Extracellular vesicles as a platform for membrane-associated therapeutic protein delivery

References

• Keller S, Sanderson MP, Stoeck A, et al. Exosomes: from biogenesis and secretion to biological function. Immunol Lett. 2006;107(2):1–15.
   Web of Science ®Google Scholar
• Madison MN, Roller RJ, Okeoma CM. Human semen contains exosomes with potent anti-HIV-1 activity. Retrovirology. 2014;11(1):102.
   PubMedGoogle Scholar
• Vella LJ, Greenwood DL, Cappai R, et al. Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet Immunol Immunopathol. 2008;124(3–4):385–393.
   Web of Science ®Google Scholar
• Ogawa Y, Miura Y, Harazono A, et al. Proteomic analysis of two types of exosomes in human whole saliva. Biol Pharm Bull. 2011;34(1):13–23.
   PubMed Web of Science ®Google Scholar
• Choi DS. Urinary extracellular vesicles for biomarker source to monitor polycystic kidney disease. Proteomics Clin Appl. 2015;9(5–6):447–448.
   Web of Science ®Google Scholar
• Turturici G, Tinnirello R, Sconzo G, et al. Extracellular membrane vesicles as a mechanism of cell-to-cell communication: advantages and disadvantages. Am J Physiol Cell Physiol. 2014;306(7):C621–33.
   PubMed Web of Science ®Google Scholar
• Ha D, Yang N, Nadithe V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B. 2016;6(4):287–296.
   PubMed Web of Science ®Google Scholar
• Pashoutan Sarvar D, Shamsasenjan K, Akbarzadehlaleh P. Mesenchymal stem cell-derived exosomes: new opportunity in cell-free therapy. Adv Pharm Bull. 2016;6(3):293–299.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Johnsen KB, Gudbergsson JM, Skov MN, et al. A comprehensive overview of exosomes as drug delivery vehicles - endogenous nanocarriers for targeted cancer therapy. Biochim Biophys Acta. 2014;1846(1):75–87.
   PubMed Web of Science ®Google Scholar
• Yang T, Martin P, Fogarty B, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res. 2015;32(6):2003–2014.
   PubMed Web of Science ®Google Scholar
• Escudier B, Dorval T, Chaput N, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med. 2005;3(1):10.
   PubMed Web of Science ®Google Scholar
• Tan A, De La Peña H, Seifalian AM. The application of exosomes as a nanoscale cancer vaccine. Int J Nanomedicine. 2010;5:889–900.
   PubMed Web of Science ®Google Scholar
• Le Pecq JB. Dexosomes as a therapeutic cancer vaccine: from bench to bedside. Blood Cells Mol Dis. 2005;35(2):129–135.
   Web of Science ®Google Scholar
• Altieri SL, Khan AN, Tomasi TB. Exosomes from plasmacytoma cells as a tumor vaccine. J Immunother. 2004;27(4):282–288.
   PubMed Web of Science ®Google Scholar
• Taïeb J, Chaput N, Zitvogel L. Dendritic cell-derived exosomes as cell-free peptide-based vaccines. Crit Rev Immunol. 2005;25(3):215–223.
   Web of Science ®Google Scholar
• Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes. Nat Med. 1998;4(5):594–600.
   PubMed Web of Science ®Google Scholar
• Phinney DG, Pittenger MF. Concise review: MSC-derived exosomes for cell-free therapy. Stem Cells. 2017;35(4):851–858.
   PubMed Web of Science ®Google Scholar
• Kishore R, Khan M. More than tiny sacks: stem cell exosomes as cell-free modality for cardiac repair. Circ Res. 2016;118(2):330–343.
   PubMed Web of Science ®Google Scholar
• Miles AJ, Wallace BA. Circular dichroism spectroscopy of membrane proteins. Chem Soc Rev. 2016;45(18):4859–4872.
   PubMed Web of Science ®Google Scholar
• Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 1998;7(4):1029–1038.
   PubMed Web of Science ®Google Scholar
• Krogh A, Larsson B, von Heijne G, et al. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–580.
   PubMed Web of Science ®Google Scholar
• Yildirim MA, Goh KI, Cusick ME, et al. Drug-target network. Nat Biotechnol. 2007;25(10):1119–1126.
   PubMed Web of Science ®Google Scholar
• Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there? Nat Rev Drug Discov. 2006;5(12):993–996.
   PubMed Web of Science ®Google Scholar
• Frauenfeld J, Loving R, Armache JP, et al. A saposin-lipoprotein nanoparticle system for membrane proteins. Nat Methods. 2016;13(4):345–351.
   PubMed Web of Science ®Google Scholar
• Tate CG. Practical considerations of membrane protein instability during purification and crystallisation. Methods Mol Biol. 2010;601:187–203.
   PubMedGoogle Scholar
• Breyton C, Pucci B, Popot JL. Amphipols and fluorinated surfactants: two alternatives to detergents for studying membrane proteins in vitro. Methods Mol Biol. 2010;601:219–245.
   PubMedGoogle Scholar
• Serebryany E, Zhu GA, Yan EC. Artificial membrane-like environments for in vitro studies of purified G-protein coupled receptors. Biochim Biophys Acta. 2012;1818(2):225–233.
   Web of Science ®Google Scholar
• Althoff T, Davies KM, Schulze S, et al. GRecon: a method for the lipid reconstitution of membrane proteins. Angew Chem Int Ed Engl. 2012;51(33):8343–8347.
   Web of Science ®Google Scholar
• Lluis MW, Godfroy JI 3rd, Yin H. Protein engineering methods applied to membrane protein targets. Protein Eng Des Sel. 2013;26(2):91–100.
   PubMed Web of Science ®Google Scholar
• Carpenter EP, Beis K, Cameron AD, et al. Overcoming the challenges of membrane protein crystallography. Curr Opin Struct Biol. 2008;18(5):581–586.
   PubMed Web of Science ®Google Scholar
• Marcus ME, Leonard JN. FedExosomes: engineering therapeutic biological nanoparticles that truly deliver. Pharmaceuticals (Basel). 2013;6(5):659–680.
   PubMedGoogle Scholar
• Ren J, He W, Zheng L, et al. From structures to functions: insights into exosomes as promising drug delivery vehicles. Biomater Sci. 2016;4(6):910–921.
   PubMed Web of Science ®Google Scholar
• Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9(8):581–593.
   PubMed Web of Science ®Google Scholar
• Shen B, Wu N, Yang JM, et al. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem. 2011;286(16):14383–14395.
   PubMed Web of Science ®Google Scholar
• Aperia A. Membrane transport proteins in health and disease. J Intern Med. 2007;261(1):2–4.
   Web of Science ®Google Scholar
• Pfeifer A, Verma IM. Gene therapy: promises and problems. Annu Rev Genomics Hum Genet. 2001;2:177–211.
   PubMed Web of Science ®Google Scholar
• Verma IM, Somia N. Gene therapy – promises, problems and prospects. Nature. 1997;389(6648):239–242.
   PubMed Web of Science ®Google Scholar
• Aihara H, Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnol. 1998;16(9):867–870.
   PubMed Web of Science ®Google Scholar
• Orive G, Hernandez RM, Rodriguez Gascon A, et al. Drug delivery in biotechnology: present and future. Curr Opin Biotechnol. 2003;14(6):659–664.
   PubMed Web of Science ®Google Scholar
• Sadelain M. Insertional oncogenesis in gene therapy: how much of a risk? Gene Ther. 2004;11(7):569–573.
   PubMed Web of Science ®Google Scholar
• Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest. 2008;118(9):3132–3142.
   PubMed Web of Science ®Google Scholar
• Briand L, Marcion G, Kriznik A, et al. A self-inducible heterologous protein expression system in Escherichia coli. Sci Rep. 2016;6:33037.
   PubMed Web of Science ®Google Scholar
• Berlec A, Strukelj B. Current state and recent advances in biopharmaceutical production in Escherichia coli, yeasts and mammalian cells. J Ind Microbiol Biotechnol. 2013;40(3–4):257–274.
   PubMed Web of Science ®Google Scholar
• Garavito RM, Ferguson-Miller S. Detergents as tools in membrane biochemistry. J Biol Chem. 2001;276(35):32403–32406.
   Web of Science ®Google Scholar
• Bayburt TH, Sligar SG. Membrane protein assembly into Nanodiscs. FEBS Lett. 2010;584(9):1721–1727.
   PubMed Web of Science ®Google Scholar
• Bowie JU. Stabilizing membrane proteins. Curr Opin Struct Biol. 2001;11(4):397–402.
   Web of Science ®Google Scholar
• Denisov IG, Sligar SG. Nanodiscs for structural and functional studies of membrane proteins. Nat Struct Mol Biol. 2016;23(6):481–486.
   PubMed Web of Science ®Google Scholar
• Cappuccio JA, Blanchette CD, Sulchek TA, et al. Cell-free co-expression of functional membrane proteins and apolipoprotein, forming soluble nanolipoprotein particles. Mol Cell Proteomics. 2008;7(11):2246–2253.
   Web of Science ®Google Scholar
• Akbarzadeh A, Rezaei-Sadabady R, Davaran S, et al. Liposome: classification, preparation, and applications. Nanoscale Res Lett. 2013;8(1):102.
   PubMed Web of Science ®Google Scholar
• Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2(8):569–579.
   PubMed Web of Science ®Google Scholar
• Yin H, Flynn AD. Drugging membrane protein interactions. Annu Rev Biomed Eng. 2016;18:51–76.
   Web of Science ®Google Scholar
• Vlassov AV, Magdaleno S, Setterquist R, et al. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta. 2012;1820(7):940–948.
   PubMed Web of Science ®Google Scholar
• Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73(10):1907–1920.
   PubMed Web of Science ®Google Scholar
• Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008;9(6):871–881.
   PubMed Web of Science ®Google Scholar
• Sahoo S, Losordo DW. Exosomes and cardiac repair after myocardial infarction. Circ Res. 2014;114(2):333–344.
   PubMed Web of Science ®Google Scholar
• Denzer K, Kleijmeer MJ, Heijnen HF, et al. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;113(Pt 19):3365–3374.
   PubMed Web of Science ®Google Scholar
• Klein-Scory S, Tehrani MM, Eilert-Micus C, et al. New insights in the composition of extracellular vesicles from pancreatic cancer cells: implications for biomarkers and functions. Proteome Sci. 2014;12(1):50.
   PubMedGoogle Scholar
• Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, et al. Sorting it out: regulation of exosome loading. Semin Cancer Biol. 2014;28:3–13.
   PubMed Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383.
   PubMed Web of Science ®Google Scholar
• Booth AM, Fang Y, Fallon JK, et al. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol. 2006;172(6):923–935.
   PubMed Web of Science ®Google Scholar
• de Gassart A, Geminard C, Fevrier B, et al. Lipid raft-associated protein sorting in exosomes. Blood. 2003;102(13):4336–4344.
   PubMed Web of Science ®Google Scholar
• Al-Nedawi K, Meehan B, Micallef J, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10(5):619–624.
   PubMed Web of Science ®Google Scholar
• Kraft JC, Freeling JP, Wang Z, et al. Emerging research and clinical development trends of liposome and lipid nanoparticle drug delivery systems. J Pharm Sci. 2014;103(1):29–52.
   PubMed Web of Science ®Google Scholar
• Gallarate M, Battaglia L, Peira E, et al. Peptide-loaded solid lipid nanoparticles prepared through coacervation technique. Int J Chem Eng. 2011;2011:6.
   Google Scholar
• Knecht S, Ricklin D, Eberle AN, et al. Oligohis-tags: mechanisms of binding to Ni2+-NTA surfaces. J Mol Recognit. 2009;22(4):270–279.
   Web of Science ®Google Scholar
• Colletier JP, Chaize B, Winterhalter M, et al. Protein encapsulation in liposomes: efficiency depends on interactions between protein and phospholipid bilayer. BMC Biotechnol. 2002;2:9.
   PubMedGoogle Scholar
• Stickney Z, Losacco J, McDevitt S, et al. Development of exosome surface display technology in living human cells. Biochem Biophys Res Commun. 2016;472(1):53–59.
   PubMed Web of Science ®Google Scholar
• Kanuma T, Yamamoto T, Kobiyama K, et al. CD63-mediated antigen delivery into extracellular vesicles via DNA vaccination results in robust CD8+ T cell responses. J Immunol. 2017;198(12):4707–4715.
   Web of Science ®Google Scholar
• Morishita M, Takahashi Y, Matsumoto A, et al. Exosome-based tumor antigens-adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA. Biomaterials. 2016;111:55–65.
   PubMed Web of Science ®Google Scholar
• Meyer C, Losacco J, Stickney Z, et al. Pseudotyping exosomes for enhanced protein delivery in mammalian cells. Int J Nanomedicine. 2017;12:3153–3170.
   PubMed Web of Science ®Google Scholar
• Takahashi Y, Nishikawa M, Shinotsuka H, et al. Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection. J Biotechnol. 2013;165(2):77–84.
   PubMed Web of Science ®Google Scholar
• SBI. XPack™ exosome protein engineering. Available from: https://www.systembio.com/xpack-exosomes/overview.
   Google Scholar
• Yim N, Ryu SW, Choi K, et al. Exosome engineering for efficient intracellular delivery of soluble proteins using optically reversible protein-protein interaction module. Nat Commun. 2016;7:12277.
   PubMed Web of Science ®Google Scholar
• Estelles A, Sperinde J, Roulon T, et al. Exosome nanovesicles displaying G protein-coupled receptors for drug discovery. Int J Nanomedicine. 2007;2(4):751–760.
   PubMed Web of Science ®Google Scholar
• Hartman ZC, Wei J, Glass OK, et al. Increasing vaccine potency through exosome antigen targeting. Vaccine. 2011;29(50):9361–9367.
   PubMed Web of Science ®Google Scholar
• Andre F, Chaput N, Schartz NE, et al. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J Immunol. 2004;172(4):2126–2136.
   PubMed Web of Science ®Google Scholar
• 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(4):341–345.
   PubMed Web of Science ®Google Scholar
• El-Andaloussi S, Lee Y, Lakhal-Littleton S, et al. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 2012;7(12):2112–2126.
   PubMed Web of Science ®Google Scholar
• Ohno S, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013;21(1):185–191.
   PubMed Web of Science ®Google Scholar
• Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35(7):2383–2390.
   PubMed Web of Science ®Google Scholar
• El Andaloussi S, Lakhal S, Mager I, et al. Exosomes for targeted siRNA delivery across biological barriers. Adv Drug Deliv Rev. 2013;65(3):391–397.
   PubMed Web of Science ®Google Scholar
• Hazan-Halevy I, Rosenblum D, Weinstein S, et al. Cell-specific uptake of mantle cell lymphoma-derived exosomes by malignant and non-malignant B-lymphocytes. Cancer Lett. 2015;364(1):59–69.
   PubMed Web of Science ®Google Scholar
• Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–335.
   PubMed Web of Science ®Google Scholar
• Rana S, Yue S, Stadel D, et al. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol. 2012;44(9):1574–1584.
   PubMed Web of Science ®Google Scholar
• Imai T, Takahashi Y, Nishikawa M, et al. Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice. J Extracell Vesicles. 2015;4:26238.
   PubMed Web of Science ®Google Scholar
• Feng D, Zhao WL, Ye YY, et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic. 2010;11(5):675–687.
   PubMed Web of Science ®Google Scholar
• Xitong D, Xiaorong Z. Targeted therapeutic delivery using engineered exosomes and its applications in cardiovascular diseases. Gene. 2016;575(2 Pt 2):377–384.
   PubMed Web of Science ®Google Scholar
• Delcayre A, Estelles A, Sperinde J, et al. Exosome Display technology: applications to the development of new diagnostics and therapeutics. Blood Cells Mol Dis. 2005;35(2):158–168.
   PubMed Web of Science ®Google Scholar
• Hung ME, Leonard JN. Stabilization of exosome-targeting peptides via engineered glycosylation. J Biol Chem. 2015;290(13):8166–8172.
   PubMed Web of Science ®Google Scholar
• Ruiss R, Jochum S, Mocikat R, et al. EBV-gp350 confers B-cell tropism to tailored exosomes and is a neo-antigen in normal and malignant B cells–a new option for the treatment of B-CLL. PLoS One. 2011;6(10):e25294.
   Web of Science ®Google Scholar
• Liu Y, Li D, Liu Z, et al. Targeted exosome-mediated delivery of opioid receptor Mu siRNA for the treatment of morphine relapse. Sci Rep. 2015;5:17543.
   PubMed Web of Science ®Google Scholar
• Yang J, Zhang X, Chen X, et al. Exosome mediated delivery of miR-124 promotes neurogenesis after ischemia. Mol Ther Nucleic Acids. 2017;7:278–287.
   PubMedGoogle Scholar
• Bellavia D, Raimondo S, Calabrese G, et al. Interleukin 3- receptor targeted exosomes inhibit in vitro and in vivo Chronic Myelogenous Leukemia cell growth. Theranostics. 2017;7(5):1333–1345.
   PubMed Web of Science ®Google Scholar
• Ohno SI, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013;21(1):185–191.
   PubMed Web of Science ®Google Scholar
• Rountree RB, Mandl SJ, Nachtwey JM, et al. Exosome targeting of tumor antigens expressed by cancer vaccines can improve antigen immunogenicity and therapeutic efficacy. Cancer Res. 2011;71(15):5235–5244.
   PubMed Web of Science ®Google Scholar
• Zeelenberg IS, Ostrowski M, Krumeich S, et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 2008;68(4):1228–1235.
   PubMed Web of Science ®Google Scholar
• Sedlik C, Vigneron J, Torrieri-Dramard L, et al. Different immunogenicity but similar antitumor efficacy of two DNA vaccines coding for an antigen secreted in different membrane vesicle-associated forms. J Extracell Vesicles. 2014;3:24646.
   Google Scholar
• Kooijmans SA, Aleza CG, Roffler SR, et al. Display of GPI-anchored anti-EGFR nanobodies on extracellular vesicles promotes tumour cell targeting. J Extracell Vesicles. 2016;5:31053.
   PubMed Web of Science ®Google Scholar
• Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature. 2017;546(7659):498–503.
   PubMed Web of Science ®Google Scholar
• Romagnoli GG, Zelante BB, Toniolo PA, et al. Dendritic cell-derived exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front Immunol. 2014;5:692.
   PubMed Web of Science ®Google Scholar
• Näslund TI, Gehrmann U, Qazi KR, et al. Dendritic cell-derived exosomes need to activate both T and B cells to induce antitumor immunity. J Immunol. 2013;190(6):2712–2719.
   PubMed Web of Science ®Google Scholar
• Besse B, Charrier M, Lapierre V, et al. Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC. Oncoimmunology. 2016;5(4):e1071008.
   PubMed Web of Science ®Google Scholar
• Morse MA, Garst J, Osada T, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med. 2005;3(1):9.
   PubMed Web of Science ®Google Scholar
• Dai S, Wei D, Wu Z, et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther. 2008;16(4):782–790.
   PubMed Web of Science ®Google Scholar
• Segura E, Nicco C, Lombard B, et al. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood. 2005;106(1):216–223.
   PubMed Web of Science ®Google Scholar
• Munich S, Sobo-Vujanovic A, Buchser WJ, et al. Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands. Oncoimmunology. 2012;1(7):1074–1083.
   PubMed Web of Science ®Google Scholar
• Viaud S, Terme M, Flament C, et al. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha. PLoS One. 2009;4(3):e4942.
   PubMed Web of Science ®Google Scholar
• Wolfers J, Lozier A, Raposo G, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7(3):297–303.
   PubMed Web of Science ®Google Scholar
• André F, Schartz NE, Chaput N, et al. Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine. 2002;20(Suppl 4):A28–31.
   Google Scholar
• Xie Y, Bai O, Zhang H, et al. 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. 2010;14(11):2655–2666.
   PubMed Web of Science ®Google Scholar
• Rigi G, Beyranvand P, Ghaedmohammadi S, et al. Comparison of the extracellular full-length and truncated recombinant protein A production in Escherichia coli BL21 (DE3). J Paramed Sci. 2015;6:3.
   Google Scholar
• Sørensen HP, Sperling-Petersen HU, Mortensen KK. Production of recombinant thermostable proteins expressed in Escherichia coli: completion of protein synthesis is the bottleneck. J Chromatogr B Analyt Technol Biomed Life Sci. 2003;786(1–2):207–214.
   Web of Science ®Google Scholar
• Frost GI. Recombinant human hyaluronidase (rHuPH20): an enabling platform for subcutaneous drug and fluid administration. Expert Opin Drug Deliv. 2007;4(4):427–440.
   PubMed Web of Science ®Google Scholar
• Ashiru O, López-Cobo S, Fernández-Messina L, et al. A GPI anchor explains the unique biological features of the common NKG2D-ligand allele MICA*008. Biochem J. 2013;454(2):295–302.
   PubMedGoogle Scholar
• Valapala M, Vishwanatha JK. Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. J Biol Chem. 2011;286(35):30911–30925.
   PubMed Web of Science ®Google Scholar
• Théry C, Regnault A, Garin J, et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol. 1999;147(3):599–610.
   PubMed Web of Science ®Google Scholar
• Katsuda T, Tsuchiya R, Kosaka N, et al. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Sci Rep. 2013;3:1197.
   PubMed Web of Science ®Google Scholar
• Hong Y, Nam G-H, Koh E, et al. Exosome as a vehicle for delivery of membrane protein therapeutics, PH20, for enhanced tumor penetration and antitumor efficacy. Adv Funct Mater. 2017;28(5):170374.
   Web of Science ®Google Scholar
• Rivoltini L, Chiodoni C, Squarcina P, et al. TNF-related apoptosis-inducing ligand (TRAIL)-armed exosomes deliver proapoptotic signals to tumor site. Clin Cancer Res. 2016;22(14):3499–3512.
   PubMed Web of Science ®Google Scholar
• Koh E, Lee EJ, Nam GH, et al. Exosome-SIRPalpha, a CD47 blockade increases cancer cell phagocytosis. Biomaterials. 2017;121:121–129.
   PubMed Web of Science ®Google Scholar
• Willingham SB, Volkmer JP, Gentles AJ, et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A. 2012;109(17):6662–6667.
   PubMed Web of Science ®Google Scholar
• Weiskopf K, Ring AM, Ho CCM, et al. Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies. Science. 2013;341(6141):88–91.
   PubMed Web of Science ®Google Scholar
• Chen Y, Zhang M, Jin H, et al. Intein-mediated site-specific synthesis of tumor-targeting protein delivery system: turning PEG dilemma into prodrug-like feature. Biomaterials. 2017;116:57–68.
   Web of Science ®Google Scholar
• Lu Y, Sun W, Gu Z. Stimuli-responsive nanomaterials for therapeutic protein delivery. J Control Release. 2014;194:1–19.
   PubMed Web of Science ®Google Scholar
• Yun Y, Cho YW, Park K. Nanoparticles for oral delivery: targeted nanoparticles with peptidic ligands for oral protein delivery. Adv Drug Deliv Rev. 2013;65(6):822–832.
   PubMed Web of Science ®Google Scholar
• Brannon-Peppas L, Blanchette JO. Nanoparticle and targeted systems for cancer therapy. Adv Drug Deliv Rev. 2004;56(11):1649–1659.
   PubMed Web of Science ®Google Scholar
• Capecchi MR. High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell. 1980;22(2 Pt 2):479–488.
   PubMed Web of Science ®Google Scholar
• Kaczmarczyk SJ, Sitaraman K, Young HA, et al. Protein delivery using engineered virus-like particles. Proc Natl Acad Sci U S A. 2011;108(41):16998–17003.
   PubMed Web of Science ®Google Scholar
• Melikov K, Chernomordik LV. Arginine-rich cell penetrating peptides: from endosomal uptake to nuclear delivery. Cell Mol Life Sci. 2005;62(23):2739–2749.
   PubMed Web of Science ®Google Scholar
• Guan X, Goddard MA, Mack DL, et al. Gene therapy in monogenic congenital myopathies. Methods. 2016;99:91–98.
   PubMed Web of Science ®Google Scholar
• de Planque MR, de Planque MR, Mendes GP, et al. Controlled delivery of membrane proteins to artificial lipid bilayers by nystatin-ergosterol modulated vesicle fusion. IEE Proc Nanobiotechnol. 2006;153(2):21–30.
   Google Scholar
• Pisal DS, Kosloski MP, Balu-Iyer SV. Delivery of therapeutic proteins. J Pharm Sci. 2010;99(6):2557–2575.
   PubMed Web of Science ®Google Scholar
• Rosano GL, Ceccarelli EA. Recombinant protein expression in Escherichia coli: advances and challenges. Front Microbiol. 2014;5:172.
   PubMed Web of Science ®Google Scholar
• Sack BK, Herzog RW. Evading the immune response upon in vivo gene therapy with viral vectors. Curr Opin Mol Ther. 2009;11(5):493–503.
   PubMedGoogle Scholar
• Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet. 2003;4(5):346–358.
   PubMed Web of Science ®Google Scholar
• Mangeot PE, Dollet S, Girard M, et al. Protein transfer into human cells by VSV-G-induced nanovesicles. Mol Ther. 2011;19(9):1656–1666.
   PubMed Web of Science ®Google Scholar
• Yang Y, Hong Y, Nam GH, et al. Virus-mimetic fusogenic exosomes for direct delivery of integral membrane proteins to target cell membranes. Adv Mater. 2017;29:13.
   Web of Science ®Google Scholar
• El-Sayed A, Futaki S, Harashima H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. Aaps J. 2009;11(1):13–22.
   PubMed Web of Science ®Google Scholar
• Erazo-Oliveras A, Muthukrishnan N, Baker R, et al. Improving the endosomal escape of cell-penetrating peptides and their cargos: strategies and challenges. Pharmaceuticals (Basel). 2012;5(11):1177–1209.
   PubMedGoogle Scholar
• Fu A, Tang R, Hardie J, et al. Promises and pitfalls of intracellular delivery of proteins. Bioconjug Chem. 2014;25(9):1602–1608.
   PubMed Web of Science ®Google Scholar
• Shahabipour F, Banach M, Sahebkar A. Exosomes as nanocarriers for siRNA delivery: paradigms and challenges. Arch Med Sci. 2016;12(6):1324–1326.
   PubMed Web of Science ®Google Scholar
• Lamichhane TN, Raiker RS, Jay SM. Exogenous DNA loading into extracellular vesicles via electroporation is size-dependent and enables limited gene delivery. Mol Pharm. 2015;12(10):3650–3657.
   PubMed Web of Science ®Google Scholar
• Kooijmans SA, Stremersch S, Braeckmans K, et al. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J Control Release. 2013;172(1):229–238.
   PubMed Web of Science ®Google Scholar
• Ferguson SW, Nguyen J. Exosomes as therapeutics: the implications of molecular composition and exosomal heterogeneity. J Control Release. 2016;228:179–190.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekström 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(6):654–659.
   PubMed Web of Science ®Google Scholar
• Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinf. 2015;13(1):17–24.
   PubMed Web of Science ®Google Scholar
• Willms E, Johansson HJ, Mäger I, et al. Cells release subpopulations of exosomes with distinct molecular and biological properties. Sci Rep. 2016;6:22519.
   PubMed Web of Science ®Google Scholar
• Xiu F, Cai Z, Yang Y, et al. Surface anchorage of superantigen SEA promotes induction of specific antitumor immune response by tumor-derived exosomes. J Mol Med (Berl). 2007;85(5):511–521.
   Web of Science ®Google Scholar
• Yang Y, Xiu F, Cai Z, et al. Increased induction of antitumor response by exosomes derived from interleukin-2 gene-modified tumor cells. J Cancer Res Clin Oncol. 2007;133(6):389–399.
   PubMed Web of Science ®Google Scholar
• Chaput N, Schartz NE, Andre F, et al. Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J Immunol. 2004;172(4):2137–2146.
   PubMed Web of Science ®Google Scholar
• Shi J, Kantoff PW, Wooster R, et al. Cancer nanomedicine: progress, challenges and opportunities. Nat Rev Cancer. 2017;17(1):20–37.
   PubMed Web of Science ®Google Scholar
• Tan S, Wu T, Zhang D, et al. Cell or cell membrane-based drug delivery systems. Theranostics. 2015;5(8):863–881.
   PubMed Web of Science ®Google Scholar
• Park K. Facing the truth about nanotechnology in drug delivery. ACS Nano. 2013;7(9):7442–7447.
   PubMed Web of Science ®Google Scholar
• Wilhelm S, Tavares AJ, Dai Q, et al. Analysis of nanoparticle delivery to tumours. Nat Rev Mater. 2016;1(5):16014.
   Web of Science ®Google Scholar
• Smyth T, Kullberg M, Malik N, et al. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release. 2015;199:145–155.
   PubMed Web of Science ®Google Scholar
• Wiklander OP, Nordin JZ, O’Loughlin A, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles. 2015;4:26316.
   PubMed Web of Science ®Google Scholar
• Leblond F, Davis SC, Valdés PA, et al. Pre-clinical whole-body fluorescence imaging: review of instruments, methods and applications. J Photochem Photobiol B. 2010;98(1):77–94.
   PubMed Web of Science ®Google Scholar
• Ntziachristos V, Bremer C, Weissleder R. Fluorescence imaging with near-infrared light: new technological advances that enable in vivo molecular imaging. Eur Radiol. 2003;13(1):195–208.
   PubMed Web of Science ®Google Scholar
• Luker KE, Luker GD. Applications of bioluminescence imaging to antiviral research and therapy: multiple luciferase enzymes and quantitation. Antiviral Res. 2008;78(3):179–187.
   PubMed Web of Science ®Google Scholar
• Miller CG, Krasnow J, Schwartz LH. Medical imaging in clinical trials. London: Springer; 2014.
   Google Scholar
• Gangadaran P, Hong CM, Ahn BC. Current perspectives on in vivo noninvasive tracking of extracellular vesicles with molecular imaging. Biomed Res Int. 2017;2017:9158319.
   Google Scholar
• Bulte JW. In vivo MRI cell tracking: clinical studies. AJR Am J Roentgenol. 2009;193(2):314–325.
   PubMed Web of Science ®Google Scholar
• Correa PL, Mesquita CT, Felix RM, et al. Assessment of intra-arterial injected autologous bone marrow mononuclear cell distribution by radioactive labeling in acute ischemic stroke. Clin Nucl Med. 2007;32(11):839–841.
   Web of Science ®Google Scholar
• Giaffer MH. Labelled leucocyte scintigraphy in inflammatory bowel disease: clinical applications. Gut. 1996;38(1):1–5.
   Web of Science ®Google Scholar
• Aryani A, Denecke B. Exosomes as a nanodelivery system: a key to the future of neuromedicine? Mol Neurobiol. 2016;53(2):818–834.
   PubMed Web of Science ®Google Scholar
• Li P, Kaslan M, Lee SH, et al. Progress in exosome isolation techniques. Theranostics. 2017;7(3):789–804.
   PubMed Web of Science ®Google Scholar
• Momen-Heravi F, Balaj L, Alian S, et al. Current methods for the isolation of extracellular vesicles. Biol Chem. 2013;394(10):1253–1262.
   PubMed Web of Science ®Google Scholar
• Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006:3.22 1-3.22. 29.
   PubMedGoogle Scholar
• Helwa I, Cai J, Drewry MD, et al. A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One. 2017;12(1):e0170628.
   PubMed Web of Science ®Google Scholar
• Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1161–1172.
   PubMed Web of Science ®Google Scholar
• Cantin R, Diou J, Belanger D, et al. Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J Immunol Methods. 2008;338(1–2):21–30.
   PubMed Web of Science ®Google Scholar
• Nordin JZ, Lee Y, Vader P, et al. Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine. 2015;11(4):879–883.
   PubMed Web of Science ®Google Scholar
• Zeringer E, Barta T, Li M, et al. Strategies for isolation of exosomes. Cold Spring Harb Protoc. 2015;2015(4):319–323.
   PubMedGoogle Scholar
• Safdar A, Saleem A, Tarnopolsky MA. The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat Rev Endocrinol. 2016;12(9):504–517.
   PubMed Web of Science ®Google Scholar
• Taylor DD, Zacharias W, Gercel-Taylor C. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol Biol. 2011;728:235–246.
   PubMedGoogle Scholar
• Antes TJ, Kwei K, Wu F. Methods for microvesicle isolation and selective removal. Unites States patent US 9,005,888 2015 Apr 14.
   Google Scholar
• Lamparski HG, Metha-Damani A, Yao JY, et al. Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods. 2002;270(2):211–226.
   PubMed Web of Science ®Google Scholar
• Logozzi M, De Milito A, Lugini L, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One. 2009;4(4):e5219.
   PubMed Web of Science ®Google Scholar
• Yeo RW, Lai RC, Zhang B, et al. Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev. 2013;65(3):336–341.
   PubMed Web of Science ®Google Scholar
• Tan A, Rajadas J, Seifalian AM. Exosomes as nano-theranostic delivery platforms for gene therapy. Adv Drug Deliv Rev. 2013;65(3):357–367.
   PubMed Web of Science ®Google Scholar
• Lakhal S, Wood MJ. Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers. Bioessays. 2011;33(10):737–741.
   PubMed Web of Science ®Google Scholar
• Momen-Heravi F, Bala S, Bukong T, et al. Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine. 2014;10(7):1517–1527.
   PubMed Web of Science ®Google Scholar
• Sun D, Zhuang X, Zhang S, et al. Exosomes are endogenous nanoparticles that can deliver biological information between cells. Adv Drug Deliv Rev. 2013;65(3):342–347.
   PubMed Web of Science ®Google Scholar
• van Dommelen SM, Vader P, Lakhal S, et al. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J Control Release. 2012;161(2):635–644.
   PubMed Web of Science ®Google Scholar
• Hao S, Moyana T, Xiang J. Review: cancer immunotherapy by exosome-based vaccines. Cancer Biother Radiopharm. 2007;22(5):692–703.
   PubMed Web of Science ®Google Scholar
• Johnstone RM. Exosomes biological significance: A concise review. Blood Cells Mol Dis. 2006;36(2):315–321.
   PubMed Web of Science ®Google Scholar
• Lasser C. Exosomes in diagnostic and therapeutic applications: biomarker, vaccine and RNA interference delivery vehicle. Expert Opin Biol Ther. 2015;15(1):103–117.
   PubMed Web of Science ®Google Scholar