Engineering of Exosomes: Steps Towards Green Production of Drug Delivery System

Author(s): Abdelrahman Y. Sherif*, Gamaleldin I. Harisa, Fars K. Alanazi, Abdullah M.E. Youssof.

Journal Name: Current Drug Targets

Volume 20 , Issue 15 , 2019

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Graphical Abstract:


Abstract:

Targeting of therapeutic agents to their specific site of action not only increases the treatment efficacy, but also reduces systemic toxicity. Therefore, various drug delivery systems (DDSs) have been developed to achieve this target. However, most of those DDSs have several issues regarding biocompatibility and environmental hazard. In contrast to the synthetic DDSs, exosome-based natural carriers are biocompatible, biodegradable and safe for the environment. Since exosomes play a role in intercellular communication, they have been widely utilized as carriers for different therapeutic agents. This article was aimed to provide an overview of exosomes as an environment-friendly DDS in terms of engineering, isolation, characterization, application and limitation.

Keywords: Drug targeting, biological DDS, green DDS, exosome, bionanocarrier, vesicular carrier.

[1]
Jhaveri A, Torchilin V. Intracellular delivery of nanocarriers and targeting to subcellular organelles. Expert Opin Drug Deliv 2016; 13(1): 49-70.
[http://dx.doi.org/10.1517/17425247.2015.1086745] [PMID: 26358656]
[2]
Ma X, Gong N, Zhong L, Sun J, Liang X-J. Future of nanotherapeutics: Targeting the cellular sub-organelles. Biomaterials 2016; 97: 10-21.
[http://dx.doi.org/10.1016/j.biomaterials.2016.04.026] [PMID: 27155363]
[3]
Li T, Dong H, Zhang C, Mo R. Cell-based drug delivery systems for biomedical applications. Nano Res 2018; 1-18.
[http://dx.doi.org/10.1007/s12274-018-2179-5]
[4]
Wang Q, Cheng H, Peng H, Zhou H, Li PY, Langer R. Non-genetic engineering of cells for drug delivery and cell-based therapy. Adv Drug Deliv Rev 2015; 91: 125-40.
[http://dx.doi.org/10.1016/j.addr.2014.12.003] [PMID: 25543006]
[5]
Bazak R, Houri M, El Achy S, Kamel S, Refaat T. Cancer active targeting by nanoparticles: a comprehensive review of literature. J Cancer Res Clin Oncol 2015; 141(5): 769-84.
[http://dx.doi.org/10.1007/s00432-014-1767-3] [PMID: 25005786]
[6]
Smith RA, Porteous CM, Coulter CV, Murphy MP. Selective targeting of an antioxidant to mitochondria. Eur J Biochem 1999; 263(3): 709-16.
[http://dx.doi.org/10.1046/j.1432-1327.1999.00543.x] [PMID: 10469134]
[7]
Sakhrani NM, Padh H. Organelle targeting: third level of drug targeting. Drug Des Devel Ther 2013; 7: 585-99.
[PMID: 23898223]
[8]
Rizzitelli S, Giustetto P, Faletto D, Delli Aime S, Terreno E. The release of Doxorubicin from liposomes monitored by MRI and triggered by a combination of US stimuli led to a complete tumor regression in a breast cancer mouse model. J Control Release 2016; 230: 57-63.
[http://dx.doi.org/10.1016/j.jconrel.2016.03.040] [PMID: 27049069]
[9]
Chen Y, Zhang W, Huang Y, Gao F, Sha X, Fang X. Pluronic-based functional polymeric mixed micelles for co-delivery of doxorubicin and paclitaxel to multidrug resistant tumor. Int J Pharm 2015; 488(1-2): 44-58.
[http://dx.doi.org/10.1016/j.ijpharm.2015.04.048] [PMID: 25899286]
[10]
Patel SK, Gajbhiye V, Jain NK. Synthesis, characterization and brain targeting potential of paclitaxel loaded thiamine-PPI nanoconjugates. J Drug Target 2012; 20(10): 841-9.
[http://dx.doi.org/10.3109/1061186X.2012.719231] [PMID: 22994427]
[11]
Harisa GI, Badran MM, AlQahtani SA, Alanazi FK, Attia SM. Pravastatin chitosan nanogels-loaded erythrocytes as a new delivery strategy for targeting liver cancer. Saudi Pharm J 2016; 24(1): 74-81.
[http://dx.doi.org/10.1016/j.jsps.2015.03.024] [PMID: 26903771]
[12]
Kim S-K, Kim SU, Park IH, et al. Human neural stem cells target experimental intracranial medulloblastoma and deliver a therapeutic gene leading to tumor regression. Clin Cancer Res 2006; 12(18): 5550-6.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-2508] [PMID: 17000692]
[13]
Coosemans A, Vanderstraeten A, Tuyaerts S, et al. Wilms’ Tumor Gene 1 (WT1)--loaded dendritic cell immunotherapy in patients with uterine tumors: a phase I/II clinical trial. Anticancer Res 2013; 33(12): 5495-500.
[PMID: 24324087]
[14]
Youssof AME, Alanazi FK, Salem-Bekhit MM, Shakeel F, Haq N. Bacterial ghosts carrying 5-Fluorouracil: a novel biological carrier for targeting colorectal cancer. AAPS PharmSciTech 2019; 20(2): 48.
[http://dx.doi.org/10.1208/s12249-018-1249-z] [PMID: 30617674]
[15]
Paukner S, Kohl G, Lubitz W. Bacterial ghosts as novel advanced drug delivery systems: antiproliferative activity of loaded doxorubicin in human Caco-2 cells. J Control Release 2004; 94(1): 63-74.
[http://dx.doi.org/10.1016/j.jconrel.2003.09.010] [PMID: 14684272]
[16]
Della Peruta M, Badar A, Rosales C, et al. Preferential targeting of disseminated liver tumors using a recombinant adeno-associated viral vector. Hum Gene Ther 2015; 26(2): 94-103.
[http://dx.doi.org/10.1089/hum.2014.052] [PMID: 25569358]
[17]
Dowd E, Monville C, Torres EM, et al. Lentivector-mediated delivery of GDNF protects complex motor functions relevant to human Parkinsonism in a rat lesion model. Eur J Neurosci 2005; 22(10): 2587-95.
[http://dx.doi.org/10.1111/j.1460-9568.2005.04414.x] [PMID: 16307601]
[18]
AlQahtani SA, Harisa GI, Badran MM, et al. Nano-erythrocyte membrane-chaperoned 5-fluorouracil liposomes as biomimetic delivery platforms to target hepatocellular carcinoma cell lines. Artif Cells Nanomed Biotechnol 2019; 47(1): 989-96.
[http://dx.doi.org/10.1080/21691401.2019.1577887] [PMID: 30873877]
[19]
Luk BT, Fang RH, Hu C-MJ, et al. Safe and immunocompatible nanocarriers cloaked in RBC membranes for drug delivery to treat solid tumors. Theranostics 2016; 6(7): 1004-11.
[http://dx.doi.org/10.7150/thno.14471] [PMID: 27217833]
[20]
Ma J, Gallo JM. Delivery of cytotoxic drugs from carrier cells to tumour cells by apoptosis. Apoptosis 1998; 3(3): 195-202.
[http://dx.doi.org/10.1023/A:1009603023214] [PMID: 14646500]
[21]
Zhang N, Miao J, Sun P, et al. Pharmacokinetics, tissue distribution and anti-tumor effect of low density lipoprotein peptide conjugated submicron emulsions. Biomed Pharmacother 2016; 82: 614-9.
[http://dx.doi.org/10.1016/j.biopha.2016.05.047] [PMID: 27470404]
[22]
Qu M, Lin Q, Huang L, et al. Dopamine-loaded blood exosomes targeted to brain for better treatment of Parkinson’s disease. J Control Release 2018; 287: 156-66.
[http://dx.doi.org/10.1016/j.jconrel.2018.08.035] [PMID: 30165139]
[23]
Giuliano E, Paolino D, Fresta M, Cosco D. Mucosal applications of poloxamer 407-based hydrogels: An overview. Pharmaceutics 2018; 10(3): 159.
[http://dx.doi.org/10.3390/pharmaceutics10030159] [PMID: 30213143]
[24]
Di Meo C, Cilurzo F, Licciardi M, et al. Polyaspartamide-doxorubicin conjugate as potential prodrug for anticancer therapy. Pharm Res 2015; 32(5): 1557-69.
[http://dx.doi.org/10.1007/s11095-014-1557-2] [PMID: 25366547]
[25]
Telrandhe R. Nanotechnology for cancer therapy: Recent developments. Eur J Pharm Med Res 2016; 3(11): 284-94.
[26]
Park W, Na K. Advances in the synthesis and application of nanoparticles for drug delivery. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2015; 7(4): 494-508.
[http://dx.doi.org/10.1002/wnan.1325] [PMID: 25583540]
[27]
De Jong WH, Borm PJ. Drug delivery and nanoparticles:applications and hazards. Int J Nanomedicine 2008; 3(2): 133-49.
[http://dx.doi.org/10.2147/IJN.S596] [PMID: 18686775]
[28]
Kanwar R, Rathee J, Salunke DB, Mehta SK. Green nanotechnology-driven drug delivery assemblies. ACS Omega 2019; 4(5): 8804-15.
[http://dx.doi.org/10.1021/acsomega.9b00304]
[29]
Di Francesco M, Celia C, Primavera R, et al. Physicochemical characterization of pH-responsive and fusogenic self-assembled non-phospholipid vesicles for a potential multiple targeting therapy. Int J Pharm 2017; 528(1-2): 18-32.
[http://dx.doi.org/10.1016/j.ijpharm.2017.05.055] [PMID: 28559215]
[30]
Sun Y, Su J, Liu G, et al. Advances of blood cell-based drug delivery systems. Eur J Pharm Sci 2017; 96: 115-28.
[http://dx.doi.org/10.1016/j.ejps.2016.07.021] [PMID: 27496050]
[31]
Vader P, Mol EA, Pasterkamp G, Schiffelers RM. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 2016; 106(Pt A): 148-56.
[http://dx.doi.org/10.1016/j.addr.2016.02.006] [PMID: 26928656]
[32]
Aboody KS, Najbauer J, Danks MK. Stem and progenitor cell-mediated tumor selective gene therapy. Gene Ther 2008; 15(10): 739-52.
[http://dx.doi.org/10.1038/gt.2008.41] [PMID: 18369324]
[33]
Menon LG, Shi VJ, Carroll RS. Mesenchymal stromal cells as a drug delivery system Stem Book Cambridge. MA: Harvard Stem Cell Institute 2009.
[34]
Breckpot K, Escors D. Dendritic cells for active anti-cancer immunotherapy: targeting activation pathways through genetic modification endocrine metabolic & immune disorders-drug targets 2009; 9(4): 328-43.
[http://dx.doi.org/10.2174/187153009789839156]
[35]
Biagiotti S, Paoletti MF, Fraternale A, Rossi L, Magnani M. Drug delivery by red blood cells. IUBMB Life 2011; 63(8): 621-31.
[http://dx.doi.org/10.1002/iub.478] [PMID: 21766411]
[36]
Villa CH, Anselmo AC, Mitragotri S, Muzykantov V. Red blood cells: Supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems. Adv Drug Deliv Rev 2016; 106(Pt A): 88-103.
[http://dx.doi.org//10.1016/j.addr.2016.02.007] [PMID: 26941164]
[37]
Stephan MT, Stephan SB, Bak P, Chen J, Irvine DJ. Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles. Biomaterials 2012; 33(23): 5776-87.
[http://dx.doi.org/10.1016/j.biomaterials.2012.04.029] [PMID: 22594972]
[38]
Ullah S, Seidel K, Türkkan S, et al. Macrophage entrapped silica coated superparamagnetic iron oxide particles for controlled drug release in a 3D cancer model. J Control Release 2019; 294: 327-36.
[http://dx.doi.org/10.1016/j.jconrel.2018.12.040] [PMID: 30586597]
[39]
Fliervoet LAL, Mastrobattista E. Drug delivery with living cells. Adv Drug Deliv Rev 2016; 106(Pt A): 63.: 72.
[http://dx.doi.org/10.1016/j.addr.2016.04.021] [PMID: 27129442]
[40]
Kudela P, Koller VJ, Lubitz W. Bacterial ghosts (BGs)--advanced antigen and drug delivery system. Vaccine 2010; 28(36): 5760-7.
[http://dx.doi.org/10.1016/j.vaccine.2010.06.087] [PMID: 20619379]
[41]
Hosseinidoust Z, Mostaghaci B, Yasa O, Park B-W, Singh AV, Sitti M. Bioengineered and biohybrid bacteria-based systems for drug delivery. Adv Drug Deliv Rev 2016; 106(Pt A): 27-44.
[http://dx.doi.org/10.1016/j.addr.2016.09.007] [PMID: 27641944]
[42]
Duan D. Systemic delivery of adeno-associated viral vectors. Curr Opin Virol 2016; 21: 16-25.
[http://dx.doi.org/10.1016/j.coviro.2016.07.006] [PMID: 27459604]
[43]
Yang N. An overview of viral and nonviral delivery systems for microRNA. Int J Pharm Investig 2015; 5(4): 179-81.
[http://dx.doi.org/10.4103/2230-973X.167646] [PMID: 26682187]
[44]
Samanta S, Rajasingh S, Drosos N, Zhou Z, Dawn B, Rajasingh J. Exosomes: new molecular targets of diseases. Acta Pharmacol Sin 2018; 39(4): 501-13.
[http://dx.doi.org/10.1038/aps.2017.162] [PMID: 29219950]
[45]
Schatz D, Vardi A. Extracellular vesicles - new players in cell-cell communication in aquatic environments. Curr Opin Microbiol 2018; 43: 148-54.
[http://dx.doi.org/10.1016/j.mib.2018.01.014] [PMID: 29448174]
[46]
van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018; 19(4): 213-28.
[http://dx.doi.org/10.1038/nrm.2017.125] [PMID: 29339798]
[47]
Tkach M, Théry C. Communication by extracellular vesicles: where we are and where we need to go. Cell 2016; 164(6): 1226-32.
[http://dx.doi.org/10.1016/j.cell.2016.01.043] [PMID: 26967288]
[48]
Ha D, Yang N, Nadithe V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B 2016; 6(4): 287-96.
[http://dx.doi.org/10.1016/j.apsb.2016.02.001] [PMID: 27471669]
[49]
Kooijmans SA, Vader P, van Dommelen SM, van Solinge WW, Schiffelers RM. Exosome mimetics: a novel class of drug delivery systems. Int J Nanomedicine 2012; 7: 1525-41.
[PMID: 22619510]
[50]
Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 2015; 13(1): 17-24.
[http://dx.doi.org/10.1016/j.gpb.2015.02.001] [PMID: 25724326]
[51]
Villarroya-Beltri C, Baixauli F, Mittelbrunn M, et al. IS Gylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat Commun 2016; 7: 13588.
[http://dx.doi.org/10.1038/ncomms13588] [PMID: 27882925]
[52]
Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014; 29: 116-25.
[http://dx.doi.org/10.1016/j.ceb.2014.05.004] [PMID: 24959705]
[53]
Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 2018; 75(2): 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[54]
Kalluri R. The biology and function of exosomes in cancer. J Clin Invest 2016; 126(4): 1208-15.
[http://dx.doi.org/10.1172/JCI81135] [PMID: 27035812]
[55]
Shyong Y-J, Chang K-C, Lin F-H. Calcium phosphate particles stimulate exosome secretion from phagocytes for the enhancement of drug delivery. Colloids Surf B Biointerfaces 2018; 171: 391-7.
[http://dx.doi.org/10.1016/j.colsurfb.2018.07.037] [PMID: 30064087]
[56]
McKelvey KJ, Powell KL, Ashton AW, Morris JM, McCracken SA. Exosomes: Mechanisms of uptake. J Circ Biomark 2015; 4: 7.
[http://dx.doi.org/10.5772/61186] [PMID: 28936243]
[57]
He C, Zheng S, Luo Y, Wang B. Exosome theranostics: biology and translational medicine. Theranostics 2018; 8(1): 237-55.
[http://dx.doi.org/10.7150/thno.21945] [PMID: 29290805]
[58]
Agrawal AK, Aqil F, Jeyabalan J, et al. Milk-derived exosomes for oral delivery of paclitaxel. Nanomedicine (Lond) 2017; 13(5): 1627-36.
[http://dx.doi.org/10.1016/j.nano.2017.03.001] [PMID: 28300659]
[59]
Haney MJ, Klyachko NL, Zhao Y, et al. 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]
[60]
Yuan D, Zhao Y, Banks WA, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials 2017; 142: 1-12.
[http://dx.doi.org/10.1016/j.biomaterials.2017.07.011] [PMID: 28715655]
[61]
Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 2014; 35(7): 2383-90.
[http://dx.doi.org/10.1016/j.biomaterials.2013.11.083] [PMID: 24345736]
[62]
Greco KA, Franzen CA, Foreman KE, Flanigan RC, Kuo PC, Gupta GN. PLK-1 silencing in bladder cancer by siRNA delivered with exosomes Urology 2016; 91(241): e1-7.
[63]
Kim SM, Yang Y, Oh SJ, Hong Y, Seo M, Jang M. Cancer-derived exosomes as a delivery platform of CRISPR/Cas9 confer cancer cell tropism-dependent targeting. J Control Release 2017; 266: 8-16.
[http://dx.doi.org/10.1016/j.jconrel.2017.09.013] [PMID: 28916446]
[64]
Jang SC, Kim OY, Yoon CM, et al. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano 2013; 7(9): 7698-710.
[http://dx.doi.org/10.1021/nn402232g] [PMID: 24004438]
[65]
Yang Z, Xie J, Zhu J, et al. Functional exosome-mimic for delivery of siRNA to cancer: in vitro and in vivo evaluation. J Control Release 2016; 243: 160-71.
[http://dx.doi.org/10.1016/j.jconrel.2016.10.008] [PMID: 27742443]
[66]
Parimon T, Garrett NE III, Chen P, Antes TJ. Isolation of extracellular vesicles from murine bronchoalveolar lavage fluid using an ultrafiltration centrifugation Technique JoVE 2018; (141): e58310
[http://dx.doi.org/10.3791/58310]
[67]
Yakimchuk K. Exosomes: isolation and characterization methods and specific markers. Mater Methods 2015; 5: 1450-3.
[http://dx.doi.org/10.13070/mm.en.5.1450]
[68]
Nath Neerukonda S, Egan NA, Patria J, et al. Comparison of exosomes purified via ultracentrifugation (UC) and Total Exosome Isolation (TEI) reagent from the serum of Marek’s disease virus (MDV)-vaccinated and tumor-bearing chickens. J Virol Methods 2019; 263: 1-9.
[http://dx.doi.org/10.1016/j.jviromet.2018.10.004] [PMID: 30316797]
[69]
Abramowicz A, Widlak P, Pietrowska M. Proteomic analysis of exosomal cargo: the challenge of high purity vesicle isolation. Mol Biosyst 2016; 12(5): 1407-19.
[http://dx.doi.org/10.1039/C6MB00082G] [PMID: 27030573]
[70]
Sharma S, Scholz-Romero K, Rice GE, Salomon C. Methods to enrich exosomes from conditioned media and biological fluids Preeclampsia. Springer 2018; pp. 103-15.
[71]
Yang F, Liao X, Tian Y, Li G. Exosome separation using microfluidic systems: size-based, immunoaffinity-based and dynamic methodologies. Biotechnol J 2017; 12(4)1600699
[http://dx.doi.org/10.1002/biot.201600699] [PMID: 28166394]
[72]
An M, Wu J, Zhu J, Lubman DM. Comparison of an optimized ultracentrifugation method versus size-exclusion chromatography for isolation of exosomes from human serum. J Proteome Res 2018; 17(10): 3599-605.
[http://dx.doi.org/10.1021/acs.jproteome.8b00479] [PMID: 30192545]
[73]
Nordin JZ, Lee Y, Vader P, et al. Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine (Lond) 2015; 11(4): 879-83.
[http://dx.doi.org/10.1016/j.nano.2015.01.003] [PMID: 25659648]
[74]
Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods 2015; 87: 3-10.
[http://dx.doi.org/10.1016/j.ymeth.2015.02.019] [PMID: 25766927]
[75]
Contreras-Naranjo JC, Wu H-J, Ugaz VM. Microfluidics for exosome isolation and analysis: enabling liquid biopsy for personalized medicine. Lab Chip 2017; 17(21): 3558-77.
[http://dx.doi.org/10.1039/C7LC00592J] [PMID: 28832692]
[76]
Lobb RJ, Becker M, Wen SW, et al. 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]
[77]
Benedikter BJ, Bouwman FG, Vajen T, et al. Ultrafiltration combined with size exclusion chromatography efficiently isolates extracellular vesicles from cell culture media for compositional and functional studies. Sci Rep 2017; 7(1): 15297.
[http://dx.doi.org/10.1038/s41598-017-15717-7] [PMID: 29127410]
[78]
Haraszti RA, Miller R, Stoppato M, et al. Exosomes produced from 3D cultures of MSCs by tangential flow filtration show higher yield and improved activity. Mol Ther 2018; 26(12): 2838-47.
[http://dx.doi.org/10.1016/j.ymthe.2018.09.015] [PMID: 30341012]
[79]
Stranska R, Gysbrechts L, Wouters J, et al. Comparison of membrane affinity-based method with size-exclusion chromatography for isolation of exosome-like vesicles from human plasma. J Transl Med 2018; 16(1): 1.
[http://dx.doi.org/10.1186/s12967-017-1374-6] [PMID: 29316942]
[80]
Baranyai T, Herczeg K, Onódi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. PLoS One 2015; 10(12)e0145686
[http://dx.doi.org/10.1371/journal.pone.0145686] [PMID: 26690353]
[81]
Nordin JZ, Lee Y, Vader P, et al. Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine (Lond) 2015; 11(4): 879-83.
[http://dx.doi.org/10.1016/j.nano.2015.01.003] [PMID: 25659648]
[82]
Bunggulawa EJ, Wang W, Yin T, et al. Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnology 2018; 16(1): 81.
[http://dx.doi.org/10.1186/s12951-018-0403-9] [PMID: 30326899]
[83]
Helwa I, Cai J, Drewry MD, et al. A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One 2017; 12(1)e0170628
[http://dx.doi.org/10.1371/journal.pone.0170628] [PMID: 28114422]
[84]
Sáenz-Cuesta M, Arbelaiz A, Oregi A, et al. Methods for extracellular vesicles isolation in a hospital setting. Front Immunol 2015; 6: 50.
[http://dx.doi.org/10.3389/fimmu.2015.00050] [PMID: 25762995]
[85]
Deregibus MC, Figliolini F, D’Antico S, et al. Charge-based precipitation of extracellular vesicles. Int J Mol Med 2016; 38(5): 1359-66.
[http://dx.doi.org/10.3892/ijmm.2016.2759] [PMID: 28025988]
[86]
Gámez-Valero A, Monguió-Tortajada M, Carreras-Planella L. Franquesa Ml, Beyer K, Borràs FE. Size-Exclusion Chromatography-based isolation minimally alters Extracellular Vesicles’ characteristics compared to precipitating agents. Sci Rep 2016; 6: 33641.
[http://dx.doi.org/10.1038/srep33641] [PMID: 27640641]
[87]
Yoo YK, Lee J, Kim H, Hwang KS, Yoon DS, Lee JH. Toward exosome-based neuronal diagnostic devices. Micromachines (Basel) 2018; 9(12): 634.
[http://dx.doi.org/10.3390/mi9120634] [PMID: 30501125]
[88]
Tauro BJ, Greening DW, Mathias RA, et al. 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]
[89]
Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010; 18(9): 1606-14.
[http://dx.doi.org/10.1038/mt.2010.105] [PMID: 20571541]
[90]
Li Y, Gao Y, Gong C, et al. A33 antibody-functionalized exosomes for targeted delivery of doxorubicin against colorectal cancer. Nanomedicine (Lond) 2018; 14(7): 1973-85.
[http://dx.doi.org/10.1016/j.nano.2018.05.020] [PMID: 29935333]
[91]
Kim MS, Haney MJ, Zhao Y, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine (Lond) 2016; 12(3): 655-64.
[http://dx.doi.org/10.1016/j.nano.2015.10.012] [PMID: 26586551]
[92]
Pascucci L, Coccè V, Bonomi A, et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Control Release 2014; 192: 262-70.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.042] [PMID: 25084218]
[93]
Hood JL, Scott MJ, Wickline SA. Maximizing exosome colloidal stability following electroporation. Anal Biochem 2014; 448: 41-9.
[http://dx.doi.org/10.1016/j.ab.2013.12.001] [PMID: 24333249]
[94]
Aqil F, Munagala R, Jeyabalan J, et al. Milk exosomes - Natural nanoparticles for siRNA delivery. Cancer Lett 2019; 449: 186-95.
[http://dx.doi.org/10.1016/j.canlet.2019.02.011] [PMID: 30771430]
[95]
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29(4): 341-5.
[http://dx.doi.org/10.1038/nbt.1807] [PMID: 21423189]
[96]
Faruqu FN, Xu L, Al-Jamal KT. Preparation of exosomes for siRNA delivery to cancer cells JoVE 2018; (142): e58814
[http://dx.doi.org/10.3791/58814]
[97]
Ohno S, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 2013; 21(1): 185-91.
[http://dx.doi.org/10.1038/mt.2012.180] [PMID: 23032975]
[98]
Kyuno D, Zhao K, Bauer N, Ryschich E, Zöller M. Therapeutic targeting cancer-initiating cell markers by exosome miRNA: efficacy and functional consequences exemplified for claudin7 and EpCAM. Transl Oncol 2019; 12(2): 191-9.
[http://dx.doi.org/10.1016/j.tranon.2018.08.021] [PMID: 30393102]
[99]
Johnsen KB, Gudbergsson JM, Skov MN, Pilgaard L, Moos T, Duroux M. A comprehensive overview of exosomes as drug delivery vehicles - endogenous nanocarriers for targeted cancer therapy. Biochim Biophys Acta 2014; 1846(1): 75-87.
[PMID: 24747178]
[100]
Wahlgren J, Karlson TDL, Brisslert M, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 2012; 40(17)e130
[http://dx.doi.org/10.1093/nar/gks463]
[101]
Kooijmans SAA, Stremersch S, Braeckmans K, et al. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J Control Release 2013; 172(1): 229-38.
[http://dx.doi.org/10.1016/j.jconrel.2013.08.014] [PMID: 23994516]
[102]
Johnsen KB, Gudbergsson JM, Skov MN, et al. Evaluation of electroporation-induced adverse effects on adipose-derived stem cell exosomes. Cytotechnology 2016; 68(5): 2125-38.
[http://dx.doi.org/10.1007/s10616-016-9952-7] [PMID: 26856590]
[103]
Darband SG, Mirza-Aghazadeh-Attari M, Kaviani M, et al. Exosomes: natural nanoparticles as bio shuttles for RNAi delivery. J Control Release 2018; 289: 158-70.
[http://dx.doi.org/10.1016/j.jconrel.2018.10.001] [PMID: 30290245]
[104]
Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM. 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]
[105]
Podolak I, Galanty A, Sobolewska D. Saponins as cytotoxic agents: a review. Phytochem Rev 2010; 9(3): 425-74.
[http://dx.doi.org/10.1007/s11101-010-9183-z] [PMID: 20835386]
[106]
Ren J, He W, Zheng L, Duan H. From structures to functions: insights into exosomes as promising drug delivery vehicles. Biomater Sci 2016; 4(6): 910-21.
[http://dx.doi.org/10.1039/C5BM00583C] [PMID: 26977477]
[107]
Sarko DK, McKinney CE. Exosomes: origins and therapeutic potential for neurodegenerative disease. Front Neurosci 2017; 11: 82.
[http://dx.doi.org/10.3389/fnins.2017.00082] [PMID: 28289371]
[108]
Kojima R, Bojar D, Rizzi G, et al. Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment. Nat Commun 2018; 9(1): 1305.
[http://dx.doi.org/10.1038/s41467-018-03733-8] [PMID: 29610454]
[109]
Najlah M, Jain M, Wan K-W, et al. Ethanol-based proliposome delivery systems of paclitaxel for in vitro application against brain cancer cells. J Liposome Res 2018; 28(1): 74-85.
[http://dx.doi.org/10.1080/08982104.2016.1259628] [PMID: 27834116]
[110]
Hadla M, Palazzolo S, Corona G, et al. Exosomes increase the therapeutic index of doxorubicin in breast and ovarian cancer mouse models. Nanomedicine (Lond) 2016; 11(18): 2431-41.
[http://dx.doi.org/10.2217/nnm-2016-0154] [PMID: 27558906]
[111]
Toffoli G, Hadla M, Corona G, et al. Exosomal doxorubicin reduces the cardiac toxicity of doxorubicin. Nanomedicine (Lond) 2015; 10(19): 2963-71.
[http://dx.doi.org/10.2217/nnm.15.118] [PMID: 26420143]
[112]
Luan X, Sansanaphongpricha K, Myers I, Chen H, Yuan H, Sun D. Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol Sin 2017; 38(6): 754-63.
[http://dx.doi.org/10.1038/aps.2017.12] [PMID: 28392567]
[113]
Aqil F, Munagala R, Jeyabalan J, et al. Milk exosomes - Natural nanoparticles for siRNA delivery. Cancer Lett 2019; 449: 186-95.
[http://dx.doi.org/10.1016/j.canlet.2019.02.011] [PMID: 30771430]
[114]
Ding Y, Cao F, Sun H, et al. Exosomes derived from human umbilical cord mesenchymal stromal cells deliver exogenous miR-145-5p to inhibit pancreatic ductal adenocarcinoma progression. Cancer Lett 2019; 442: 351-61.
[http://dx.doi.org/10.1016/j.canlet.2018.10.039] [PMID: 30419348]
[115]
Chen X, Zhou J, Li X, Wang X, Lin Y, Wang X. Exosomes derived from hypoxic epithelial ovarian cancer cells deliver microRNAs to macrophages and elicit a tumor-promoted phenotype. Cancer Lett 2018; 435: 80-91.
[http://dx.doi.org/10.1016/j.canlet.2018.08.001] [PMID: 30098399]
[116]
Li P, Kaslan M, Lee SH, 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]
[117]
Escudier B, Dorval T, Chaput N, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 2005; 3(1): 10.
[http://dx.doi.org/10.1186/1479-5876-3-10] [PMID: 15740633]
[118]
Morse MA, Garst J, Osada T, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 2005; 3(1): 9.
[http://dx.doi.org/10.1186/1479-5876-3-9] [PMID: 15723705]
[119]
Dai S, Wei D, Wu Z, et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther 2008; 16(4): 782-90.
[http://dx.doi.org/10.1038/mt.2008.1] [PMID: 18362931]


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VOLUME: 20
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Year: 2019
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DOI: 10.2174/1389450120666190715104100
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