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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Current Perspectives on Delivery Systems Using Extracellular Vesicles in Neurological Disease

Author(s): Phuong H.L. Tran, Wei Duan, Beom-Jin Lee and Thao T.D. Tran*

Volume 26, Issue 7, 2020

Page: [764 - 771] Pages: 8

DOI: 10.2174/1381612826666200102125847

Price: $65

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Abstract

Extracellular vesicles have an excellent ability to transfer their contents to cells. Extracellular vesicles can also be engineered to deliver therapeutic molecules to target cells. Although a number of studies have exploited synthesized nanoparticles in the treatment of neurological disease in the past few years, extracellular vesicles have been investigated and shown tremendous promise for clinical applications because they are safe and have strong targeting specificity. Different types of extracellular vesicles have been studied and modified for delivering therapeutic factors in neurological disease, including extracellular vesicles loaded with natural therapeutic factors and therapeutic molecules. In this review, we discuss delivery systems using extracellular vesicles containing molecules of interest and then focus on main strategies used for EV loading and surface modification. Discussing these important issues will support and facilitate the design and development of promising techniques and products for neurological therapy.

Keywords: Extracellular vesicles, neurological disease, therapeutic molecules, loading, delivery system, specificity.

[1]
Batool A, Kamal MA, Rizvi SMD, Rashid S. Topical discoveries on multi-target approach to manage Alzheimer’s disease. Curr Drug Metab 2018; 19(8): 704-13.
[http://dx.doi.org/10.2174/1389200219666180305152553] [PMID: 29512457]
[2]
Tran CTM, Tran PHL, Tran TTD. pH-independent dissolution enhancement for multiple poorly water-soluble drugs by nano-sized solid dispersions based on hydrophobic-hydrophilic conjugates. Drug Dev Ind Pharm 2019; 45(3): 514-9.
[http://dx.doi.org/10.1080/03639045.2018.1562466] [PMID: 30575412]
[3]
Dinh HTT, Tran PHL, Duan W, Lee B-J, Tran TTD. Nano-sized solid dispersions based on hydrophobic-hydrophilic conjugates for dissolution enhancement of poorly water-soluble drugs. Int J Pharm 2017; 533(1): 93-8.
[http://dx.doi.org/10.1016/j.ijpharm.2017.09.065] [PMID: 28951346]
[4]
Barnabas W. Drug targeting strategies into the brain for treating neurological diseases. J Neurosci Methods 2019; 311: 133-46.
[http://dx.doi.org/10.1016/j.jneumeth.2018.10.015] [PMID: 30336221]
[5]
Iman K, Mirza MU, Mazhar N, Vanmeert M, Irshad I, Kamal MA. In silico structure-based identification of novel acetylcholinesterase inhibitors against Alzheimer’s disease. CNS Neurol Disord Drug Targets 2018; 17(1): 54-68.
[http://dx.doi.org/10.2174/1871527317666180115162422] [PMID: 29336270]
[6]
Tran TTD, Tran PHL. Nanoconjugation and encapsulation strategies for improving drug delivery and therapeutic efficacy of poorly water-soluble drugs. Pharmaceutics 2019; 11(7) E325
[http://dx.doi.org/10.3390/pharmaceutics11070325] [PMID: 31295947]
[7]
Vader P, Mol EA, Pasterkamp G, Schiffelers RM. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 2016; 106(Pt A): 148-56.
[http://dx.doi.org/10.1016/j.addr.2016.02.006] [PMID: 26928656]
[8]
Batrakova EV, Kim MS. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Control Release 2015; 219: 396-405.
[http://dx.doi.org/10.1016/j.jconrel.2015.07.030] [PMID: 26241750]
[9]
Kalani A, Tyagi A, Tyagi N. Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol Neurobiol 2014; 49(1): 590-600.
[http://dx.doi.org/10.1007/s12035-013-8544-1] [PMID: 23999871]
[10]
Raeven P, Zipperle J, Drechsler S. Extracellular vesicles as markers and mediators in sepsis. Theranostics 2018; 8(12): 3348-65.
[http://dx.doi.org/10.7150/thno.23453] [PMID: 29930734]
[11]
Li P, Kaslan M, Lee SH, Yao J, Gao Z. Progress in exosome isolation techniques. Theranostics 2017; 7(3): 789-804.
[http://dx.doi.org/10.7150/thno.18133] [PMID: 28255367]
[12]
Verma M, Lam TK, Hebert E, Divi RL. Extracellular vesicles: potential applications in cancer diagnosis, prognosis, and epidemiology. BMC Clin Pathol 2015; 15(1): 6.
[http://dx.doi.org/10.1186/s12907-015-0005-5] [PMID: 25883534]
[13]
Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30(1): 255-89.
[http://dx.doi.org/10.1146/annurev-cellbio-101512-122326] [PMID: 25288114]
[14]
Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol 2015; 40: 41-51.
[http://dx.doi.org/10.1016/j.semcdb.2015.02.010] [PMID: 25721812]
[15]
Song L, Tang S, Han X, et al. KIBRA controls exosome secretion via inhibiting the proteasomal degradation of Rab27a. Nat Commun 2019; 10(1): 1639.
[http://dx.doi.org/10.1038/s41467-019-09720-x] [PMID: 30967557]
[16]
Dong X, Gao X, Dai Y, Ran N, Yin H. Serum exosomes can restore cellular function in vitro and be used for diagnosis in dysferlinopathy. Theranostics 2018; 8(5): 1243-55.
[http://dx.doi.org/10.7150/thno.22856] [PMID: 29507617]
[17]
Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 2018; 75(2): 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[18]
Edgar JRQ. Q&A: What are exosomes, exactly? BMC Biol 2016; 14: 46-6.
[http://dx.doi.org/10.1186/s12915-016-0268-z] [PMID: 27296830]
[19]
Ha D, Yang N, Nadithe V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B 2016; 6(4): 287-96.
[http://dx.doi.org/10.1016/j.apsb.2016.02.001] [PMID: 27471669]
[20]
Turturici G, Tinnirello R, Sconzo G, Geraci F. Extracellular membrane vesicles as a mechanism of cell-to-cell communication: advantages and disadvantages. Am J Physiol Cell Physiol 2014; 306(7): C621-33.
[http://dx.doi.org/10.1152/ajpcell.00228.2013] [PMID: 24452373]
[21]
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[22]
Cai J, Han Y, Ren H, et al. Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol 2013; 5(4): 227-38.
[http://dx.doi.org/10.1093/jmcb/mjt011] [PMID: 23580760]
[23]
Cooper JM, Wiklander PBO, Nordin JZ, et al. Systemic exosomal siRNA delivery reduced alpha-synuclein aggregates in brains of transgenic mice. Mov Disord 2014; 29(12): 1476-85.
[http://dx.doi.org/10.1002/mds.25978] [PMID: 25112864]
[24]
Jiang X-C, Gao J-Q. Exosomes as novel bio-carriers for gene and drug delivery. Int J Pharm 2017; 521(1-2): 167-75.
[http://dx.doi.org/10.1016/j.ijpharm.2017.02.038] [PMID: 28216464]
[25]
Tkach M, Théry C. Communication by extracellular vesicles: where we are and where we need to go. Cell 2016; 164(6): 1226-32.
[http://dx.doi.org/10.1016/j.cell.2016.01.043] [PMID: 26967288]
[26]
Rani S, O’Brien K, Kelleher FC, et al. Isolation of exosomes for subsequent mrna, microrna, and protein profilinggene expression profiling: methods and protocols. Totowa, NJ: Humana Press 2011; pp. 181-95.
[http://dx.doi.org/10.1007/978-1-61779-289-2_13]
[27]
Ahmed KA, Xiang J. Mechanisms of cellular communication through intercellular protein transfer. J Cell Mol Med 2011; 15(7): 1458-73.
[http://dx.doi.org/10.1111/j.1582-4934.2010.01008.x] [PMID: 20070437]
[28]
Théry C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 2011; 3: 15-5.
[http://dx.doi.org/10.3410/B3-15] [PMID: 21876726]
[29]
Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002; 2(8): 569-79.
[http://dx.doi.org/10.1038/nri855] [PMID: 12154376]
[30]
Keerthikumar S, Gangoda L, Gho YS, Mathivanan S. Bioinformatics tools for extracellular vesicles research exosomes and microvesicles: methods and protocols. New York, NY: Springer New York 2017; pp. 189-96.
[http://dx.doi.org/10.1007/978-1-4939-6728-5_13]
[31]
Jalalian SH, Ramezani M, Jalalian SA, Abnous K, Taghdisi SM. Exosomes, new biomarkers in early cancer detection. Anal Biochem 2019; 571: 1-13.
[http://dx.doi.org/10.1016/j.ab.2019.02.013] [PMID: 30776327]
[32]
Bastos N, Ruivo CF, da Silva S, Melo SA. Exosomes in cancer: use them or target them? Semin Cell Dev Biol 2018; 78: 13-21.
[http://dx.doi.org/10.1016/j.semcdb.2017.08.009] [PMID: 28803894]
[33]
Wee I, Syn N, Sethi G, Goh BC, Wang L. Role of tumor-derived exosomes in cancer metastasis. Biochimica et Biophysica Acta (BBA) -. Rev Can 2019; 1871(1): 12-9.
[34]
Bansal S, Sharma M, R R, Mohanakumar T. The role of exosomes in allograft immunity. Cell Immunol 2018; 331: 85-92.
[http://dx.doi.org/10.1016/j.cellimm.2018.06.003] [PMID: 29907298]
[35]
Kawikova I, Askenase PW. Diagnostic and therapeutic potentials of exosomes in CNS diseases. Brain Res 2015; 1617: 63-71.
[http://dx.doi.org/10.1016/j.brainres.2014.09.070] [PMID: 25304360]
[36]
Selmaj I, Mycko MP, Raine CS, Selmaj KW. The role of exosomes in CNS inflammation and their involvement in multiple sclerosis. J Neuroimmunol 2017; 306: 1-10.
[http://dx.doi.org/10.1016/j.jneuroim.2017.02.002] [PMID: 28385180]
[37]
Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji MM. Exosome mediated communication within the tumor microenvironment. J Control Release 2015; 219: 278-94.
[http://dx.doi.org/10.1016/j.jconrel.2015.06.029] [PMID: 26143224]
[38]
Natasha G, Gundogan B, Tan A, et al. Exosomes as immunotheranostic nanoparticles. Clin Ther 2014; 36(6): 820-9.
[http://dx.doi.org/10.1016/j.clinthera.2014.04.019] [PMID: 24863261]
[39]
Tran T-H, Mattheolabakis G, Aldawsari H, Amiji M. Exosomes as nanocarriers for immunotherapy of cancer and inflammatory diseases. Clin Immunol 2015; 160(1): 46-58.
[http://dx.doi.org/10.1016/j.clim.2015.03.021] [PMID: 25842185]
[40]
Kao C-Y, Papoutsakis ET. Extracellular vesicles: exosomes, microparticles, their parts, and their targets to enable their biomanufacturing and clinical applications. Curr Opin Biotechnol 2019; 60: 89-98.
[http://dx.doi.org/10.1016/j.copbio.2019.01.005] [PMID: 30851486]
[41]
Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 2010; 107(9): 1047-57.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.226456] [PMID: 21030722]
[42]
Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9(8): 581-93.
[http://dx.doi.org/10.1038/nri2567] [PMID: 19498381]
[43]
Boilard E, Nigrovic PA, Larabee K, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327(5965): 580-3.
[http://dx.doi.org/10.1126/science.1181928] [PMID: 20110505]
[44]
Tang K, Zhang Y, Zhang H, et al. Delivery of chemotherapeutic drugs in tumour cell-derived microparticles. Nat Commun 2012; 3: 1282.
[http://dx.doi.org/10.1038/ncomms2282] [PMID: 23250412]
[45]
Galieva LR, James V, Mukhamedshina YO, Rizvanov AA. Therapeutic potential of extracellular vesicles for the treatment of nerve disorders. Front Neurosci 2019; 13: 163.
[http://dx.doi.org/10.3389/fnins.2019.00163] [PMID: 30890911]
[46]
Osorio-Querejeta I, Alberro A, Muñoz-Culla M, Mäger I, Otaegui D. Therapeutic potential of extracellular vesicles for demyelinating diseases; challenges and opportunities. Front Mol Neurosci 2018; 11: 434-4.
[http://dx.doi.org/10.3389/fnmol.2018.00434] [PMID: 30532691]
[47]
Casella G, Colombo F, Finardi A, et al. Extracellular vesicles containing IL-4 modulate neuroinflammation in a mouse model of multiple sclerosis. Mol Ther 2018; 26(9): 2107-18.
[http://dx.doi.org/10.1016/j.ymthe.2018.06.024] [PMID: 30017878]
[48]
Laso-García F, Ramos-Cejudo J, Carrillo-Salinas FJ, et al. Therapeutic potential of extracellular vesicles derived from human mesenchymal stem cells in a model of progressive multiple sclerosis. PLoS One 2018; 13(9) e0202590
[http://dx.doi.org/10.1371/journal.pone.0202590] [PMID: 30231069]
[49]
Campanella C, Caruso Bavisotto C, Logozzi M, et al. On the choice of the extracellular vesicles for therapeutic purposes. Int J Mol Sci 2019; 20(2) E236
[http://dx.doi.org/10.3390/ijms20020236] [PMID: 30634425]
[50]
Rani S, Ryan AE, Griffin MD, Ritter T. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther 2015; 23(5): 812-23.
[http://dx.doi.org/10.1038/mt.2015.44] [PMID: 25868399]
[51]
Baulch JE, Acharya MM, Allen BD, et al. Cranial grafting of stem cell-derived microvesicles improves cognition and reduces neuropathology in the irradiated brain. Proc Natl Acad Sci USA 2016; 113(17): 4836-41.
[http://dx.doi.org/10.1073/pnas.1521668113] [PMID: 27044087]
[52]
Rajendran L, Bali J, Barr MM, et al. Emerging roles of extracellular vesicles in the nervous system. J Neurosci 2014; 34(46): 15482-9.
[http://dx.doi.org/10.1523/JNEUROSCI.3258-14.2014] [PMID: 25392515]
[53]
Skog J, Würdinger 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(12): 1470-6.
[http://dx.doi.org/10.1038/ncb1800] [PMID: 19011622]
[54]
Grey M, Dunning CJ, Gaspar R, et al. Acceleration of α-synuclein aggregation by exosomes. J Biol Chem 2015; 290(5): 2969-82.
[http://dx.doi.org/10.1074/jbc.M114.585703] [PMID: 25425650]
[55]
Stuendl A, Kunadt M, Kruse N, et al. Induction of α-synuclein aggregate formation by CSF exosomes from patients with Parkinson’s disease and dementia with Lewy bodies. Brain 2016; 139(Pt 2): 481-94.
[http://dx.doi.org/10.1093/brain/awv346] [PMID: 26647156]
[56]
Yuan D, Zhao Y, Banks WA, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials 2017; 142: 1-12.
[http://dx.doi.org/10.1016/j.biomaterials.2017.07.011] [PMID: 28715655]
[57]
Xu L, Cao H, Xie Y, et al. Exosome-shuttled miR-92b-3p from ischemic preconditioned astrocytes protects neurons against oxygen and glucose deprivation. Brain Res 2019; 1717: 66-73.
[http://dx.doi.org/10.1016/j.brainres.2019.04.009] [PMID: 30986407]
[58]
Zhao C, Wang H, Xiong C, Liu Y. Hypoxic glioblastoma release exosomal VEGF-A induce the permeability of blood-brain barrier. Biochem Biophys Res Commun 2018; 502(3): 324-31.
[http://dx.doi.org/10.1016/j.bbrc.2018.05.140] [PMID: 29787762]
[59]
Li Y, Chopp M. Marrow stromal cell transplantation in stroke and traumatic brain injury. Neurosci Lett 2009; 456(3): 120-3.
[http://dx.doi.org/10.1016/j.neulet.2008.03.096] [PMID: 19429146]
[60]
Abdallah BM, Kassem M. Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther 2008; 15(2): 109-16.
[http://dx.doi.org/10.1038/sj.gt.3303067] [PMID: 17989700]
[61]
Kim DK, Nishida H, An SY, Shetty AK, Bartosh TJ, Prockop DJ. Chromatographically isolated CD63+CD81+ extracellular vesicles from mesenchymal stromal cells rescue cognitive impairments after TBI. Proc Natl Acad Sci USA 2016; 113(1): 170-5.
[http://dx.doi.org/10.1073/pnas.1522297113] [PMID: 26699510]
[62]
Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell 2012; 10(6): 709-16.
[http://dx.doi.org/10.1016/j.stem.2012.05.015] [PMID: 22704511]
[63]
Qu C, Mahmood A, Lu D, Goussev A, Xiong Y, Chopp M. Treatment of traumatic brain injury in mice with marrow stromal cells. Brain Res 2008; 1208: 234-9.
[http://dx.doi.org/10.1016/j.brainres.2008.02.042] [PMID: 18384759]
[64]
Hofstetter CP, Schwarz EJ, Hess D, et al. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 2002; 99(4): 2199-204.
[http://dx.doi.org/10.1073/pnas.042678299] [PMID: 11854516]
[65]
Ohtaki H, Ylostalo JH, Foraker JE, et al. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci USA 2008; 105(38): 14638-43.
[http://dx.doi.org/10.1073/pnas.0803670105] [PMID: 18794523]
[66]
Lim PK, Patel SA, Gregory LA, Rameshwar P. Neurogenesis: role for microRNAs and mesenchymal stem cells in pathological states. Curr Med Chem 2010; 17(20): 2159-67.
[http://dx.doi.org/10.2174/092986710791299894] [PMID: 20423304]
[67]
Lee RH, Yu JM, Foskett AM, et al. TSG-6 as a biomarker to predict efficacy of human mesenchymal stem/progenitor cells (hMSCs) in modulating sterile inflammation in vivo. Proc Natl Acad Sci USA 2014; 111(47): 16766-71.
[http://dx.doi.org/10.1073/pnas.1416121111] [PMID: 25385603]
[68]
Oh JY, Roddy GW, Choi H, et al. Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. Proc Natl Acad Sci USA 2010; 107(39): 16875-80.
[http://dx.doi.org/10.1073/pnas.1012451107] [PMID: 20837529]
[69]
Lee RH, Pulin AA, Seo MJ, et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009; 5(1): 54-63.
[http://dx.doi.org/10.1016/j.stem.2009.05.003] [PMID: 19570514]
[70]
Yáñez-Mó M, Siljander PRM, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015; 4: 27066-6.
[http://dx.doi.org/10.3402/jev.v4.27066] [PMID: 25979354]
[71]
György B, Hung ME, Breakefield XO, Leonard JN. Therapeutic applications of extracellular vesicles: clinical promise and open questions. Annu Rev Pharmacol Toxicol 2015; 55(1): 439-64.
[http://dx.doi.org/10.1146/annurev-pharmtox-010814-124630] [PMID: 25292428]
[72]
Xin H, Li Y, Buller B, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 2012; 30(7): 1556-64.
[http://dx.doi.org/10.1002/stem.1129] [PMID: 22605481]
[73]
Xin H, Li Y, Cui Y, Yang JJ, Zhang ZG, Chopp M. Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J Cereb Blood Flow Metab 2013; 33(11): 1711-5.
[http://dx.doi.org/10.1038/jcbfm.2013.152] [PMID: 23963371]
[74]
Xin H, Li Y, Liu Z, et al. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. Stem Cells 2013; 31(12): 2737-46.
[http://dx.doi.org/10.1002/stem.1409] [PMID: 23630198]
[75]
Chen J, Li Y, Katakowski M, et al. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 2003; 73(6): 778-86.
[http://dx.doi.org/10.1002/jnr.10691] [PMID: 12949903]
[76]
Chen J, Li Y, Wang L, et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001; 32(4): 1005-11.
[http://dx.doi.org/10.1161/01.STR.32.4.1005] [PMID: 11283404]
[77]
Pusic AD, Pusic KM, Clayton BLL, Kraig RP. IFNγ-stimulated dendritic cell exosomes as a potential therapeutic for remyelination. J Neuroimmunol 2014; 266(1-2): 12-23.
[http://dx.doi.org/10.1016/j.jneuroim.2013.10.014] [PMID: 24275061]
[78]
Pusic AD, Kraig RP. Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination. Glia 2014; 62(2): 284-99.
[http://dx.doi.org/10.1002/glia.22606] [PMID: 24339157]
[79]
Takeda YS, Xu Q. Neuronal differentiation of human mesenchymal stem cells using exosomes derived from differentiating neuronal cells. PLoS One 2015; 10(8) e0135111
[http://dx.doi.org/10.1371/journal.pone.0135111] [PMID: 26248331]
[80]
Yuyama K, Sun H, Mitsutake S, Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia. J Biol Chem 2012; 287(14): 10977-89.
[http://dx.doi.org/10.1074/jbc.M111.324616] [PMID: 22303002]
[81]
Yuyama K, Sun H, Sakai S, et al. Decreased amyloid-β pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in Alzheimer model mice. J Biol Chem 2014; 289(35): 24488-98.
[http://dx.doi.org/10.1074/jbc.M114.577213] [PMID: 25037226]
[82]
Fernandes A, Ribeiro AR, Monteiro M, Garcia G, Vaz AR, Brites D. Secretome from SH-SY5Y APPSwe cells trigger time-dependent CHME3 microglia activation phenotypes, ultimately leading to miR-21 exosome shuttling. Biochimie 2018; 155: 67-82.
[http://dx.doi.org/10.1016/j.biochi.2018.05.015] [PMID: 29857185]
[83]
Nguyen KT, Pham MN, Vo TV, Duan W, Tran PH, Tran TT. Strategies of engineering nanoparticles for treating neurodegenerative disorders. Curr Drug Metab 2017; 18(9): 786-97.
[http://dx.doi.org/10.2174/1389200218666170125114751] [PMID: 28124594]
[84]
Khanh TMT, Wei D, Tran PHL, Tran TTD. Nanotechnology in neuroscience and its perspective as gene carrier. Curr Top Med Chem 2017; 17(12): 1379-89.
[http://dx.doi.org/10.2174/1568026616666161222145654] [PMID: 28017150]
[85]
Rufino-Ramos D, Albuquerque PR, Carmona V, Perfeito R, Nobre RJ, Pereira de Almeida L. Extracellular vesicles: novel promising delivery systems for therapy of brain diseases. J Control Release 2017; 262: 247-58.
[http://dx.doi.org/10.1016/j.jconrel.2017.07.001] [PMID: 28687495]
[86]
Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 2014; 35(7): 2383-90.
[http://dx.doi.org/10.1016/j.biomaterials.2013.11.083] [PMID: 24345736]
[87]
Bunggulawa EJ, Wang W, Yin T, et al. Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnology 2018; 16(1): 81-1.
[http://dx.doi.org/10.1186/s12951-018-0403-9] [PMID: 30326899]
[88]
Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010; 18(9): 1606-14.
[http://dx.doi.org/10.1038/mt.2010.105] [PMID: 20571541]
[89]
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(10): 1769-79.
[http://dx.doi.org/10.1038/mt.2011.164] [PMID: 21915101]
[90]
Qu M, Lin Q, Huang L, et al. Dopamine-loaded blood exosomes targeted to brain for better treatment of Parkinson’s disease. J Control Release 2018; 287: 156-66.
[http://dx.doi.org/10.1016/j.jconrel.2018.08.035] [PMID: 30165139]
[91]
Pascucci L, Coccè V, Bonomi A, et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Control Release 2014; 192: 262-70.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.042] [PMID: 25084218]
[92]
Haney MJ, Klyachko NL, Zhao Y, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release 2015; 207: 18-30.
[http://dx.doi.org/10.1016/j.jconrel.2015.03.033] [PMID: 25836593]
[93]
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJA. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29(4): 341-5.
[http://dx.doi.org/10.1038/nbt.1807] [PMID: 21423189]
[94]
Yang J, Zhang X, Chen X, Wang L, Yang G. Exosome mediated delivery of miR-124 promotes neurogenesis after ischemia. Mol Ther Nucleic Acids 2017; 7: 278-87.
[http://dx.doi.org/10.1016/j.omtn.2017.04.010] [PMID: 28624203]
[95]
Tian T, Zhang H-X, He C-P, et al. Surface functionalized exosomes as targeted drug delivery vehicles for cerebral ischemia therapy. Biomaterials 2018; 150: 137-49.
[http://dx.doi.org/10.1016/j.biomaterials.2017.10.012] [PMID: 29040874]
[96]
McKinlay A, Radford K, Kato M, et al. Blood monocytes, myeloid dendritic cells and the cytokines interleukin (IL)-7 and IL-15 maintain human CD4+ T memory cells with mixed helper/regulatory function. Immunology 2007; 120(3): 392-403.
[http://dx.doi.org/10.1111/j.1365-2567.2006.02515.x] [PMID: 17239200]
[97]
Livshits MA, Khomyakova E, Evtushenko EG, et al. Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol. Sci Rep 2015; 5: 17319.
[http://dx.doi.org/10.1038/srep17319] [PMID: 26616523]
[98]
Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methodsproteomic profiling: methods and protocols. New York, NY: Springer New York 2015; pp. 179-209.
[http://dx.doi.org/10.1007/978-1-4939-2550-6_15]
[99]
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): 2003-14.
[http://dx.doi.org/10.1007/s11095-014-1593-y] [PMID: 25609010]
[100]
Didiot M-C, Hall LM, Coles AH, et al. Exosome-mediated delivery of hydrophobically modified siRNA for huntingtin mRNA silencing. Mol Ther 2016; 24(10): 1836-47.
[http://dx.doi.org/10.1038/mt.2016.126] [PMID: 27506293]
[101]
Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20(9): 1487-95.
[http://dx.doi.org/10.1038/sj.leu.2404296] [PMID: 16791265]
[102]
György B, Módos K, Pállinger E, et al. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood 2011; 117(4): e39-48.
[http://dx.doi.org/10.1182/blood-2010-09-307595] [PMID: 21041717]
[103]
Pessina A, Bonomi A, Coccè V, et al. Mesenchymal stromal cells primed with paclitaxel provide a new approach for cancer therapy. PLoS One 2011; 6(12) e28321
[http://dx.doi.org/10.1371/journal.pone.0028321] [PMID: 22205945]
[104]
Amidzadeh Z, Behbahani AB, Erfani N, et al. Assessment of different permeabilization methods of minimizing damage to the adherent cells for detection of intracellular RNA by flow cytometry. Avicenna J Med Biotechnol 2014; 6(1): 38-46.
[PMID: 24523954]
[105]
Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM. Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J Control Release 2015; 205: 35-44.
[http://dx.doi.org/10.1016/j.jconrel.2014.11.029] [PMID: 25483424]
[106]
Jamur MC, Oliver C. Permeabilization of cell membranesimmunocytochemical methods and protocols. Totowa, NJ: Humana Press 2010; pp. 63-6.
[http://dx.doi.org/10.1007/978-1-59745-324-0_9]
[107]
Kim MS, Haney MJ, Zhao Y, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine (Lond) 2016; 12(3): 655-64.
[http://dx.doi.org/10.1016/j.nano.2015.10.012] [PMID: 26586551]
[108]
Kim MS, Haney MJ, Zhao Y, et al. Engineering macrophage-derived exosomes for targeted paclitaxel delivery to pulmonary metastases: in vitro and in vivo evaluations. Nanomedicine (Lond) 2018; 14(1): 195-204.
[http://dx.doi.org/10.1016/j.nano.2017.09.011] [PMID: 28982587]
[109]
Wahlgren J, De L, Karlson T, Brisslert M, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 2012; 40(17): e130-0.
[http://dx.doi.org/10.1093/nar/gks463] [PMID: 22618874]
[110]
Aqil F, Munagala R, Jeyabalan J, et al. Milk exosomes - Natural nanoparticles for siRNA delivery. Cancer Lett 2019; 449: 186-95.
[http://dx.doi.org/10.1016/j.canlet.2019.02.011] [PMID: 30771430]
[111]
Weaver JC. Electroporation: a general phenomenon for manipulating cells and tissues. J Cell Biochem 1993; 51(4): 426-35.
[http://dx.doi.org/10.1002/jcb.2400510407] [PMID: 8496245]
[112]
Hood JL, Scott MJ, Wickline SA. Maximizing exosome colloidal stability following electroporation. Anal Biochem 2014; 448: 41-9.
[http://dx.doi.org/10.1016/j.ab.2013.12.001] [PMID: 24333249]
[113]
Gilligan KE, Dwyer RM. Engineering exosomes for cancer therapy. Int J Mol Sci 2017; 18(6) E1122
[http://dx.doi.org/10.3390/ijms18061122] [PMID: 28538671]
[114]
Bai J, Duan J, Liu R, et al. Engineered targeting tLyp-1 exosomes as gene therapy vectors for efficient delivery of siRNA into lung cancer cells. Asian Journal of Pharmaceutical Sciences 2019. In Press
[http://dx.doi.org/10.1016/j.ajps.2019.04.002]
[115]
Katakowski M, Buller B, Zheng X, et al. Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett 2013; 335(1): 201-4.
[http://dx.doi.org/10.1016/j.canlet.2013.02.019] [PMID: 23419525]
[116]
Thorne RG, Pronk GJ, Padmanabhan V, Frey WH II. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 2004; 127(2): 481-96.
[http://dx.doi.org/10.1016/j.neuroscience.2004.05.029] [PMID: 15262337]
[117]
Xie X, Wu H, Li M, et al. Progress in the application of exosomes as therapeutic vectors in tumor-targeted therapy. Cytotherapy 2019; 21(5): 509-24.
[http://dx.doi.org/10.1016/j.jcyt.2019.01.001] [PMID: 30686589]
[118]
Cui GH, Guo HD, Li H, et al. RVG-modified exosomes derived from mesenchymal stem cells rescue memory deficits by regulating inflammatory responses in a mouse model of Alzheimer’s disease. Immun Ageing 2019; 16(1): 10.
[http://dx.doi.org/10.1186/s12979-019-0150-2] [PMID: 31114624]
[119]
Chen Q, Wang X, Wang C, Feng L, Li Y, Liu Z. Drug-induced self-assembly of modified albumins as nano-theranostics for tumor-targeted combination therapy. ACS Nano 2015; 9(5): 5223-33.
[http://dx.doi.org/10.1021/acsnano.5b00640] [PMID: 25950506]
[120]
Guell K, Bix GJ. Brain endothelial cell specific integrins and ischemic stroke. Expert Rev Neurother 2014; 14(11): 1287-92.
[http://dx.doi.org/10.1586/14737175.2014.964210] [PMID: 25262658]
[121]
Haubner R, Wester HJ, Burkhart F, et al. Glycosylated RGD-containing peptides: tracer for tumor targeting and angiogenesis imaging with improved biokinetics. J Nucl Med 2001; 42(2): 326-36.
[PMID: 11216533]
[122]
Arosio D, Casagrande C. Advancement in integrin facilitated drug delivery. Adv Drug Deliv Rev 2016; 97: 111-43.
[http://dx.doi.org/10.1016/j.addr.2015.12.001] [PMID: 26686830]

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