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Trends in the biological functions and medical applications of extracellular vesicles and analogues


Posted: 2021-09-15 19:00:00
Review Acta Pharm Sin B . 2021 Aug;11(8):2114-2135. doi: 10.1016/j.apsb.2021.03.012. Epub 2021 Mar 10. Yan Zhao 1 2 , Xiaolu Li 2 , Wenbo Zhang 2 , Lanlan Yu 2 , Yang Wang 2 , Zhun Deng 2 , Mingwei Liu 2 , Shanshan Mo 2 , Ruonan Wang 2 , Jinming Zhao 1 , Shuli Liu 3 , Yun Hao 1 , Xiangdong Wang 1 , Tianjiao Ji 4 5 , Luo Zhang 1 6 , Chenxuan Wang 2 Affiliations Expand Affiliations 1 Department of Otolaryngology Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University and Beijing Key Laboratory of Nasal Diseases, Beijing Institute of Otolaryngology, Beijing 100005, China. 2 State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100005, China. 3 Department of Clinical Laboratory, Peking University Civil Aviation School of Clinical Medicine, Beijing 100123, China. 4 CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China. 5 Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China. 6 Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100005, China. Item in Clipboard Review Yan Zhao et al. Acta Pharm Sin B. 2021 Aug. Show details Display options Display options Format Acta Pharm Sin B . 2021 Aug;11(8):2114-2135. doi: 10.1016/j.apsb.2021.03.012. Epub 2021 Mar 10. Authors Yan Zhao 1 2 , Xiaolu Li 2 , Wenbo Zhang 2 , Lanlan Yu 2 , Yang Wang 2 , Zhun Deng 2 , Mingwei Liu 2 , Shanshan Mo 2 , Ruonan Wang 2 , Jinming Zhao 1 , Shuli Liu 3 , Yun Hao 1 , Xiangdong Wang 1 , Tianjiao Ji 4 5 , Luo Zhang 1 6 , Chenxuan Wang 2 Affiliations 1 Department of Otolaryngology Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University and Beijing Key Laboratory of Nasal Diseases, Beijing Institute of Otolaryngology, Beijing 100005, China. 2 State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100005, China. 3 Department of Clinical Laboratory, Peking University Civil Aviation School of Clinical Medicine, Beijing 100123, China. 4 CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China. 5 Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China. 6 Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100005, China. Item in Clipboard CiteDisplay options Display options Format Abstract Natural extracellular vesicles (EVs) play important roles in many life processes such as in the intermolecular transfer of substances and genetic information exchanges. Investigating the origins and working mechanisms of natural EVs may provide an understanding of life activities, especially regarding the occurrence and development of diseases. Additionally, due to their vesicular structure, EVs (in small molecules, nucleic acids, proteins, etc.) could act as efficient drug-delivery carriers. Herein, we describe the sources and biological functions of various EVs, summarize the roles of EVs in disease diagnosis and treatment, and review the application of EVs as drug-delivery carriers. We also assess the challenges and perspectives of EVs in biomedical applications. Keywords: Biomarkers; Drug delivery; Exosomes; Extracellular vesicles; Intercellular communications. © 2021 Chinese Pharmaceutical Association and Institute of Materia Medica, Chinese Academy of Medical Sciences. Production and hosting by Elsevier B.V. Figures Graphical abstract Graphical abstract Graphical abstract Figure 1 The discrete structural and compositional… Figure 1 The discrete structural and compositional characteristics of four types of extracellular vesicles. Figure 1 The discrete structural and compositional characteristics of four types of extracellular vesicles. Figure 2 The biogenesis and release of… Figure 2 The biogenesis and release of exosomes in mammalian cells. The inward budding of… Figure 2 The biogenesis and release of exosomes in mammalian cells. The inward budding of the plasma membrane packages cytosolic and transmembrane cargos to form early endosomes, which transform into late endosomes (MVBs) with intraluminal vesicles through ESCRT-dependent pathways or ESCRT-independent pathways. The MVBs fuse with the plasma membrane and release intraluminal vesicles as exosomes. Figure 3 The proposed models for the… Figure 3 The proposed models for the biogenesis and secretion of extracellular vesicles in plant… Figure 3 The proposed models for the biogenesis and secretion of extracellular vesicles in plant cells and in Gram-negative bacteria. (A) In plant cells, the trans-Golgi network plays a similar function as the early endosome in mammalian cells. (B) In Gram-negative bacteria, the outer membrane is an asymmetrical bilayer membranous structure with lipopolysaccharide in the outer leaflet and phospholipids in the inner leaflet. The phospholipid layer possesses different molecular packing manners and triggers the budding of the outer membrane (① and ②). Finally, the budding of the outer membrane is enclosed and released as outer-membrane vesicles (③). Figure 4 The cellular internalization of extracellular… Figure 4 The cellular internalization of extracellular vesicles. Membrane fusion, phagocytosis, micropinocytosis, clathrin-mediated endocytosis, and… Figure 4 The cellular internalization of extracellular vesicles. Membrane fusion, phagocytosis, micropinocytosis, clathrin-mediated endocytosis, and caveolin-dependent endocytosis processes are separately illustrated. Figure 5 The application of extracellular vesicles… Figure 5 The application of extracellular vesicles as disease biomarkers. (A) EGFR + extracellular vesicles… Figure 5 The application of extracellular vesicles as disease biomarkers. (A) EGFR+ extracellular vesicles (EVs) are non-invasive biomarkers in glioma. The TEM image of EVs isolated from the serum of patients with glioma (left). The flow cytometry data and percentage of EGFR+ EVs showed the expression level of EGFR on the surface of EVs in healthy individuals (n = 12), preoperative glioma patients (n = 23), and postoperative glioma patients (n = 8) (middle). The ROC curve showed the discriminative ability of EGFR+ EVs in differentiating patients with glioma (n = 23) from healthy donors (n = 12) (right). Adapted with permission from Ref. 137. Copyright © 2019 Ivyspring International Publisher. (B) A liquid chromatography tandem-mass spectrometry-based proteomic analysis of EVs and particles identified the tumor-associated EVs and particle signatures in the surgically removed tissues and plasma from patients with multiple tumor types. The predictive values were predicted by random forest algorithm. The number of samples identified is noted in each box. Adapted with permission from Ref. 140. Copyright © 2020 Elsevier Inc. Figure 6 Dendritic cell-derived extracellular vesicles modulate… Figure 6 Dendritic cell-derived extracellular vesicles modulate innate and adaptive immune responses. The extracellular vesicles… Figure 6 Dendritic cell-derived extracellular vesicles modulate innate and adaptive immune responses. The extracellular vesicles (EVs) released from mature dendritic cells stimulate the innate immune response in immune cells and other cell types. They could induce the cytotoxic activity of natural killer cells or stimulate epithelial cells to secrete cytokines (left). The EVs released from mature dendritic cells present peptide–MHC complexes that could directly target CD4+ T cells or CD8+ T cells, and consequently promote the activation of adaptive immune responses (right). Figure 7 The role of extracellular vesicles… Figure 7 The role of extracellular vesicles in regulating cellular proliferation and differentiation. (A) The… Figure 7 The role of extracellular vesicles in regulating cellular proliferation and differentiation. (A) The role of tumor-derived extracellular vesicles (EVs) in the tumor microenvironment. The tumor-derived EVs activate the normal fibroblasts to initialize the differentiation into cancer-associated fibroblasts. They could also induce lymphocyte apoptosis and convert dendritic cells into a non-responsive phenotype. (B) The role of endothelial progenitor cell-derived EVs in the repair of blood vessels and wound healing. EPC-derived EVs increase the level of a series of pro-angiogenic cytokines and improve the proliferation and migration ability of human microvascular endothelial cells, which facilitates tissue repair and regeneration. Figure 8 Applications of extracellular vesicles in… Figure 8 Applications of extracellular vesicles in drug delivery. (A)‒(C) The antitumor activity of TRAIL… Figure 8 Applications of extracellular vesicles in drug delivery. (A)‒(C) The antitumor activity of TRAIL extracellular vesicle treatments against KMS11 multiple myeloma. (A) Intratumor treatment. KMS11-bearing mice were treated by TRAIL EVs every 48 h and then measured by the TUNEL assay. (B) and (C) Systematic treatment. Hematoxylin and eosin staining images (B) and determination of necrotic areas (C) of tumors of KMS11-bearing mice were treated by four intravenous treatments of TRAIL EVs, NGFR EVs, or saline every 48 h (n = 5–6 saline and mice accepting NGFR EVs; n = 10 mice accepting TRAIL EVs). Adapted with permission from Ref. 195. Copyright © 2016 American Association for Cancer Research. (D)–(F) Treatment with JSI124-EVs prevents the in vivo growth of injected brain tumor cells. (D) The surviving rate of mice treated with EV-JSI124, JSI124, EV and control administration. (E) and (F) A representative photo of brain tumor signals (E) and the growth potential of cells (F) of mice treated with JSI124, EV, or EV-JSI124. Adapted with permission from Ref. 190. Copyright © 2011 The American Society of Gene & Cell Therapy. (G) The human adipose stem cell-derived EVs loaded with miR-21-5p improved diabetic wound healing. Adapted with permission from Ref. 194. Copyright © 2020 American Chemical Society. Figure 9 The applications of plant-derived vesicles.… Figure 9 The applications of plant-derived vesicles. Regulation of host gene expression (left) and delivery… Figure 9 The applications of plant-derived vesicles. Regulation of host gene expression (left) and delivery systems for RNA and chemotherapy drugs (right). Figure 10 The applications of vesicles derived… Figure 10 The applications of vesicles derived from bacteria. Outer-membrane vesicles (OMVs) derived from bacteria… Figure 10 The applications of vesicles derived from bacteria. Outer-membrane vesicles (OMVs) derived from bacteria serve as antibiotics against bacterial infection (left). OMVs are potential vaccines against bacterial infections (middle). OMVs can also be used as competent adjuvants in vaccines (right). All figures (11) References O'Brien K., Breyne K., Ughetto S., Laurent L.C., Breakefield X.O. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020;21:585–606. - PMC - PubMed Deatherage B.L., Cookson B.T. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun. 2012;80:1948–1957. - PMC - PubMed van der Pol E., Boing A.N., Harrison P., Sturk A., Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012;64:676–705. - PubMed Gyorgy B., Szabo T.G., Pasztoi M., Pal Z., Misjak P., Aradi B. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68:2667–2688. - PMC - PubMed Chargaff E., West R. The biological significance of the thromboplastic protein of blood. J Biol Chem. 1946;166:189–197. - PubMed Show all 249 references Publication types [x] Cite Copy Format: Send To [x]

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