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Focus on Bio-inspired nanomaterials

Latest advances in extracellular vesicles: from bench to bedside

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Pages 746-757 | Received 18 Jan 2019, Accepted 06 Jun 2019, Published online: 08 Jul 2019

References

  • Denzer K, Kleijmeer M, Heijnen H, et al. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;19:3365–3374.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373–383.
  • Yanez-Mo M, Siljander P, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.
  • Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 2015;25:364–372.
  • Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.
  • Kosaka N, Yoshioka Y, Hagiwara K, et al. Trash or Treasure: extracellular microRNAs and cell-to-cell communication. Front Genet. 2013;4:173.
  • Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659.
  • Pegtel M, Cosmopoulos K, Thorley-Lawson A, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107:6328–6333.
  • Kosaka N, Iguchi H, Yoshioka Y, et al. Competitive interactions of cancer cells and normal cells via secretory microRNAs. J Biol Chem. 2012;287:1397–1405.
  • Zhang Y, Liu D, Chen X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–144.
  • Kosaka N, Iguchi H, Yoshioka Y, et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285:17442–17452.
  • Takahashi A, Okada R, Nagao K, et al. Exosomes maintain cellular homeostasis by excreting harmful DNA from cells. Nat Commun. 2017;8:15287.
  • Caby MP, Lankar D, Vincendeau-Scherrer C, et al. Exosomal-like vesicles are present in human blood plasma. Int Immunol. 2005;17:879–887.
  • Gonzales PA, Zhou H, Pisitkun T, et al. Isolation and purification of exosomes in urine. Methods Mol Biol. 2010;641:89–99.
  • Palanisamy V, Sharma S, Deshpande A, et al. Nanostructural and transcriptomic analyses of human saliva derived exosomes. PloS One. 2010;5:e8577.
  • Njock MS, Guiot J, Henket MA, et al. Sputum exosomes: promising biomarkers for idiopathic pulmonary fibrosis. Thorax. 2019;74:309–312.
  • Admyre C, Johansson SM, Qazi KR, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol. 2007;179:1969–1978.
  • Poliakov A, Spilman M, Dokland T, et al. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate. 2009;69:159–167.
  • Borroto-Escuela DO, Agnati LF, Bechter K, et al. The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks. Philos Trans R Soc Lond B Biol Sci. 2015;370:1672.
  • Yoshioka Y, Konishi Y, Kosaka N, et al. Comparative marker analysis of extracellular vesicles in different human cancer types. J Extracell Vesicles. 2013;2.
  • Simpson RJ, Lim JW, Moritz RL, et al. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009;6:267–283.
  • Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016 23;113:E968–77.
  • Konoshenko MY, Lekchnov EA, Vlassov AV, et al. Isolation of extracellular vesicles: general methodologies and latest trends. Biomed Res Int. 2018;8545347.
  • Popovic M, Mazzega E, Toffoletto B, et al. Isolation of anti-extra-cellular vesicle single-domain antibodies by direct panning on vesicle-enriched fractions. Microb Cell Fact. 2018;17:6.
  • 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.
  • Gupta S, Rawat S, Arora V, et al. An improvised one-step sucrose cushion ultracentrifugation method for exosome isolation from culture supernatants of mesenchymal stem cells. Stem Cell Res Ther. 2018;9:180.
  • Cai S, Luo B, Jiang P, et al. Immuno-modified superparamagnetic nanoparticles via host–guest interactions for high-purity capture and mild release of exosomes. Nanoscale. 2018;10:14280–14289.
  • Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;3:3–22.
  • Niu Z, Pang RTK, Liu W, et al. Polymer-based precipitation preserves biological activities of extracellular vesicles from an endometrial cell line. PLoS One. 2017;12:e0186534.
  • Xu R, Greening DW, Rai A, et al. Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods. 2015;87:11–25.
  • Xu R, Simpson RJ, Greening DW. A protocol for isolation and proteomic characterization of distinct extracellular vesicle subtypes by sequential centrifugal ultrafiltration. Methods Mol Biol. 2017;1545:91–116.
  • Hung ME, Lenzini SB, Stranford DM, et al. Enrichment of extracellular vesicle subpopulations via affinity chromatography. Methods Mol Biol. 2018;1740:109–124.
  • Li K, Wong DK, Hong KY, et al. Cushioned–density gradient ultracentrifugation (C-DGUC): a refined and high performance method for the isolation, characterization, and use of exosomes. Methods Mol Biol. 2018;1740:69–83.
  • Oeyen E, Van Mol K, Baggerman G, et al. Ultrafiltration and size exclusion chromatography combined with asymmetrical-flow field-flow fractionation for the isolation and characterisation of extracellular vesicles from urine. J Extracell Vesicles. 2018;7:1490143.
  • Livshits MA, Khomyakova E, Evtushenko EG, et al. Isolation of exosomes by differential centrifugation: theoreticalanalysis of a commonly used protocol. Sci Rep. 2015;5:17319.
  • Wataru N, Takeshi Y, Diego D, et al. A novel affinity-based method for the isolation of highly purified extracellular vesicles. Sci Rep. 2016;6:33935.
  • Mengxi W, Yingshi O, Zeyu W, et al. Isolation of exosomes from whole blood by integrating acoustics and microfluidics. Proc Natl Acad Sci U S A. 2017;114:10584–10589.
  • Cui H, Seubert B, Stahl E, et al. Tissue inhibitor of metalloproteinases-1 induces a pro-tumourigenic increase of miR-210 in lung adenocarcinoma cells and their exosomes. Oncogene. 2015;34:3640–3650.
  • Chen X, Zhou J, Li X, et al. Exosomes derived from hypoxic epithelial ovarian cancer cells deliver microRNAs to macrophages and elicit a tumor-promoted phenotype. Cancer Lett. 2018;435:80–91.
  • Treps L, Perret R, Edmond S, et al. Glioblastoma stem-like cells secrete the pro-angiogenic VEGF-A factor in extracellular vesicles. J Extracell Vesicles. 2017;6:1359479.
  • Fang T, Lv H, Lv G, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.
  • Zeng Z, Li Y, Pan Y, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 2018;9:5395.
  • Tominaga N, Kosaka N, Ono M, et al. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun. 2015;6:6716.
  • Shtam T, Naryzhny S, Samsonov R, et al. Plasma exosomes stimulate breast cancer metastasis through surface interactions and activation of FAK signaling. Breast Cancer Res Treat. 2019;174:129–141.
  • Kurtz JM, Spitalier JM, Amalric R. Late breast recurrence after lumpectomy and irradiation. Int J Radiat Oncol Biol Phys. 1983;9:1191–1194.
  • Vallabhaneni KC, Penfornis P, Xing F, et al. Stromal cell extracellular vesicular cargo mediated regulation of breast cancer cell metastasis via ubiquitin conjugating enzyme E2 N pathway. Oncotarget. 2017;8:109861–109876.
  • Sansone P, Savini C, Kurelac I, et al. Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci U S A. 2017;114:E9066–E9075.
  • Ono M, Kosaka N, Tominaga N. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal. 2014;7:ra63.
  • Yu T, Wang X, Zhi T, et al. Delivery of MGMT mRNA to glioma cells by reactive astrocyte-derived exosomes confers a temozolomide resistance phenotype. Cancer Lett. 2018;433:210–220.
  • Labani-Motlagh A, Israelsson P, Ottander U, et al. Differential expression of ligands for NKG2D and DNAM-1 receptors by epithelial ovarian cancer-derived exosomes and its influence on NK cell cytotoxicity. Tumour Biol. 2016;37:5455–5466.
  • Xiao H, Lässer C, Shelke GV, et al. Mast cell exosomes promote lung adenocarcinoma cell proliferation - role of KIT-stem cell factor signaling. Cell Commun Signal. 2014;12:64.
  • Dabbah M, Attar-Schneider O, Tartakover Matalon S, et al. Microvesicles derived from normal and multiple myeloma bone marrow mesenchymal stem cells differentially modulate myeloma cells’ phenotype and translation initiation. Carcinogenesis. 2017;38:708–716.
  • Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560:382–386.
  • Rajkumar SV, Moreau P. Decade in review-haematological cancer: advances in biology and therapy. Nat Rev Clin Oncol. 2014;11:628–630.
  • Vyas N, Yiannakis D, Turner A, et al. Occupational exposure to anti-cancer drugs: A review of effects of new technology. J Oncol Pharm Pract. 2014;20:278–287.
  • Haque S, Whittaker MR, McIntosh MP, et al. Disposition and safety of inhaled biodegradable nanomedicines: opportunities and challenges. Nanomedicine. 2016;12:1703–1724.
  • Sun L, Wu QJ, Peng F, et al. Strategies of polymeric nanoparticles for enhanced internalization in cancer therapy. Colloid Surf B. 2015;135:56–72.
  • Suk JS, Xu QG, Kim N, et al. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv Drug Deliv Rev. 2016;99:28–51.
  • He XY, Liu BY, Wu JL, et al. A Dual Macrophage Targeting Nanovector for Delivery of Oligodeoxynucleotides To Overcome Cancer-Associated Immunosuppression. ACS Appl Mater Interfaces. 2017;9:42566–42576.
  • Parodi A, Molinaro R, Sushnitha M, et al. Bio-inspired engineering of cell- and virus-like nanoparticles for drug delivery. Biomaterials. 2017;147:155–168.
  • Robert MC, Frenette M, Zhou C, et al. A drug delivery system for administration of anti-TNF-α antibody. Transl Vis Sci Technol. 2016;5:11.
  • Fujimori K, Covell DG, Fletcher JE, et al. Modeling analysis of the global and microscopic distribution of immunoglobulin G, F (ab1), and Fab in Tumors. Cancer Res. 1989;49:5656–5663.
  • Hood JL. Post isolation modification of exosomes for nanomedicine applications. Nanomedicine (Lond). 2016;11:1745–1756.
  • Vader P, Mol EA, Pasterkamp G, et al. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev. 2016;106:148–156.
  • Ohno S, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013;21:185–191.
  • 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;18:1606–1614.
  • Li Y, Gao Y, Gong C, et al. A33 antibody-functionalized exosomes for targeted delivery of doxorubicin against colorectal Cancer. Nanomedicine. 2018;14:1973–1985.
  • Hatzidaki E, Vlachou I, Elka A, et al. The use of serum extracellular vesicles for novel small molecule inhibitor cell delivery. Anticancer Drugs. 2019;30:271–280.
  • Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther. 2011;19:1769–1779.
  • 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.
  • Shtam TA, Kovalev RA, Varfolomeeva EY, et al. Exosomes are natural carriers of exogenous siRNA to human cells in vitro. Cell Commun Signal. 2013;11:1186–1196.
  • El-Andaloussi S, Lee Y, Lakhal-Littleton S, et al. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 2012;7:2112–2126.
  • Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341–345.
  • Srivastava A, Amreddy N, Babu A, et al. Nanosomes carrying doxorubicin exhibit potent anticancer activityagainst human lung cancer cells. Sci Rep. 2016;6:38541.
  • Sato YT, Umezaki K, Sawada S, et al. Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep. 2016;6:21933.
  • Zhang KL, Wang YJ, Sun J, et al. Artificial chimeric exosomes for anti-phagocytosis and targeted cancer therapy. Chem Sci. 2018;10:1555–1561.
  • Lin Y, Wu J, Gu W, et al. Exosome–liposome hybrid nanoparticles deliver CRISPR/Cas9 system in MSCs. Adv Sci (Weinh). 2018;5:1700611.
  • Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic kras in pancreatic cancer. Nature. 2017;546:498–503.
  • ClinicalTrials.gov Identifier: NCT03608631 https://clinicaltrials.gov/ct2/show/NCT03608631?term=exosome&cntry=US&state=US%3ATX&rank=1
  • Manca S, Upadhyaya B, Mutai E, et al. Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Sci Rep. 2018;8:11321.
  • Somiya M, Yoshioka Y, Ochiya T. Biocompatibility of highly purified bovine milk-derived extracellular vesicles. J Extracell Vesicles. 2018;7:1440132.
  • Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novelcell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594–600.
  • Mi P, Zhang P, Liu G. Bio-inspired virus-like nanovesicle for effective vaccination. Hum Vaccin Immunother. 2016;12:2090–2091.
  • Zhang P, Chen Y, Zeng Y, et al. Virus-mimetic nanovesicles as a versatile antigen-delivery system. Proc Natl Acad Sci U S A. 2015;112:E6129–38.
  • Chettimada S, Lorenz DR, Misra V, et al. Exosome markers associated with immune activation and oxidative stress in HIV patients on antiretroviral therapy. Sci Rep. 2018;8:7227.
  • Deng L, Jiang W, Wang X, et al. Syntenin regulates hepatitis C virus sensitivity to neutralizing antibody by promoting E2 secretion through exosomes. J Hepatol. 2019;71:52–61.
  • Cocozza F, Menay F, Tsacalian R, et al. Cyclophosphamide enhances the release of tumor exosomes that elicit a specific immune response in vivo in a murine T-cell lymphoma. Vaccine. 2019;37:1565–1576.
  • Yadav DK, Bai X, Yadav RK, et al. Liquid biopsy in pancreatic cancer: the beginning of a new era. Oncotarget. 2018;9:26900–26933.
  • Hallal S, Russell BP, Wei H, et al. Extracellular vesicles from neurosurgical aspirates identifies chaperonin containing TCP1 subunit 6A (CCT6A) as a potential glioblastoma biomarker with prognostic significance, tumor-derived EVs as a novel source of protein biomarkers for cancer diagnosis and monitoring. Proteomics. 2019;19:e1800157.
  • Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–1476.
  • Manier S, Liu CJ, Avet-Loiseau H, et al. Prognostic role of circulating exosomal miRNAs in multiple myeloma. Blood. 2017;129:2429–2436.
  • Yokoi A, Yoshioka Y, Yamamoto Y, et al. Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer. Nat Commun. 2017;8:14470.
  • Zhang P, Crow J, Lella D, et al. Ultrasensitive quantification of tumor mRNAs in extracellular vesicles with an integrated microfluidic digital analysis chip. Lab Chip. 2018;18:3790–3801.
  • Woo HK, Park J, Ku JY, et al. Urine-based liquid biopsy: non-invasive and sensitive AR-V7 detection in urinary EVs from patients with prostate cancer. Lab Chip. 2018;19:87–97.
  • Fish L, Zhang S, Yu JX, et al. Cancer cells exploit an orphan RNA to drive metastatic progression. Nat Med. 2018;24:1743–1751.
  • Lewis JM, Vyas AD, Qiu Y, et al. Integrated analysis of exosomal protein biomarkers on alternating current electrokinetic chips enables rapid detection of pancreatic cancer in patient blood. ACS Nano. 2018;12:3311−3320.
  • Tian Q, He C, Liu G, et al. Nanoparticle counting by microscopic digital detection: selective quantitative analysis of exosomes via surface-anchored nucleic acid amplification. Anal Chem. 2018;90:6556–6562.
  • Im H, Shao H, Park YI, et al. label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat Biotechnol. 2014;32:490–495.
  • Kilic T, Valinhas ATS, Wall I, et al. Label-free detection of hypoxia-induced extracellular vesicle secretion from MCF-7 cells. Sci Rep. 2018;8:9402.
  • Mastoridis S, Bertolino GM, Whitehouse G, et al. Multiparametric analysis of circulating exosomes and other small extracellular vesicles by advanced imaging flow cytometry. Front Immunol. 2018;9:1583.
  • Yoshioka Y, Kosaka N, Konishi Y, et al. Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen. Nat Commun. 2014;5:3591.
  • Sedlarikova L, Bollova B, Radova L, et al. Circulating exosomal long noncoding RNA PRINS—first findings in monoclonal gammopathies. Hematol Oncol. 2018;36:786–791.
  • Nishida-Aoki N, Tominaga N, Takeshita F. Disruption of circulating extracellular vesicles as a novel therapeutic strategy against cancer metastasis. Mol Ther. 2017;25:181–191.
  • Marleau AM, Chen CS, Joyce JA, et al. Exosome removal as a therapeutic adjuvant in cancer. J Transl Med. 2012;10:134.
  • Ciravolo V, Huber V, Ghedini GC, et al. Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy. J Cell Physiol. 2012;227:658–667.
  • Kosaka N, Iguchi H, Hagiwara K, et al. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288:10849–10859.
  • Leone DA, Peschel A, Brown M, et al. Surface LAMP-2 is an endocytic receptor that diverts antigen internalized by human dendritic cells into highly immunogenic exosomes. J Immunol. 2017;199:531–546.
  • Wiedmer T, Blank A, Pantasis S, et al. Autophagy inhibition improves sunitinib efficacy in pancreatic neuroendocrine tumors via a lysosome-dependent mechanism. Mol Cancer Ther. 2017;16:2502–2515.
  • Kurywchak P, Tavormina J, Kalluri R. The emerging roles of exosomes in the modulation of immune responses in cancer. Genome Med. 2018;10:23.
  • Kitai Y, Kawasaki T, Sueyoshi T, et al. DNA-containing exosomes derived from cancer cells treated with topotecan activate a STING-dependent pathway and reinforce antitumor immunity. J Immunol. 2017;198:1649–1659.