal transition.
Figure 3 Functions of extracellular vesicles with a role in modulating radiation response. EV-extracellular vesicle; CSC-cancer stem cell; EMT-epithelial-mesenchymal transition.CC BY · PubMed Central
Figure 4 Schematic diagram depicting the potential roles of extracellular vesicles as nanocarriers for radiosensitizing agents.
Figure 4 Schematic diagram depicting the potential roles of extracellular vesicles as nanocarriers for radiosensitizing agents.CC BY · PubMed Central

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Metadata

Authors
Szatmári, T., Hargitai, R., Sáfrány, G., & Lumniczky, K.
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2019-11-06
Volume
20
Issue
22
Pages
5527
ISSN
1422-0067
DOI
10.3390/ijms20225527
PMC
PMC6888126
Cited by
52
References
10
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Horizon 2020 Framework Programme (Concert 662287)
  • the Hungarian National Research, Development and Innovation Office ( NKFI) (NKFI-124879)

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Szatmári, T., Hargitai, R., Sáfrány, G., & Lumniczky, K. (2019). Extracellular Vesicles in Modifying the Effects of Ionizing Radiation. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms20225527