Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Review Article

Progression in the Relationship between Exosome Production and Atherosclerosis

Author(s): Yi Yang, Jinxi Luo, Yunan Kang, Wenqian Wu, Yajie Lu, Jie Fu, Xiaoyun Zhang, Min Cheng* and Xiaodong Cui*

Volume 25, Issue 9, 2024

Published on: 04 August, 2023

Page: [1099 - 1111] Pages: 13

DOI: 10.2174/1389201024666230726114920

Price: $65

Abstract

Atherosclerosis (AS) is the leading cause of cardiovascular disease, causing a major burden on patients as well as families and society. Exosomes generally refer to various lipid bilayer microvesicles originating from different cells that deliver various bioactive molecules to the recipient cells, exerting biological effects in cellular communication and thereby changing the internal environment of the body. The mechanisms of correlation between exosomes and the disease process of atherosclerosis have been recently clarified. Exosomes are rich in nucleic acid molecules and proteins. For example, the exosome miRNAs reportedly play important roles in the progression of atherosclerotic diseases. In this review, we focus on the composition of exosomes, the mechanism of their biogenesis and release, and the commonly used methods for exosome extraction. By summarizing the latest research progress on exosomes and atherosclerosis, we can explore the advances in the roles of exosomes in atherosclerosis to provide new ideas and targets for atherosclerosis prevention, diagnosis, and treatment.

Keywords: Atherosclerosis, cardiovascular disease, exosome, extracellular vesicles, biogenesis, isolation technique.

Graphical Abstract
[1]
Libby, P.; Buring, J.E.; Badimon, L.; Hansson, G.K.; Deanfield, J.; Bittencourt, M.S.; Tokgözoğlu, L.; Lewis, E.F. Atherosclerosis. Nat. Rev. Dis. Primers, 2019, 5(1), 56.
[http://dx.doi.org/10.1038/s41572-019-0106-z] [PMID: 31420554]
[2]
Petty, R.G.; Pearson, J.D. Endothelium--the axis of vascular health and disease. J. R. Coll. Physicians Lond., 1989, 23(2), 92-102.
[PMID: 2659784]
[3]
Bartling, B.; Tostlebe, H.; Darmer, D.; Holtz, J.; Silber, R.E.; Morawietz, H. Shear stress-dependent expression of apoptosis-regulating genes in endothelial cells. Biochem. Biophys. Res. Commun., 2000, 278(3), 740-746.
[http://dx.doi.org/10.1006/bbrc.2000.3873] [PMID: 11095978]
[4]
Wang, C.; Li, Z.; Liu, Y.; Yuan, L. Exosomes in atherosclerosis: performers, bystanders, biomarkers, and therapeutic targets. Theranostics, 2021, 11(8), 3996-4010.
[http://dx.doi.org/10.7150/thno.56035] [PMID: 33664877]
[5]
Gurung, S.; Perocheau, D.; Touramanidou, L.; Baruteau, J. The exosome journey: from biogenesis to uptake and intracellular signalling. Cell Commun. Signal., 2021, 19(1), 47.
[http://dx.doi.org/10.1186/s12964-021-00730-1] [PMID: 33892745]
[6]
Peinado, H.; Alečković, M.; Lavotshkin, S.; Matei, I.; Costa-Silva, B.; Moreno-Bueno, G.; Hergueta-Redondo, M.; Williams, C.; García-Santos, G.; Ghajar, C.M.; Nitadori-Hoshino, A.; Hoffman, C.; Badal, K.; Garcia, B.A.; Callahan, M.K.; Yuan, J.; Martins, V.R.; Skog, J.; Kaplan, R.N.; Brady, M.S.; Wolchok, J.D.; Chapman, P.B.; Kang, Y.; Bromberg, J.; Lyden, D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med., 2012, 18(6), 883-891.
[http://dx.doi.org/10.1038/nm.2753] [PMID: 22635005]
[7]
Wang, H.; Xie, Y.; Salvador, A.M.; Zhang, Z.; Chen, K.; Li, G.; Xiao, J. Exosomes: Multifaceted messengers in atherosclerosis. Curr. Atheroscler. Rep., 2020, 22(10), 57.
[http://dx.doi.org/10.1007/s11883-020-00871-7] [PMID: 32772195]
[8]
Nguyen, M.A.; Karunakaran, D.; Geoffrion, M.; Cheng, H.S.; Tandoc, K.; Perisic Matic, L.; Hedin, U.; Maegdefessel, L.; Fish, J.E.; Rayner, K.J. Extracellular vesicles secreted by atherogenic macrophages transfer MicroRNA to inhibit cell migration. Arterioscler. Thromb. Vasc. Biol., 2018, 38(1), 49-63.
[http://dx.doi.org/10.1161/ATVBAHA.117.309795] [PMID: 28882869]
[9]
Zhu, J.; Liu, B.; Wang, Z.; Wang, D.; Ni, H.; Zhang, L.; Wang, Y. Exosomes from nicotine-stimulated macrophages accelerate atherosclerosis through miR-21-3p/PTEN-mediated VSMC migration and proliferation. Theranostics, 2019, 9(23), 6901-6919.
[http://dx.doi.org/10.7150/thno.37357] [PMID: 31660076]
[10]
Men, Y.; Yelick, J.; Jin, S.; Tian, Y.; Chiang, M.S.R.; Higashimori, H.; Brown, E.; Jarvis, R.; Yang, Y. Exosome reporter mice reveal the involvement of exosomes in mediating neuron to astroglia communication in the CNS. Nat. Commun., 2019, 10(1), 4136.
[http://dx.doi.org/10.1038/s41467-019-11534-w] [PMID: 31515491]
[11]
D’Souza-Schorey, C.; Schorey, J.S. Regulation and mechanisms of extracellular vesicle biogenesis and secretion. Essays Biochem., 2018, 62(2), 125-133.
[http://dx.doi.org/10.1042/EBC20170078] [PMID: 29666210]
[12]
Davies, B.A.; Lee, J.R.E.; Oestreich, A.J.; Katzmann, D.J. Membrane protein targeting to the MVB/lysosome. Chem. Rev., 2009, 109(4), 1575-1586.
[http://dx.doi.org/10.1021/cr800473s] [PMID: 19243135]
[13]
Wei, D.; Zhan, W.; Gao, Y.; Huang, L.; Gong, R.; Wang, W.; Zhang, R.; Wu, Y.; Gao, S.; Kang, T. RAB31 marks and controls an ESCRT-independent exosome pathway. Cell Res., 2021, 31(2), 157-177.
[http://dx.doi.org/10.1038/s41422-020-00409-1] [PMID: 32958903]
[14]
Mathieu, M.; Martin-Jaular, L.; Lavieu, G.; Théry, C. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat. Cell Biol., 2019, 21(1), 9-17.
[http://dx.doi.org/10.1038/s41556-018-0250-9] [PMID: 30602770]
[15]
Rana, S.; Zöller, M. Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem. Soc. Trans., 2011, 39(2), 559-562.
[http://dx.doi.org/10.1042/BST0390559] [PMID: 21428939]
[16]
Zhao, L.; Gu, C.; Gan, Y.; Shao, L.; Chen, H.; Zhu, H. Exosome-mediated siRNA delivery to suppress postoperative breast cancer metastasis. J. Control. Release, 2020, 318, 1-15.
[17]
Mathieu, M.; Névo, N.; Jouve, M.; Valenzuela, J.I.; Maurin, M.; Verweij, F.J.; Palmulli, R.; Lankar, D.; Dingli, F.; Loew, D.; Rubinstein, E.; Boncompain, G.; Perez, F.; Théry, C. Specificities of exosome versus small ectosome secretion revealed by live intracellular tracking of CD63 and CD9. Nat. Commun., 2021, 12(1), 4389.
[http://dx.doi.org/10.1038/s41467-021-24384-2] [PMID: 34282141]
[18]
Larios, J.; Mercier, V.; Roux, A.; Gruenberg, J. ALIX- and ESCRT-III–dependent sorting of tetraspanins to exosomes. J. Cell Biol., 2020, 219(3), e201904113.
[http://dx.doi.org/10.1083/jcb.201904113] [PMID: 32049272]
[19]
Lin, T.H.; Bis-Brewer, D.M.; Sheehan, A.E.; Townsend, L.N.; Maddison, D.C.; Züchner, S.; Smith, G.A.; Freeman, M.R. TSG101 negatively regulates mitochondrial biogenesis in axons. Proc. Natl. Acad. Sci. USA, 2021, 118(20), e2018770118.
[http://dx.doi.org/10.1073/pnas.2018770118] [PMID: 33972422]
[20]
Yan, C.; Tian, X.; Li, J.; Liu, D.; Ye, D.; Xie, Z.; Han, Y.; Zou, M.H. A high-fat diet attenuates AMPK α1 in adipocytes to induce exosome shedding and nonalcoholic fatty liver development in vivo. Diabetes, 2021, 70(2), 577-588.
[http://dx.doi.org/10.2337/db20-0146] [PMID: 33262120]
[21]
Costa Verdera, H.; Gitz-Francois, J.J.; Schiffelers, R.M.; Vader, P. Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. J. Control. Release, 2017, 266, 100-108.
[22]
Zhang, H.; Freitas, D.; Kim, H.S.; Fabijanic, K.; Li, Z.; Chen, H.; Mark, M.T.; Molina, H.; Martin, A.B.; Bojmar, L.; Fang, J.; Rampersaud, S.; Hoshino, A.; Matei, I.; Kenific, C.M.; Nakajima, M.; Mutvei, A.P.; Sansone, P.; Buehring, W.; Wang, H.; Jimenez, J.P.; Cohen-Gould, L.; Paknejad, N.; Brendel, M.; Manova-Todorova, K.; Magalhães, A.; Ferreira, J.A.; Osório, H.; Silva, A.M.; Massey, A.; Cubillos-Ruiz, J.R.; Galletti, G.; Giannakakou, P.; Cuervo, A.M.; Blenis, J.; Schwartz, R.; Brady, M.S.; Peinado, H.; Bromberg, J.; Matsui, H.; Reis, C.A.; Lyden, D. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat. Cell Biol., 2018, 20(3), 332-343.
[http://dx.doi.org/10.1038/s41556-018-0040-4] [PMID: 29459780]
[23]
Vietri, M.; Radulovic, M.; Stenmark, H. The many functions of ESCRTs. Nat. Rev. Mol. Cell Biol., 2020, 21(1), 25-42.
[http://dx.doi.org/10.1038/s41580-019-0177-4] [PMID: 31705132]
[24]
Skotland, T.; Hessvik, N.P.; Sandvig, K.; Llorente, A. Exosomal lipid composition and the role of ether lipids and phosphoinositides in exosome biology. J. Lipid Res., 2019, 60(1), 9-18.
[http://dx.doi.org/10.1194/jlr.R084343] [PMID: 30076207]
[25]
Guay, C.; Regazzi, R. Exosomes as new players in metabolic organ cross-talk. Diabetes Obes. Metab., 2017, 19(Suppl. 1), 137-146.
[http://dx.doi.org/10.1111/dom.13027] [PMID: 28880477]
[26]
Castaño, C.; Kalko, S.; Novials, A.; Párrizas, M. Obesity-associated exosomal miRNAs modulate glucose and lipid metabolism in mice. Proc. Natl. Acad. Sci. USA, 2018, 115(48), 12158-12163.
[http://dx.doi.org/10.1073/pnas.1808855115] [PMID: 30429322]
[27]
Zhu, W.; Sun, L.; Zhao, P.; Liu, Y.; Zhang, J.; Zhang, Y.; Hong, Y.; Zhu, Y.; Lu, Y.; Zhao, W.; Chen, X.; Zhang, F. Macrophage migration inhibitory factor facilitates the therapeutic efficacy of mesenchymal stem cells derived exosomes in acute myocardial infarction through upregulating miR-133a-3p. J. Nanobiotechnology, 2021, 19(1), 61.
[http://dx.doi.org/10.1186/s12951-021-00808-5] [PMID: 33639970]
[28]
Roth, T.F.; Porter, K.R. Yolk protein uptake in the oocyte of the mosquito aedes aegypti. L. J. Cell Biol., 1964, 20(2), 313-332.
[http://dx.doi.org/10.1083/jcb.20.2.313] [PMID: 14126875]
[29]
Schmid, E.M.; McMahon, H.T. Integrating molecular and network biology to decode endocytosis. Nature, 2007, 448(7156), 883-888.
[http://dx.doi.org/10.1038/nature06031] [PMID: 17713526]
[30]
Nishimura, T.; Morone, N.; Suetsugu, S. Membrane re-modelling by BAR domain superfamily proteins via molecular and non-molecular factors. Biochem. Soc. Trans., 2018, 46(2), 379-389.
[http://dx.doi.org/10.1042/BST20170322] [PMID: 29540508]
[31]
Roux, A.; Uyhazi, K.; Frost, A.; De Camilli, P. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature, 2006, 441(7092), 528-531.
[http://dx.doi.org/10.1038/nature04718] [PMID: 16648839]
[32]
Doherty, G.J.; McMahon, H.T. Mechanisms of endocytosis. Annu. Rev. Biochem., 2009, 78(1), 857-902.
[http://dx.doi.org/10.1146/annurev.biochem.78.081307.110540] [PMID: 19317650]
[33]
Klumperman, J.; Raposo, G. The complex ultrastructure of the endolysosomal system. Cold Spring Harb. Perspect. Biol., 2014, 6(10), a016857.
[http://dx.doi.org/10.1101/cshperspect.a016857] [PMID: 24851870]
[34]
Shafaq-Zadah, M.; Dransart, E.; Johannes, L. Clathrin-independent endocytosis, retrograde trafficking, and cell polarity. Curr. Opin. Cell Biol., 2020, 65, 112-121.
[http://dx.doi.org/10.1016/j.ceb.2020.05.009] [PMID: 32688213]
[35]
Frühbeis, C.; Fröhlich, D.; Kuo, W.P.; Amphornrat, J.; Thilemann, S.; Saab, A.S.; Kirchhoff, F.; Möbius, W.; Goebbels, S.; Nave, K.A.; Schneider, A.; Simons, M.; Klugmann, M.; Trotter, J.; Krämer-Albers, E.M. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol., 2013, 11(7), e1001604.
[http://dx.doi.org/10.1371/journal.pbio.1001604] [PMID: 23874151]
[36]
Nolan, J.P.; Duggan, E. Analysis of individual extracellular vesicles by flow cytometry. Methods Mol. Biol., 2018, 1678, 79-92.
[http://dx.doi.org/10.1007/978-1-4939-7346-0_5] [PMID: 29071676]
[37]
Mashouri, L.; Yousefi, H.; Aref, A.R.; Ahadi, A.; Molaei, F.; Alahari, S.K. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol. Cancer, 2019, 18(1), 75.
[http://dx.doi.org/10.1186/s12943-019-0991-5] [PMID: 30940145]
[38]
Raiborg, C.; Wesche, J.; Malerød, L.; Stenmark, H. Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J. Cell Sci., 2006, 119(12), 2414-2424.
[http://dx.doi.org/10.1242/jcs.02978] [PMID: 16720641]
[39]
Takahashi, H.; Mayers, J.R.; Wang, L.; Edwardson, J.M.; Audhya, A. Hrs and STAM function synergistically to bind ubiquitin-modified cargoes in vitro. Biophys. J., 2015, 108(1), 76-84.
[http://dx.doi.org/10.1016/j.bpj.2014.11.004] [PMID: 25564854]
[40]
Ju, Y.; Bai, H.; Ren, L.; Zhang, L. The role of exosome and the ESCRT pathway on enveloped virus infection. Int. J. Mol. Sci., 2021, 22(16), 9060.
[http://dx.doi.org/10.3390/ijms22169060] [PMID: 34445766]
[41]
Raiborg, C.; Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature, 2009, 458(7237), 445-452.
[http://dx.doi.org/10.1038/nature07961] [PMID: 19325624]
[42]
Slagsvold, T.; Aasland, R.; Hirano, S.; Bache, K.G.; Raiborg, C.; Trambaiolo, D.; Wakatsuki, S.; Stenmark, H. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem., 2005, 280(20), 19600-19606.
[http://dx.doi.org/10.1074/jbc.M501510200] [PMID: 15755741]
[43]
Gill, D.J.; Teo, H.; Sun, J.; Perisic, O.; Veprintsev, D.B.; Emr, S.D.; Williams, R.L. Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J., 2007, 26(2), 600-612.
[http://dx.doi.org/10.1038/sj.emboj.7601501] [PMID: 17215868]
[44]
Han, H.; Hill, C.P. Structure and mechanism of the ESCRT pathway AAA+ ATPase Vps4. Biochem. Soc. Trans., 2019, 47(1), 37-45.
[http://dx.doi.org/10.1042/BST20180260] [PMID: 30647138]
[45]
Harker-Kirschneck, L.; Baum, B.; Šarić, A. Changes in ESCRT-III filament geometry drive membrane remodelling and fission in silico. BMC Biol., 2019, 17(1), 82.
[http://dx.doi.org/10.1186/s12915-019-0700-2] [PMID: 31640700]
[46]
van Niel, G.; Charrin, S.; Simoes, S.; Romao, M.; Rochin, L.; Saftig, P.; Marks, M.S.; Rubinstein, E.; Raposo, G. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell, 2011, 21(4), 708-721.
[http://dx.doi.org/10.1016/j.devcel.2011.08.019] [PMID: 21962903]
[47]
Cheng, Q.; Li, X.; Wang, Y.; Dong, M.; Zhan, F.; Liu, J. The ceramide pathway is involved in the survival, apoptosis and exosome functions of human multiple myeloma cells in vitro. Acta Pharmacol. Sin., 2018, 39(4), 561-568.
[http://dx.doi.org/10.1038/aps.2017.118] [PMID: 28858294]
[48]
Charrin, S.; Jouannet, S.; Boucheix, C.; Rubinstein, E. Tetraspanins at a glance. J. Cell Sci., 2014, 127(Pt 17), 3641-3648.
[PMID: 25128561]
[49]
Ferreira, J.V.; da Rosa Soares, A.; Ramalho, J.; Máximo Carvalho, C.; Cardoso, M.H.; Pintado, P.; Carvalho, A.S.; Beck, H.C.; Matthiesen, R.; Zuzarte, M.; Girão, H.; van Niel, G.; Pereira, P. LAMP2A regulates the loading of proteins into exosomes. Sci. Adv., 2022, 8(12), eabm1140.
[http://dx.doi.org/10.1126/sciadv.abm1140] [PMID: 35333565]
[50]
Colombo, M.; Raposo, G.; Théry, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol., 2014, 30(1), 255-289.
[http://dx.doi.org/10.1146/annurev-cellbio-101512-122326] [PMID: 25288114]
[51]
Hoshino, D.; Kirkbride, K.C.; Costello, K.; Clark, E.S.; Sinha, S.; Grega-Larson, N.; Tyska, M.J.; Weaver, A.M. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep., 2013, 5(5), 1159-1168.
[http://dx.doi.org/10.1016/j.celrep.2013.10.050] [PMID: 24290760]
[52]
Baixauli, F.; López-Otín, C.; Mittelbrunn, M. Exosomes and autophagy: coordinated mechanisms for the maintenance of cellular fitness. Front. Immunol., 2014, 5, 403.
[http://dx.doi.org/10.3389/fimmu.2014.00403] [PMID: 25191326]
[53]
Kanemoto, S.; Nitani, R.; Murakami, T.; Kaneko, M.; Asada, R.; Matsuhisa, K.; Saito, A.; Imaizumi, K. Multivesicular body formation enhancement and exosome release during endoplasmic reticulum stress. Biochem. Biophys. Res. Commun., 2016, 480(2), 166-172.
[http://dx.doi.org/10.1016/j.bbrc.2016.10.019] [PMID: 27725157]
[54]
Savina, A.; Vidal, M.; Colombo, M.I. The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci., 2002, 115(12), 2505-2515.
[http://dx.doi.org/10.1242/jcs.115.12.2505] [PMID: 12045221]
[55]
Ostrowski, M.; Carmo, N.B.; Krumeich, S.; Fanget, I.; Raposo, G.; Savina, A.; Moita, C.F.; Schauer, K.; Hume, A.N.; Freitas, R.P.; Goud, B.; Benaroch, P.; Hacohen, N.; Fukuda, M.; Desnos, C.; Seabra, M.C.; Darchen, F.; Amigorena, S.; Moita, L.F.; Thery, C. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol., 2010, 12(1), 1-13.
[http://dx.doi.org/10.1038/ncb2000]
[56]
Hsu, C.; Morohashi, Y.; Yoshimura, S.; Manrique-Hoyos, N.; Jung, S.; Lauterbach, M.A.; Bakhti, M.; Grønborg, M.; Möbius, W.; Rhee, J.; Barr, F.A.; Simons, M. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A–C. J. Cell Biol., 2010, 189(2), 223-232.
[http://dx.doi.org/10.1083/jcb.200911018] [PMID: 20404108]
[57]
Koles, K.; Nunnari, J.; Korkut, C.; Barria, R.; Brewer, C.; Li, Y.; Leszyk, J.; Zhang, B.; Budnik, V. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J. Biol. Chem., 2012, 287(20), 16820-16834.
[http://dx.doi.org/10.1074/jbc.M112.342667] [PMID: 22437826]
[58]
Baietti, M.F.; Zhang, Z.; Mortier, E.; Melchior, A.; Degeest, G.; Geeraerts, A.; Ivarsson, Y.; Depoortere, F.; Coomans, C.; Vermeiren, E.; Zimmermann, P.; David, G. Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat. Cell Biol., 2012, 14(7), 677-685.
[http://dx.doi.org/10.1038/ncb2502] [PMID: 22660413]
[59]
Bonifacino, J.S.; Glick, B.S. The mechanisms of vesicle budding and fusion. Cell, 2004, 116(2), 153-166.
[http://dx.doi.org/10.1016/S0092-8674(03)01079-1] [PMID: 14744428]
[60]
Fader, C.M.; Sánchez, D.G.; Mestre, M.B.; Colombo, M.I. TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta Mol. Cell Res., 2009, 1793(12), 1901-1916.
[http://dx.doi.org/10.1016/j.bbamcr.2009.09.011] [PMID: 19781582]
[61]
Gross, J.C.; Chaudhary, V.; Bartscherer, K.; Boutros, M. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol., 2012, 14(10), 1036-1045.
[http://dx.doi.org/10.1038/ncb2574] [PMID: 22983114]
[62]
Savina, A.; Furlán, M.; Vidal, M.; Colombo, M.I. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem., 2003, 278(22), 20083-20090.
[http://dx.doi.org/10.1074/jbc.M301642200] [PMID: 12639953]
[63]
Phuyal, S.; Skotland, T.; Hessvik, N.P.; Simolin, H.; Øverbye, A.; Brech, A.; Parton, R.G.; Ekroos, K.; Sandvig, K.; Llorente, A. The ether lipid precursor hexadecylglycerol stimulates the release and changes the composition of exosomes derived from PC-3 cells. J. Biol. Chem., 2015, 290(7), 4225-4237.
[http://dx.doi.org/10.1074/jbc.M114.593962] [PMID: 25519911]
[64]
Wang, T.; Li, L.; Hong, W. SNARE proteins in membrane trafficking. Traffic, 2017, 18(12), 767-775.
[http://dx.doi.org/10.1111/tra.12524] [PMID: 28857378]
[65]
Shao, H.; Im, H.; Castro, C.M.; Breakefield, X.; Weissleder, R.; Lee, H. New technologies for analysis of extracellular vesicles. Chem. Rev., 2018, 118(4), 1917-1950.
[http://dx.doi.org/10.1021/acs.chemrev.7b00534] [PMID: 29384376]
[66]
Jia, Y.; Yu, L.; Ma, T.; Xu, W.; Qian, H.; Sun, Y.; Shi, H. Small extracellular vesicles isolation and separation: Current techniques, pending questions and clinical applications. Theranostics, 2022, 12(15), 6548-6575.
[http://dx.doi.org/10.7150/thno.74305] [PMID: 36185597]
[67]
Gardiner, C.; Vizio, D.D.; Sahoo, S.; Théry, C.; Witwer, K.W.; Wauben, M.; Hill, A.F. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J. Extracell. Vesicles, 2016, 5(1), 32945.
[http://dx.doi.org/10.3402/jev.v5.32945] [PMID: 27802845]
[68]
Royo, F.; Théry, C.; Falcón-Pérez, J.M.; Nieuwland, R.; Witwer, K.W. Methods for separation and characterization of extracellular vesicles: Results of a worldwide survey performed by the ISEV rigor and standardization subcommittee. Cells, 2020, 9(9), 1955.
[http://dx.doi.org/10.3390/cells9091955] [PMID: 32854228]
[69]
Alzhrani, G.N.; Alanazi, S.T.; Alsharif, S.Y.; Albalawi, A.M.; Alsharif, A.A.; Abdel-Maksoud, M.S.; Elsherbiny, N. Exosomes: Isolation, characterization, and biomedical applications. Cell Biol. Int., 2021, 45(9), 1807-1831.
[http://dx.doi.org/10.1002/cbin.11620] [PMID: 33913604]
[70]
Purushothaman, A. Exosomes from cell culture-conditioned medium: isolation by ultracentrifugation and characterization. Methods Mol. Biol., 2019, 1952, 233-244.
[http://dx.doi.org/10.1007/978-1-4939-9133-4_19] [PMID: 30825179]
[71]
Jeppesen, D.K.; Hvam, M.L.; Primdahl-Bengtson, B.; Boysen, A.T.; Whitehead, B.; Dyrskjøt, L.; Ørntoft, T.F.; Howard, K.A.; Ostenfeld, M.S. Comparative analysis of discrete exosome fractions obtained by differential centrifugation. J. Extracell. Vesicles, 2014, 3(1), 25011.
[http://dx.doi.org/10.3402/jev.v3.25011] [PMID: 25396408]
[72]
Zhu, L.; Sun, H.T.; Wang, S.; Huang, S.L.; Zheng, Y.; Wang, C.Q.; Hu, B.Y.; Qin, W.; Zou, T.T.; Fu, Y.; Shen, X.T.; Zhu, W.W.; Geng, Y.; Lu, L.; Jia, H.; Qin, L.X.; Dong, Q.Z. Isolation and characterization of exosomes for cancer research. J. Hematol. Oncol., 2020, 13(1), 152.
[http://dx.doi.org/10.1186/s13045-020-00987-y] [PMID: 33168028]
[73]
Langevin, S.M.; Kuhnell, D.; Orr-Asman, M.A.; Biesiada, J.; Zhang, X.; Medvedovic, M.; Thomas, H.E. Balancing yield, purity and practicality: a modified differential ultracentrifugation protocol for efficient isolation of small extracellular vesicles from human serum. RNA Biol., 2019, 16(1), 5-12.
[http://dx.doi.org/10.1080/15476286.2018.1564465] [PMID: 30604646]
[74]
Li, P.; Kaslan, M.; Lee, S.H.; Yao, J.; Gao, Z. Progress in exosome isolation techniques. Theranostics, 2017, 7(3), 789-804.
[http://dx.doi.org/10.7150/thno.18133] [PMID: 28255367]
[75]
Liangsupree, T.; Multia, E.; Riekkola, M.L. Modern isolation and separation techniques for extracellular vesicles. J. Chromatogr. A, 2021, 1636461773.
[http://dx.doi.org/10.1016/j.chroma.2020.461773] [PMID: 33316564]
[76]
Lamparski, H.G.; Metha-Damani, A.; Yao, J.Y.; Patel, S.; Hsu, D.H.; Ruegg, C.; Le Pecq, J.B. Production and characterization of clinical grade exosomes derived from dendritic cells. J. Immunol. Methods, 2002, 270(2), 211-226.
[http://dx.doi.org/10.1016/S0022-1759(02)00330-7] [PMID: 12379326]
[77]
Wang, J.; Ma, P.; Kim, D.H.; Liu, B.F.; Demirci, U. Towards microfluidic-based exosome isolation and detection for tumor therapy. Nano Today, 2021, 37101066.
[http://dx.doi.org/10.1016/j.nantod.2020.101066] [PMID: 33777166]
[78]
Busatto, S.; Vilanilam, G.; Ticer, T.; Lin, W.L.; Dickson, D.; Shapiro, S.; Bergese, P.; Wolfram, J. Tangential flow filtration for highly efficient concentration of extracellular vesicles from large volumes of fluid. Cells, 2018, 7(12), 273.
[http://dx.doi.org/10.3390/cells7120273] [PMID: 30558352]
[79]
Zeng, X.; Yi, X.; Chen, L.; Zhang, H.; Zhou, R.; Wu, J.; Chen, Y.; Huang, W.; Zhang, L.; Zheng, J.; Xiao, Y.; Yang, F. Characterization and bioassays of extracellular vesicles extracted by tangential flow filtration. Regen. Med., 2022, 17(3), 141-154.
[http://dx.doi.org/10.2217/rme-2021-0038] [PMID: 35073731]
[80]
Rho, J.; Chung, J.; Im, H.; Liong, M.; Shao, H.; Castro, C.M.; Weissleder, R.; Lee, H. Magnetic nanosensor for detection and profiling of erythrocyte-derived microvesicles. ACS Nano, 2013, 7(12), 11227-11233.
[http://dx.doi.org/10.1021/nn405016y] [PMID: 24295203]
[81]
Vlassov, A.V.; Magdaleno, S.; Setterquist, R.; Conrad, R. Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta, Gen. Subj., 2012, 1820(7), 940-948.
[http://dx.doi.org/10.1016/j.bbagen.2012.03.017] [PMID: 22503788]
[82]
Soares Martins, T.; Catita, J.; Martins Rosa, I.; A B da Cruz E Silva, O.; Henriques, A.G. Exosome isolation from distinct biofluids using precipitation and column-based approaches. PLoS One, 2018, 13(6), e0198820.
[http://dx.doi.org/10.1371/journal.pone.0198820] [PMID: 29889903]
[83]
Niu, Z.; Pang, R.T.K.; Liu, W.; Li, Q.; Cheng, R.; Yeung, W.S.B. Polymer-based precipitation preserves biological activities of extracellular vesicles from an endometrial cell line. PLoS One, 2017, 12(10), e0186534.
[http://dx.doi.org/10.1371/journal.pone.0186534] [PMID: 29023592]
[84]
Rekker, K.; Saare, M.; Roost, A.M.; Kubo, A.L.; Zarovni, N.; Chiesi, A.; Salumets, A.; Peters, M. Comparison of serum exosome isolation methods for microRNA profiling. Clin. Biochem., 2014, 47(1-2), 135-138.
[http://dx.doi.org/10.1016/j.clinbiochem.2013.10.020] [PMID: 24183884]
[85]
Zhu, J.; Zhang, J.; Ji, X.; Tan, Z.; Lubman, D.M. Column-based Technology for CD9-HPLC immunoaffinity isolation of serum extracellular vesicles. J. Proteome Res., 2021, 20(10), 4901-4911.
[http://dx.doi.org/10.1021/acs.jproteome.1c00549] [PMID: 34473505]
[86]
Oksvold, M.P.; Neurauter, A.; Pedersen, K.W. Magnetic bead-based isolation of exosomes. Methods Mol. Biol., 2015, 1218, 465-481.
[http://dx.doi.org/10.1007/978-1-4939-1538-5_27] [PMID: 25319668]
[87]
Tauro, B.J.; Greening, D.W.; Mathias, R.A.; Ji, H.; Mathivanan, S.; Scott, A.M.; Simpson, R.J. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods, 2012, 56(2), 293-304.
[http://dx.doi.org/10.1016/j.ymeth.2012.01.002] [PMID: 22285593]
[88]
Yoo, C.E.; Kim, G.; Kim, M.; Park, D.; Kang, H.J.; Lee, M.; Huh, N. A direct extraction method for microRNAs from exosomes captured by immunoaffinity beads. Anal. Biochem., 2012, 431(2), 96-98.
[http://dx.doi.org/10.1016/j.ab.2012.09.008] [PMID: 22982508]
[89]
Greening, D.W.; Xu, R.; Ji, H.; Tauro, B.J.; Simpson, R.J. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol. Biol., 2015, 1295, 179-209.
[http://dx.doi.org/10.1007/978-1-4939-2550-6_15] [PMID: 25820723]
[90]
Shtam, T.A.; Burdakov, V.S.; Landa, S.B.; Naryzhny, S.N.; Bairamukov, V.Y.; Malek, A.V.; Orlov, Y.N.; Filatov, M.V. Aggregation by lectin-methodical approach for effective isolation of exosomes from cell culture supernatant for proteome profiling. Tsitologiia, 2017, 59(1), 5-12.
[PMID: 30188097]
[91]
Groot Kormelink, T.; Arkesteijn, G.J.; Nauwelaers, F.A.; van den Engh, G.; Nolte-'t Hoen, E.N.; Wauben, M.H. Prerequisites for the analysis and sorting of extracellular vesicle subpopulations by high-resolution flow cytometry. Cytometry, 2016, 89(2), 135-147.
[92]
Lin, B.; Yang, J.; Song, Y.; Dang, G.; Feng, J. Exosomes and Atherogenesis. Front. Cardiovasc. Med., 2021, 8738031.
[http://dx.doi.org/10.3389/fcvm.2021.738031] [PMID: 34513963]
[93]
Patel, N.; Chin, D.D.; Chung, E.J. Exosomes in atherosclerosis, a double-edged sword: their role in disease pathogenesis and their potential as novel therapeutics. AAPS J., 2021, 23(5), 95.
[http://dx.doi.org/10.1208/s12248-021-00621-w] [PMID: 34312734]
[94]
Hergenreider, E.; Heydt, S.; Tréguer, K.; Boettger, T.; Horrevoets, A.J.G.; Zeiher, A.M.; Scheffer, M.P.; Frangakis, A.S.; Yin, X.; Mayr, M.; Braun, T.; Urbich, C.; Boon, R.A.; Dimmeler, S. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol., 2012, 14(3), 249-256.
[http://dx.doi.org/10.1038/ncb2441] [PMID: 22327366]
[95]
Cordes, K.R.; Sheehy, N.T.; White, M.P.; Berry, E.C.; Morton, S.U.; Muth, A.N.; Lee, T.H.; Miano, J.M.; Ivey, K.N.; Srivastava, D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature, 2009, 460(7256), 705-710.
[http://dx.doi.org/10.1038/nature08195] [PMID: 19578358]
[96]
Boettger, T.; Beetz, N.; Kostin, S.; Schneider, J.; Krüger, M.; Hein, L.; Braun, T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Invest., 2009, 119(9), 2634-2647.
[http://dx.doi.org/10.1172/JCI38864] [PMID: 19690389]
[97]
Zernecke, A.; Bidzhekov, K.; Noels, H.; Shagdarsuren, E.; Gan, L.; Denecke, B.; Hristov, M.; Köppel, T.; Jahantigh, M.N.; Lutgens, E.; Wang, S.; Olson, E.N.; Schober, A.; Weber, C. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal., 2009, 2(100), ra81.
[http://dx.doi.org/10.1126/scisignal.2000610] [PMID: 19996457]
[98]
Chistiakov, D.; Orekhov, A.; Bobryshev, Y. Cardiac extracellular vesicles in normal and infarcted heart. Int. J. Mol. Sci., 2016, 17(1), 63.
[http://dx.doi.org/10.3390/ijms17010063] [PMID: 26742038]
[99]
Li, L.; Wen, J.; Li, H.; He, Y.; Cui, X.; Zhang, X.; Guan, X.; Li, Z.; Cheng, M. Exosomal circ-1199 derived from EPCs exposed to oscillating shear stress acts as a sponge of let-7g-5p to promote endothelial-mesenchymal transition of EPCs by increasing HMGA2 expression. Life Sci., 2023, 312121223.
[http://dx.doi.org/10.1016/j.lfs.2022.121223] [PMID: 36435223]
[100]
Gao, S.; Wassler, M.; Zhang, L.; Li, Y.; Wang, J.; Zhang, Y.; Shelat, H.; Williams, J.; Geng, Y.J. MicroRNA-133a regulates insulin-like growth factor-1 receptor expression and vascular smooth muscle cell proliferation in murine atherosclerosis. Atherosclerosis, 2014, 232(1), 171-179.
[http://dx.doi.org/10.1016/j.atherosclerosis.2013.11.029] [PMID: 24401233]
[101]
Goettsch, C.; Hutcheson, J.D.; Aikawa, M.; Iwata, H.; Pham, T.; Nykjaer, A.; Kjolby, M.; Rogers, M.; Michel, T.; Shibasaki, M.; Hagita, S.; Kramann, R.; Rader, D.J.; Libby, P.; Singh, S.A.; Aikawa, E. Sortilin mediates vascular calcification via its recruitment into extracellular vesicles. J. Clin. Invest., 2016, 126(4), 1323-1336.
[http://dx.doi.org/10.1172/JCI80851] [PMID: 26950419]
[102]
Xie, Z.; Wang, X.; Liu, X.; Du, H.; Sun, C.; Shao, X.; Tian, J.; Gu, X.; Wang, H.; Tian, J.; Yu, B. Adipose-derived exosomes exert proatherogenic effects by regulating macrophage foam cell formation and polarization. J. Am. Heart Assoc., 2018, 7(5), e007442.
[http://dx.doi.org/10.1161/JAHA.117.007442] [PMID: 29502100]
[103]
Jansen, F.; Yang, X.; Proebsting, S.; Hoelscher, M.; Przybilla, D.; Baumann, K.; Schmitz, T.; Dolf, A.; Endl, E.; Franklin, B.S.; Sinning, J.M.; Vasa-Nicotera, M.; Nickenig, G.; Werner, N. MicroRNA expression in circulating microvesicles predicts cardiovascular events in patients with coronary artery disease. J. Am. Heart Assoc., 2014, 3(6), e001249.
[http://dx.doi.org/10.1161/JAHA.114.001249] [PMID: 25349183]
[104]
Zheng, B.; Yin, W.N.; Suzuki, T.; Zhang, X.H.; Zhang, Y.; Song, L.L.; Jin, L.S.; Zhan, H.; Zhang, H.; Li, J.S.; Wen, J.K. Exosome-mediated miR-155 transfer from smooth muscle cells to endothelial cells induces endothelial injury and promotes atherosclerosis. Mol. Ther., 2017, 25(6), 1279-1294.
[105]
Li, L.; Wang, Z.; Hu, X.; Wan, T.; Wu, H.; Jiang, W.; Hu, R. Human aortic smooth muscle cell-derived exosomal miR-221/222 inhibits autophagy via a PTEN/Akt signaling pathway in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun., 2016, 479(2), 343-350.
[http://dx.doi.org/10.1016/j.bbrc.2016.09.078] [PMID: 27644883]
[106]
Gao, W.; Liu, H.; Yuan, J.; Wu, C.; Huang, D.; Ma, Y.; Zhu, J.; Ma, L.; Guo, J.; Shi, H.; Zou, Y.; Ge, J. Exosomes derived from mature dendritic cells increase endothelial inflammation and atherosclerosis via membrane TNF α mediated NF κB pathway. J. Cell. Mol. Med., 2016, 20(12), 2318-2327.
[http://dx.doi.org/10.1111/jcmm.12923] [PMID: 27515767]
[107]
Chen, L.; Yang, W.; Guo, Y.; Chen, W.; Zheng, P.; Zeng, J.; Tong, W. Exosomal lncRNA GAS5 regulates the apoptosis of macrophages and vascular endothelial cells in atherosclerosis. PLoS One, 2017, 12(9), e0185406.
[http://dx.doi.org/10.1371/journal.pone.0185406] [PMID: 28945793]
[108]
Li, J.; Tan, M.; Xiang, Q.; Zhou, Z.; Yan, H. Thrombin-activated platelet-derived exosomes regulate endothelial cell expression of ICAM-1 via microRNA-223 during the thrombosis-inflammation response. Thromb. Res., 2017, 154, 96-105.
[http://dx.doi.org/10.1016/j.thromres.2017.04.016] [PMID: 28460288]
[109]
Yang, W.; Yin, R.; Zhu, X.; Yang, S.; Wang, J.; Zhou, Z.; Pan, X.; Ma, A. Mesenchymal stem-cell-derived exosomal miR-145 inhibits atherosclerosis by targeting JAM-A. Mol. Ther. Nucleic Acids, 2021, 23, 119-131.
[http://dx.doi.org/10.1016/j.omtn.2020.10.037] [PMID: 33335797]
[110]
Li, J.; Xue, H.; Li, T.; Chu, X.; Xin, D.; Xiong, Y.; Qiu, W.; Gao, X.; Qian, M.; Xu, J.; Wang, Z.; Li, G. Exosomes derived from mesenchymal stem cells attenuate the progression of atherosclerosis in ApoE−/- mice via miR-let7 mediated infiltration and polarization of M2 macrophage. Biochem. Biophys. Res. Commun., 2019, 510(4), 565-572.
[http://dx.doi.org/10.1016/j.bbrc.2019.02.005] [PMID: 30739785]
[111]
Bouchareychas, L.; Duong, P.; Covarrubias, S.; Alsop, E.; Phu, T.A.; Chung, A.; Gomes, M.; Wong, D.; Meechoovet, B.; Capili, A.; Yamamoto, R.; Nakauchi, H.; McManus, M.T.; Carpenter, S.; Van Keuren-Jensen, K.; Raffai, R.L. Macrophage exosomes resolve atherosclerosis by regulating hematopoiesis and inflammation via MicroRNA cargo. Cell Rep., 2020, 32(2), 107881.
[http://dx.doi.org/10.1016/j.celrep.2020.107881] [PMID: 32668250]
[112]
Basatemur, G.L.; Jørgensen, H.F.; Clarke, M.C.H.; Bennett, M.R.; Mallat, Z. Vascular smooth muscle cells in atherosclerosis. Nat. Rev. Cardiol., 2019, 16(12), 727-744.
[http://dx.doi.org/10.1038/s41569-019-0227-9] [PMID: 31243391]
[113]
Wang, C.; Liu, C.; Shi, J.; Li, H.; Jiang, S.; Zhao, P.; Zhang, M.; Du, G.; Fu, S.; Li, S.; Wang, Z.; Wang, X.; Gao, F.; Sun, P.; Tian, J. Nicotine exacerbates endothelial dysfunction and drives atherosclerosis via extracellular vesicle-miRNA. Cardiovasc. Res., 2022.
[PMID: 36006370]
[114]
Goetzl, E.J.; Schwartz, J.B.; Mustapic, M.; Lobach, I.V.; Daneman, R.; Abner, E.L.; Jicha, G.A. Altered cargo proteins of human plasma endothelial cell–derived exosomes in atherosclerotic cerebrovascular disease. FASEB J., 2017, 31(8), 3689-3694.
[http://dx.doi.org/10.1096/fj.201700149] [PMID: 28476896]
[115]
Al-Rawaf, H.A. Circulating microRNAs and adipokines as markers of metabolic syndrome in adolescents with obesity. Clin. Nutr., 2019, 38(5), 2231-2238.
[http://dx.doi.org/10.1016/j.clnu.2018.09.024] [PMID: 30309709]
[116]
Lu, M.; Yuan, S.; Li, S.; Li, L.; Liu, M.; Wan, S. The exosome-derived biomarker in atherosclerosis and its clinical application. J. Cardiovasc. Transl. Res., 2019, 12(1), 68-74.
[http://dx.doi.org/10.1007/s12265-018-9796-y] [PMID: 29802541]
[117]
Li, X.; He, X.; Wang, J.; Wang, D.; Cong, P.; Zhu, A.; Chen, W. The regulation of exosome-derived miRNA on heterogeneity of macrophages in atherosclerotic plaques. Front. Immunol., 2020, 11, 2175.
[http://dx.doi.org/10.3389/fimmu.2020.02175] [PMID: 33013913]
[118]
Wu, W.; Pan, Y.; Cai, M.; Cen, J.; Chen, C.; Zheng, L.; Liu, X.; Xiong, X. Plasma-derived exosomal circular RNA hsa_circ_0005540 as a novel diagnostic biomarker for coronary artery disease. Dis. Markers, 2020, 2020, 1-7.
[http://dx.doi.org/10.1155/2020/3178642] [PMID: 32670434]
[119]
Wiklander, O.P.B.; Brennan, M.Á.; Lötvall, J.; Breakefield, X.O.; EL Andaloussi, S. Advances in therapeutic applications of extracellular vesicles. Sci. Transl. Med., 2019, 11(492), eaav8521.
[http://dx.doi.org/10.1126/scitranslmed.aav8521] [PMID: 31092696]
[120]
Shi, C.; Ulke-Lemée, A.; Deng, J.; Batulan, Z.; O’Brien, E.R. Characterization of heat shock protein 27 in extracellular vesicles: a potential anti-inflammatory therapy. FASEB J., 2019, 33(2), 1617-1630.
[http://dx.doi.org/10.1096/fj.201800987R] [PMID: 30188755]
[121]
Guo, Z.; Zhao, Z.; Yang, C.; Song, C. Transfer of microRNA-221 from mesenchymal stem cell-derived extracellular vesicles inhibits atherosclerotic plaque formation. Transl. Res., 2020, 226, 83-95.
[http://dx.doi.org/10.1016/j.trsl.2020.07.003] [PMID: 32659442]
[122]
Venkat, P.; Cui, C.; Chopp, M.; Zacharek, A.; Wang, F.; Landschoot-Ward, J.; Shen, Y.; Chen, J. MiR-126 mediates brain endothelial cell exosome treatment–induced neurorestorative effects after stroke in type 2 diabetes mellitus mice. Stroke, 2019, 50(10), 2865-2874.
[http://dx.doi.org/10.1161/STROKEAHA.119.025371] [PMID: 31394992]
[123]
Milano, G.; Biemmi, V.; Lazzarini, E.; Balbi, C.; Ciullo, A.; Bolis, S.; Ameri, P.; Di Silvestre, D.; Mauri, P.; Barile, L.; Vassalli, G. Intravenous administration of cardiac progenitor cell-derived exosomes protects against doxorubicin/trastuzumab-induced cardiac toxicity. Cardiovasc. Res., 2020, 116(2), 383-392.
[PMID: 31098627]
[124]
Casado-Díaz, A.; Quesada-Gómez, J.M.; Dorado, G. Extracellular vesicles derived from mesenchymal stem cells (MSC) in regenerative medicine: applications in skin wound healing. Front. Bioeng. Biotechnol., 2020, 8, 146.
[http://dx.doi.org/10.3389/fbioe.2020.00146] [PMID: 32195233]
[125]
Cui, G.H.; Guo, H.D.; Li, H.; Zhai, Y.; Gong, Z.B.; Wu, J.; Liu, J.S.; Dong, Y.R.; Hou, S.X.; Liu, J.R. RVG-modified exosomes derived from mesenchymal stem cells rescue memory deficits by regulating inflammatory responses in a mouse model of Alzheimer's disease. Immun. Ageing, 2019, 16, 10.
[126]
Villata, S.; Canta, M.; Cauda, V. EVs and bioengineering: from cellular products to engineered nanomachines. Int. J. Mol. Sci., 2020, 21(17), 6048.
[http://dx.doi.org/10.3390/ijms21176048] [PMID: 32842627]
[127]
Sun, D.; Zhuang, X.; Xiang, X.; Liu, Y.; Zhang, S.; Liu, C.; Barnes, S.; Grizzle, W.; Miller, D.; Zhang, H.G. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther., 2010, 18(9), 1606-1614.
[128]
Ma, Q.; Fan, Q.; Han, X.; Dong, Z.; Xu, J.; Bai, J.; Tao, W.; Sun, D.; Wang, C. Platelet-derived extracellular vesicles to target plaque inflammation for effective anti-atherosclerotic therapy. J. Control. Release, 2021, 329, 445-453.
[129]
Zhang, Y.; Bi, J.; Huang, J.; Tang, Y.; Du, S.; Li, P. Exosome: A review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int. J. Nanomedicine, 2020, 15, 6917-6934.
[http://dx.doi.org/10.2147/IJN.S264498] [PMID: 33061359]
[130]
Antimisiaris, S.; Mourtas, S.; Marazioti, A. Exosomes and exosome-inspired vesicles for targeted drug delivery. Pharmaceutics, 2018, 10(4), 218.
[http://dx.doi.org/10.3390/pharmaceutics10040218] [PMID: 30404188]
[131]
Tian, Y.; Li, S.; Song, J.; Ji, T.; Zhu, M.; Anderson, G.J.; Wei, J.; Nie, G. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials, 2014, 35(7), 2383-2390.
[http://dx.doi.org/10.1016/j.biomaterials.2013.11.083] [PMID: 24345736]
[132]
Zhu, Q.; Ling, X.; Yang, Y.; Zhang, J.; Li, Q.; Niu, X.; Hu, G.; Chen, B.; Li, H.; Wang, Y.; Deng, Z. Embryonic stem cells-derived exosomes endowed with targeting properties as chemotherapeutics delivery vehicles for glioblastoma therapy. Adv. Sci. (Weinh.), 2019, 6(6), 1801899.
[http://dx.doi.org/10.1002/advs.201801899] [PMID: 30937268]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy