Engineering Extracellular Vesicles for Cancer Therapy.
Cancer therapy
Cargo loading
Clinical trials
Disease
Drug delivery
Exosome therapy
Extracellular vesicles
Extracellular vesicles sources
Pathology
Journal
Sub-cellular biochemistry
ISSN: 0306-0225
Titre abrégé: Subcell Biochem
Pays: United States
ID NLM: 0316571
Informations de publication
Date de publication:
2021
2021
Historique:
entrez:
29
3
2021
pubmed:
30
3
2021
medline:
28
4
2021
Statut:
ppublish
Résumé
Extracellular vesicles (EVs) are lipid bilayer containing nanovesicles that have a predominant role in intercellular communication and cargo delivery. EVs have recently been used as a means for drug delivery and have been depicted to elicit no or minimal immune response in vivo. The stability, biocompatibility and manipulatable tumour homing capabilities of these biological vessels make them an attractive target for the packaging and delivery of drugs and molecules to treat various diseases including cancer. The following chapter will summarise current EV engineering techniques for the purpose of delivering putative drugs and therapeutic molecules for the treatment of cancer. The relevance of EV source will be discussed, as well as the specific modifications required to manufacture them into suitable vehicles for molecular drug delivery. Furthermore, methods of EV cargo encapsulation will be evaluated with emphasis on intercellular coordination to allow for the effective emptying of therapeutic contents into target cells. While EVs possess properties making them naturally suitable nanocarriers for drugs and molecules, many challenges with clinical translation of EV-based platforms remain. These issues need to be addressed in order to harness the true potential of the EV-based therapeutic avenue.
Identifiants
pubmed: 33779924
doi: 10.1007/978-3-030-67171-6_14
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
375-392Références
Agrawal AK, Aqil F, Jeyabalan J, Spencer WA, Beck J, Gachuki BW, Alhakeem SS, Oben K, Munagala R, Bondada S, Gupta RC (2017) Milk-derived exosomes for oral delivery of paclitaxel. Nanomedicine 13(5):1627–1636
pubmed: 28300659
doi: 10.1016/j.nano.2017.03.001
Anand S, Samuel M, Kumar S, Mathivanan S (2019) Ticket to a bubble ride: cargo sorting into exosomes and extracellular vesicles. Biochim Biophys Acta Proteins Proteom. https://doi.org/10.1016/j.bbapap.2019.02.005
Andrews WD (2000 [cited 2016 Oct 20]) Pilot immunotherapy trial for recurrent malignant gliomas. Thomas Jefferson University. National Library of Medicine (US), Bethesda, MD
Aqil F, Jeyabalan J, Agrawal AK, Kyakulaga AH, Munagala R, Parker L, Gupta RC (2017a) Exosomal delivery of berry anthocyanidins for the management of ovarian cancer. Food Funct 8(11):4100–4107
pubmed: 28991298
doi: 10.1039/C7FO00882A
Aqil F, Munagala R, Jeyabalan J, Agrawal AK, Gupta R (2017b) Exosomes for the enhanced tissue bioavailability and efficacy of curcumin. AAPS J 19(6):1691–1702
pubmed: 29047044
doi: 10.1208/s12248-017-0154-9
Arms L, Smith DW, Flynn J, Palmer W, Martin A, Woldu A, Hua S (2018) Advantages and limitations of current techniques for analyzing the biodistribution of nanoparticles. Front Pharmacol 9:802
pubmed: 30154715
pmcid: 6102329
doi: 10.3389/fphar.2018.00802
Aspe JR, Diaz Osterman CJ, Jutzy JM, Deshields S, Whang S, Wall NR (2014) Enhancement of gemcitabine sensitivity in pancreatic adenocarcinoma by novel exosome-mediated delivery of the Survivin-T34A mutant. J Extracell Vesicles 3
Batrakova EV, Kim MS (2015) Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Control Release 219:396–405
pubmed: 26241750
pmcid: 4656109
doi: 10.1016/j.jconrel.2015.07.030
Baxter AA, Phan TK, Hanssen E, Liem M, Hulett MD, Mathivanan S, Poon IKH (2019) Analysis of extracellular vesicles generated from monocytes under conditions of lytic cell death. Sci Rep 9(1):7538
pubmed: 31101910
pmcid: 6525174
doi: 10.1038/s41598-019-44021-9
Benameur T, Chappard D, Fioleau E, Andriantsitohaina R, Martinez MC, Clere N, Marchand-Libouban H (2013) Plasma cells release membrane microparticles in a mouse model of multiple myeloma. Micron 54–55:75–81
pubmed: 24055121
doi: 10.1016/j.micron.2013.08.010
Besse B, Charrier M, Lapierre V, Dansin E, Lantz O, Planchard D, Le Chevalier T, Livartoski A, Barlesi F, Laplanche A, Ploix S, Vimond N, Peguillet I, Thery C, Lacroix L, Zoernig I, Dhodapkar K, Dhodapkar M, Viaud S, Soria JC, Reiners KS, Pogge von Strandmann E, Vely F, Rusakiewicz S, Eggermont A, Pitt JM, Zitvogel L, Chaput N (2016) Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC. Onco Targets Ther 5(4):e1071008
Bushweller JH (2019) Targeting transcription factors in cancer - from undruggable to reality. Nat Rev Cancer 19(11):611–624
pubmed: 31511663
doi: 10.1038/s41568-019-0196-7
Cha JM, Shin EK, Sung JH, Moon GJ, Kim EH, Cho YH, Park HD, Bae H, Kim J, Bang OY (2018) Efficient scalable production of therapeutic microvesicles derived from human mesenchymal stem cells. Sci Rep 8(1):1171
pubmed: 29352188
pmcid: 5775399
doi: 10.1038/s41598-018-19211-6
Chaput N, Schartz NE, Andre F, Taieb J, Novault S, Bonnaventure P, Aubert N, Bernard J, Lemonnier F, Merad M, Adema G, Adams M, Ferrantini M, Carpentier AF, Escudier B, Tursz T, Angevin E, Zitvogel L (2004) Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J Immunol 172(4):2137–2146
pubmed: 14764679
doi: 10.4049/jimmunol.172.4.2137
Chen Z, Meng H, Xing G, Chen C, Zhao Y, Jia G, Wang T, Yuan H, Ye C, Zhao F, Chai Z, Zhu C, Fang X, Ma B, Wan L (2006) Acute toxicological effects of copper nanoparticles in vivo. Toxicol Lett 163(2):109–120
pubmed: 16289865
doi: 10.1016/j.toxlet.2005.10.003
Cho JA, Yeo DJ, Son HY, Kim HW, Jung DS, Ko JK, Koh JS, Kim YN, Kim CW (2005) Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int J Cancer 114(4):613–622
pubmed: 15609328
doi: 10.1002/ijc.20757
Costa AP, Xu X, Burgess DJ (2014) Freeze-anneal-thaw cycling of unilamellar liposomes: effect on encapsulation efficiency. Pharm Res 31(1):97–103
pubmed: 23881305
doi: 10.1007/s11095-013-1135-z
Cully M (2018) Targeted therapy: tipping the splicing balance to kill cancer cells. Nat Rev Cancer 18(4):209
pubmed: 29563598
doi: 10.1038/nrc.2018.27
Daassi D, Mahoney KM, Freeman GJ (2020) The importance of exosomal PDL1 in tumour immune evasion. Nat Rev Immunol 20(4):209–215
pubmed: 31965064
doi: 10.1038/s41577-019-0264-y
Dai S, Wei D, Wu Z, Zhou X, Wei X, Huang H, Li G (2008) Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther 16(4):782–790
pubmed: 18362931
pmcid: 7106337
doi: 10.1038/mt.2008.1
De Jong WH, Borm PJ (2008) Drug delivery and nanoparticles:applications and hazards. Int J Nanomedicine 3(2):133–149
pubmed: 18686775
pmcid: 2527668
doi: 10.2147/IJN.S596
Escudier B, Dorval T, Chaput N, Andre F, Caby MP, Novault S, Flament C, Leboulaire C, Borg C, Amigorena S, Boccaccio C, Bonnerot C, Dhellin O, Movassagh M, Piperno S, Robert C, Serra V, Valente N, Le Pecq JB, Spatz A, Lantz O, Tursz T, Angevin E, Zitvogel L (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 3(1):10
pubmed: 15740633
pmcid: 554765
doi: 10.1186/1479-5876-3-10
Fonseka P, Liem M, Ozcitti C, Adda CG, Ang CS, Mathivanan S (2019) Exosomes from N-Myc amplified neuroblastoma cells induce migration and confer chemoresistance to non-N-Myc amplified cells: implications of intra-tumour heterogeneity. J Extracell Vesicles 8(1):1597614
pubmed: 31007876
pmcid: 6461098
doi: 10.1080/20013078.2019.1597614
Frydrychowicz M, Kolecka-Bednarczyk A, Madejczyk M, Yasar S, Dworacki G (2015) Exosomes - structure, biogenesis and biological role in non-small-cell lung cancer. Scand J Immunol 81(1):2–10
pubmed: 25359529
doi: 10.1111/sji.12247
Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM (2015) Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J Control Release 205:35–44
pubmed: 25483424
doi: 10.1016/j.jconrel.2014.11.029
Gheinani AH, Vogeli M, Baumgartner U, Vassella E, Draeger A, Burkhard FC, Monastyrskaya K (2018) Improved isolation strategies to increase the yield and purity of human urinary exosomes for biomarker discovery. Sci Rep 8(1):3945
pubmed: 29500443
pmcid: 5834546
doi: 10.1038/s41598-018-22142-x
Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, Yates JR (2009) Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res 8(3):1304–1314
pubmed: 19199708
pmcid: 2693447
doi: 10.1021/pr800658c
Haney MJ, Klyachko NL, Zhaoa YL, Gupta R, Plotnikova EG, He ZJ, Patel T, Piroyan A, Sokolsky M, Kabanov AV, Batrakova EV (2015) Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Control Release 207:18–30
pubmed: 25836593
pmcid: 4430381
doi: 10.1016/j.jconrel.2015.03.033
Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW (2015) Exosomes released from breast cancer carcinomas stimulate cell movement. PLoS One 10(3):e0117495
pubmed: 25798887
pmcid: 4370373
doi: 10.1371/journal.pone.0117495
Kalra H, Drummen GP, Mathivanan S (2016) Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci 17(2):170
pubmed: 26861301
pmcid: 4783904
doi: 10.3390/ijms17020170
Kalra H, Gangoda L, Fonseka P, Chitti SV, Liem M, Keerthikumar S, Samuel M, Boukouris S, Al Saffar H, Collins C, Adda CG, Ang CS, Mathivanan S (2019) Extracellular vesicles containing oncogenic mutant beta-catenin activate Wnt signalling pathway in the recipient cells. J Extracell Vesicles 8(1):1690217
pubmed: 31819794
pmcid: 6883417
doi: 10.1080/20013078.2019.1690217
Kamerkar S, LeBleu VS, Sugimoto H, Yang S, Ruivo CF, Melo SA, Lee JJ, Kalluri R (2017) Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 546(7659):498–503
pubmed: 28607485
pmcid: 5538883
doi: 10.1038/nature22341
Katakowski M, Buller B, Zheng X, Lu Y, Rogers T, Osobamiro O, Shu W, Jiang F, Chopp M (2013) Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett 335(1):201–204
pubmed: 23419525
pmcid: 3665755
doi: 10.1016/j.canlet.2013.02.019
Kikuchi T, Akasaki Y, Irie M, Homma S, Abe T, Ohno T (2001) Results of a phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol Immunother 50(7):337–344
pubmed: 11676393
doi: 10.1007/s002620100205
Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, Klyachko NL, Inskoe E, Piroyan A, Sokolsky M, Okolie O, Hingtgen SD, Kabanov AV, Batrakova EV (2016) Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine 12(3):655–664
pubmed: 26586551
doi: 10.1016/j.nano.2015.10.012
Koh E, Lee EJ, Nam GH, Hong Y, Cho E, Yang Y, Kim IS (2017) Exosome-SIRPalpha, a CD47 blockade increases cancer cell phagocytosis. Biomaterials 121:121–129
pubmed: 28086180
doi: 10.1016/j.biomaterials.2017.01.004
Kolhe R, Hunter M, Liu S, Jadeja RN, Pundkar C, Mondal AK, Mendhe B, Drewry M, Rojiani MV, Liu Y, Isales CM, Guldberg RE, Hamrick MW, Fulzele S (2017) Gender-specific differential expression of exosomal miRNA in synovial fluid of patients with osteoarthritis. Sci Rep 7(1):2029
pubmed: 28515465
pmcid: 5435729
doi: 10.1038/s41598-017-01905-y
Kooijmans SA, Aleza CG, Roffler SR, van Solinge WW, Vader P, Schiffelers RM (2016) Display of GPI-anchored anti-EGFR nanobodies on extracellular vesicles promotes tumour cell targeting. J Extracell Vesicles 5:31053
pubmed: 26979463
doi: 10.3402/jev.v5.31053
Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M, Thery C (2016) Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA 113(8):E968–E977
pubmed: 26858453
doi: 10.1073/pnas.1521230113
pmcid: 26858453
Lee HY, Chen CK, Ho CM, Lee SS, Chang CY, Chen KJ, Jou YS (2018) EIF3C-enhanced exosome secretion promotes angiogenesis and tumorigenesis of human hepatocellular carcinoma. Oncotarget 9(17):13193–13205
pubmed: 29568350
pmcid: 5862571
doi: 10.18632/oncotarget.24149
Liang G, Zhu Y, Ali DJ, Tian T, Xu H, Si K, Sun B, Chen B, Xiao Z (2020) Engineered exosomes for targeted co-delivery of miR-21 inhibitor and chemotherapeutics to reverse drug resistance in colon cancer. J Nanobiotechnology 18(1):10
pubmed: 31918721
pmcid: 6950820
doi: 10.1186/s12951-019-0563-2
Liu L, Chang S, Sun J, Zhu S, Yin M, Zhu Y, Wang Z, Xu RX (2015) Ultrasound-mediated destruction of paclitaxel and oxygen loaded lipid microbubbles for combination therapy in ovarian cancer xenografts. Cancer Lett 361(1):147–154
pubmed: 25754815
doi: 10.1016/j.canlet.2015.02.052
Lopez-Leal R, Diaz-Viraque F, Catalan RJ, Saquel C, Enright A, Iraola G, Court FA (2020) Schwann cell reprogramming into repair cells increases miRNA-21 expression in exosomes promoting axonal growth. J Cell Sci 133(12):jcs239004
pubmed: 32409566
doi: 10.1242/jcs.239004
Loureiro JA, Ramalho MJ, Pereira MD (2020) Immuno-nanocarriers for brain delivery: limitations from in vitro to preclinical and clinical studies. Nanomedicine 15(6):543–545
pubmed: 32056491
doi: 10.2217/nnm-2019-0402
Luan X, Sansanaphongpricha K, Myers I, Chen HW, Yuan HB, Sun DX (2017) Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol Sin 38(6):754–763
pubmed: 28392567
pmcid: 5520184
doi: 10.1038/aps.2017.12
Lunavat TR, Jang SC, Nilsson L, Park HT, Repiska G, Lasser C, Nilsson JA, Gho YS, Lotvall J (2016) RNAi delivery by exosome-mimetic nanovesicles - implications for targeting c-Myc in cancer. Biomaterials 102:231–238
pubmed: 27344366
doi: 10.1016/j.biomaterials.2016.06.024
Maroto R, Zhao Y, Jamaluddin M, Popov VL, Wang H, Kalubowilage M, Zhang Y, Luisi J, Sun H, Culbertson CT, Bossmann SH, Motamedi M, Brasier AR (2017) Effects of storage temperature on airway exosome integrity for diagnostic and functional analyses. J Extracell Vesicles 6(1):1359478
pubmed: 28819550
pmcid: 5556670
doi: 10.1080/20013078.2017.1359478
Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ (2010) Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 9(2):197–208
pubmed: 19837982
doi: 10.1074/mcp.M900152-MCP200
Mirza AH, Kaur S, Nielsen LB, Storling J, Yarani R, Roursgaard M, Mathiesen ER, Damm P, Svare J, Mortensen HB, Pociot F (2019) Breast milk-derived extracellular vesicles enriched in exosomes from mothers with type 1 diabetes contain aberrant levels of microRNAs. Front Immunol 10:2543
pubmed: 31708933
pmcid: 6823203
doi: 10.3389/fimmu.2019.02543
Momen-Heravi F, Bala S, Bukong T, Szabo G (2014) Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomed Nanotechnol Biol Med 10(7):1517–1527
doi: 10.1016/j.nano.2014.03.014
Morse MA, Garst J, Osada T, Khan S, Hobeika A, Clay TM, Valente N, Shreeniwas R, Sutton MA, Delcayre A, Hsu DH, Le Pecq JB, Lyerly HK (2005) A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3(1):9
pubmed: 15723705
pmcid: 551593
doi: 10.1186/1479-5876-3-9
Muller L, Hong CS, Stolz DB, Watkins SC, Whiteside TL (2014) Isolation of biologically-active exosomes from human plasma. J Immunol Methods 411:55–65
pubmed: 24952243
pmcid: 4260336
doi: 10.1016/j.jim.2014.06.007
Munagala R, Aqil F, Jeyabalan J, Gupta RC (2016) Bovine milk-derived exosomes for drug delivery. Cancer Lett 371(1):48–61
pubmed: 26604130
doi: 10.1016/j.canlet.2015.10.020
Nordin JZ, Lee Y, Vader P, Mager I, Johansson HJ, Heusermann W, Wiklander OP, Hallbrink M, Seow Y, Bultema JJ, Gilthorpe J, Davies T, Fairchild PJ, Gabrielsson S, Meisner-Kober NC, Lehtio J, Smith CI, Wood MJ, El Andaloussi S (2015) Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine 11(4):879–883
pubmed: 25659648
doi: 10.1016/j.nano.2015.01.003
Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T, Gotoh N, Kuroda M (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21(1):185–191
pubmed: 23032975
doi: 10.1038/mt.2012.180
Paolicelli RC, Bergamini G, Rajendran L (2019) Cell-to-cell communication by extracellular vesicles: focus on microglia. Neuroscience 405:148–157
pubmed: 29660443
doi: 10.1016/j.neuroscience.2018.04.003
Pathan M, Fonseka P, Chitti SV, Kang T, Sanwlani R, Van Deun J, Hendrix A, Mathivanan S (2019) Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Res 47(D1):D516–D519
pubmed: 30395310
doi: 10.1093/nar/gky1029
Pomatto MAC, Bussolati B, D'Antico S, Ghiotto S, Tetta C, Brizzi MF, Camussi G (2019) Improved loading of plasma-derived extracellular vesicles to encapsulate antitumor miRNAs. Mol Ther Methods Clin Dev 13:133–144
pubmed: 30788382
pmcid: 6370572
doi: 10.1016/j.omtm.2019.01.001
Qi H, Liu C, Long L, Ren Y, Zhang S, Chang X, Qian X, Jia H, Zhao J, Sun J, Hou X, Yuan X, Kang C (2016) Blood exosomes endowed with magnetic and targeting properties for cancer therapy. ACS Nano 10(3):3323–3333
pubmed: 26938862
doi: 10.1021/acsnano.5b06939
Rana S, Yue S, Stadel D, Zoller M (2012) Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol 44(9):1574–1584
pubmed: 22728313
doi: 10.1016/j.biocel.2012.06.018
Ren R, Sun H, Ma C, Liu J, Wang H (2019) Colon cancer cells secrete exosomes to promote self-proliferation by shortening mitosis duration and activation of STAT3 in a hypoxic environment. Cell Biosci 9:62
pubmed: 31402975
pmcid: 6683569
doi: 10.1186/s13578-019-0325-8
Rivoltini L, Chiodoni C, Squarcina P, Tortoreto M, Villa A, Vergani B, Burdek M, Botti L, Arioli I, Cova A, Mauri G, Vergani E, Bianchi B, Della Mina P, Cantone L, Bollati V, Zaffaroni N, Gianni AM, Colombo MP, Huber V (2016) TNF-related apoptosis-inducing ligand (TRAIL)-armed exosomes deliver proapoptotic signals to tumor site. Clin Cancer Res 22(14):3499–3512
pubmed: 26944067
doi: 10.1158/1078-0432.CCR-15-2170
Romagnoli GG, Zelante BB, Toniolo PA, Migliori IK, Barbuto JA (2014) Dendritic cell-derived Exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front Immunol 5:692
pubmed: 25646096
Sanwlani R, Fonseka P, Chitti SV, Mathivanan S (2020) Milk-derived extracellular vesicles in inter-organism, cross-species communication and drug delivery. Proteomes 8(2):11
pubmed: 32414045
pmcid: 7356197
doi: 10.3390/proteomes8020011
Sato YT, Umezaki K, Sawada S, Mukai SA, Sasaki Y, Harada N, Shiku H, Akiyoshi K (2016) Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep 6:21933
pubmed: 26911358
pmcid: 4766490
doi: 10.1038/srep21933
Schroeder A, Heller DA, Winslow MM, Dahlman JE, Pratt GW, Langer R, Jacks T, Anderson DG (2011) Treating metastatic cancer with nanotechnology. Nat Rev Cancer 12(1):39–50
pubmed: 22193407
doi: 10.1038/nrc3180
Shimbo K, Miyaki S, Ishitobi H, Kato Y, Kubo T, Shimose S, Ochi M (2014) Exosome-formed synthetic microRNA-143 is transferred to osteosarcoma cells and inhibits their migration. Biochem Biophys Res Commun 445(2):381–387
pubmed: 24525123
doi: 10.1016/j.bbrc.2014.02.007
Soltani F, Parhiz H, Mokhtarzadeh A, Ramezani M (2015) Synthetic and biological vesicular nano-carriers designed for gene delivery. Curr Pharm Des 21(42):6214–6235
pubmed: 26503143
doi: 10.2174/1381612821666151027153410
Stickney Z, Losacco J, McDevitt S, Zhang Z, Lu B (2016) Development of exosome surface display technology in living human cells. Biochem Biophys Res Commun 472(1):53–59
pubmed: 26902116
doi: 10.1016/j.bbrc.2016.02.058
Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, Barnes S, Grizzle W, Miller D, Zhang HG (2010) A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 18(9):1606–1614
pubmed: 20571541
pmcid: 2956928
doi: 10.1038/mt.2010.105
Tang K, Zhang Y, Zhang H, Xu P, Liu J, Ma J, Lv M, Li D, Katirai F, Shen GX, Zhang G, Feng ZH, Ye D, Huang B (2012) Delivery of chemotherapeutic drugs in tumour cell-derived microparticles. Nat Commun 3:1282
pubmed: 23250412
doi: 10.1038/ncomms2282
Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ (2012) Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 56(2):293–304
pubmed: 22285593
doi: 10.1016/j.ymeth.2012.01.002
Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166(12):7309–7318
pubmed: 11390481
doi: 10.4049/jimmunol.166.12.7309
Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 3:22
pubmed: 18228490
Tian Y, Li S, Song J, Ji T, Zhu M, Anderson GJ, Wei J, Nie G (2014) A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 35(7):2383–2390
pubmed: 24345736
doi: 10.1016/j.biomaterials.2013.11.083
Tomihari M, Chung JS, Akiyoshi H, Cruz PD Jr, Ariizumi K (2010) DC-HIL/glycoprotein Nmb promotes growth of melanoma in mice by inhibiting the activation of tumor-reactive T cells. Cancer Res 70(14):5778–5787
pubmed: 20570888
pmcid: 2905472
doi: 10.1158/0008-5472.CAN-09-2538
Vader P, Mol EA, Pasterkamp G, Schiffelers RM (2016) Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 106(Pt A):148–156
pubmed: 26928656
doi: 10.1016/j.addr.2016.02.006
Wahlgren J, Karlson TD, Brisslert M, Sani FV, Telemo E, Sunnerhagen P, Valadi H (2012) Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 40(17):e130
pubmed: 22618874
pmcid: 3458529
doi: 10.1093/nar/gks463
Wahlund CJE, Gucluler G, Hiltbrunner S, Veerman RE, Naslund TI, Gabrielsson S (2017) Exosomes from antigen-pulsed dendritic cells induce stronger antigen-specific immune responses than microvesicles in vivo. Sci Rep 7(1):17095
pubmed: 29213052
pmcid: 5719080
doi: 10.1038/s41598-017-16609-6
Wang L, Xie Y, Ahmed KA, Ahmed S, Sami A, Chibbar R, Xu Q, Kane SE, Hao S, Mulligan SJ, Xiang J (2013) Exosomal pMHC-I complex targets T cell-based vaccine to directly stimulate CTL responses leading to antitumor immunity in transgenic FVBneuN and HLA-A2/HER2 mice and eradicating trastuzumab-resistant tumor in athymic nude mice. Breast Cancer Res Treat 140(2):273–284
pubmed: 23881522
doi: 10.1007/s10549-013-2626-7
Wang Q, Ren Y, Mu J, Egilmez NK, Zhuang X, Deng Z, Zhang L, Yan J, Miller D, Zhang HG (2015) Grapefruit-derived nanovectors use an activated leukocyte trafficking pathway to deliver therapeutic agents to inflammatory tumor sites. Cancer Res 75(12):2520–2529
pubmed: 25883092
pmcid: 4470740
doi: 10.1158/0008-5472.CAN-14-3095
Wang F, Li L, Piontek K, Sakaguchi M, Selaru FM (2018) Exosome miR-335 as a novel therapeutic strategy in hepatocellular carcinoma. Hepatology 67(3):940–954
pubmed: 29023935
pmcid: 5826829
doi: 10.1002/hep.29586
Watson DC, Bayik D, Srivatsan A, Bergamaschi C, Valentin A, Niu G, Bear J, Monninger M, Sun M, Morales-Kastresana A, Jones JC, Felber BK, Chen X, Gursel I, Pavlakis GN (2016) Efficient production and enhanced tumor delivery of engineered extracellular vesicles. Biomaterials 105:195–205
pubmed: 27522254
pmcid: 7156278
doi: 10.1016/j.biomaterials.2016.07.003
Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, Angevin E, Amigorena S, Zitvogel L (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7(3):297–303
pubmed: 11231627
doi: 10.1038/85438
Xie YF, Bai O, Zhang HF, Yuan JY, Zong S, Chibbar R, Slattery K, Qureshi M, Wei YD, Deng YL, Xiang J (2010) Membrane-bound HSP70-engineered myeloma cell-derived exosomes stimulate more efficient CD8(+) CTL- and NK-mediated antitumour immunity than exosomes released from heat-shocked tumour cells expressing cytoplasmic HSP70. J Cell Mol Med 14(11):2655–2666
pubmed: 19627400
doi: 10.1111/j.1582-4934.2009.00851.x
Yaddanapudi K, Meng S, Whitt AG, Al Rayyan N, Richie J, Tu A, Eaton JW, Li C (2019) Exosomes from GM-CSF expressing embryonic stem cells are an effective prophylactic vaccine for cancer prevention. Onco Targets Ther 8(3):1561119
Yan IK, Shukla N, Borrelli DA, Patel T (2018) Use of a hollow Fiber bioreactor to collect extracellular vesicles from cells in culture. Methods Mol Biol 1740:35–41
pubmed: 29388134
doi: 10.1007/978-1-4939-7652-2_4
Yang T, Martin P, Fogarty B, Brown A, Schurman K, Phipps R, Yin VP, Lockman P, Bai S (2015) Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res 32(6):2003–2014
pubmed: 25609010
pmcid: 4520542
doi: 10.1007/s11095-014-1593-y
Yang Z, Shi J, Xie J, Wang Y, Sun J, Liu T, Zhao Y, Zhao X, Wang X, Ma Y, Malkoc V, Chiang C, Deng W, Chen Y, Fu Y, Kwak KJ, Fan Y, Kang C, Yin C, Rhee J, Bertani P, Otero J, Lu W, Yun K, Lee AS, Jiang W, Teng L, Kim BYS, Lee LJ (2020a) Large-scale generation of functional mRNA-encapsulating exosomes via cellular nanoporation. Nat Biomed Eng 4(1):69–83
pubmed: 31844155
doi: 10.1038/s41551-019-0485-1
Yang D, Zhang W, Zhang H, Zhang F, Chen L, Ma L, Larcher LM, Chen S, Liu N, Zhao Q, Tran PHL, Chen C, Veedu RN, Wang T (2020b) Progress, opportunity, and perspective on exosome isolation - efforts for efficient exosome-based theranostics. Theranostics 10(8):3684–3707
pubmed: 32206116
pmcid: 7069071
doi: 10.7150/thno.41580
Zaborowski MP, Balaj L, Breakefield XO, Lai CP (2015) Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience 65(8):783–797
pubmed: 26955082
pmcid: 4776721
doi: 10.1093/biosci/biv084
Zhang Q, Liu RX, Chan KW, Hu J, Zhang J, Wei L, Tan H, Yang X, Liu H (2019) Exosomal transfer of p-STAT3 promotes acquired 5-FU resistance in colorectal cancer cells. J Exp Clin Cancer Res 38(1):320
pubmed: 31324203
pmcid: 6642525
doi: 10.1186/s13046-019-1314-9
Zhao L, Gu C, Gan Y, Shao L, Chen H, Zhu H (2020) Exosome-mediated siRNA delivery to suppress postoperative breast cancer metastasis. J Control Release 318:1–15
pubmed: 31830541
doi: 10.1016/j.jconrel.2019.12.005
Zomer A, Maynard C, Verweij FJ, Kamermans A, Schafer R, Beerling E, Schiffelers RM, de Wit E, Berenguer J, Ellenbroek SIJ, Wurdinger T, Pegtel DM, van Rheenen J (2015) Vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell 161(5):1046–1057
pubmed: 26000481
pmcid: 4448148
doi: 10.1016/j.cell.2015.04.042