Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Exosome-like Nanovectors for Drug Delivery in Cancer

Author(s): Noemi Arrighetti, Claudia Corbo, Michael Evangelopoulos, Anna Pastò, Valentina Zuco and Ennio Tasciotti*

Volume 26, Issue 33, 2019

Page: [6132 - 6148] Pages: 17

DOI: 10.2174/0929867325666180831150259

Price: $65

Abstract

Cancer treatment still represents a formidable challenge, despite substantial advancements in available therapies being made over the past decade. One major issue is poor therapeutic efficacy due to lack of specificity and low bioavailability. The progress of nanotechnology and the development of a variety of nanoplatforms have had a significant impact in improving the therapeutic outcome of chemotherapeutics. Nanoparticles can overcome various biological barriers and localize at tumor site, while simultaneously protecting a therapeutic cargo and increasing its circulation time. Despite this, due to their synthetic origin, nanoparticles are often detected by the immune system and preferentially sequestered by filtering organs. Exosomes have recently been investigated as suitable substitutes for the shortcomings of nanoparticles due to their biological compatibility and particularly small size (i.e., 30-150 nm). In addition, exosomes have been found to play important roles in cell communication, acting as natural carriers of biological cargoes throughout the body. This review aims to highlight the use of exosomes as drug delivery vehicles for cancer and showcases the various attempts used to exploit exosomes with a focus on the delivery of chemotherapeutics and nucleic acids.

Keywords: Chemotherapy, drug delivery, exosomes, extracellular vesicles, gene therapy, nanoparticles, nanotechnology, surface modifications.

« Previous Next »
[1]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[2]
Blanco, E.; Shen, H.; Ferrari, M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotechnol., 2015, 33(9), 941-951.
[http://dx.doi.org/10.1038/nbt.3330] [PMID: 26348965]
[3]
Son, B.; Lee, S.; Youn, H.; Kim, E.; Kim, W.; Youn, B. The role of tumor microenvironment in therapeutic resistance. Oncotarget, 2017, 8(3), 3933-3945.
[http://dx.doi.org/10.18632/oncotarget.13907] [PMID: 27965469]
[4]
Damia, G.; Garattini, S. The pharmacological point of view of resistance to therapy in tumors. Cancer Treat. Rev., 2014, 40(8), 909-916.
[http://dx.doi.org/10.1016/j.ctrv.2014.05.008] [PMID: 24969326]
[5]
Martinez, J.O.; Evangelopoulos, M.; Bhavane, R.; Acciardo, S.; Salvatore, F.; Liu, X.; Ferrari, M.; Tasciotti, E. Multistage Nanovectors Enhance the Delivery of Free and Encapsulated Drugs. Curr. Drug Targets, 2015, 16(14), 1582-1590.
[http://dx.doi.org/10.2174/1389450115666141015113914] [PMID: 25316273]
[6]
Khaled, S.Z.; Cevenini, A.; Yazdi, I.K.; Parodi, A.; Evangelopoulos, M.; Corbo, C.; Scaria, S.; Hu, Y.; Haddix, S.G.; Corradetti, B.; Salvatore, F.; Tasciotti, E. One-pot synthesis of pH-responsive hybrid nanogel particles for the intracellular delivery of small interfering RNA. Biomaterials, 2016, 87, 57-68.
[http://dx.doi.org/10.1016/j.biomaterials.2016.01.052] [PMID: 26901429]
[7]
Martinez, J.O.; Evangelopoulos, M.; Chiappini, C.; Liu, X.; Ferrari, M.; Tasciotti, E. Degradation and biocompatibility of multistage nanovectors in physiological systems. J. Biomed. Mater. Res. A, 2014, 102(10), 3540-3549.
[http://dx.doi.org/10.1002/jbm.a.35017] [PMID: 25269799]
[8]
Martinez, J.O.; Boada, C.; Yazdi, I.K.; Evangelopoulos, M.; Brown, B.S.; Liu, X.; Ferrari, M.; Tasciotti, E. Short and long term, in vitro and in vivo correlations of cellular and tissue responses to mesoporous silicon nanovectors. Small, 2013, 9(9-10), 1722-1733.
[http://dx.doi.org/10.1002/smll.201201939] [PMID: 23255523]
[9]
Balasubramanian, K.; Evangelopoulos, M.; Brown, B.S.; Parodi, A.; Celia, C.; Yazdi, I.K.; Tasciotti, E. Ghee butter as a therapeutic delivery system. J. Nanosci. Nanotechnol., 2017, 17(2), 977-982.
[http://dx.doi.org/10.1166/jnn.2017.12623] [PMID: 29671486]
[10]
Molinaro, R.; Corbo, C.; Livingston, M.; Evangelopoulos, M.; Parodi, A.; Boada, C.; Agostini, M.; Tasciotti, E. Inflammation and cancer: in medio stat nano. Curr. Med. Chem., 2018, 25(34), 4208-4223.
[http://dx.doi.org/10.2174/0929867324666170920160030] [PMID: 28933296]
[11]
Corradetti, B.; Taraballi, F.; Martinez, J.O.; Minardi, S.; Basu, N.; Bauza, G.; Evangelopoulos, M.; Powell, S.; Corbo, C.; Tasciotti, E. Hyaluronic acid coatings as a simple and efficient approach to improve MSC homing toward the site of inflammation. Sci. Rep., 2017, 7(1), 7991.
[http://dx.doi.org/10.1038/s41598-017-08687-3] [PMID: 28801676]
[12]
Näkki, S.; Martinez, J.O.; Evangelopoulos, M.; Xu, W.; Lehto, V.P.; Tasciotti, E. Chlorin e6 Functionalized Theranostic Multistage Nanovectors Transported by Stem Cells for Effective Photodynamic Therapy. ACS Appl. Mater. Interfaces, 2017, 9(28), 23441-23449.
[http://dx.doi.org/10.1021/acsami.7b05766] [PMID: 28640590]
[13]
Scavo, M.P.; Gentile, E.; Wolfram, J.; Gu, J.; Barone, M.; Evangelopoulos, M.; Martinez, J.O.; Liu, X.; Celia, C.; Tasciotti, E.; Vilar, E.; Shen, H. Multistage vector delivery of sulindac and silymarin for prevention of colon cancer. Colloids Surf. B Biointerfaces, 2015, 136, 694-703.
[http://dx.doi.org/10.1016/j.colsurfb.2015.10.005] [PMID: 26513752]
[14]
Fernandez-Moure, J.S.; Evangelopoulos, M.; Colvill, K.; Van Eps, J.L.; Tasciotti, E. Nanoantibiotics: a new paradigm for the treatment of surgical infection. Nanomedicine (Lond.), 2017, 12(11), 1319-1334.
[http://dx.doi.org/10.2217/nnm-2017-0401] [PMID: 28520517]
[15]
Wang, A.Z.; Langer, R.; Farokhzad, O.C. Nanoparticle delivery of cancer drugs. Annu. Rev. Med., 2012, 63, 185-198.
[http://dx.doi.org/10.1146/annurev-med-040210-162544] [PMID: 21888516]
[16]
Ngoune, R.; Peters, A.; von Elverfeldt, D.; Winkler, K.; Pütz, G. Accumulating nanoparticles by EPR: A route of no return. J. Control. Release, 2016, 238, 58-70.
[http://dx.doi.org/10.1016/j.jconrel.2016.07.028] [PMID: 27448444]
[17]
Xu, X.; Saw, P.E.; Tao, W.; Li, Y.; Ji, X.; Bhasin, S.; Liu, Y.; Ayyash, D.; Rasmussen, J.; Huo, M.; Shi, J.; Farokhzad, O.C. ROS-responsive polyprodrug nanoparticles for triggered drug delivery and effective cancer therapy. Adv. Mater., 2017, 29(33), 33.
[http://dx.doi.org/10.1002/adma.201700141] [PMID: 28681981]
[18]
Zolnik, B.S.; González-Fernández, A.; Sadrieh, N.; Dobrovolskaia, M.A. Nanoparticles and the immune system. Endocrinology, 2010, 151(2), 458-465.
[http://dx.doi.org/10.1210/en.2009-1082] [PMID: 20016026]
[19]
Song, G.; Petschauer, J.S.; Madden, A.J.; Zamboni, W.C. Nanoparticles and the mononuclear phagocyte system: pharmacokinetics and applications for inflammatory diseases. Curr. Rheumatol. Rev., 2014, 10(1), 22-34.
[http://dx.doi.org/10.2174/1573403X10666140914160554] [PMID: 25229496]
[20]
Tran, S.; DeGiovanni, P.J.; Piel, B.; Rai, P. Cancer nanomedicine: a review of recent success in drug delivery. Clin. Transl. Med., 2017, 6(1), 44.
[http://dx.doi.org/10.1186/s40169-017-0175-0] [PMID: 29230567]
[21]
Milla, P.; Dosio, F.; Cattel, L. PEGylation of proteins and liposomes: a powerful and flexible strategy to improve the drug delivery. Curr. Drug Metab., 2012, 13(1), 105-119.
[http://dx.doi.org/10.2174/138920012798356934] [PMID: 21892917]
[22]
Gabizon, A.A. Stealth liposomes and tumor targeting: one step further in the quest for the magic bullet. Clin. Cancer Res., 2001, 7(2), 223-225.
[PMID: 11234871]
[23]
Parodi, A.; Molinaro, R.; Sushnitha, M.; Evangelopoulos, M.; Martinez, J.O.; Arrighetti, N.; Corbo, C.; Tasciotti, E. Bio-inspired engineering of cell- and virus-like nanoparticles for drug delivery. Biomaterials, 2017, 147, 155-168.
[http://dx.doi.org/10.1016/j.biomaterials.2017.09.020] [PMID: 28946131]
[24]
He, C.; Zheng, S.; Luo, Y.; Wang, B. Exosome theranostics: biology and translational medicine. Theranostics, 2018, 8(1), 237-255.
[http://dx.doi.org/10.7150/thno.21945] [PMID: 29290805]
[25]
Clayton, A.; Court, J.; Navabi, H.; Adams, M.; Mason, M.D.; Hobot, J.A.; Newman, G.R.; Jasani, B. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J. Immunol. Methods, 2001, 247(1-2), 163-174.
[http://dx.doi.org/10.1016/S0022-1759(00)00321-5] [PMID: 11150547]
[26]
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(3), 1161-1172.
[http://dx.doi.org/10.1084/jem.183.3.1161] [PMID: 8642258]
[27]
Clayton, A.; Harris, C.L.; Court, J.; Mason, M.D.; Morgan, B.P. Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59. Eur. J. Immunol., 2003, 33(2), 522-531.
[http://dx.doi.org/10.1002/immu.200310028] [PMID: 12645951]
[28]
Mathivanan, S.; Ji, H.; Simpson, R.J. Exosomes: extracellular organelles important in intercellular communication. J. Proteomics, 2010, 73(10), 1907-1920.
[http://dx.doi.org/10.1016/j.jprot.2010.06.006] [PMID: 20601276]
[29]
Cocucci, E.; Meldolesi, J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol., 2015, 25(6), 364-372.
[http://dx.doi.org/10.1016/j.tcb.2015.01.004] [PMID: 25683921]
[30]
Mulcahy, L.A.; Pink, R.C.; Carter, D.R. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles, 2014, 3, 24641.
[http://dx.doi.org/10.3402/jev.v3.24641] [PMID: 25143819]
[31]
Parolini, I.; Federici, C.; Raggi, C.; Lugini, L.; Palleschi, S.; De Milito, A.; Coscia, C.; Iessi, E.; Logozzi, M.; Molinari, A.; Colone, M.; Tatti, M.; Sargiacomo, M.; Fais, S. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem., 2009, 284(49), 34211-34222.
[http://dx.doi.org/10.1074/jbc.M109.041152] [PMID: 19801663]
[32]
E.L., Andaloussi S.; Mäger, I.; Breakefield, X.O.; Wood, M.J. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov., 2013, 12(5), 347-357.
[http://dx.doi.org/10.1038/nrd3978] [PMID: 23584393]
[33]
Whiteside, T.L. Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment Semin. Immunol., 2017. S1044-5323, 30010-6.
[34]
Yue, S.; Mu, W.; Erb, U.; Zöller, M. The tetraspanins CD151 and Tspan8 are essential exosome components for the crosstalk between cancer initiating cells and their surrounding. Oncotarget, 2015, 6(4), 2366-2384.
[http://dx.doi.org/10.18632/oncotarget.2958] [PMID: 25544774]
[35]
Koch, R.; Aung, T.; Vogel, D.; Chapuy, B.; Wenzel, D.; Becker, S.; Sinzig, U.; Venkataramani, V.; von Mach, T.; Jacob, R.; Truemper, L.; Wulf, G.G. Nuclear Trapping through Inhibition of Exosomal Export by Indomethacin Increases Cytostatic Efficacy of Doxorubicin and Pixantrone. Clin. Cancer Res., 2016, 22(2), 395-404.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0577] [PMID: 26369630]
[36]
Goler-Baron, V.; Assaraf, Y.G. Overcoming multidrug resistance via photodestruction of ABCG2-rich extracellular vesicles sequestering photosensitive chemotherapeutics. PLoS One, 2012, 7(4)e35487
[http://dx.doi.org/10.1371/journal.pone.0035487] [PMID: 22530032]
[37]
Sharma, A. Chemoresistance in cancer cells: exosomes as potential regulators of therapeutic tumor heterogeneity. Nanomedicine (Lond.), 2017, 12(17), 2137-2148.
[http://dx.doi.org/10.2217/nnm-2017-0184] [PMID: 28805111]
[38]
García-Manrique, P.; Matos, M.; Gutiérrez, G.; Pazos, C.; Blanco-López, M.C. Therapeutic biomaterials based on extracellular vesicles: classification of bio-engineering and mimetic preparation routes. J. Extracell. Vesicles, 2018, 7(1)1422676
[http://dx.doi.org/10.1080/20013078.2017.1422676] [PMID: 29372017]
[39]
Wahlund, C.J.E.; Güclüler, G.; Hiltbrunner, S.; Veerman, R.E.; Näslund, T.I.; Gabrielsson, S. Exosomes from antigen-pulsed dendritic cells induce stronger antigen-specific immune responses than microvesicles in vivo. Sci. Rep., 2017, 7(1), 17095.
[http://dx.doi.org/10.1038/s41598-017-16609-6] [PMID: 29213052]
[40]
Tian, T.; Zhang, H.X.; He, C.P.; Fan, S.; Zhu, Y.L.; Qi, C.; Huang, N.P.; Xiao, Z.D.; Lu, Z.H.; Tannous, B.A.; Gao, J. Surface functionalized exosomes as targeted drug delivery vehicles for cerebral ischemia therapy. Biomaterials, 2018, 150, 137-149.
[http://dx.doi.org/10.1016/j.biomaterials.2017.10.012] [PMID: 29040874]
[41]
Study investigating the ability of plant exosomes to deliver curcumin to normal and colon cancer tissue. Available at: clinicaltrials.gov/
[42]
Taylor, D.D.; Zacharias, W.; Gercel-Taylor, C. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol. Biol., 2011, 728, 235-246.
[http://dx.doi.org/10.1007/978-1-61779-068-3_15] [PMID: 21468952]
[43]
Lässer, C.; Eldh, M.; Lötvall, J. Isolation and characterization of RNA-containing exosomes. J. Vis. Exp., 2012, 59(59)e3037
[http://dx.doi.org/ 10.3791/3037] [PMID: 22257828]
[44]
Alvarez, M.L.; Khosroheidari, M.; Kanchi Ravi, R.; DiStefano, J.K. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int., 2012, 82(9), 1024-1032.
[http://dx.doi.org/10.1038/ki.2012.256] [PMID: 22785172]
[45]
Tauro, B.J.; Greening, D.W.; Mathias, R.A.; Ji, H.; Mathivanan, S.; Scott, A.M.; Simpson, R.J. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods, 2012, 56(2), 293-304.
[http://dx.doi.org/10.1016/j.ymeth.2012.01.002] [PMID: 22285593]
[46]
Bobrie, A.; Colombo, M.; Krumeich, S.; Raposo, G.; Théry, C. Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J. Extracell. Vesicles, 2012, 1, 1.
[http://dx.doi.org/10.3402/jev.v1i0.18397] [PMID: 24009879]
[47]
Cheruvanky, A.; Zhou, H.; Pisitkun, T.; Kopp, J.B.; Knepper, M.A.; Yuen, P.S.; Star, R.A. Rapid isolation of urinary exosomal biomarkers using a nanomembrane ultrafiltration concentrator. Am. J. Physiol. Renal Physiol., 2007, 292(5), F1657-F1661.
[http://dx.doi.org/10.1152/ajprenal.00434.2006] [PMID: 17229675]
[48]
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. Proteomics Clin. Appl., 2010, 4(1), 84-96.
[http://dx.doi.org/10.1002/prca.200800093] [PMID: 21137018]
[49]
Yoo, C.E.; Kim, G.; Kim, M.; Park, D.; Kang, H.J.; Lee, M.; Huh, N. A direct extraction method for microRNAs from exosomes captured by immunoaffinity beads. Anal. Biochem., 2012, 431(2), 96-98.
[http://dx.doi.org/10.1016/j.ab.2012.09.008] [PMID: 22982508]
[50]
Mathivanan, S.; Lim, J.W.; Tauro, B.J.; Ji, H.; Moritz, R.L.; Simpson, R.J. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol. Cell. Proteomics, 2010, 9(2), 197-208.
[http://dx.doi.org/10.1074/mcp.M900152-MCP200] [PMID: 19837982]
[51]
Kanwar, S.S.; Dunlay, C.J.; Simeone, D.M.; Nagrath, S. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip, 2014, 14, 1891-1900.
[52]
Liga, A.; Vliegenthart, A.D.; Oosthuyzen, W.; Dear, J.W.; Kersaudy-Kerhoas, M. Exosome isolation: a microfluidic road-map. Lab Chip, 2015, 15(11), 2388-2394.
[http://dx.doi.org/10.1039/C5LC00240K] [PMID: 25940789]
[53]
Jang, S.C.; Kim, O.Y.; Yoon, C.M.; Choi, D.S.; Roh, T.Y.; Park, J.; Nilsson, J.; Lötvall, J.; Kim, Y.K.; Gho, Y.S. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano, 2013, 7(9), 7698-7710.
[http://dx.doi.org/10.1021/nn402232g] [PMID: 24004438]
[54]
Lai, R.C.; Yeo, R.W.Y.; Tan, K.H.; Lim, S.K. Exosomes for drug delivery - a novel application for the mesenchymal stem cell. Biotechnol. Adv., 2013, 31(5), 543-551.
[http://dx.doi.org/10.1016/j.biotechadv.2012.08.008] [PMID: 22959595]
[55]
Jamur, M.C.; Oliver, C. Permeabilization of cell membranes. Methods Mol. Biol., 2010, 588, 63-66.
[http://dx.doi.org/10.1007/978-1-59745-324-0_9] [PMID: 20012820]
[56]
Sato, Y.T.; Umezaki, K.; Sawada, S.; Mukai, S.A.; Sasaki, Y.; Harada, N.; Shiku, H.; Akiyoshi, K. Engineering hybrid exosomes by membrane fusion with liposomes. Sci. Rep., 2016, 6, 21933.
[http://dx.doi.org/10.1038/srep21933] [PMID: 26911358]
[57]
Kim, M.S.; Haney, M.J.; Zhao, Y.; Mahajan, V.; Deygen, I.; Klyachko, N.L.; Inskoe, E.; Piroyan, A.; Sokolsky, M.; Okolie, O.; Hingtgen, S.D.; Kabanov, A.V.; Batrakova, E.V. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine (Lond.), 2016, 12(3), 655-664.
[http://dx.doi.org/10.1016/j.nano.2015.10.012] [PMID: 26586551]
[58]
Luan, X.; Sansanaphongpricha, K.; Myers, I.; Chen, H.; Yuan, H.; Sun, D. Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol. Sin., 2017, 38(6), 754-763.
[http://dx.doi.org/10.1038/aps.2017.12] [PMID: 28392567]
[59]
Fuhrmann, G.; Serio, A.; Mazo, M.; Nair, R.; Stevens, M.M. 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]
[60]
Pascucci, L.; Coccè, V.; Bonomi, A.; Ami, D.; Ceccarelli, P.; Ciusani, E.; Viganò, L.; Locatelli, A.; Sisto, F.; Doglia, S.M.; Parati, E.; Bernardo, M.E.; Muraca, M.; Alessandri, G.; Bondiolotti, G.; Pessina, A. 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, 262-270.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.042] [PMID: 25084218]
[61]
Monopoli, M.P.; Zendrini, A.; Wu, D.; Cheung, S.; Sampedro, G.; Ffrench, B.; Nolan, J.; Piskareva, O.; Stalings, R.L.; Ducoli, S.; Bergese, P.; O’Shea, D.F. Endogenous exosome labelling with an amphiphilic NIR-fluorescent probe. Chem. Commun. (Camb.), 2018, 54(52), 7219-7222.
[http://dx.doi.org/10.1039/C8CC02135J] [PMID: 29900459]
[62]
Whiteside, T.L. Tumor-derived exosomes and their role in cancer progression. Adv. Clin. Chem., 2016, 74, 103-141.
[http://dx.doi.org/10.1016/bs.acc.2015.12.005] [PMID: 27117662]
[63]
Romagnoli, G.G.; Zelante, B.B.; Toniolo, P.A.; Migliori, I.K.; Barbuto, J.A.M. Dendritic cell-derived exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front. Immunol., 2015, 5, 692.
[http://dx.doi.org/10.3389/fimmu.2014.00692] [PMID: 25646096]
[64]
Vader, P.; Mol, E.A.; Pasterkamp, G.; Schiffelers, R.M. Extracellular vesicles for drug delivery Adv. Drug Deliv. Rev., ., 2016, 106(Pt A), 148-156.
[http://dx.doi.org/10.1016/j.addr.2016.02.006] [PMID: 26928656]
[65]
Smyth, T.; Kullberg, M.; Malik, N.; Smith-Jones, P.; Graner, M.W.; Anchordoquy, T.J. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J. Control. Release, 2015, 199, 145-155.
[http://dx.doi.org/10.1016/j.jconrel.2014.12.013] [PMID: 25523519]
[66]
Whiteside, T.L. The effect of tumor-derived exosomes on immune regulation and cancer immunotherapy. Future Oncol., 2017, 13(28), 2583-2592.
[http://dx.doi.org/10.2217/fon-2017-0343] [PMID: 29198150]
[67]
Taylor, D.D.; Gercel-Taylor, C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol., 2008, 110(1), 13-21.
[http://dx.doi.org/10.1016/j.ygyno.2008.04.033] [PMID: 18589210]
[68]
Jin, H.; Tan, X. Differential proteomic analysis of pancreatic cancer cell-derived exosomes provides new insights into cancer metastasis and novel biomarkers for early detection. Pancreatology, 2017, 17, S23.
[http://dx.doi.org/10.1016/j.pan.2017.07.077]
[69]
Henderson, M.C.; Azorsa, D.O. The genomic and proteomic content of cancer cell-derived exosomes. Front. Oncol., 2012, 2, 38.
[http://dx.doi.org/10.3389/fonc.2012.00038] [PMID: 22649786]
[70]
Kharaziha, P.; Ceder, S.; Li, Q.; Panaretakis, T. Tumor cell-derived exosomes: a message in a bottle. Biochim. Biophys. Acta, 2012, 1826(1), 103-111.
[http://dx.doi.org/ 10.1016/j.bbcan.2012.03.006] [PMID: 22503823]
[71]
Izumi, H.; Tsuda, M.; Sato, Y.; Kosaka, N.; Ochiya, T.; Iwamoto, H.; Namba, K.; Takeda, Y. Bovine milk exosomes contain microRNA and mRNA and are taken up by human macrophages. J. Dairy Sci., 2015, 98(5), 2920-2933.
[http://dx.doi.org/10.3168/jds.2014-9076] [PMID: 25726110]
[72]
Yamada, T.; Inoshima, Y.; Matsuda, T.; Ishiguro, N. Comparison of methods for isolating exosomes from bovine milk. J. Vet. Med. Sci., 2012, 74(11), 1523-1525.
[http://dx.doi.org/10.1292/jvms.12-0032] [PMID: 22785357]
[73]
Hata, T.; Murakami, K.; Nakatani, H.; Yamamoto, Y.; Matsuda, T.; Aoki, N. Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem. Biophys. Res. Commun., 2010, 396(2), 528-533.
[http://dx.doi.org/10.1016/j.bbrc.2010.04.135] [PMID: 20434431]
[74]
Ju, S.; Mu, J.; Dokland, T.; Zhuang, X.; Wang, Q.; Jiang, H.; Xiang, X.; Deng, Z.B.; Wang, B.; Zhang, L.; Roth, M.; Welti, R.; Mobley, J.; Jun, Y.; Miller, D.; Zhang, H.G. Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis. Mol. Ther., 2013, 21(7), 1345-1357.
[http://dx.doi.org/10.1038/mt.2013.64] [PMID: 23752315]
[75]
Raimondo, S.; Naselli, F.; Fontana, S.; Monteleone, F.; Lo Dico, A.; Saieva, L.; Zito, G.; Flugy, A.; Manno, M.; Di Bella, M.A.; De Leo, G.; Alessandro, R. Citrus limon-derived nanovesicles inhibit cancer cell proliferation and suppress CML xenograft growth by inducing TRAIL-mediated cell death. Oncotarget, 2015, 6(23), 19514-19527.
[http://dx.doi.org/10.18632/oncotarget.4004] [PMID: 26098775]
[76]
Kooijmans, S.A.; Vader, P.; van Dommelen, S.M.; van Solinge, W.W.; Schiffelers, R.M. Exosome mimetics: a novel class of drug delivery systems. Int. J. Nanomedicine, 2012, 7, 1525-1541.
[PMID: 22619510]
[77]
Palomba, R.; Parodi, A.; Evangelopoulos, M.; Acciardo, S.; Corbo, C.; de Rosa, E.; Yazdi, I.K.; Scaria, S.; Molinaro, R.; Furman, N.E.; You, J.; Ferrari, M.; Salvatore, F.; Tasciotti, E. Biomimetic carriers mimicking leukocyte plasma membrane to increase tumor vasculature permeability. Sci. Rep., 2016, 6, 34422.
[http://dx.doi.org/10.1038/srep34422] [PMID: 27703233]
[78]
Evangelopoulos, M.; Parodi, A.; Martinez, J.O.; Yazdi, I.K.; Cevenini, A.; van de Ven, A.L.; Quattrocchi, N.; Boada, C.; Taghipour, N.; Corbo, C.; Brown, B.S.; Scaria, S.; Liu, X.; Ferrari, M.; Tasciotti, E. Cell source determines the immunological impact of biomimetic nanoparticles. Biomaterials, 2016, 82, 168-177.
[http://dx.doi.org/10.1016/j.biomaterials.2015.11.054] [PMID: 26761780]
[79]
Molinaro, R.; Corbo, C.; Martinez, J.O.; Taraballi, F.; Evangelopoulos, M.; Minardi, S.; Yazdi, I.K.; Zhao, P.; De Rosa, E.; Sherman, M.B.; De Vita, A.; Toledano Furman, N.E.; Wang, X.; Parodi, A.; Tasciotti, E. Biomimetic proteolipid vesicles for targeting inflamed tissues. Nat. Mater., 2016, 15(9), 1037-1046.
[http://dx.doi.org/10.1038/nmat4644] [PMID: 27213956]
[80]
Marlin, S.D.; Springer, T.A. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell, 1987, 51(5), 813-819.
[http://dx.doi.org/10.1016/0092-8674(87)90104-8] [PMID: 3315233]
[81]
Martinez, J.O.; Molinaro, R.; Hartman, K.A.; Boada, C.; Sukhovershin, R.; De Rosa, E.; Kirui, D.; Zhang, S.; Evangelopoulos, M.; Carter, A.M.; Bibb, J.A.; Cooke, J.P.; Tasciotti, E. Biomimetic nanoparticles with enhanced affinity towards activated endothelium as versatile tools for theranostic drug delivery. Theranostics, 2018, 8(4), 1131-1145.
[http://dx.doi.org/10.7150/thno.22078] [PMID: 29464004]
[82]
Corbo, C.; Parodi, A.; Evangelopoulos, M.; Engler, D.A.; Matsunami, R.K.; Engler, A.C.; Molinaro, R.; Scaria, S.; Salvatore, F.; Tasciotti, E. Proteomic profiling of a biomimetic drug delivery platform. Curr. Drug Targets, 2015, 16(13), 1540-1547.
[http://dx.doi.org/10.2174/1389450115666141109211413] [PMID: 25382209]
[83]
Corbo, C.; Molinaro, R.; Taraballi, F.; Toledano Furman, N.E.; Sherman, M.B.; Parodi, A.; Salvatore, F.; Tasciotti, E. Effects of the protein corona on liposome-liposome and liposome-cell interactions. Int. J. Nanomedicine, 2016, 11, 3049-3063.
[http://dx.doi.org/10.2147/IJN.S109059] [PMID: 27445473]
[84]
Corbo, C.; Molinaro, R.; Parodi, A.; Toledano Furman, N.E.; Salvatore, F.; Tasciotti, E. The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery. Nanomedicine (Lond.), 2016, 11(1), 81-100.
[http://dx.doi.org/10.2217/nnm.15.188] [PMID: 26653875]
[85]
Corbo, C.; Molinaro, R.; Tabatabaei, M.; Farokhzad, O.C.; Mahmoudi, M. Personalized protein corona on nanoparticles and its clinical implications. Biomater. Sci., 2017, 5(3), 378-387.
[http://dx.doi.org/10.1039/C6BM00921B] [PMID: 28133653]
[86]
Corbo, C.; Molinaro, R.; Taraballi, F.; Toledano Furman, N.E.; Hartman, K.A.; Sherman, M.B.; De Rosa, E.; Kirui, D.K.; Salvatore, F.; Tasciotti, E. Unveiling the in vivo protein corona of circulating leukocyte-like carriers. ACS Nano, 2017, 11(3), 3262-3273.
[http://dx.doi.org/10.1021/acsnano.7b00376] [PMID: 28264157]
[87]
Salvati, A.; Pitek, A.S.; Monopoli, M.P.; Prapainop, K.; Bombelli, F.B.; Hristov, D.R.; Kelly, P.M.; Åberg, C.; Mahon, E.; Dawson, K.A. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol., 2013, 8(2), 137-143.
[http://dx.doi.org/10.1038/nnano.2012.237] [PMID: 23334168]
[88]
Corbo, C.; Cromer, W.E.; Molinaro, R.; Toledano Furman, N.E.; Hartman, K.A.; De Rosa, E.; Boada, C.; Wang, X.; Zawieja, D.C.; Agostini, M.; Salvatore, F.; Abraham, B.P.; Tasciotti, E. Engineered biomimetic nanovesicles show intrinsic anti-inflammatory properties for the treatment of inflammatory bowel diseases. Nanoscale, 2017, 9(38), 14581-14591.
[http://dx.doi.org/10.1039/C7NR04734G] [PMID: 28932838]
[89]
Molinaro, R.; Evangelopoulos, M.; Hoffman, J.R.; Corbo, C.; Taraballi, F.; Martinez, J.O.; Hartman, K.A.; Cosco, D.; Costa, G.; Romeo, I.; Sherman, M.; Paolino, D.; Alcaro, S.; Tasciotti, E. Design and development of biomimetic nanovesicles using a microfluidic approach. Adv. Mater., 2018, 30(15)e1702749
[http://dx.doi.org/10.1002/adma.201702749] [PMID: 29512198]
[90]
Alvarez-Erviti, L.; Seow, Y.; Yin, H.; Betts, C.; Lakhal, S.; Wood, M.J. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol., 2011, 29(4), 341-345.
[http://dx.doi.org/10.1038/nbt.1807] [PMID: 21423189]
[91]
Ohno, S.; Takanashi, M.; Sudo, K.; Ueda, S.; Ishikawa, A.; Matsuyama, N.; Fujita, K.; Mizutani, T.; Ohgi, T.; Ochiya, T.; Gotoh, N.; Kuroda, M. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther., 2013, 21(1), 185-191.
[http://dx.doi.org/10.1038/mt.2012.180] [PMID: 23032975]
[92]
Wang, S.; El-Deiry, W.S. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene, 2003, 22(53), 8628-8633.
[http://dx.doi.org/10.1038/sj.onc.1207232] [PMID: 14634624]
[93]
Rivoltini, L.; Chiodoni, C.; Squarcina, P.; Tortoreto, M.; Villa, A.; Vergani, B.; Bürdek, M.; Botti, L.; Arioli, I.; Cova, A.; Mauri, G.; Vergani, E.; Bianchi, B.; Della Mina, P.; Cantone, L.; Bollati, V.; Zaffaroni, N.; Gianni, A.M.; Colombo, M.P.; Huber, V. TNF-Related Apoptosis-Inducing Ligand (TRAIL)-armed exosomes deliver proapoptotic signals to tumor site. Clin. Cancer Res., 2016, 22(14), 3499-3512.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2170] [PMID: 26944067]
[94]
Yang, Y.; Chen, Y.; Zhang, F.; Zhao, Q.; Zhong, H. Increased anti-tumour activity by exosomes derived from doxorubicin-treated tumour cells via heat stress. Int. J. Hyperthermia, 2015, 31(5), 498-506.
[http://dx.doi.org/10.3109/02656736.2015.1036384] [PMID: 25955015]
[95]
Khalyfa, A.; Almendros, I.; Gileles-Hillel, A.; Akbarpour, M.; Trzepizur, W.; Mokhlesi, B.; Huang, L.; Andrade, J.; Farré, R.; Gozal, D. Circulating exosomes potentiate tumor malignant properties in a mouse model of chronic sleep fragmentation. Oncotarget, 2016, 7(34), 54676-54690.
[http://dx.doi.org/10.18632/oncotarget.10578] [PMID: 27419627]
[96]
Skog, J.; Würdinger, T.; van Rijn, S.; Meijer, D.H.; Gainche, L.; Sena-Esteves, M.; Curry, W.T., Jr; 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(12), 1470-1476.
[http://dx.doi.org/10.1038/ncb1800] [PMID: 19011622]
[97]
Gu, H.; Ji, R.; Zhang, X.; Wang, M.; Zhu, W.; Qian, H.; Chen, Y.; Jiang, P.; Xu, W. Exosomes derived from human mesenchymal stem cells promote gastric cancer cell growth and migration via the activation of the Akt pathway. Mol. Med. Rep., 2016, 14(4), 3452-3458.
[http://dx.doi.org/10.3892/mmr.2016.5625] [PMID: 27513187]
[98]
Wang, Z.; Chen, J.Q.; Liu, J.L.; Tian, L. Exosomes in tumor microenvironment: novel transporters and biomarkers. J. Transl. Med., 2016, 14(1), 297.
[http://dx.doi.org/10.1186/s12967-016-1056-9] [PMID: 27756426]
[99]
Katoh, M. Therapeutics targeting angiogenesis: genetics and epigenetics, extracellular miRNAs and signaling networks. Review Int. J. Mol. Med., 2013, 32(4), 763-767.
[http://dx.doi.org/10.3892/ijmm.2013.1444] [PMID: 23863927]
[100]
Harris, D.A.; Patel, S.H.; Gucek, M.; Hendrix, A.; Westbroek, W.; Taraska, J.W. Exosomes released from breast cancer carcinomas stimulate cell movement. PLoS One, 2015, 10(3)e0117495
[http://dx.doi.org/10.1371/journal.pone.0117495] [PMID: 25798887]
[101]
Kim, J.W.; Wieckowski, E.; Taylor, D.D.; Reichert, T.E.; Watkins, S.; Whiteside, T.L. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin. Cancer Res., 2005, 11(3), 1010-1020.
[PMID: 15709166]
[102]
Taylor, D.D.; Gercel-Taylor, C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin. Immunopathol., 2011, 33(5), 441-454.
[http://dx.doi.org/10.1007/s00281-010-0234-8] [PMID: 21688197]
[103]
Koyama, Y.; Ito, T.; Hasegawa, A.; Eriguchi, M.; Inaba, T.; Ushigusa, T.; Sugiura, K. Exosomes derived from tumor cells genetically modified to express Mycobacterium tuberculosis antigen: a novel vaccine for cancer therapy. Biotechnol. Lett., 2016, 38(11), 1857-1866.
[http://dx.doi.org/10.1007/s10529-016-2185-1] [PMID: 27484689]
[104]
Wang, J.; Li, W.; Zhang, L.; Ban, L.; Chen, P.; Du, W.; Feng, X.; Liu, B.F. Chemically edited exosomes with dual ligand urified by microfluidic device for active targeted grug delivery to tumor cells. ACS Appl. Mater. Interfaces, 2017, 9(33), 27441-27452.
[http://dx.doi.org/10.1021/acsami.7b06464] [PMID: 28762264]
[105]
Théry, C.; Ostrowski, M.; Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol., 2009, 9(8), 581-593.
[http://dx.doi.org/10.1038/nri2567] [PMID: 19498381]
[106]
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(7), 2383-2390.
[http://dx.doi.org/10.1016/j.biomaterials.2013.11.083] [PMID: 24345736]
[107]
Yin, H.; Yang, J.; Zhang, Q.; Yang, J.; Wang, H.; Xu, J.; Zheng, J. iRGD as a tumor penetrating peptide for cancer therapy (Review). Mol. Med. Rep., 2017, 15(5), 2925-2930.
[http://dx.doi.org/10.3892/mmr.2017.6419] [PMID: 28358432]
[108]
Dai, S.; Wei, D.; Wu, Z.; Zhou, X.; Wei, X.; Huang, H.; Li, G. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol. Ther., 2008, 16(4), 782-790.
[http://dx.doi.org/10.1038/mt.2008.1] [PMID: 18362931]
[109]
Escudier, B.; Dorval, T.; Chaput, N.; André, F.; Caby, M.P.; Novault, S.; Flament, C.; Leboulaire, C.; Borg, C.; Amigorena, S.; Boccaccio, C.; Bonnerot, C.; Dhellin, O.; Movassagh, M.; Piperno, S.; Robert, C.; Serra, V.; Valente, N.; Le Pecq, J.B.; Spatz, A.; Lantz, O.; Tursz, T.; Angevin, E.; Zitvogel, L. 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.
[http://dx.doi.org/10.1186/1479-5876-3-10] [PMID: 15740633]
[110]
Morse, M.A.; Garst, J.; Osada, T.; Khan, S.; Hobeika, A.; Clay, T.M.; Valente, N.; Shreeniwas, R.; Sutton, M.A.; Delcayre, A.; Hsu, D.H.; Le Pecq, J.B.; Lyerly, H.K. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J. Transl. Med., 2005, 3(1), 9.
[http://dx.doi.org/10.1186/1479-5876-3-9] [PMID: 15723705]
[111]
Zajac, P.; Schultz-Thater, E.; Tornillo, L.; Sadowski, C.; Trella, E.; Mengus, C.; Iezzi, G.; Spagnoli, G.C. MAGE-A antigens and cancer immunotherapy. Front. Med. (Lausanne), 2017, 4, 18.
[http://dx.doi.org/10.3389/fmed.2017.00018] [PMID: 28337438]
[112]
Yang, T.; Martin, P.; Fogarty, B.; Brown, A.; Schurman, K.; Phipps, R.; Yin, V.P.; Lockman, P.; Bai, S. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm. Res., 2015, 32(6), 2003-2014.
[http://dx.doi.org/10.1007/s11095-014-1593-y] [PMID: 25609010]
[113]
Yang, T.; Fogarty, B.; LaForge, B.; Aziz, S.; Pham, T.; Lai, L.; Bai, S. Delivery of small interfering RNA to inhibit vascular endothelial growth factor in zebrafish using natural brain endothelia cell-secreted exosome nanovesicles for the treatment of brain cancer. AAPS J., 2017, 19(2), 475-486.
[http://dx.doi.org/10.1208/s12248-016-0015-y] [PMID: 27882487]
[114]
Niidome, T.; Huang, L. Gene therapy progress and prospects: nonviral vectors. Gene Ther., 2002, 9(24), 1647-1652.
[http://dx.doi.org/10.1038/sj.gt.3301923] [PMID: 12457277]
[115]
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. Nanomedicine, 2018, 13, 585-599.
[http://dx.doi.org/10.2147/IJN.S154458] [PMID: 29430178]
[116]
Kumar, P.; Wu, H.; McBride, J.L.; Jung, K.E.; Kim, M.H.; Davidson, B.L.; Lee, S.K.; Shankar, P.; Manjunath, N. Transvascular delivery of small interfering RNA to the central nervous system. Nature, 2007, 448(7149), 39-43.
[http://dx.doi.org/10.1038/nature05901] [PMID: 17572664]
[117]
Liu, Y.; Li, D.; Liu, Z.; Zhou, Y.; Chu, D.; Li, X.; Jiang, X.; Hou, D.; Chen, X.; Chen, Y.; Yang, Z.; Jin, L.; Jiang, W.; Tian, C.; Zhou, G.; Zen, K.; Zhang, J.; Zhang, Y.; Li, J.; Zhang, C.Y. Targeted exosome-mediated delivery of opioid receptor Mu siRNA for the treatment of morphine relapse. Sci. Rep., 2015, 5, 17543.
[http://dx.doi.org/10.1038/srep17543] [PMID: 26633001]
[118]
Lunavat, T.R.; Jang, S.C.; Nilsson, L.; Park, H.T.; Repiska, G.; Lässer, C.; Nilsson, J.A.; Gho, Y.S.; Lötvall, J. RNAi delivery by exosome-mimetic nanovesicles - Implications for targeting c-Myc in cancer. Biomaterials, 2016, 102, 231-238.
[http://dx.doi.org/10.1016/j.biomaterials.2016.06.024] [PMID: 27344366]
[119]
Wang, X.; Zhang, H.; Bai, M.; Ning, T.; Ge, S.; Deng, T.; Liu, R.; Zhang, L.; Ying, G.; Ba, Y. Exosomes serve as nanoparticles to deliver anti-mir-214 to reverse chemoresistance to cisplatin in gastric cancer. Mol. Ther., 2018, 26(3), 774-783.
[http://dx.doi.org/10.1016/j.ymthe.2018.01.001] [PMID: 29456019]

Rights & Permissions Print Cite
Article Metrics
66
1
© 2024 Bentham Science Publishers | Privacy Policy