Login Register Cart 0
Generic placeholder image

Current Drug Delivery

Editor-in-Chief

ISSN (Print): 1567-2018
ISSN (Online): 1875-5704

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Exosomes as Targeted Delivery Drug System: Advances in Exosome Loading, Surface Functionalization and Potential for Clinical Application

Author(s): Zun Y. Guo, Yue Tang* and Yi C. Cheng

Volume 21, Issue 4, 2024

Published on: 29 December, 2022

Page: [473 - 487] Pages: 15

DOI: 10.2174/1567201819666220613150814

Price: $65

conference banner
Abstract

Exosomes are subtypes of vesicles secreted by almost all cells and can play an important role in intercellular communication. They contain various proteins, lipids, nucleic acids and other natural substances from their metrocytes. Exosomes are expected to be a new generation of drug delivery systems due to their low immunogenicity, high potential to transfer bioactive substances and biocompatibility. However, exosomes themselves are not highly targeted, it is necessary to develop new surface modification techniques and targeted drug delivery strategies, which are the focus of drug delivery research. In this review, we introduced the biogenesis of exosomes and their role in intercellular communication. We listed various advanced exosome drug-loading techniques. Emphatically, we summarized different exosome surface modification techniques and targeted drug delivery strategies. In addition, we discussed the application of exosomes in vaccines and briefly introduced milk exosomes. Finally, we clarified the clinical application prospects and shortcomings of exosomes.

Keywords: Exosomes, Drug delivery system, Surface modification, Biothreapy, Nanoparticles, Nanotechnology.

Next »
[1]
Stahl, P.D.; Raposo, G. Extracellular vesicles: Exosomes and microvesicles, integrators of homeostasis. Physiology (Bethesda), 2019, 34(3), 169-177.
[http://dx.doi.org/10.1152/physiol.00045.2018] [PMID: 30968753]
[2]
Paolicelli, R.C.; Bergamini, G.; Rajendran, L. Cell-to-cell communication by extracellular vesicles: Focus on microglia. Neuroscience, 2019, 405, 148-157.
[http://dx.doi.org/10.1016/j.neuroscience.2018.04.003] [PMID: 29660443]
[3]
Xiao, T.; Zhang, W.; Jiao, B.; Pan, C.Z.; Liu, X.; Shen, L. The role of exosomes in the pathogenesis of Alzheimer’ disease. Transl. Neurodegener., 2017, 6(1), 3.
[http://dx.doi.org/10.1186/s40035-017-0072-x] [PMID: 28184302]
[4]
Urbanelli, L.; Magini, A.; Buratta, S.; Brozzi, A.; Sagini, K.; Polchi, A.; Tancini, B.; Emiliani, C. Signaling pathways in exosomes biogene-sis, secretion and fate. Genes (Basel), 2013, 4(2), 152-170.
[http://dx.doi.org/10.3390/genes4020152] [PMID: 24705158]
[5]
E.L., Andaloussi S.; Mäger, I.; Breakefield, X.O.; Wood, M.J. Extracellular vesicles: Biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov., 2013, 12(5), 347-357.
[http://dx.doi.org/10.1038/nrd3978] [PMID: 23584393]
[6]
Bodega, G.; Alique, M.; Puebla, L.; Carracedo, J.; Ramírez, R.M. Microvesicles: ROS scavengers and ROS producers. J. Extracell. Vesicles, 2019, 8(1), 1626654.
[http://dx.doi.org/10.1080/20013078.2019.1626654] [PMID: 31258880]
[7]
Li, W.; Li, C.; Zhou, T.; Liu, X.; Liu, X.; Li, X.; Chen, D. Role of exosomal proteins in cancer diagnosis. Mol. Cancer, 2017, 16(1), 145.
[http://dx.doi.org/10.1186/s12943-017-0706-8] [PMID: 28851367]
[8]
Février, B.; Raposo, G. Exosomes: Endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol., 2004, 16(4), 415-421.
[http://dx.doi.org/10.1016/j.ceb.2004.06.003] [PMID: 15261674]
[9]
Li, N.; Zhao, L.; Wei, Y.; Ea, V.L.; Nian, H.; Wei, R. Recent advances of exosomes in immune-mediated eye diseases. Stem Cell Res. Ther., 2019, 10(1), 278.
[http://dx.doi.org/10.1186/s13287-019-1372-0] [PMID: 31470892]
[10]
Cui, S.; Cheng, Z.; Qin, W.; Jiang, L. Exosomes as a liquid biopsy for lung cancer. Lung Cancer, 2018, 116, 46-54.
[http://dx.doi.org/10.1016/j.lungcan.2017.12.012] [PMID: 29413050]
[11]
Hesari, A.; Golrokh Moghadam, S.A.; Siasi, A.; Rahmani, M.; Behboodi, N.; Rastgar-Moghadam, A.; Ferns, G.A.; Ghasemi, F.; Avan, A. Tumor-derived exosomes: Potential biomarker or therapeutic target in breast cancer? J. Cell. Biochem., 2018, 119(6), 4236-4240.
[http://dx.doi.org/10.1002/jcb.26364] [PMID: 28833502]
[12]
Cho, Y.E.; Song, B.J.; Akbar, M.; Baek, M.C. Extracellular vesicles as potential biomarkers for alcohol- and drug-induced liver injury and their therapeutic applications. Pharmacol. Ther., 2018, 187, 180-194.
[http://dx.doi.org/10.1016/j.pharmthera.2018.03.009] [PMID: 29621595]
[13]
Hao, Z.C.; Lu, J.; Wang, S.Z.; Wu, H.; Zhang, Y.T.; Xu, S.G. Stem cell-derived exosomes: A promising strategy for fracture healing. Cell Prolif., 2017, 50(5), e12359.
[http://dx.doi.org/10.1111/cpr.12359] [PMID: 28741758]
[14]
Kluszczyńska, K.; Czernek, L.; Cypryk, W.; Pęczek, Ł.; Düchler, M. Methods for the determination of the purity of exosomes. Curr. Pharm. Des., 2019, 25(42), 4464-4485.
[http://dx.doi.org/10.2174/1381612825666191206162712] [PMID: 31808383]
[15]
Serrano-Pertierra, E.; Oliveira-Rodríguez, M.; Rivas, M.; Oliva, P.; Villafani, J.; Navarro, A.; Blanco-López, M.C.; Cernuda-Morollón, E. Characterization of plasma-derived extracellular vesicles isolated by different methods: A comparison study. Bioengineering (Basel), 2019, 6(1), E8.
[http://dx.doi.org/10.3390/bioengineering6010008] [PMID: 30658418]
[16]
Kalra, H.; Adda, C.G.; Liem, M.; Ang, C.S.; Mechler, A.; Simpson, R.J.; Hulett, M.D.; Mathivanan, S. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics, 2013, 13(22), 3354-3364.
[http://dx.doi.org/10.1002/pmic.201300282] [PMID: 24115447]
[17]
Lobb, R.J.; Becker, M.; Wen, S.W.; Wong, C.S.; Wiegmans, A.P.; Leimgruber, A.; Möller, A. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J. Extracell. Vesicles, 2015, 4(1), 27031.
[http://dx.doi.org/10.3402/jev.v4.27031] [PMID: 26194179]
[18]
Monguió-Tortajada, M.; Gálvez-Montón, C.; Bayes-Genis, A.; Roura, S.; Borràs, F.E. Extracellular vesicle isolation methods: Rising im-pact of size-exclusion chromatography. Cell. Mol. Life Sci., 2019, 76(12), 2369-2382.
[http://dx.doi.org/10.1007/s00018-019-03071-y] [PMID: 30891621]
[19]
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]
[20]
Cao, F.; Gao, Y.; Chu, Q.; Wu, Q.; Zhao, L.; Lan, T.; Zhao, L. Proteomics comparison of exosomes from serum and plasma between ul-tracentrifugation and polymer-based precipitation kit methods. Electrophoresis, 2019, 40(23-24), 3092-3098.
[http://dx.doi.org/10.1002/elps.201900295] [PMID: 31621929]
[21]
Zhao, Z.; McGill, J.; Gamero-Kubota, P.; He, M. Microfluidic on-demand engineering of exosomes towards cancer immunotherapy. Lab Chip, 2019, 19(10), 1877-1886.
[http://dx.doi.org/10.1039/C8LC01279B] [PMID: 31044204]
[22]
Cumba Garcia, L.M.; Peterson, T.E.; Cepeda, M.A.; Johnson, A.J.; Parney, I.F. Isolation and analysis of plasma-derived exosomes in patients with glioma. Front. Oncol., 2019, 9, 651.
[http://dx.doi.org/10.3389/fonc.2019.00651] [PMID: 31380286]
[23]
Brown, J.A.; Codreanu, S.G.; Shi, M.; Sherrod, S.D.; Markov, D.A.; Neely, M.D.; Britt, C.M.; Hoilett, O.S.; Reiserer, R.S.; Samson, P.C.; McCawley, L.J.; Webb, D.J.; Bowman, A.B.; McLean, J.A.; Wikswo, J.P. Metabolic consequences of inflammatory disruption of the blood-brain barrier in an organ-on-chip model of the human neurovascular unit. J. Neuroinflammation, 2016, 13(1), 306.
[http://dx.doi.org/10.1186/s12974-016-0760-y] [PMID: 27955696]
[24]
Cocozza, F.; Grisard, E.; Martin-Jaular, L.; Mathieu, M.; Théry, C. SnapShot: Extracellular vesicles. Cell, 2020, 182(1), 262-262.e1.
[http://dx.doi.org/10.1016/j.cell.2020.04.054] [PMID: 32649878]
[25]
Freitas, D.; Balmaña, M.; Poças, J.; Campos, D.; Osório, H.; Konstantinidi, A.; Vakhrushev, S.Y.; Magalhães, A.; Reis, C.A. Different iso-lation approaches lead to diverse glycosylated extracellular vesicle populations. J. Extracell. Vesicles, 2019, 8(1), 1621131.
[http://dx.doi.org/10.1080/20013078.2019.1621131] [PMID: 31236201]
[26]
Yue, B.; Yang, H.; Wang, J.; Ru, W.; Wu, J.; Huang, Y.; Lan, X.; Lei, C.; Chen, H. Exosome biogenesis, secretion and function of exoso-mal miRNAs in skeletal muscle myogenesis. Cell Prolif., 2020, 53(7), e12857.
[http://dx.doi.org/10.1111/cpr.12857] [PMID: 32578911]
[27]
Cobelli, N.J.; Leong, D.J.; Sun, H.B. Exosomes: Biology, therapeutic potential, and emerging role in musculoskeletal repair and regenera-tion. Ann. N. Y. Acad. Sci., 2017, 1410(1), 57-67.
[http://dx.doi.org/10.1111/nyas.13469] [PMID: 29125180]
[28]
Miyado, M.; Kang, W.; Kawano, N.; Miyado, K. Microexosomes versus exosomes: Shared components but distinct structures. Regen. Ther., 2019, 11, 31-33.
[http://dx.doi.org/10.1016/j.reth.2019.04.013] [PMID: 31193153]
[29]
Zhang, X.; Tu, H.; Yang, Y.; Fang, L.; Wu, Q.; Li, J. Mesenchymal stem cell-derived extracellular vesicles: Roles in tumor growth, pro-gression, and drug resistance. Stem Cells Int., 2017, 2017, 1758139.
[http://dx.doi.org/10.1155/2017/1758139] [PMID: 28377788]
[30]
Pegtel, D.M.; Gould, S.J. Exosomes. Annu. Rev. Biochem., 2019, 88(1), 487-514.
[http://dx.doi.org/10.1146/annurev-biochem-013118-111902] [PMID: 31220978]
[31]
Jiao, W.; Mi, X.; Qin, Y.; Zhao, S. Stem cell transplantation improves ovarian function through paracrine mechanisms. Curr. Gene Ther., 2020, 20(5), 347-355.
[http://dx.doi.org/10.2174/1566523220666200928142333] [PMID: 32988352]
[32]
Marshall, H.T.; Djamgoz, M.B.A. Immuno-Oncology: Emerging Targets and Combination Therapies. Front. Oncol., 2018, 8, 315.
[http://dx.doi.org/10.3389/fonc.2018.00315] [PMID: 30191140]
[33]
Chettimada, S.; Lorenz, D.R.; Misra, V.; Dillon, S.T.; Reeves, R.K.; Manickam, C.; Morgello, S.; Kirk, G.D.; Mehta, S.H.; Gabuzda, D. Exosome markers associated with immune activation and oxidative stress in HIV patients on antiretroviral therapy. Sci. Rep., 2018, 8(1), 7227.
[http://dx.doi.org/10.1038/s41598-018-25515-4] [PMID: 29740045]
[34]
Sardar Sinha, M.; Ansell-Schultz, A.; Civitelli, L.; Hildesjö, C.; Larsson, M.; Lannfelt, L.; Ingelsson, M.; Hallbeck, M. Alzheimer’s disease pathology propagation by exosomes containing toxic amyloid-beta oligomers. Acta Neuropathol., 2018, 136(1), 41-56.
[http://dx.doi.org/10.1007/s00401-018-1868-1] [PMID: 29934873]
[35]
Guo, M.; Wang, J.; Zhao, Y.; Feng, Y.; Han, S.; Dong, Q.; Cui, M.; Tieu, K. Microglial exosomes facilitate α-synuclein transmission in Parkinson’s disease. Brain, 2020, 143(5), 1476-1497.
[http://dx.doi.org/10.1093/brain/awaa090] [PMID: 32355963]
[36]
Kalluri, R.; LeBleu, V.S. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478), eaau6977.
[http://dx.doi.org/10.1126/science.aau6977] [PMID: 32029601]
[37]
Meldolesi, J. Exosomes and ectosomes in intercellular communication. Curr. Biol., 2018, 28(8), R435-R444.
[http://dx.doi.org/10.1016/j.cub.2018.01.059] [PMID: 29689228]
[38]
Gupta, R.; Radicioni, G.; Abdelwahab, S.; Dang, H.; Carpenter, J.; Chua, M.; Mieczkowski, P.A.; Sheridan, J.T.; Randell, S.H.; Kesimer, M. Intercellular communication between airway epithelial cells is mediated by exosome-like vesicles. Am. J. Respir. Cell Mol. Biol., 2019, 60(2), 209-220.
[http://dx.doi.org/10.1165/rcmb.2018-0156OC] [PMID: 30230353]
[39]
Wortzel, I.; Dror, S.; Kenific, C.M.; Lyden, D. Exosome-mediated metastasis: Communication from a distance. Dev. Cell, 2019, 49(3), 347-360.
[http://dx.doi.org/10.1016/j.devcel.2019.04.011] [PMID: 31063754]
[40]
Salimian, J.; Mirzaei, H.; Moridikia, A.; Harchegani, A.B.; Sahebkar, A.; Salehi, H. Chronic obstructive pulmonary disease: MicroRNAs and exosomes as new diagnostic and therapeutic biomarkers. J. Res. Med. Sci., 2018, 23(1), 27.
[http://dx.doi.org/10.4103/jrms.JRMS_1054_17] [PMID: 29692824]
[41]
McGough, I.J.; Vincent, J.P. Exosomes in developmental signalling. Development, 2016, 143(14), 2482-2493.
[http://dx.doi.org/10.1242/dev.126516] [PMID: 27436038]
[42]
Dave, K.M.; Zhao, W.; Hoover, C.; D’Souza, A.S.; Manickam, D. Extracellular vesicles derived from a human brain endothelial cell line increase cellular ATP levels. AAPS PharmSciTech, 2021, 22(1), 18.
[http://dx.doi.org/10.1208/s12249-020-01892-w] [PMID: 33389284]
[43]
Ickenstein, L.M.; Garidel, P. Lipid-based nanoparticle formulations for small molecules and RNA drugs. Expert Opin. Drug Deliv., 2019, 16(11), 1205-1226.
[http://dx.doi.org/10.1080/17425247.2019.1669558] [PMID: 31530041]
[44]
Colino, C.I.; Lanao, J.M.; Gutierrez-Millan, C. Targeting of hepatic macrophages by therapeutic nanoparticles. Front. Immunol., 2020, 11, 218.
[http://dx.doi.org/10.3389/fimmu.2020.00218] [PMID: 32194546]
[45]
Wang, Y.; Grainger, D.W. Lyophilized liposome-based parenteral drug development: Reviewing complex product design strategies and current regulatory environments. Adv. Drug Deliv. Rev., 2019, 151-152, 56-71.
[http://dx.doi.org/10.1016/j.addr.2019.03.003] [PMID: 30898571]
[46]
Nordmeier, S.; Ke, W.; Afonin, K.A.; Portnoy, V. Exosome mediated delivery of functional nucleic acid nanoparticles (NANPs). Nanomedicine, 2020, 30, 102285.
[http://dx.doi.org/10.1016/j.nano.2020.102285] [PMID: 32781137]
[47]
Xu, Z.H.; Miao, Z.W.; Jiang, Q.Z.; Gan, D.X.; Wei, X.G.; Xue, X.Z.; Li, J.Q.; Zheng, F.; Qin, X.X.; Fang, W.G.; Chen, Y.H.; Li, B. Brain microvascular endothelial cell exosome-mediated S100A16 up-regulation confers small-cell lung cancer cell survival in brain. FASEB J., 2019, 33(2), 1742-1757.
[http://dx.doi.org/10.1096/fj.201800428R] [PMID: 30183374]
[48]
Subhan, M.A.; Torchilin, V.P. siRNA based drug design, quality, delivery and clinical translation. Nanomedicine, 2020, 29, 102239.
[http://dx.doi.org/10.1016/j.nano.2020.102239] [PMID: 32544449]
[49]
Kamerkar, S.; LeBleu, V.S.; Sugimoto, H.; Yang, S.; Ruivo, C.F.; Melo, S.A.; Lee, J.J.; Kalluri, R. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature, 2017, 546(7659), 498-503.
[http://dx.doi.org/10.1038/nature22341] [PMID: 28607485]
[50]
Katakowski, M.; Buller, B.; Zheng, X.; Lu, Y.; Rogers, T.; Osobamiro, O.; Shu, W.; Jiang, F.; Chopp, M. Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett., 2013, 335(1), 201-204.
[http://dx.doi.org/10.1016/j.canlet.2013.02.019] [PMID: 23419525]
[51]
Pascucci, L.; Coccè, V.; Bonomi, A.; Ami, D.; Ceccarelli, P.; Ciusani, E.; Viganò, L.; Locatelli, A.; Sisto, F.; Doglia, S.M.; Parati, E.; Ber-nardo, M.E.; Muraca, M.; Alessandri, G.; Bondiolotti, G.; Pessina, A. Paclitaxel is incorporated by mesenchymal stromal cells and re-leased in exosomes that inhibit in vitro tumor growth: A new approach for drug delivery. J. Control. Release, 2014, 192, 262-270.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.042] [PMID: 25084218]
[52]
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 de-livery system: The anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther., 2010, 18(9), 1606-1614.
[http://dx.doi.org/10.1038/mt.2010.105] [PMID: 20571541]
[53]
Salarpour, S.; Forootanfar, H.; Pournamdari, M.; Ahmadi-Zeidabadi, M.; Esmaeeli, M.; Pardakhty, A. Paclitaxel incorporated exosomes derived from glioblastoma cells: Comparative study of two loading techniques. Daru, 2019, 27(2), 533-539.
[http://dx.doi.org/10.1007/s40199-019-00280-5] [PMID: 31317441]
[54]
Hood, J.L.; Scott, M.J.; Wickline, S.A. Maximizing exosome colloidal stability following electroporation. Anal. Biochem., 2014, 448, 41-49.
[http://dx.doi.org/10.1016/j.ab.2013.12.001] [PMID: 24333249]
[55]
Pomatto, M.A.C.; Bussolati, B.; D’Antico, S.; Ghiotto, S.; Tetta, C.; Brizzi, M.F.; Camussi, G. Improved loading of plasma-derived extra-cellular vesicles to encapsulate antitumor miRNAs. Mol. Ther. Methods Clin. Dev., 2019, 13, 133-144.
[http://dx.doi.org/10.1016/j.omtm.2019.01.001] [PMID: 30788382]
[56]
Taghikhani, A.; Hassan, Z.M.; Ebrahimi, M.; Moazzeni, S.M. MicroRNA modified tumor-derived exosomes as novel tools for maturation of dendritic cells. J. Cell. Physiol., 2019, 234(6), 9417-9427.
[http://dx.doi.org/10.1002/jcp.27626] [PMID: 30362582]
[57]
Tapparo, M.; Bruno, S.; Collino, F.; Togliatto, G.; Deregibus, M.C.; Provero, P.; Wen, S.; Quesenberry, P.J.; Camussi, G. Renal regenera-tive potential of extracellular vesicles derived from miRNA-engineered mesenchymal stromal cells. Int. J. Mol. Sci., 2019, 20(10), E2381.
[http://dx.doi.org/10.3390/ijms20102381] [PMID: 31091699]
[58]
Le Saux, S.; Aarrass, H.; Lai-Kee-Him, J.; Bron, P.; Armengaud, J.; Miotello, G.; Bertrand-Michel, J.; Dubois, E.; George, S.; Faklaris, O.; Devoisselle, J.M.; Legrand, P.; Chopineau, J.; Morille, M. Post-production modifications of murine Mesenchymal Stem Cell (mMSC) de-rived Extracellular Vesicles (EVs) and impact on their cellular interaction. Biomaterials, 2020, 231, 119675.
[http://dx.doi.org/10.1016/j.biomaterials.2019.119675] [PMID: 31838346]
[59]
Kim, M.S.; Haney, M.J.; Zhao, Y.; Mahajan, V.; Deygen, I.; Klyachko, N.L.; Inskoe, E.; Piroyan, A.; Sokolsky, M.; Okolie, O.; Hingtgen, S.D.; Kabanov, A.V.; Batrakova, E.V. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine, 2016, 12(3), 655-664.
[http://dx.doi.org/10.1016/j.nano.2015.10.012] [PMID: 26586551]
[60]
Van Deun, J.; Roux, Q.; Deville, S.; Van Acker, T.; Rappu, P.; Miinalainen, I.; Heino, J.; Vanhaecke, F.; De Geest, B.G.; De Wever, O.; Hendrix, A. Feasibility of mechanical extrusion to coat nanoparticles with extracellular vesicle membranes. Cells, 2020, 9(8), E1797.
[http://dx.doi.org/10.3390/cells9081797] [PMID: 32751082]
[61]
Haney, M.J.; Klyachko, N.L.; Zhao, Y.; Gupta, R.; Plotnikova, E.G.; He, Z.; Patel, T.; Piroyan, A.; Sokolsky, M.; Kabanov, A.V.; Batrako-va, E.V. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J. Control. Release, 2015, 207, 18-30.
[http://dx.doi.org/10.1016/j.jconrel.2015.03.033] [PMID: 25836593]
[62]
Lv, L.L.; Cao, Y.; Liu, D.; Xu, M.; Liu, H.; Tang, R.N.; Ma, K.L.; Liu, B.C. Isolation and quantification of microRNAs from urinary exo-somes/microvesicles for biomarker discovery. Int. J. Biol. Sci., 2013, 9(10), 1021-1031.
[http://dx.doi.org/10.7150/ijbs.6100] [PMID: 24250247]
[63]
Sato, Y.T.; Umezaki, K.; Sawada, S.; Mukai, S.A.; Sasaki, Y.; Harada, N.; Shiku, H.; Akiyoshi, K. Engineering hybrid exosomes by mem-brane fusion with liposomes. Sci. Rep., 2016, 6(1), 21933.
[http://dx.doi.org/10.1038/srep21933] [PMID: 26911358]
[64]
Richter, M.; Fuhrmann, K.; Fuhrmann, G. Evaluation of the storage stability of extracellular vesicles. J. Vis. Exp., 2019, 147
[http://dx.doi.org/10.379/59584]
[65]
Fuhrmann, G.; Serio, A.; Mazo, M.; Nair, R.; Stevens, M.M. Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J. Control. Release, 2015, 205, 35-44.
[http://dx.doi.org/10.1016/j.jconrel.2014.11.029] [PMID: 25483424]
[66]
Jang, S.C.; Kim, O.Y.; Yoon, C.M.; Choi, D.S.; Roh, T.Y.; Park, J.; Nilsson, J.; Lötvall, J.; Kim, Y.K.; Gho, Y.S. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano, 2013, 7(9), 7698-7710.
[http://dx.doi.org/10.1021/nn402232g] [PMID: 24004438]
[67]
Liu, X.; Lu, Y.; Xu, Y.; Hou, S.; Huang, J.; Wang, B.; Zhao, J.; Xia, S.; Fan, S.; Yu, X.; Du, Y.; Hou, L.; Li, Z.; Ding, Z.; An, S.; Huang, B.; Li, L.; Tang, J.; Ju, J.; Guan, H.; Song, B. Exosomal transfer of miR-501 confers doxorubicin resistance and tumorigenesis via targeting of BLID in gastric cancer. Cancer Lett., 2019, 459, 122-134.
[http://dx.doi.org/10.1016/j.canlet.2019.05.035] [PMID: 31173853]
[68]
Li, Y.; Wang, J.; Chen, S.; Wu, P.; Xu, S.; Wang, C.; Shi, H.; Bihl, J. miR-137 boosts the neuroprotective effect of endothelial progenitor cell-derived exosomes in oxyhemoglobin-treated SH-SY5Y cells partially via COX2/PGE2 pathway. Stem Cell Res. Ther., 2020, 11(1), 330.
[http://dx.doi.org/10.1186/s13287-020-01836-y] [PMID: 33100224]
[69]
Shtam, T.A.; Kovalev, R.A.; Varfolomeeva, E.Y.; Makarov, E.M.; Kil, Y.V.; Filatov, M.V. Exosomes are natural carriers of exogenous siRNA to human cells in vitro. Cell Commun. Signal., 2013, 11(1), 88.
[http://dx.doi.org/10.1186/1478-811X-11-88] [PMID: 24245560]
[70]
Lin, Y.; Lu, Y.; Li, X. Biological characteristics of exosomes and genetically engineered exosomes for the targeted delivery of therapeutic agents. J. Drug Target., 2020, 28(2), 129-141.
[http://dx.doi.org/10.1080/1061186X.2019.1641508] [PMID: 31280623]
[71]
Benichou, G.; Wang, M.; Ahrens, K.; Madsen, J.C. Extracellular vesicles in allograft rejection and tolerance. Cell. Immunol., 2020, 349, 104063.
[http://dx.doi.org/10.1016/j.cellimm.2020.104063] [PMID: 32087929]
[72]
Tang, T.T.; Wang, B.; Lv, L.L.; Liu, B.C. Extracellular vesicle-based nanotherapeutics: Emerging frontiers in anti-inflammatory therapy. Theranostics, 2020, 10(18), 8111-8129.
[http://dx.doi.org/10.7150/thno.47865] [PMID: 32724461]
[73]
Tamura, R.; Uemoto, S.; Tabata, Y. Augmented liver targeting of exosomes by surface modification with cationized pullulan. Acta Biomater., 2017, 57, 274-284.
[http://dx.doi.org/10.1016/j.actbio.2017.05.013] [PMID: 28483695]
[74]
Zhuang, M.; Chen, X.; Du, D.; Shi, J.; Deng, M.; Long, Q.; Yin, X.; Wang, Y.; Rao, L. SPION decorated exosome delivery of TNF-α to cancer cell membranes through magnetism. Nanoscale, 2020, 12(1), 173-188.
[http://dx.doi.org/10.1039/C9NR05865F] [PMID: 31803890]
[75]
Choi, E.S.; Song, J.; Kang, Y.Y.; Mok, H. Mannose-modified serum exosomes for the elevated uptake to murine dendritic cells and lym-phatic accumulation. Macromol. Biosci., 2019, 19(7), e1900042.
[http://dx.doi.org/10.1002/mabi.201900042] [PMID: 31141293]
[76]
Jiang, L.; Gu, Y.; Du, Y.; Tang, X.; Wu, X.; Liu, J. Engineering exosomes endowed with targeted delivery of triptolide for malignant mela-noma therapy. ACS Appl. Mater. Interfaces, 2021, 13(36), 42411-42428.
[http://dx.doi.org/10.1021/acsami.1c10325] [PMID: 34464081]
[77]
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]
[78]
Li, L.; He, D.; Guo, Q.; Zhang, Z.; Ru, D.; Wang, L.; Gong, K.; Liu, F.; Duan, Y.; Li, H. Exosome-liposome hybrid nanoparticle codelivery of TP and miR497 conspicuously overcomes chemoresistant ovarian cancer. J. Nanobiotechnology, 2022, 20(1), 50.
[http://dx.doi.org/10.1186/s12951-022-01264-5] [PMID: 35078498]
[79]
Salunkhe, S. Dheeraj; Basak, M.; Chitkara, D.; Mittal, A. Surface functionalization of exosomes for target-specific delivery and in vivo imaging & tracking: Strategies and significance. J. Control. Release, 2020, 326, 599-614.
[http://dx.doi.org/10.1016/j.jconrel.2020.07.042] [PMID: 32730952]
[80]
Kim, Y.; Mok, H. Citraconylated exosomes for improved internalization into macrophages. Appl. Biol. Chem., 2019, 62(1), 26.
[81]
Bunka, D.H.; Stockley, P.G. Aptamers come of age - at last. Nat. Rev. Microbiol., 2006, 4(8), 588-596.
[http://dx.doi.org/10.1038/nrmicro1458] [PMID: 16845429]
[82]
Zou, J.; Shi, M.; Liu, X.; Jin, C.; Xing, X.; Qiu, L.; Tan, W. Aptamer-functionalized exosomes: Elucidating the cellular uptake mechanism and the potential for cancer-targeted chemotherapy. Anal. Chem., 2019, 91(3), 2425-2430.
[http://dx.doi.org/10.1021/acs.analchem.8b05204] [PMID: 30620179]
[83]
Han, Q.; Xie, Q.R.; Li, F.; Cheng, Y.; Wu, T.; Zhang, Y.; Lu, X.; Wong, A.S.T.; Sha, J.; Xia, W. Targeted inhibition of SIRT6 via engi-neered exosomes impairs tumorigenesis and metastasis in prostate cancer. Theranostics, 2021, 11(13), 6526-6541.
[http://dx.doi.org/10.7150/thno.53886] [PMID: 33995674]
[84]
Zhang, H.; Wu, J.; Wu, J.; Fan, Q.; Zhou, J.; Wu, J.; Liu, S.; Zang, J.; Ye, J.; Xiao, M.; Tian, T.; Gao, J. Exosome-mediated targeted deliv-ery of miR-210 for angiogenic therapy after cerebral ischemia in mice. J. Nanobiotechnology, 2019, 17(1), 29.
[http://dx.doi.org/10.1186/s12951-019-0461-7] [PMID: 30782171]
[85]
Zou, Y.; Sun, Y.; Guo, B.; Wei, Y.; Xia, Y.; Huangfu, Z.; Meng, F.; van Hest, J.C.M.; Yuan, J.; Zhong, Z. α3β1 integrin-targeting poly-mersomal docetaxel as an advanced nanotherapeutic for nonsmall cell lung cancer treatment. ACS Appl. Mater. Interfaces, 2020, 12(13), 14905-14913.
[http://dx.doi.org/10.1021/acsami.0c01069] [PMID: 32148016]
[86]
Xu, H.; Liao, C.; Liang, S.; Ye, B.C. A novel peptide-equipped exosomes platform for delivery of antisense oligonucleotides. ACS Appl. Mater. Interfaces, 2021, 13(9), 10760-10767.
[http://dx.doi.org/10.1021/acsami.1c00016] [PMID: 33621039]
[87]
Cheng, H.; Fan, J.H.; Zhao, L.P.; Fan, G.L.; Zheng, R.R.; Qiu, X.Z.; Yu, X.Y.; Li, S.Y.; Zhang, X.Z. Chimeric peptide engineered exosomes for dual-stage light guided plasma membrane and nucleus targeted photodynamic therapy. Biomaterials, 2019, 211, 14-24.
[http://dx.doi.org/10.1016/j.biomaterials.2019.05.004] [PMID: 31078049]
[88]
Liu, Y.; Bai, L.; Guo, K.; Jia, Y.; Zhang, K.; Liu, Q.; Wang, P.; Wang, X. Focused ultrasound-augmented targeting delivery of nanosono-sensitizers from homogenous exosomes for enhanced sonodynamic cancer therapy. Theranostics, 2019, 9(18), 5261-5281.
[http://dx.doi.org/10.7150/thno.33183] [PMID: 31410214]
[89]
Wang, J.; Chen, P.; Dong, Y.; Xie, H.; Wang, Y.; Soto, F.; Ma, P.; Feng, X.; Du, W.; Liu, B.F. Designer exosomes enabling tumor targeted efficient chemo/gene/photothermal therapy. Biomaterials, 2021, 276, 121056.
[http://dx.doi.org/10.1016/j.biomaterials.2021.121056] [PMID: 34364178]
[90]
Royo, F.; Cossío, U.; Ruiz de Angulo, A.; Llop, J.; Falcon-Perez, J.M. Modification of the glycosylation of extracellular vesicles alters their biodistribution in mice. Nanoscale, 2019, 11(4), 1531-1537.
[http://dx.doi.org/10.1039/C8NR03900C] [PMID: 30623961]
[91]
Galley, J.D.; Besner, G.E. The therapeutic potential of breast milk-derived extracellular vesicles. Nutrients, 2020, 12(3), E745.
[http://dx.doi.org/10.3390/nu12030745] [PMID: 32168961]
[92]
Zempleni, J.; Sukreet, S.; Zhou, F.; Wu, D.; Mutai, E. Milk-derived exosomes and metabolic regulation. Annu. Rev. Anim. Biosci., 2019, 7(1), 245-262.
[http://dx.doi.org/10.1146/annurev-animal-020518-115300] [PMID: 30285461]
[93]
Lönnerdal, B. Human milk microRNAs/exosomes: Composition and biological effects. Nestle Nutr. Inst. Workshop Ser., 2019, 90, 83-92.
[http://dx.doi.org/10.1159/000490297] [PMID: 30865991]
[94]
Li, B.; Hock, A.; Wu, R.Y.; Minich, A.; Botts, S.R.; Lee, C.; Antounians, L.; Miyake, H.; Koike, Y.; Chen, Y.; Zani, A.; Sherman, P.M.; Pierro, A. Bovine milk-derived exosomes enhance goblet cell activity and prevent the development of experimental necrotizing enterocol-itis. PLoS One, 2019, 14(1), e0211431.
[http://dx.doi.org/10.1371/journal.pone.0211431] [PMID: 30699187]
[95]
Wang, L.; Shi, Z.; Wang, X.; Mu, S.; Xu, X.; Shen, L.; Li, P. Protective effects of bovine milk exosomes against oxidative stress in IEC-6 cells. Eur. J. Nutr., 2021, 60(1), 317-327.
[http://dx.doi.org/10.1007/s00394-020-02242-z] [PMID: 32328746]
[96]
Kahn, S.; Liao, Y.; Du, X.; Xu, W.; Li, J.; Lönnerdal, B. Exosomal microRNAs in milk from mothers delivering preterm infants survive in vitro digestion and are taken up by human intestinal cells. Mol. Nutr. Food Res., 2018, 62(11), e1701050.
[http://dx.doi.org/10.1002/mnfr.201701050] [PMID: 29644801]
[97]
Samuel, M.; Chisanga, D.; Liem, M.; Keerthikumar, S.; Anand, S.; Ang, C.S.; Adda, C.G.; Versteegen, E.; Jois, M.; Mathivanan, S. Bovine milk-derived exosomes from colostrum are enriched with proteins implicated in immune response and growth. Sci. Rep., 2017, 7(1), 5933.
[http://dx.doi.org/10.1038/s41598-017-06288-8] [PMID: 28725021]
[98]
Betker, J.L.; Angle, B.M.; Graner, M.W.; Anchordoquy, T.J. The potential of exosomes from cow milk for oral delivery. J. Pharm. Sci., 2019, 108(4), 1496-1505.
[http://dx.doi.org/10.1016/j.xphs.2018.11.022] [PMID: 30468828]
[99]
Aqil, F.; Munagala, R.; Jeyabalan, J.; Agrawal, A.K.; Kyakulaga, A.H.; Wilcher, S.A.; Gupta, R.C. Milk exosomes - Natural nanoparticles for siRNA delivery. Cancer Lett., 2019, 449, 186-195.
[http://dx.doi.org/10.1016/j.canlet.2019.02.011] [PMID: 30771430]
[100]
Li, S.; Tang, Y.; Dou, Y. The potential of milk-derived exosomes for drug delivery. Curr. Drug Deliv., 2021, 18(6), 688-699.
[http://dx.doi.org/10.2174/1567201817666200817112503] [PMID: 32807052]
[101]
Sedykh, S.; Kuleshova, A.; Nevinsky, G. Milk exosomes: Perspective agents for anticancer drug delivery. Int. J. Mol. Sci., 2020, 21(18), E6646.
[http://dx.doi.org/10.3390/ijms21186646] [PMID: 32932782]
[102]
Manca, S.; Upadhyaya, B.; Mutai, E.; Desaulniers, A.T.; Cederberg, R.A.; White, B.R.; Zempleni, J. Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Sci. Rep., 2018, 8(1), 11321.
[http://dx.doi.org/10.1038/s41598-018-29780-1] [PMID: 30054561]
[103]
Kugeratski, F.G.; Kalluri, R. Exosomes as mediators of immune regulation and immunotherapy in cancer. FEBS J., 2021, 288(1), 10-35.
[http://dx.doi.org/10.1111/febs.15558] [PMID: 32910536]
[104]
Raposo, G.; Nijman, H.W.; Stoorvogel, W.; Liejendekker, R.; Harding, C.V.; Melief, C.J.; Geuze, H.J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med., 1996, 183(3), 1161-1172.
[http://dx.doi.org/10.1084/jem.183.3.1161] [PMID: 8642258]
[105]
Théry, C.; Ostrowski, M.; Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol., 2009, 9(8), 581-593.
[http://dx.doi.org/10.1038/nri2567] [PMID: 19498381]
[106]
Denzer, K.; Kleijmeer, M.J.; Heijnen, H.F.; Stoorvogel, W.; Geuze, H.J. Exosome: From internal vesicle of the multivesicular body to in-tercellular signaling device. J. Cell Sci., 2000, 113(Pt 19), 3365-3374.
[http://dx.doi.org/10.1242/jcs.113.19.3365] [PMID: 10984428]
[107]
Chen, X.; Yang, T.; Wang, W.; Xi, W.; Zhang, T.; Li, Q.; Yang, A.; Wang, T. Circular RNAs in immune responses and immune diseases. Theranostics, 2019, 9(2), 588-607.
[http://dx.doi.org/10.7150/thno.29678] [PMID: 30809295]
[108]
Engin, A. Dark-side of exosomes. Adv. Exp. Med. Biol., 2021, 1275, 101-131.
[http://dx.doi.org/10.1007/978-3-030-49844-3_4] [PMID: 33539013]
[109]
Wang, J.; Teng, Y.; Zhao, G.; Li, F.; Hou, A.; Sun, B.; Kong, W.; Gao, F.; Cai, L.; Jiang, C. Exosome-mediated delivery of inducible miR-423-5p enhances resistance of MRC-5 cells to rabies virus infection. Int. J. Mol. Sci., 2019, 20(7), E1537.
[http://dx.doi.org/10.3390/ijms20071537] [PMID: 30934732]
[110]
Deng, L.; Jiang, W.; Wang, X.; Merz, A.; Hiet, M.S.; Chen, Y.; Pan, X.; Jiu, Y.; Yang, Y.; Yu, B.; He, Y.; Tu, Z.; Niu, J.; Bartenschlager, R.; Long, G. Syntenin regulates hepatitis C virus sensitivity to neutralizing antibody by promoting E2 secretion through exosomes. J. Hepatol., 2019, 71(1), 52-61.
[http://dx.doi.org/10.1016/j.jhep.2019.03.006] [PMID: 30880226]
[111]
Ramos-Zayas, Y.; Franco-Molina, M.A.; Hernádez-Granados, A.J.; Zárate-Triviño, D.G.; Coronado-Cerda, E.E.; Mendoza-Gamboa, E.; Zapata-Benavides, P.; Ramírez-Romero, R.; Santana-Krymskaya, S.E.; Tamez-Guerra, R.; Rodríguez-Padilla, C. Immunotherapy for the treatment of canine transmissible venereal tumor based in dendritic cells pulsed with tumoral exosomes. Immunopharmacol. Immunotoxicol., 2019, 41(1), 48-54.
[http://dx.doi.org/10.1080/08923973.2018.1533969] [PMID: 30334465]
[112]
Lu, Y.T.; Delijani, K.; Mecum, A.; Goldkorn, A. Current status of liquid biopsies for the detection and management of prostate cancer. Cancer Manag. Res., 2019, 11, 5271-5291.
[http://dx.doi.org/10.2147/CMAR.S170380] [PMID: 31239778]
[113]
Chen, C.; Zong, S.; Liu, Y.; Wang, Z.; Zhang, Y.; Chen, B.; Cui, Y. Profiling of exosomal biomarkers for accurate cancer identification: Combining DNA-PAINT with machine- learning-based classification. Small, 2019, 15(43), e1901014.
[http://dx.doi.org/10.1002/smll.201901014] [PMID: 31478613]
[114]
Mader, S.; Pantel, K. Liquid biopsy: Current status and future perspectives. Oncol. Res. Treat., 2017, 40(7-8), 404-408.
[http://dx.doi.org/10.1159/000478018] [PMID: 28693023]
[115]
Vaidyanathan, R.; Soon, R.H.; Zhang, P.; Jiang, K.; Lim, C.T. Cancer diagnosis: From tumor to liquid biopsy and beyond. Lab Chip, 2018, 19(1), 11-34.
[http://dx.doi.org/10.1039/C8LC00684A] [PMID: 30480287]
[116]
Wang, J.; Ni, J.; Beretov, J.; Thompson, J.; Graham, P.; Li, Y. Exosomal microRNAs as liquid biopsy biomarkers in prostate cancer. Crit. Rev. Oncol. Hematol., 2020, 145, 102860.
[http://dx.doi.org/10.1016/j.critrevonc.2019.102860] [PMID: 31874447]
[117]
Nonaka, T.; Wong, D.T.W. Liquid biopsy in head and neck cancer: Promises and challenges. J. Dent. Res., 2018, 97(6), 701-708.
[http://dx.doi.org/10.1177/0022034518762071] [PMID: 29513618]
[118]
Giannopoulou, L.; Zavridou, M.; Kasimir-Bauer, S.; Lianidou, E.S. Liquid biopsy in ovarian cancer: The potential of circulating miRNAs and exosomes. Transl. Res., 2019, 205, 77-91.
[http://dx.doi.org/10.1016/j.trsl.2018.10.003] [PMID: 30391474]
[119]
Geeurickx, E.; Hendrix, A. Targets, pitfalls and reference materials for liquid biopsy tests in cancer diagnostics. Mol. Aspects Med., 2020, 72, 100828.
[http://dx.doi.org/10.1016/j.mam.2019.10.005] [PMID: 31711714]
[120]
Di Meo, A.; Bartlett, J.; Cheng, Y.; Pasic, M.D.; Yousef, G.M. Liquid biopsy: A step forward towards precision medicine in urologic ma-lignancies. Mol. Cancer, 2017, 16(1), 80.
[http://dx.doi.org/10.1186/s12943-017-0644-5] [PMID: 28410618]
[121]
Wang, Y.; Liu, J.; Ma, J.; Sun, T.; Zhou, Q.; Wang, W.; Wang, G.; Wu, P.; Wang, H.; Jiang, L.; Yuan, W.; Sun, Z.; Ming, L. Exosomal circRNAs: Biogenesis, effect and application in human diseases. Mol. Cancer, 2019, 18(1), 116.
[http://dx.doi.org/10.1186/s12943-019-1041-z] [PMID: 31277663]
[122]
Wang, H.; Jiang, D.; Li, W.; Xiang, X.; Zhao, J.; Yu, B.; Wang, C.; He, Z.; Zhu, L.; Yang, Y. Evaluation of serum extracellular vesicles as noninvasive diagnostic markers of glioma. Theranostics, 2019, 9(18), 5347-5358.
[http://dx.doi.org/10.7150/thno.33114] [PMID: 31410219]
[123]
Grimolizzi, F.; Monaco, F.; Leoni, F.; Bracci, M.; Staffolani, S.; Bersaglieri, C.; Gaetani, S.; Valentino, M.; Amati, M.; Rubini, C.; Saccucci, F.; Neuzil, J.; Tomasetti, M.; Santarelli, L. Exosomal miR-126 as a circulating biomarker in non-small-cell lung cancer regulating cancer progression. Sci. Rep., 2017, 7(1), 15277.
[http://dx.doi.org/10.1038/s41598-017-15475-6] [PMID: 29127370]

Rights & Permissions Print Cite
Article Metrics
12
© 2024 Bentham Science Publishers | Privacy Policy