Tiny Actors in the Big Cellular World: Extracellular Vesicles Playing Critical Roles in Cancer

. 2020 Oct 17 ; 21 (20) : . [epub] 20201017

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33080788

Communications among cells can be achieved either via direct interactions or via secretion of soluble factors. The emergence of extracellular vesicles (EVs) as entities that play key roles in cell-to-cell communication offer opportunities in exploring their features for use in therapeutics; i.e., management and treatment of various pathologies, such as those used for cancer. The potential use of EVs as therapeutic agents is attributed not only for their cell membrane-bound components, but also for their cargos, mostly bioactive molecules, wherein the former regulate interactions with a recipient cell while the latter trigger cellular functions/molecular mechanisms of a recipient cell. In this article, we highlight the involvement of EVs in hallmarks of a cancer cell, particularly focusing on those molecular processes that are influenced by EV cargos. Moreover, we explored the roles of RNA species and proteins carried by EVs in eliciting drug resistance phenotypes. Interestingly, engineered EVs have been investigated and proposed as therapeutic agents in various in vivo and in vitro studies, as well as in several clinical trials.

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Maia J., Caja S., Strano Moraes M.C., Couto N., Costa-Silva B. Exosome-Based Cell-Cell Communication in the Tumor Microenvironment. Front. Cell Dev. Biol. 2018;6:18. doi: 10.3389/fcell.2018.00018. PubMed DOI PMC

McCrea P.D., Gu D., Balda M.S. Junctional Music that the Nucleus Hears: Cell-Cell Contact Signaling and the Modulation of Gene Activity. Cold Spring Harb. Perspect. Biol. 2009;1:a002923. doi: 10.1101/cshperspect.a002923. PubMed DOI PMC

Brücher B.L.D.M., Jamall I.S. Cell-Cell Communication in the Tumor Microenvironment, Carcinogenesis, and Anticancer Treatment. Cell Physiol. Biochem. 2014;34:213–243. doi: 10.1159/000362978. PubMed DOI

Lee Y., EL Andaloussi S., Wood M.J.A. Exosomes and microvesicles: Extracellular vesicles for genetic information transfer and gene therapy. Hum. Mol. Genet. 2012;21:R125–R134. doi: 10.1093/hmg/dds317. PubMed DOI

Harding C., Heuser J., Stahl P. Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: Demonstration of a pathway for receptor shedding. Eur. J. Cell Biol. 1984;35:256–263. PubMed

Lai R.C., Chen T.S., Lim S.K. Mesenchymal stem cell exosome: A novel stem cell-based therapy for cardiovascular disease. Regen. Med. 2011;6:481–492. doi: 10.2217/rme.11.35. PubMed DOI

Guescini M., Genedani S., Stocchi V., Agnati L.F. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. 2010;117:1–4. doi: 10.1007/s00702-009-0288-8. PubMed DOI

Ratajczak J., Miekus K., Kucia M., Zhang J., Reca R., Dvorak P., Ratajczak M.Z. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20:847–856. doi: 10.1038/sj.leu.2404132. PubMed DOI

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;183:1161–1172. doi: 10.1084/jem.183.3.1161. PubMed DOI PMC

Gatti S., Bruno S., Deregibus M.C., Sordi A., Cantaluppi V., Tetta C., Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol. Dial. Transplant. 2011;26:1474–1483. doi: 10.1093/ndt/gfr015. PubMed DOI

Olejarz W., Dominiak A., Żołnierzak A., Kubiak-Tomaszewska G., Lorenc T. Tumor-Derived Exosomes in Immunosuppression and Immunotherapy. J. Immunol. Res. 2020;2020:6272498. doi: 10.1155/2020/6272498. PubMed DOI PMC

Besse B., Charrier M., Lapierre V., Dansin E., Lantz O., Planchard D., Le Chevalier T., Livartoski A., Barlesi F., Laplanche A., et al. Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC. OncoImmunology. 2016;5:e1071008. doi: 10.1080/2162402X.2015.1071008. PubMed DOI PMC

Rak J., Guha A. Extracellular vesicles—Vehicles that spread cancer genes. Bioessays. 2012;34:489–497. doi: 10.1002/bies.201100169. PubMed DOI

Bellingham S.A., Guo B.B., Coleman B.M., Hill A.F. Exosomes: Vehicles for the Transfer of Toxic Proteins Associated with Neurodegenerative Diseases? Front. Physiol. 2012;3:124. doi: 10.3389/fphys.2012.00124. PubMed DOI PMC

Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S.D., Ntzouni M., Margaritis L.H., Stefanis L., Vekrellis K. Cell-Produced -Synuclein Is Secreted in a Calcium-Dependent Manner by Exosomes and Impacts Neuronal Survival. J. Neurosci. 2010;30:6838–6851. doi: 10.1523/JNEUROSCI.5699-09.2010. PubMed DOI PMC

Tai Y.-L., Chu P.-Y., Lee B.-H., Chen K.-C., Yang C.-Y., Kuo W.-H., Shen T.-L. Basics and applications of tumor-derived extracellular vesicles. J. Biomed. Sci. 2019;26:35. doi: 10.1186/s12929-019-0533-x. PubMed DOI PMC

EL Andaloussi S., Mäger I., Breakefield X.O., Wood M.J.A. Extracellular vesicles: Biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov. 2013;12:347–357. doi: 10.1038/nrd3978. PubMed DOI

Jurj A., Pasca S., Teodorescu P., Tomuleasa C., Berindan-Neagoe I. Basic knowledge on BCR-ABL1-positive extracellular vesicles. Biomark. Med. 2020;14:451–458. doi: 10.2217/bmm-2019-0510. PubMed DOI

Gebara N., Rossi A., Skovronova R., Aziz J.M., Asthana A., Bussolati B. Extracellular Vesicles, Apoptotic Bodies and Mitochondria: Stem Cell Bioproducts for Organ Regeneration. Curr. Transpl. Rep. 2020;7:105–113. doi: 10.1007/s40472-020-00282-2. DOI

Kakarla R., Hur J., Kim Y.J., Kim J., Chwae Y.-J. Apoptotic cell-derived exosomes: Messages from dying cells. Exp. Mol. Med. 2020;52:1–6. doi: 10.1038/s12276-019-0362-8. PubMed DOI PMC

Gardai S.J., McPhillips K.A., Frasch S.C., Janssen W.J., Starefeldt A., Murphy-Ullrich J.E., Bratton D.L., Oldenborg P.-A., Michalak M., Henson P.M. Cell-Surface Calreticulin Initiates Clearance of Viable or Apoptotic Cells through trans-Activation of LRP on the Phagocyte. Cell. 2005;123:321–334. doi: 10.1016/j.cell.2005.08.032. PubMed DOI

Lunavat T.R., Cheng L., Kim D.-K., Bhadury J., Jang S.C., Lässer C., Sharples R.A., López M.D., Nilsson J., Gho Y.S., et al. Small RNA deep sequencing discriminates subsets of extracellular vesicles released by melanoma cells—Evidence of unique microRNA cargos. RNA Biol. 2015;12:810–823. doi: 10.1080/15476286.2015.1056975. PubMed DOI PMC

Caruso S., Poon I.K.H. Apoptotic Cell-Derived Extracellular Vesicles: More Than Just Debris. Front. Immunol. 2018;9:1486. doi: 10.3389/fimmu.2018.01486. PubMed DOI PMC

Akers J.C., Gonda D., Kim R., Carter B.S., Chen C.C. Biogenesis of extracellular vesicles (EV): Exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J. Neurooncol. 2013;113:1–11. doi: 10.1007/s11060-013-1084-8. PubMed DOI PMC

Jurj A., Zanoaga O., Braicu C., Lazar V., Tomuleasa C., Irimie A., Berindan-Neagoe I. A Comprehensive Picture of Extracellular Vesicles and Their Contents. Molecular Transfer to Cancer Cells. Cancers. 2020;12:298. doi: 10.3390/cancers12020298. PubMed DOI PMC

Borges F.T., Reis L.A., Schor N. Extracellular vesicles: Structure, function, and potential clinical uses in renal diseases. Braz. J. Med. Biol. Res. 2013;46:824–830. doi: 10.1590/1414-431X20132964. PubMed DOI PMC

Ailawadi S., Wang X., Gu H., Fan G.-C. Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2015;1852:1–11. doi: 10.1016/j.bbadis.2014.10.008. PubMed DOI PMC

Kajimoto T., Okada T., Miya S., Zhang L., Nakamura S. Ongoing activation of sphingosine 1-phosphate receptors mediates maturation of exosomal multivesicular endosomes. Nat. Commun. 2013;4:2712. doi: 10.1038/ncomms3712. PubMed DOI

Kowal J., Tkach M., Théry C. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol. 2014;29:116–125. doi: 10.1016/j.ceb.2014.05.004. PubMed DOI

Ekström E.J., Bergenfelz C., von Bülow V., Serifler F., Carlemalm E., Jönsson G., Andersson T., Leandersson K. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol. Cancer. 2014;13:88. doi: 10.1186/1476-4598-13-88. PubMed DOI PMC

Chuo S.T.-Y., Chien J.C.-Y., Lai C.P.-K. Imaging extracellular vesicles: Current and emerging methods. J. Biomed. Sci. 2018;25:91. doi: 10.1186/s12929-018-0494-5. PubMed DOI PMC

Willms E., Cabañas C., Mäger I., Wood M.J.A., Vader P. Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression. Front. Immunol. 2018;9:738. doi: 10.3389/fimmu.2018.00738. PubMed DOI PMC

Doyle L., Wang M. Overview of Extracellular Vesicles, Their Origin, Composition, Purpose, and Methods for Exosome Isolation and Analysis. Cells. 2019;8:727. doi: 10.3390/cells8070727. PubMed DOI PMC

Xie C., Ji N., Tang Z., Li J., Chen Q. The role of extracellular vesicles from different origin in the microenvironment of head and neck cancers. Mol. Cancer. 2019;18:83. doi: 10.1186/s12943-019-0985-3. PubMed DOI PMC

Zhang Y., Liu Y., Liu H., Tang W.H. Exosomes: Biogenesis, biologic function and clinical potential. Cell Biosci. 2019;9:19. doi: 10.1186/s13578-019-0282-2. PubMed DOI PMC

Zaborowski M.P., Balaj L., Breakefield X.O., Lai C.P. Extracellular Vesicles: Composition, Biological Relevance, and Methods of Study. BioScience. 2015;65:783–797. doi: 10.1093/biosci/biv084. PubMed DOI PMC

Simeone P., Bologna G., Lanuti P., Pierdomenico L., Guagnano M.T., Pieragostino D., Del Boccio P., Vergara D., Marchisio M., Miscia S., et al. Extracellular Vesicles as Signaling Mediators and Disease Biomarkers across Biological Barriers. Int. J. Mol. Sci. 2020;21:2514. doi: 10.3390/ijms21072514. PubMed DOI PMC

Catalano M., O’Driscoll L. Inhibiting extracellular vesicles formation and release: A review of EV inhibitors. J. Extracell. Vesicles. 2020;9:1703244. doi: 10.1080/20013078.2019.1703244. PubMed DOI PMC

Joshi B.S., de Beer M.A., Giepmans B.N.G., Zuhorn I.S. Endocytosis of Extracellular Vesicles and Release of Their Cargo from Endosomes. ACS Nano. 2020;14:4444–4455. doi: 10.1021/acsnano.9b10033. PubMed DOI PMC

Théry C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009;9:581–593. doi: 10.1038/nri2567. PubMed DOI

Villarroya-Beltri C., Baixauli F., Gutiérrez-Vázquez C., Sánchez-Madrid F., Mittelbrunn M. Sorting it out: Regulation of exosome loading. Semin. Cancer Biol. 2014;28:3–13. doi: 10.1016/j.semcancer.2014.04.009. PubMed DOI PMC

Thakur B.K., Zhang H., Becker A., Matei I., Huang Y., Costa-Silva B., Zheng Y., Hoshino A., Brazier H., Xiang J., et al. Double-stranded DNA in exosomes: A novel biomarker in cancer detection. Cell Res. 2014;24:766–769. doi: 10.1038/cr.2014.44. PubMed DOI PMC

Fischer S., Cornils K., Speiseder T., Badbaran A., Reimer R., Indenbirken D., Grundhoff A., Brunswig-Spickenheier B., Alawi M., Lange C. Indication of Horizontal DNA Gene Transfer by Extracellular Vesicles. PLoS ONE. 2016;11:e0163665. doi: 10.1371/journal.pone.0163665. PubMed DOI PMC

Shelke G., Jang S.C., Yin Y., Lässer C., Lötvall J. Human mast cells release extracellular vesicle-associated DNA. Matters. 2016;2:e201602000034. doi: 10.19185/matters.201602000034. DOI

Kawamura Y., Yamamoto Y., Sato T.-A., Ochiya T. Extracellular vesicles as trans-genomic agents: Emerging roles in disease and evolution. Cancer Sci. 2017;108:824–830. doi: 10.1111/cas.13222. PubMed DOI PMC

Record M., Subra C., Silvente-Poirot S., Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors. Biochem. Pharmacol. 2011;81:1171–1182. doi: 10.1016/j.bcp.2011.02.011. PubMed DOI

Choi D.-S., Kim D.-K., Kim Y.-K., Gho Y.S. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013;13:1554–1571. doi: 10.1002/pmic.201200329. PubMed DOI

Yáñez-Mó M., Siljander P.R.-M., Andreu Z., Bedina Zavec A., Borràs F.E., Buzas E.I., Buzas K., Casal E., Cappello F., Carvalho J., et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles. 2015;4:27066. doi: 10.3402/jev.v4.27066. PubMed DOI PMC

Chen T., Guo J., Yang M., Zhu X., Cao X. Chemokine-Containing Exosomes Are Released from Heat-Stressed Tumor Cells via Lipid Raft-Dependent Pathway and Act as Efficient Tumor Vaccine. J. Immunol. 2011;186:2219–2228. doi: 10.4049/jimmunol.1002991. PubMed DOI

Li I., Nabet B.Y. Exosomes in the tumor microenvironment as mediators of cancer therapy resistance. Mol. Cancer. 2019;18:32. doi: 10.1186/s12943-019-0975-5. PubMed DOI PMC

Cvjetkovic A., Lötvall J., Lässer C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J. Extracell. Vesicles. 2014;3:23111. doi: 10.3402/jev.v3.23111. PubMed DOI PMC

Konoshenko M.Y., Lekchnov E.A., Vlassov A.V., Laktionov P.P. Isolation of Extracellular Vesicles: General Methodologies and Latest Trends. Biomed. Res. Int. 2018;2018:8545347. doi: 10.1155/2018/8545347. PubMed DOI PMC

Böing A.N., van der Pol E., Grootemaat A.E., Coumans F.A.W., Sturk A., Nieuwland R. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J. Extracell. Vesicles. 2014;3:23430. doi: 10.3402/jev.v3.23430. PubMed DOI PMC

Yamamoto K.R., Alberts B.M., Benzinger R., Lawhorne L., Treiber G. Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology. 1970;40:734–744. doi: 10.1016/0042-6822(70)90218-7. PubMed DOI

Li P., Kaslan M., Lee S.H., Yao J., Gao Z. Progress in Exosome Isolation Techniques. Theranostics. 2017;7:789–804. doi: 10.7150/thno.18133. PubMed DOI PMC

Liu F., Vermesh O., Mani V., Ge T.J., Madsen S.J., Sabour A., Hsu E.-C., Gowrishankar G., Kanada M., Jokerst J.V., et al. The Exosome Total Isolation Chip. ACS Nano. 2017;11:10712–10723. doi: 10.1021/acsnano.7b04878. PubMed DOI PMC

Wu M., Ouyang Y., Wang Z., Zhang R., Huang P.-H., Chen C., Li H., Li P., Quinn D., Dao M., et al. Isolation of exosomes from whole blood by integrating acoustics and microfluidics. Proc. Natl. Acad. Sci. USA. 2017;114:10584–10589. doi: 10.1073/pnas.1709210114. PubMed DOI PMC

Gallart-Palau X., Serra A., Wong A.S.W., Sandin S., Lai M.K.P., Chen C.P., Kon O.L., Sze S.K. Extracellular vesicles are rapidly purified from human plasma by PRotein Organic Solvent PRecipitation (PROSPR) Sci. Rep. 2015;5:14664. doi: 10.1038/srep14664. PubMed DOI PMC

Heath N., Grant L., De Oliveira T.M., Rowlinson R., Osteikoetxea X., Dekker N., Overman R. Rapid isolation and enrichment of extracellular vesicle preparations using anion exchange chromatography. Sci. Rep. 2018;8:5730. doi: 10.1038/s41598-018-24163-y. PubMed DOI PMC

Merchant M.L., Powell D.W., Wilkey D.W., Cummins T.D., Deegens J.K., Rood I.M., McAfee K.J., Fleischer C., Klein E., Klein J.B. Microfiltration isolation of human urinary exosomes for characterization by MS. Proteom. Clin. Appl. 2010;4:84–96. doi: 10.1002/prca.200800093. PubMed DOI

Usman W.M., Pham T.C., Kwok Y.Y., Vu L.T., Ma V., Peng B., Chan Y.S., Wei L., Chin S.M., Azad A., et al. Efficient RNA drug delivery using red blood cell extracellular vesicles. Nat. Commun. 2018;9:2359. doi: 10.1038/s41467-018-04791-8. PubMed DOI PMC

Gercel-Taylor C., Atay S., Tullis R.H., Kesimer M., Taylor D.D. Nanoparticle analysis of circulating cell-derived vesicles in ovarian cancer patients. Anal. Biochem. 2012;428:44–53. doi: 10.1016/j.ab.2012.06.004. PubMed DOI

Vestad B., Llorente A., Neurauter A., Phuyal S., Kierulf B., Kierulf P., Skotland T., Sandvig K., Haug K.B.F., Øvstebø R. Size and concentration analyses of extracellular vesicles by nanoparticle tracking analysis: A variation study. J. Extracell. Vesicles. 2017;6:1344087. doi: 10.1080/20013078.2017.1344087. PubMed DOI PMC

Headland S.E., Jones H.R., D’Sa A.S.V., Perretti M., Norling L.V. Cutting-edge analysis of extracellular microparticles using ImageStream(X) imaging flow cytometry. Sci. Rep. 2014;4:5237. doi: 10.1038/srep05237. PubMed DOI PMC

Linares R., Tan S., Gounou C., Brisson A.R. Imaging and Quantification of Extracellular Vesicles by Transmission Electron Microscopy. Methods Mol. Biol. 2017;1545:43–54. doi: 10.1007/978-1-4939-6728-5_4. PubMed DOI

Sprague D.L., Elzey B.D., Crist S.A., Waldschmidt T.J., Jensen R.J., Ratliff T.L. Platelet-mediated modulation of adaptive immunity: Unique delivery of CD154 signal by platelet-derived membrane vesicles. Blood. 2008;111:5028–5036. doi: 10.1182/blood-2007-06-097410. PubMed DOI PMC

Baj-Krzyworzeka M., Mytar B., Szatanek R., Surmiak M., Węglarczyk K., Baran J., Siedlar M. Colorectal cancer-derived microvesicles modulate differentiation of human monocytes to macrophages. J. Transl. Med. 2016;14:36. doi: 10.1186/s12967-016-0789-9. PubMed DOI PMC

Simhadri V.R., Reiners K.S., Hansen H.P., Topolar D., Simhadri V.L., Nohroudi K., Kufer T.A., Engert A., Pogge von Strandmann E. Dendritic Cells Release HLA-B-Associated Transcript-3 Positive Exosomes to Regulate Natural Killer Function. PLoS ONE. 2008;3:e3377. doi: 10.1371/journal.pone.0003377. PubMed DOI PMC

Clayton A., Mitchell J.P., Court J., Linnane S., Mason M.D., Tabi Z. Human Tumor-Derived Exosomes Down-Modulate NKG2D Expression. J. Immunol. 2008;180:7249–7258. doi: 10.4049/jimmunol.180.11.7249. PubMed DOI

Eken C., Gasser O., Zenhaeusern G., Oehri I., Hess C., Schifferli J.A. Polymorphonuclear Neutrophil-Derived Ectosomes Interfere with the Maturation of Monocyte-Derived Dendritic Cells. J. Immunol. 2008;180:817–824. doi: 10.4049/jimmunol.180.2.817. PubMed DOI

Yu S., Liu C., Su K., Wang J., Liu Y., Zhang L., Li C., Cong Y., Kimberly R., Grizzle W.E., et al. Tumor Exosomes Inhibit Differentiation of Bone Marrow Dendritic Cells. J. Immunol. 2007;178:6867–6875. doi: 10.4049/jimmunol.178.11.6867. PubMed DOI

Camussi G., Deregibus M.-C., Bruno S., Grange C., Fonsato V., Tetta C. Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am. J. Cancer Res. 2011;1:98–110. PubMed PMC

Jang Y.-Y., Collector M.I., Baylin S.B., Diehl A.M., Sharkis S.J. Hematopoietic stem cells convert into liver cells within days without fusion. Nat. Cell Biol. 2004;6:532–539. doi: 10.1038/ncb1132. PubMed DOI

Quesenberry P.J., Aliotta J.M. Cellular phenotype switching and microvesicles. Adv. Drug Deliv. Rev. 2010;62:1141–1148. doi: 10.1016/j.addr.2010.06.001. PubMed DOI PMC

Peinado H., Alečković M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., Hergueta-Redondo M., Williams C., García-Santos G., Ghajar C., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012;18:883–891. doi: 10.1038/nm.2753. PubMed DOI PMC

Skog J., Würdinger T., van Rijn S., Meijer D.H., Gainche L., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008;10:1470–1476. doi: 10.1038/ncb1800. PubMed DOI PMC

Al-Nedawi K., Meehan B., Kerbel R.S., Allison A.C., Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. USA. 2009;106:3794–3799. doi: 10.1073/pnas.0804543106. PubMed DOI PMC

Hu C., Meiners S., Lukas C., Stathopoulos G.T., Chen J. Role of exosomal microRNAs in lung cancer biology and clinical applications. Cell Prolif. 2020;53 doi: 10.1111/cpr.12828. PubMed DOI PMC

Kumar A., Deep G. Exosomes in hypoxia-induced remodeling of the tumor microenvironment. Cancer Lett. 2020;488:1–8. doi: 10.1016/j.canlet.2020.05.018. PubMed DOI

Lee J.-K., Park S.-R., Jung B.-K., Jeon Y.-K., Lee Y.-S., Kim M.-K., Kim Y.-G., Jang J.-Y., Kim C.-W. Exosomes Derived from Mesenchymal Stem Cells Suppress Angiogenesis by Down-Regulating VEGF Expression in Breast Cancer Cells. PLoS ONE. 2013;8:e84256. doi: 10.1371/journal.pone.0084256. PubMed DOI PMC

Umezu T., Ohyashiki K., Kuroda M., Ohyashiki J.H. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene. 2013;32:2747–2755. doi: 10.1038/onc.2012.295. PubMed DOI

Kalinina N., Klink G., Glukhanyuk E., Lopatina T., Efimenko A., Akopyan Z., Tkachuk V. miR-92a regulates angiogenic activity of adipose-derived mesenchymal stromal cells. Exp. Cell Res. 2015;339:61–66. doi: 10.1016/j.yexcr.2015.10.007. PubMed DOI

Liu Y., Luo F., Wang B., Li H., Xu Y., Liu X., Shi L., Lu X., Xu W., Lu L., et al. STAT3-regulated exosomal miR-21 promotes angiogenesis and is involved in neoplastic processes of transformed human bronchial epithelial cells. Cancer Lett. 2016;370:125–135. doi: 10.1016/j.canlet.2015.10.011. PubMed DOI

Mao G., Liu Y., Fang X., Liu Y., Fang L., Lin L., Liu X., Wang N. Tumor-derived microRNA-494 promotes angiogenesis in non-small cell lung cancer. Angiogenesis. 2015;18:373–382. doi: 10.1007/s10456-015-9474-5. PubMed DOI

Grange C., Tapparo M., Collino F., Vitillo L., Damasco C., Deregibus M.C., Tetta C., Bussolati B., Camussi G. Microvesicles Released from Human Renal Cancer Stem Cells Stimulate Angiogenesis and Formation of Lung Premetastatic Niche. Cancer Res. 2011;71:5346–5356. doi: 10.1158/0008-5472.CAN-11-0241. PubMed DOI

Sidhu S.S., Mengistab A.T., Tauscher A.N., LaVail J., Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor–stromal interactions. Oncogene. 2004;23:956–963. doi: 10.1038/sj.onc.1207070. PubMed DOI

Le M.T.N., Hamar P., Guo C., Basar E., Perdigão-Henriques R., Balaj L., Lieberman J. miR-200–containing extracellular vesicles promote breast cancer cell metastasis. J. Clin. Invest. 2014;124:5109–5128. doi: 10.1172/JCI75695. PubMed DOI PMC

Liao J., Liu R., Shi Y.-J., Yin L.-H., Pu Y.-P. Exosome-shuttling microRNA-21 promotes cell migration and invasion-targeting PDCD4 in esophageal cancer. Int. J. Oncol. 2016;48:2567–2579. doi: 10.3892/ijo.2016.3453. PubMed DOI

Zhou W., Fong M.Y., Min Y., Somlo G., Liu L., Palomares M.R., Yu Y., Chow A., O’Connor S.T.F., Chin A.R., et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014;25:501–515. doi: 10.1016/j.ccr.2014.03.007. PubMed DOI PMC

Wang L., He J., Hu H., Tu L., Sun Z., Liu Y., Luo F. Lung CSC-derived exosomal miR-210-3p contributes to a pro-metastatic phenotype in lung cancer by targeting FGFRL1. J. Cell Mol. Med. 2020;24:6324–6339. doi: 10.1111/jcmm.15274. PubMed DOI PMC

Higginbotham J.N., Demory Beckler M., Gephart J.D., Franklin J.L., Bogatcheva G., Kremers G.-J., Piston D.W., Ayers G.D., McConnell R.E., Tyska M.J., et al. Amphiregulin Exosomes Increase Cancer Cell Invasion. Curr. Biol. 2011;21:779–786. doi: 10.1016/j.cub.2011.03.043. PubMed DOI PMC

Al-Nedawi K., Meehan B., Micallef J., Lhotak V., May L., Guha A., Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008;10:619–624. doi: 10.1038/ncb1725. PubMed DOI

Fong M.Y., Zhou W., Liu L., Alontaga A.Y., Chandra M., Ashby J., Chow A., O’Connor S.T.F., Li S., Chin A.R., et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat. Cell Biol. 2015;17:183–194. doi: 10.1038/ncb3094. PubMed DOI PMC

Garnier D., Magnus N., Meehan B., Kislinger T., Rak J. Qualitative changes in the proteome of extracellular vesicles accompanying cancer cell transition to mesenchymal state. Exp. Cell Res. 2013;319:2747–2757. doi: 10.1016/j.yexcr.2013.08.003. PubMed DOI

Tauro B.J., Mathias R.A., Greening D.W., Gopal S.K., Ji H., Kapp E.A., Coleman B.M., Hill A.F., Kusebauch U., Hallows J.L., et al. Oncogenic H-Ras Reprograms Madin-Darby Canine Kidney (MDCK) Cell-derived Exosomal Proteins Following Epithelial-Mesenchymal Transition. Mol. Cell Proteom. 2013;12:2148–2159. doi: 10.1074/mcp.M112.027086. PubMed DOI PMC

Aga M., Bentz G.L., Raffa S., Torrisi M.R., Kondo S., Wakisaka N., Yoshizaki T., Pagano J.S., Shackelford J. Exosomal HIF1α supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes. Oncogene. 2014;33:4613–4622. doi: 10.1038/onc.2014.66. PubMed DOI PMC

Cai Z., Yang F., Yu L., Yu Z., Jiang L., Wang Q., Yang Y., Wang L., Cao X., Wang J. Activated T Cell Exosomes Promote Tumor Invasion via Fas Signaling Pathway. J. Immunol. 2012;188:5954–5961. doi: 10.4049/jimmunol.1103466. PubMed DOI

Gao F., Zhao Z.-L., Zhao W.-T., Fan Q.-R., Wang S.-C., Li J., Zhang Y.-Q., Shi J.-W., Lin X.-L., Yang S., et al. miR-9 modulates the expression of interferon-regulated genes and MHC class I molecules in human nasopharyngeal carcinoma cells. Biochem. Biophys. Res. Commun. 2013;431:610–616. doi: 10.1016/j.bbrc.2012.12.097. PubMed DOI

Fabbri M., Paone A., Calore F., Galli R., Gaudio E., Santhanam R., Lovat F., Fadda P., Mao C., Nuovo G.J., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA. 2012;109:E2110–E2116. doi: 10.1073/pnas.1209414109. PubMed DOI PMC

Ma X., Chen Z., Hua D., He D., Wang L., Zhang P., Wang J., Cai Y., Gao C., Zhang X., et al. Essential role for TrpC5-containing extracellular vesicles in breast cancer with chemotherapeutic resistance. Proc. Natl. Acad. Sci. USA. 2014;111:6389–6394. doi: 10.1073/pnas.1400272111. PubMed DOI PMC

Klibi J., Niki T., Riedel A., Pioche-Durieu C., Souquere S., Rubinstein E., Le Moulec S., Guigay J., Hirashima M., Guemira F., et al. Blood diffusion and Th1-suppressive effects of galectin-9–containing exosomes released by Epstein-Barr virus–infected nasopharyngeal carcinoma cells. Blood. 2009;113:1957–1966. doi: 10.1182/blood-2008-02-142596. PubMed DOI

Yang M., Chen J., Su F., Yu B., Su F., Lin L., Liu Y., Huang J.-D., Song E. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer. 2011;10:117. doi: 10.1186/1476-4598-10-117. PubMed DOI PMC

Zhou M., Chen J., Zhou L., Chen W., Ding G., Cao L. Pancreatic cancer derived exosomes regulate the expression of TLR4 in dendritic cells via miR-203. Cell. Immunol. 2014;292:65–69. doi: 10.1016/j.cellimm.2014.09.004. PubMed DOI

Berchem G., Noman M.Z., Bosseler M., Paggetti J., Baconnais S., Le cam E., Nanbakhsh A., Moussay E., Mami-Chouaib F., Janji B., et al. Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer. OncoImmunology. 2016;5:e1062968. doi: 10.1080/2162402X.2015.1062968. PubMed DOI PMC

Huber V., Fais S., Iero M., Lugini L., Canese P., Squarcina P., Zaccheddu A., Colone M., Arancia G., Gentile M., et al. Human Colorectal Cancer Cells Induce T-Cell Death Through Release of Proapoptotic Microvesicles: Role in Immune Escape. Gastroenterology. 2005;128:1796–1804. doi: 10.1053/j.gastro.2005.03.045. PubMed DOI

Clayton A., Mitchell J.P., Court J., Mason M.D., Tabi Z. Human Tumor-Derived Exosomes Selectively Impair Lymphocyte Responses to Interleukin-2. Cancer Res. 2007;67:7458–7466. doi: 10.1158/0008-5472.CAN-06-3456. PubMed DOI

Ashiru O., Boutet P., Fernandez-Messina L., Aguera-Gonzalez S., Skepper J.N., Vales-Gomez M., Reyburn H.T. Natural Killer Cell Cytotoxicity Is Suppressed by Exposure to the Human NKG2D Ligand MICA*008 That Is Shed by Tumor Cells in Exosomes. Cancer Res. 2010;70:481–489. doi: 10.1158/0008-5472.CAN-09-1688. PubMed DOI PMC

Condamine T., Ramachandran I., Youn J.-I., Gabrilovich D.I. Regulation of Tumor Metastasis by Myeloid-Derived Suppressor Cells. Annu. Rev. Med. 2015;66:97–110. doi: 10.1146/annurev-med-051013-052304. PubMed DOI PMC

Xiang X., Poliakov A., Liu C., Liu Y., Deng Z., Wang J., Cheng Z., Shah S.V., Wang G.-J., Zhang L., et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer. 2009;124:2621–2633. doi: 10.1002/ijc.24249. PubMed DOI PMC

Khan S., Jutzy J.M.S., Aspe J.R., McGregor D.W., Neidigh J.W., Wall N.R. Survivin is released from cancer cells via exosomes. Apoptosis. 2011;16:1–12. doi: 10.1007/s10495-010-0534-4. PubMed DOI PMC

Cappellesso R., Tinazzi A., Giurici T., Simonato F., Guzzardo V., Ventura L., Crescenzi M., Chiarelli S., Fassina A. Programmed cell death 4 and microRNA 21 inverse expression is maintained in cells and exosomes from ovarian serous carcinoma effusions: PDCD4 and miR-21 Expression in OSC and Exosomes. Cancer Cytopathol. 2014;122:685–693. doi: 10.1002/cncy.21442. PubMed DOI

Taylor D.D., Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008;110:13–21. doi: 10.1016/j.ygyno.2008.04.033. PubMed DOI

Yu X., Harris S.L., Levine A.J. The Regulation of Exosome Secretion: A Novel Function of the p53 Protein. Cancer Res. 2006;66:4795–4801. doi: 10.1158/0008-5472.CAN-05-4579. PubMed DOI

Xavier C.P.R., Caires H.R., Barbosa M.A.G., Bergantim R., Guimarães J.E., Vasconcelos M.H. The Role of Extracellular Vesicles in the Hallmarks of Cancer and Drug Resistance. Cells. 2020;9:1141. doi: 10.3390/cells9051141. PubMed DOI PMC

Graner M.W., Alzate O., Dechkovskaia A.M., Keene J.D., Sampson J.H., Mitchell D.A., Bigner D.D. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009;23:1541–1557. doi: 10.1096/fj.08-122184. PubMed DOI PMC

Webber J., Stone T.C., Katilius E., Smith B.C., Gordon B., Mason M.D., Tabi Z., Brewis I.A., Clayton A. Proteomics Analysis of Cancer Exosomes Using a Novel Modified Aptamer-based Array (SOMAscanTM) Platform. Mol. Cell Proteom. 2014;13:1050–1064. doi: 10.1074/mcp.M113.032136. PubMed DOI PMC

Welton J.L., Khanna S., Giles P.J., Brennan P., Brewis I.A., Staffurth J., Mason M.D., Clayton A. Proteomics Analysis of Bladder Cancer Exosomes. Mol. Cell Proteom. 2010;9:1324–1338. doi: 10.1074/mcp.M000063-MCP201. PubMed DOI PMC

Demory Beckler M., Higginbotham J.N., Franklin J.L., Ham A.-J., Halvey P.J., Imasuen I.E., Whitwell C., Li M., Liebler D.C., Coffey R.J. Proteomic Analysis of Exosomes from Mutant KRAS Colon Cancer Cells Identifies Intercellular Transfer of Mutant KRAS. Mol. Cell Proteom. 2013;12:343–355. doi: 10.1074/mcp.M112.022806. PubMed DOI PMC

Soldevilla B., Rodríguez M., San Millán C., García V., Fernández-Periañez R., Gil-Calderón B., Martín P., García-Grande A., Silva J., Bonilla F., et al. Tumor-derived exosomes are enriched in ΔNp73, which promotes oncogenic potential in acceptor cells and correlates with patient survival. Hum. Mol. Genet. 2014;23:467–478. doi: 10.1093/hmg/ddt437. PubMed DOI

Ohshima K., Inoue K., Fujiwara A., Hatakeyama K., Kanto K., Watanabe Y., Muramatsu K., Fukuda Y., Ogura S., Yamaguchi K., et al. Let-7 MicroRNA Family Is Selectively Secreted into the Extracellular Environment via Exosomes in a Metastatic Gastric Cancer Cell Line. PLoS ONE. 2010;5:e13247. doi: 10.1371/journal.pone.0013247. PubMed DOI PMC

Abd Elmageed Z.Y., Yang Y., Thomas R., Ranjan M., Mondal D., Moroz K., Fang Z., Rezk B.M., Moparty K., Sikka S.C., et al. Neoplastic Reprogramming of Patient-Derived Adipose Stem Cells by Prostate Cancer Cell-Associated Exosomes: Tumor Exosomes Trigger Stem Cell Transformation. Stem Cells. 2014;32:983–997. doi: 10.1002/stem.1619. PubMed DOI PMC

Ostenfeld M.S., Jeppesen D.K., Laurberg J.R., Boysen A.T., Bramsen J.B., Primdal-Bengtson B., Hendrix A., Lamy P., Dagnaes-Hansen F., Rasmussen M.H., et al. Cellular Disposal of miR23b by RAB27-Dependent Exosome Release Is Linked to Acquisition of Metastatic Properties. Cancer Res. 2014;74:5758–5771. doi: 10.1158/0008-5472.CAN-13-3512. PubMed DOI

Putz U., Howitt J., Doan A., Goh C.-P., Low L.-H., Silke J., Tan S.-S. The Tumor Suppressor PTEN Is Exported in Exosomes and Has Phosphatase Activity in Recipient Cells. Sci. Signal. 2012;5:ra70. doi: 10.1126/scisignal.2003084. PubMed DOI

Meehan K., Vella L.J. The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit. Rev. Clin. Lab. Sci. 2016;53:121–131. doi: 10.3109/10408363.2015.1092496. PubMed DOI

Xiao H., Lässer C., Shelke G.V., Wang J., Rådinger M., Lunavat T.R., Malmhäll C., Lin L.H., Li J., Li L., et al. Mast cell exosomes promote lung adenocarcinoma cell proliferation—Role of KIT-stem cell factor signaling. Cell Commun. Signal. 2014;12:64. doi: 10.1186/s12964-014-0064-8. PubMed DOI PMC

Li C. CD97 promotes gastric cancer cell proliferation and invasion through exosome-mediated MAPK signaling pathway. World J. Gastroenterol. WJG. 2015;21:6215. doi: 10.3748/wjg.v21.i20.6215. PubMed DOI PMC

Qu J.-L., Qu X.-J., Zhao M.-F., Teng Y.-E., Zhang Y., Hou K.-Z., Jiang Y.-H., Yang X.-H., Liu Y.-P. Gastric cancer exosomes promote tumour cell proliferation through PI3K/Akt and MAPK/ERK activation. Dig. Liver Dis. 2009;41:875–880. doi: 10.1016/j.dld.2009.04.006. PubMed DOI

Vella L.J., Behren A., Coleman B., Greening D.W., Hill A.F., Cebon J. Intercellular Resistance to BRAF Inhibition Can Be Mediated by Extracellular Vesicle–Associated PDGFRβ. Neoplasia. 2017;19:932–940. doi: 10.1016/j.neo.2017.07.002. PubMed DOI PMC

Yang L., Wu X.-H., Wang D., Luo C.-L., Chen L.-X. Bladder cancer cell-derived exosomes inhibit tumor cell apoptosis and induce cell proliferation in vitro. Mol. Med. Rep. 2013;8:1272–1278. doi: 10.3892/mmr.2013.1634. PubMed DOI

Setti M., Osti D., Richichi C., Ortensi B., Del Bene M., Fornasari L., Beznoussenko G., Mironov A., Rappa G., Cuomo A., et al. Extracellular vesicle-mediated transfer of CLIC1 protein is a novel mechanism for the regulation of glioblastoma growth. Oncotarget. 2015;6:31413–31427. doi: 10.18632/oncotarget.5105. PubMed DOI PMC

The Australian Prostate Cancer Collaboration BioResource. Soekmadji C., Riches J.D., Russell P.J., Ruelcke J.E., McPherson S., Wang C., Hovens C.M., Corcoran N.M., Hill M.M., et al. Modulation of paracrine signaling by CD9 positive small extracellular vesicles mediates cellular growth of androgen deprived prostate cancer. Oncotarget. 2017;8:52237–52255. doi: 10.18632/oncotarget.11111. PubMed DOI PMC

Matsumoto A., Takahashi Y., Nishikawa M., Sano K., Morishita M., Charoenviriyakul C., Saji H., Takakura Y. Accelerated growth of B16 BL 6 tumor in mice through efficient uptake of their own exosomes by B16 BL 6 cells. Cancer Sci. 2017;108:1803–1810. doi: 10.1111/cas.13310. PubMed DOI PMC

Liu M.X., Liao J., Xie M., Gao Z.K., Wang X.H., Zhang Y., Shang M.H., Yin L.H., Pu Y.P., Liu R. miR-93-5p Transferred by Exosomes Promotes the Proliferation of Esophageal Cancer Cells via Intercellular Communication by Targeting PTEN. Biomed. Environ. Sci. 2018;31:171–185. doi: 10.3967/bes2018.023. PubMed DOI

Teng Y., Ren Y., Hu X., Mu J., Samykutty A., Zhuang X., Deng Z., Kumar A., Zhang L., Merchant M.L., et al. MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nat. Commun. 2017;8:14448. doi: 10.1038/ncomms14448. PubMed DOI PMC

Lee J.C., Zhao J.-T., Gundara J., Serpell J., Bach L.A., Sidhu S. Papillary thyroid cancer–derived exosomes contain miRNA-146b and miRNA-222. J. Surg. Res. 2015;196:39–48. doi: 10.1016/j.jss.2015.02.027. PubMed DOI

Graner M.W., Schnell S., Olin M.R. Tumor-derived exosomes, microRNAs, and cancer immune suppression. Semin. Immunopathol. 2018;40:505–515. doi: 10.1007/s00281-018-0689-6. PubMed DOI PMC

Lässer C., Théry C., Buzás E.I., Mathivanan S., Zhao W., Gho Y.S., Lötvall J. The International Society for Extracellular Vesicles launches the first massive open online course on extracellular vesicles. J. Extracell. Vesicles. 2016;5:34299. doi: 10.3402/jev.v5.34299. PubMed DOI PMC

Kogure T., Lin W.-L., Yan I.K., Braconi C., Patel T. Intercellular nanovesicle-mediated microRNA transfer: A mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 2011;54:1237–1248. doi: 10.1002/hep.24504. PubMed DOI PMC

You Y., Shan Y., Chen J., Yue H., You B., Shi S., Li X., Cao X. Matrix metalloproteinase 13-containing exosomes promote nasopharyngeal carcinoma metastasis. Cancer Sci. 2015;106:1669–1677. doi: 10.1111/cas.12818. PubMed DOI PMC

Ramteke A., Ting H., Agarwal C., Mateen S., Somasagara R., Hussain A., Graner M., Frederick B., Agarwal R., Deep G. Exosomes secreted under hypoxia enhance invasiveness and stemness of prostate cancer cells by targeting adherens junction molecules: Hypoxic-exosomes role in pca aggressiveness. Mol. Carcinog. 2015;54:554–565. doi: 10.1002/mc.22124. PubMed DOI PMC

Franzen C.A., Blackwell R.H., Todorovic V., Greco K.A., Foreman K.E., Flanigan R.C., Kuo P.C., Gupta G.N. Urothelial cells undergo epithelial-to-mesenchymal transition after exposure to muscle invasive bladder cancer exosomes. Oncogenesis. 2015;4:e163. doi: 10.1038/oncsis.2015.21. PubMed DOI PMC

Rahman M.A., Barger J.F., Lovat F., Gao M., Otterson G.A., Nana-Sinkam P. Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget. 2016;7:54852–54866. doi: 10.18632/oncotarget.10243. PubMed DOI PMC

Fabbri M., Paone A., Calore F., Galli R., Croce C.M. A new role for microRNAs, as ligands of Toll-like receptors. RNA Biol. 2013;10:169–174. doi: 10.4161/rna.23144. PubMed DOI PMC

Kim C.W., Lee H.M., Lee T.H., Kang C., Kleinman H.K., Gho Y.S. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res. 2002;62:6312–6317. PubMed

Kholia S., Ranghino A., Garnieri P., Lopatina T., Deregibus M.C., Rispoli P., Brizzi M.F., Camussi G. Extracellular vesicles as new players in angiogenesis. Vasc. Pharmacol. 2016;86:64–70. doi: 10.1016/j.vph.2016.03.005. PubMed DOI

Lombardo G., Dentelli P., Togliatto G., Rosso A., Gili M., Gallo S., Deregibus M.C., Camussi G., Brizzi M.F. Activated Stat5 trafficking Via Endothelial Cell-derived Extracellular Vesicles Controls IL-3 Pro-angiogenic Paracrine Action. Sci. Rep. 2016;6:25689. doi: 10.1038/srep25689. PubMed DOI PMC

van Balkom B.W.M., de Jong O.G., Smits M., Brummelman J., den Ouden K., de Bree P.M., van Eijndhoven M.A.J., Pegtel D.M., Stoorvogel W., Würdinger T., et al. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 2013;121:3997–4006. doi: 10.1182/blood-2013-02-478925. PubMed DOI

Teng X., Chen L., Chen W., Yang J., Yang Z., Shen Z. Mesenchymal Stem Cell-Derived Exosomes Improve the Microenvironment of Infarcted Myocardium Contributing to Angiogenesis and Anti-Inflammation. Cell Physiol. Biochem. 2015;37:2415–2424. doi: 10.1159/000438594. PubMed DOI

Zeng Z., Li Y., Pan Y., Lan X., Song F., Sun J., Zhou K., Liu X., Ren X., Wang F., et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat. Commun. 2018;9:5395. doi: 10.1038/s41467-018-07810-w. PubMed DOI PMC

Fang J., Zhang Z., Shang L., Luo Y., Lin Y., Yuan Y., Zhuang S. Hepatoma cell-secreted exosomal microRNA-103 increases vascular permeability and promotes metastasis by targeting junction proteins. Hepatology. 2018;68:1459–1475. doi: 10.1002/hep.29920. PubMed DOI

Lawson J., Dickman C., MacLellan S., Towle R., Jabalee J., Lam S., Garnis C. Selective secretion of microRNAs from lung cancer cells via extracellular vesicles promotes CAMK1D-mediated tube formation in endothelial cells. Oncotarget. 2017;8:83913–83924. doi: 10.18632/oncotarget.19996. PubMed DOI PMC

Zhuang G., Wu X., Jiang Z., Kasman I., Yao J., Guan Y., Oeh J., Modrusan Z., Bais C., Sampath D., et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012;31:3513–3523. doi: 10.1038/emboj.2012.183. PubMed DOI PMC

Qu J., Lu D., Guo H., Miao W., Wu G., Zhou M. MicroRNA-9 regulates osteoblast differentiation and angiogenesis via the AMPK signaling pathway. Mol. Cell. Biochem. 2016;411:23–33. doi: 10.1007/s11010-015-2565-1. PubMed DOI

Simon T., Pinioti S., Schellenberger P., Rajeeve V., Wendler F., Cutillas P.R., King A., Stebbing J., Giamas G. Shedding of bevacizumab in tumour cells-derived extracellular vesicles as a new therapeutic escape mechanism in glioblastoma. Mol. Cancer. 2018;17:132. doi: 10.1186/s12943-018-0878-x. PubMed DOI PMC

Feng Q., Zhang C., Lum D., Druso J.E., Blank B., Wilson K.F., Welm A., Antonyak M.A., Cerione R.A. A class of extracellular vesicles from breast cancer cells activates VEGF receptors and tumour angiogenesis. Nat. Commun. 2017;8:14450. doi: 10.1038/ncomms14450. PubMed DOI PMC

Qu Z., Wu J., Wu J., Luo D., Jiang C., Ding Y. Exosomes derived from HCC cells induce sorafenib resistance in hepatocellular carcinoma both in vivo and in vitro. J. Exp. Clin. Cancer Res. 2016;35:159. doi: 10.1186/s13046-016-0430-z. PubMed DOI PMC

Takahashi K., Yan I.K., Kogure T., Haga H., Patel T. Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellular cancer. FEBS Open Bio. 2014;4:458–467. doi: 10.1016/j.fob.2014.04.007. PubMed DOI PMC

Stone L. Exosome transmission of sunitinib resistance. Nat. Rev. Urol. 2016;13:297. doi: 10.1038/nrurol.2016.88. PubMed DOI

Wieckowski E.U., Visus C., Szajnik M., Szczepanski M.J., Storkus W.J., Whiteside T.L. Tumor-Derived Microvesicles Promote Regulatory T Cell Expansion and Induce Apoptosis in Tumor-Reactive Activated CD8 + T Lymphocytes. J. Immunol. 2009;183:3720–3730. doi: 10.4049/jimmunol.0900970. PubMed DOI PMC

Vu L.T., Peng B., Zhang D.X., Ma V., Mathey-Andrews C.A., Lam C.K., Kiomourtzis T., Jin J., McReynolds L., Huang L., et al. Tumor-secreted extracellular vesicles promote the activation of cancer-associated fibroblasts via the transfer of microRNA-125b. J. Extracell. Vesicles. 2019;8:1599680. doi: 10.1080/20013078.2019.1599680. PubMed DOI PMC

Poggio M., Hu T., Pai C.-C., Chu B., Belair C.D., Chang A., Montabana E., Lang U.E., Fu Q., Fong L., et al. Suppression of Exosomal PD-L1 Induces Systemic Anti-tumor Immunity and Memory. Cell. 2019;177:414–427.e13. doi: 10.1016/j.cell.2019.02.016. PubMed DOI PMC

Del Re M., Marconcini R., Pasquini G., Rofi E., Vivaldi C., Bloise F., Restante G., Arrigoni E., Caparello C., Bianco M.G., et al. PD-L1 mRNA expression in plasma-derived exosomes is associated with response to anti-PD-1 antibodies in melanoma and NSCLC. Br. J. Cancer. 2018;118:820–824. doi: 10.1038/bjc.2018.9. PubMed DOI PMC

Theodoraki M.-N., Yerneni S., Gooding W.E., Ohr J., Clump D.A., Bauman J.E., Ferris R.L., Whiteside T.L. Circulating exosomes measure responses to therapy in head and neck cancer patients treated with cetuximab, ipilimumab, and IMRT. OncoImmunology. 2019;8:e1593805. doi: 10.1080/2162402X.2019.1593805. PubMed DOI PMC

Yen E.-Y., Miaw S.-C., Yu J.-S., Lai I.-R. Exosomal TGF-β1 is correlated with lymphatic metastasis of gastric cancers. Am. J. Cancer Res. 2017;7:2199–2208. PubMed PMC

Que R., Lin C., Ding G., Wu Z., Cao L. Increasing the immune activity of exosomes: The effect of miRNA-depleted exosome proteins on activating dendritic cell/cytokine-induced killer cells against pancreatic cancer. J. Zhejiang Univ. Sci. B. 2016;17:352–360. doi: 10.1631/jzus.B1500305. PubMed DOI PMC

Feitelson M.A., Arzumanyan A., Kulathinal R.J., Blain S.W., Holcombe R.F., Mahajna J., Marino M., Martinez-Chantar M.L., Nawroth R., Sanchez-Garcia I., et al. Sustained proliferation in cancer: Mechanisms and novel therapeutic targets. Semin. Cancer Biol. 2015;35:S25–S54. doi: 10.1016/j.semcancer.2015.02.006. PubMed DOI PMC

Yin Y., Cai X., Chen X., Liang H., Zhang Y., Li J., Wang Z., Chen X., Zhang W., Yokoyama S., et al. Tumor-secreted miR-214 induces regulatory T cells: A major link between immune evasion and tumor growth. Cell Res. 2014;24:1164–1180. doi: 10.1038/cr.2014.121. PubMed DOI PMC

Cesi G., Philippidou D., Kozar I., Kim Y.J., Bernardin F., Van Niel G., Wienecke-Baldacchino A., Felten P., Letellier E., Dengler S., et al. A new ALK isoform transported by extracellular vesicles confers drug resistance to melanoma cells. Mol. Cancer. 2018;17:145. doi: 10.1186/s12943-018-0886-x. PubMed DOI PMC

Kalra H., Gangoda L., Fonseka P., Chitti S.V., Liem M., Keerthikumar S., Samuel M., Boukouris S., Al Saffar H., Collins C., et al. Extracellular vesicles containing oncogenic mutant β-catenin activate Wnt signalling pathway in the recipient cells. J. Extracell. Vesicles. 2019;8:1690217. doi: 10.1080/20013078.2019.1690217. PubMed DOI PMC

Yadav A.K., Desai N.S. Cancer Stem Cells: Acquisition, Characteristics, Therapeutic Implications, Targeting Strategies and Future Prospects. Stem Cell Rev. Rep. 2019;15:331–355. doi: 10.1007/s12015-019-09887-2. PubMed DOI

Wang L., Yang G., Zhao D., Wang J., Bai Y., Peng Q., Wang H., Fang R., Chen G., Wang Z., et al. CD103-positive CSC exosome promotes EMT of clear cell renal cell carcinoma: Role of remote MiR-19b-3p. Mol. Cancer. 2019;18:86. doi: 10.1186/s12943-019-0997-z. PubMed DOI PMC

Sun Z., Wang L., Dong L., Wang X. Emerging role of exosome signalling in maintaining cancer stem cell dynamic equilibrium. J. Cell Mol. Med. 2018;22:3719–3728. doi: 10.1111/jcmm.13676. PubMed DOI PMC

Gabrusiewicz K., Li X., Wei J., Hashimoto Y., Marisetty A.L., Ott M., Wang F., Hawke D., Yu J., Healy L.M., et al. Glioblastoma stem cell-derived exosomes induce M2 macrophages and PD-L1 expression on human monocytes. OncoImmunology. 2018;7:e1412909. doi: 10.1080/2162402X.2017.1412909. PubMed DOI PMC

Hardin H., Helein H., Meyer K., Robertson S., Zhang R., Zhong W., Lloyd R.V. Thyroid cancer stem-like cell exosomes: Regulation of EMT via transfer of lncRNAs. Lab. Invest. 2018;98:1133–1142. doi: 10.1038/s41374-018-0065-0. PubMed DOI PMC

Hwang W.-L., Lan H.-Y., Cheng W.-C., Huang S.-C., Yang M.-H. Tumor stem-like cell-derived exosomal RNAs prime neutrophils for facilitating tumorigenesis of colon cancer. J. Hematol. Oncol. 2019;12:10. doi: 10.1186/s13045-019-0699-4. PubMed DOI PMC

Bouvy C., Wannez A., Laloy J., Chatelain C., Dogné J.-M. Transfer of multidrug resistance among acute myeloid leukemia cells via extracellular vesicles and their microRNA cargo. Leuk. Res. 2017;62:70–76. doi: 10.1016/j.leukres.2017.09.014. PubMed DOI

Aung T., Chapuy B., Vogel D., Wenzel D., Oppermann M., Lahmann M., Weinhage T., Menck K., Hupfeld T., Koch R., et al. Exosomal evasion of humoral immunotherapy in aggressive B-cell lymphoma modulated by ATP-binding cassette transporter A3. Proc. Natl. Acad. Sci. USA. 2011;108:15336–15341. doi: 10.1073/pnas.1102855108. PubMed DOI PMC

Bebawy M., Combes V., Lee E., Jaiswal R., Gong J., Bonhoure A., Grau G.E.R. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia. 2009;23:1643–1649. doi: 10.1038/leu.2009.76. PubMed DOI

Lu J.F., Luk F., Gong J., Jaiswal R., Grau G.E.R., Bebawy M. Microparticles mediate MRP1 intercellular transfer and the re-templating of intrinsic resistance pathways. Pharmacol. Res. 2013;76:77–83. doi: 10.1016/j.phrs.2013.07.009. PubMed DOI

Lu J.F., Pokharel D., Bebawy M. A novel mechanism governing the transcriptional regulation of ABC transporters in MDR cancer cells. Drug Deliv. Transl. Res. 2017;7:276–285. doi: 10.1007/s13346-016-0353-4. PubMed DOI

Dong Y., Pan Q., Jiang L., Chen Z., Zhang F., Liu Y., Xing H., Shi M., Li J., Li X., et al. Tumor endothelial expression of P-glycoprotein upon microvesicular transfer of TrpC5 derived from adriamycin-resistant breast cancer cells. Biochem. Biophys. Res. Commun. 2014;446:85–90. doi: 10.1016/j.bbrc.2014.02.076. PubMed DOI

Zhang Q., Liu R.-X., Chan K.-W., Hu J., Zhang J., Wei L., Tan H., Yang X., Liu H. Exosomal transfer of p-STAT3 promotes acquired 5-FU resistance in colorectal cancer cells. J. Exp. Clin. Cancer Res. 2019;38:320. doi: 10.1186/s13046-019-1314-9. PubMed DOI PMC

Zhao K., Wang Z., Li X., Liu J., Tian L., Chen J. Exosome-mediated transfer of CLIC1 contributes to the vincristine-resistance in gastric cancer. Mol. Cell Biochem. 2019;462:97–105. doi: 10.1007/s11010-019-03613-9. PubMed DOI

Gu Y.Y., Yu J., Zhang J.F., Wang C. Suppressing the secretion of exosomal miR-19b by gw4869 could regulate oxaliplatin sensitivity in colorectal cancer. Neoplasma. 2019;66:39–45. doi: 10.4149/neo_2018_180306N155. PubMed DOI

Ma Y., Yuwen D., Chen J., Zheng B., Gao J., Fan M., Xue W., Wang Y., Li W., Shu Y., et al. Exosomal Transfer Of Cisplatin-Induced miR-425-3p Confers Cisplatin Resistance In NSCLC Through Activating Autophagy. Int. J. Nanomed. 2019;14:8121–8132. doi: 10.2147/IJN.S221383. PubMed DOI PMC

Wu H., Zhou J., Mei S., Wu D., Mu Z., Chen B., Xie Y., Ye Y., Liu J. Circulating exosomal microRNA-96 promotes cell proliferation, migration and drug resistance by targeting LMO7. J. Cell. Mol. Med. 2017;21:1228–1236. doi: 10.1111/jcmm.13056. PubMed DOI PMC

Wang J., Lv B., Su Y., Wang X., Bu J., Yao L. Exosome-Mediated Transfer of lncRNA HOTTIP Promotes Cisplatin Resistance in Gastric Cancer Cells by Regulating HMGA1/miR-218 Axis. OncoTargets Therapy. 2019;12:11325–11338. doi: 10.2147/OTT.S231846. PubMed DOI PMC

Cao Y.-L., Zhuang T., Xing B.-H., Li N., Li Q. Exosomal DNMT1 mediates cisplatin resistance in ovarian cancer. Cell Biochem. Funct. 2017;35:296–303. doi: 10.1002/cbf.3276. PubMed DOI

Akao Y., Khoo F., Kumazaki M., Shinohara H., Miki K., Yamada N. Extracellular Disposal of Tumor-Suppressor miRs-145 and -34a via Microvesicles and 5-FU Resistance of Human Colon Cancer Cells. Int. J. Mol. Sci. 2014;15:1392–1401. doi: 10.3390/ijms15011392. PubMed DOI PMC

Yu D., Wu Y., Zhang X., Lv M., Chen W., Chen X., Yang S., Shen H., Zhong S., Tang J., et al. Exosomes from adriamycin-resistant breast cancer cells transmit drug resistance partly by delivering miR-222. Tumor Biol. 2016;37:3227–3235. doi: 10.1007/s13277-015-4161-0. PubMed DOI

Wei Y., Lai X., Yu S., Chen S., Ma Y., Zhang Y., Li H., Zhu X., Yao L., Zhang J. Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells. Breast Cancer Res. Treat. 2014;147:423–431. doi: 10.1007/s10549-014-3037-0. PubMed DOI

Mikamori M., Yamada D., Eguchi H., Hasegawa S., Kishimoto T., Tomimaru Y., Asaoka T., Noda T., Wada H., Kawamoto K., et al. MicroRNA-155 Controls Exosome Synthesis and Promotes Gemcitabine Resistance in Pancreatic Ductal Adenocarcinoma. Sci. Rep. 2017;7:42339. doi: 10.1038/srep42339. PubMed DOI PMC

de Souza P.S., Cruz A.L.S., Viola J.P.B., Maia R.C. Microparticles induce multifactorial resistance through oncogenic pathways independently of cancer cell type. Cancer Sci. 2015;106:60–68. doi: 10.1111/cas.12566. PubMed DOI PMC

Yin J., Zeng A., Zhang Z., Shi Z., Yan W., You Y. Exosomal transfer of miR-1238 contributes to temozolomide-resistance in glioblastoma. EBioMedicine. 2019;42:238–251. doi: 10.1016/j.ebiom.2019.03.016. PubMed DOI PMC

Powers M.P. The ever-changing world of gene fusions in cancer: A secondary gene fusion and progression. Oncogene. 2019;38:7197–7199. doi: 10.1038/s41388-019-1057-2. PubMed DOI

Li Q., Zhong Z., Zeng C., Meng L., Li C., Luo Y., Wang H., Li W., Wang J., Cheng F., et al. A clinical observation of Chinese chronic myelogenous leukemia patients after discontinuation of tyrosine kinase inhibitors. Oncotarget. 2016;7 doi: 10.18632/oncotarget.11281. PubMed DOI PMC

Kumar-Sinha C., Tomlins S.A., Chinnaiyan A.M. Recurrent gene fusions in prostate cancer. Nat. Rev. Cancer. 2008;8:497–511. doi: 10.1038/nrc2402. PubMed DOI PMC

Fujita K., Nonomura N. Urinary biomarkers of prostate cancer. Int. J. Urol. 2018;25:770–779. doi: 10.1111/iju.13734. PubMed DOI

Wong C.-H., Chen Y.-C. Clinical significance of exosomes as potential biomarkers in cancer. World J. Clin. Cases. 2019;7:171–190. doi: 10.12998/wjcc.v7.i2.171. PubMed DOI PMC

Schey K.L., Luther J.M., Rose K.L. Proteomics characterization of exosome cargo. Methods. 2015;87:75–82. doi: 10.1016/j.ymeth.2015.03.018. PubMed DOI PMC

Mohammadi S., Yousefi F., Shabaninejad Z., Movahedpour A., Mahjoubin Tehran M., Shafiee A., Moradizarmehri S., Hajighadimi S., Savardashtaki A., Mirzaei H. Exosomes and cancer: From oncogenic roles to therapeutic applications. IUBMB Life. 2020;72:724–748. doi: 10.1002/iub.2182. PubMed DOI

Luan X., Sansanaphongpricha K., Myers I., Chen H., Yuan H., Sun D. Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharm. Sin. 2017;38:754–763. doi: 10.1038/aps.2017.12. PubMed DOI PMC

Liang G., Kan S., Zhu Y., Feng S., Feng W., Gao S. Engineered exosome-mediated delivery of functionally active miR-26a and its enhanced suppression effect in HepG2 cells. Int. J. Nanomed. 2018;13:585–599. doi: 10.2147/IJN.S154458. PubMed DOI PMC

Vader P., Mol E.A., Pasterkamp G., Schiffelers R.M. Extracellular vesicles for drug delivery. Adv. Drug Deliv. Rev. 2016;106:148–156. doi: 10.1016/j.addr.2016.02.006. PubMed DOI

Li Y., Zheng Q., Bao C., Li S., Guo W., Zhao J., Chen D., Gu J., He X., Huang S. Circular RNA is enriched and stable in exosomes: A promising biomarker for cancer diagnosis. Cell Res. 2015;25:981–984. doi: 10.1038/cr.2015.82. PubMed DOI PMC

Wiklander O.P.B., Nordin J.Z., O’Loughlin A., Gustafsson Y., Corso G., Mäger I., Vader P., Lee Y., Sork H., Seow Y., et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J. Extracell. Vesicles. 2015;4:26316. doi: 10.3402/jev.v4.26316. PubMed DOI PMC

Johnsen K.B., Gudbergsson J.M., Skov M.N., Pilgaard L., Moos T., Duroux M. A comprehensive overview of exosomes as drug delivery vehicles—Endogenous nanocarriers for targeted cancer therapy. Biochim. Biophys. Acta (BBA) Rev. Cancer. 2014;1846:75–87. doi: 10.1016/j.bbcan.2014.04.005. PubMed DOI

Ma J., Zhang Y., Tang K., Zhang H., Yin X., Li Y., Xu P., Sun Y., Ma R., Ji T., et al. Reversing drug resistance of soft tumor-repopulating cells by tumor cell-derived chemotherapeutic microparticles. Cell Res. 2016;26:713–727. doi: 10.1038/cr.2016.53. PubMed DOI PMC

Parolini I., Federici C., Raggi C., Lugini L., Palleschi S., De Milito A., Coscia C., Iessi E., Logozzi M., Molinari A., et al. Microenvironmental pH Is a Key Factor for Exosome Traffic in Tumor Cells. J. Biol. Chem. 2009;284:34211–34222. doi: 10.1074/jbc.M109.041152. PubMed DOI PMC

Kim M.S., Haney M.J., Zhao Y., Mahajan V., Deygen I., Klyachko N.L., Inskoe E., Piroyan A., Sokolsky M., Okolie O., et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomed. Nanotechnol. Biol. Med. 2016;12:655–664. doi: 10.1016/j.nano.2015.10.012. PubMed DOI PMC

Qiao L., Hu S., Huang K., Su T., Li Z., Vandergriff A., Cores J., Dinh P.-U., Allen T., Shen D., et al. Tumor cell-derived exosomes home to their cells of origin and can be used as Trojan horses to deliver cancer drugs. Theranostics. 2020;10:3474–3487. doi: 10.7150/thno.39434. PubMed DOI PMC

Hao D., Li Y., Zhao G., Zhang M. Soluble fms-like tyrosine kinase-1-enriched exosomes suppress the growth of small cell lung cancer by inhibiting endothelial cell migration. Thorac. Cancer. 2019;10:1962–1972. doi: 10.1111/1759-7714.13175. PubMed DOI PMC

Liu T., Zhang X., Du L., Wang Y., Liu X., Tian H., Wang L., Li P., Zhao Y., Duan W., et al. Exosome-transmitted miR-128-3p increase chemosensitivity of oxaliplatin-resistant colorectal cancer. Mol. Cancer. 2019;18:43. doi: 10.1186/s12943-019-0981-7. PubMed DOI PMC

Wan F.-Z., Chen K.-H., Sun Y.-C., Chen X.-C., Liang R.-B., Chen L., Zhu X.-D. Exosomes overexpressing miR-34c inhibit malignant behavior and reverse the radioresistance of nasopharyngeal carcinoma. J. Transl. Med. 2020;18:12. doi: 10.1186/s12967-019-02203-z. PubMed DOI PMC

Kobayashi M., Sawada K., Miyamoto M., Shimizu A., Yamamoto M., Kinose Y., Nakamura K., Kawano M., Kodama M., Hashimoto K., et al. Exploring the potential of engineered exosomes as delivery systems for tumor-suppressor microRNA replacement therapy in ovarian cancer. Biochem. Biophys. Res. Commun. 2020;527:153–161. doi: 10.1016/j.bbrc.2020.04.076. PubMed DOI

Tian H., Li W. Dendritic cell-derived exosomes for cancer immunotherapy: Hope and challenges. Ann. Transl. Med. 2017;5:221. doi: 10.21037/atm.2017.02.23. PubMed DOI PMC

Liu C., Guo J., Tian F., Yang N., Yan F., Ding Y., Wei J., Hu G., Nie G., Sun J. Field-Free Isolation of Exosomes from Extracellular Vesicles by Microfluidic Viscoelastic Flows. ACS Nano. 2017;11:6968–6976. doi: 10.1021/acsnano.7b02277. PubMed DOI

Chen T., Arslan F., Yin Y., Tan S., Lai R., Choo A., Padmanabhan J., Lee C., de Kleijn D.P., Lim S. Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J. Transl. Med. 2011;9:47. doi: 10.1186/1479-5876-9-47. PubMed DOI PMC

Lener T., Gimona M., Aigner L., Börger V., Buzas E., Camussi G., Chaput N., Chatterjee D., Court F.A., del Portillo H.A., et al. Applying extracellular vesicles based therapeutics in clinical trials—An ISEV position paper. J. Extracell. Vesicles. 2015;4:30087. doi: 10.3402/jev.v4.30087. PubMed DOI PMC

Nie W., Wu G., Zhang J., Huang L., Ding J., Jiang A., Zhang Y., Liu Y., Li J., Pu K., et al. Responsive Exosome Nano-bioconjugates for Synergistic Cancer Therapy. Angew. Chem. Int. Ed. 2020;59:2018–2022. doi: 10.1002/anie.201912524. PubMed DOI

Yong T., Zhang X., Bie N., Zhang H., Zhang X., Li F., Hakeem A., Hu J., Gan L., Santos H.A., et al. Tumor exosome-based nanoparticles are efficient drug carriers for chemotherapy. Nat. Commun. 2019;10:3838. doi: 10.1038/s41467-019-11718-4. PubMed DOI PMC

Bai L., Liu Y., Guo K., Zhang K., Liu Q., Wang P., Wang X. Ultrasound Facilitates Naturally Equipped Exosomes Derived from Macrophages and Blood Serum for Orthotopic Glioma Treatment. ACS Appl. Mater. Interfaces. 2019;11:14576–14587. doi: 10.1021/acsami.9b00893. PubMed DOI

Zhang K.-L., Wang Y.-J., Sun J., Zhou J., Xing C., Huang G., Li J., Yang H. Artificial chimeric exosomes for anti-phagocytosis and targeted cancer therapy. Chem. Sci. 2019;10:1555–1561. doi: 10.1039/C8SC03224F. PubMed DOI PMC

Pomatto M.A.C., Bussolati B., D’Antico S., Ghiotto S., Tetta C., Brizzi M.F., Camussi G. Improved Loading of Plasma-Derived Extracellular Vesicles to Encapsulate Antitumor miRNAs. Mol. Ther. Methods Clin. Dev. 2019;13:133–144. doi: 10.1016/j.omtm.2019.01.001. PubMed DOI PMC

Gomari H., Forouzandeh Moghadam M., Soleimani M. Targeted cancer therapy using engineered exosome as a natural drug delivery vehicle. OncoTargets Therapy. 2018;11:5753–5762. doi: 10.2147/OTT.S173110. PubMed DOI PMC

Limoni S.K., Moghadam M.F., Moazzeni S.M., Gomari H., Salimi F. Engineered Exosomes for Targeted Transfer of siRNA to HER2 Positive Breast Cancer Cells. Appl. Biochem. Biotechnol. 2019;187:352–364. doi: 10.1007/s12010-018-2813-4. PubMed DOI

O’Brien K.P., Khan S., Gilligan K.E., Zafar H., Lalor P., Glynn C., O’Flatharta C., Ingoldsby H., Dockery P., De Bhulbh A., et al. Employing mesenchymal stem cells to support tumor-targeted delivery of extracellular vesicle (EV)-encapsulated microRNA-379. Oncogene. 2018;37:2137–2149. doi: 10.1038/s41388-017-0116-9. PubMed DOI

Kim M.S., Haney M.J., Zhao Y., Yuan D., Deygen I., Klyachko N.L., Kabanov A.V., Batrakova E.V. Engineering macrophage-derived exosomes for targeted paclitaxel delivery to pulmonary metastases: In vitro and in vivo evaluations. Nanomed. Nanotechnol. Biol. Med. 2018;14:195–204. doi: 10.1016/j.nano.2017.09.011. PubMed DOI

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;546:498–503. doi: 10.1038/nature22341. PubMed DOI PMC

Bellavia D., Raimondo S., Calabrese G., Forte S., Cristaldi M., Patinella A., Memeo L., Manno M., Raccosta S., Diana P., et al. Interleukin 3-receptor targeted exosomes inhibit in vitro and in vivo Chronic Myelogenous Leukemia cell growth. Theranostics. 2017;7:1333–1345. doi: 10.7150/thno.17092. PubMed DOI PMC

Morishita M., Takahashi Y., Matsumoto A., Nishikawa M., Takakura Y. Exosome-based tumor antigens–adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA. Biomaterials. 2016;111:55–65. doi: 10.1016/j.biomaterials.2016.09.031. PubMed DOI

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;35:2383–2390. doi: 10.1016/j.biomaterials.2013.11.083. PubMed DOI

Ohno S., Takanashi M., Sudo K., Ueda S., Ishikawa A., Matsuyama N., Fujita K., Mizutani T., Ohgi T., Ochiya T., et al. Systemically Injected Exosomes Targeted to EGFR Deliver Antitumor MicroRNA to Breast Cancer Cells. Mol. Ther. 2013;21:185–191. doi: 10.1038/mt.2012.180. PubMed DOI PMC

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