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Engineering exosomes as refined biological nanoplatforms for drug delivery
Open accessAbstract
Exosomes, a subgroup of extracellular vesicles (EVs), have been recognized as important mediators of long distance intercellular communication and are involved in a diverse range of biological processes. Because of their ideal native structure and characteristics, exosomes are promising nanocarriers for clinical use. Exosomes are engineered at the cellular level under natural conditions, but successful exosome modification requires further exploration. The focus of this paper is to summarize passive and active loading approaches, as well as specific exosome modifications and examples of the delivery of therapeutic and imaging molecules. Examples of exosomes derived from a variety of biological origins are also provided. The biocompatible characteristics of exosomes, with suitable modifications, can increase the stability and efficacy of imaging probes and therapeutics while enhancing cellular uptake. Challenges in clinical translation of exosome-based platforms from different cell sources and the advantages of each are also reviewed and discussed.
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1 retracted
Rana, S., Yue, S., Stadel, D., & Zöller, M. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.06.018 · Cited by 663
RetractedDelivery of siRNA to the mouse brain by systemic injection of targeted exosomes
Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., & Wood, M. J. A. (2011) · Nature Biotechnology · doi:10.1038/nbt.1807 · Cited by 4,930
PEGylation as a strategy for improving nanoparticle-based drug and gene delivery
Suk, J. S., Xu, Q., Kim, N., Hanes, J., & Ensign, L. M. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.09.012 · Cited by 4,523
Exosomes as drug delivery vehicles for Parkinson’s disease therapy
Haney, M. J., Klyachko, N. L., Zhao, Y., Gupta, R., Plotnikova, E. G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., Kabanov, A. V., et al. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.03.033 · Cited by 2,009
Systemically Injected Exosomes Targeted to EGFR Deliver Antitumor MicroRNA to Breast Cancer Cells
Ohno, S.-I., Takanashi, M., Sudo, K., Ueda, S., Ishikawa, A., Matsuyama, N., Fujita, K., Mizutani, T., Ohgi, T., Ochiya, T., et al. (2013) · Molecular Therapy · doi:10.1038/mt.2012.180 · Cited by 1,666
Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming
Wolfers, J., Lozier, A., Raposo, G., Regnault, A., Théry, C., Masurier, C., Flament, C., Pouzieux, S., Faure, F., Tursz, T., et al. (2001) · Nature Medicine · doi:10.1038/85438 · Cited by 1,640
Sun, D., Zhuang, X., Xiang, X., Liu, Y., Zhang, S., Liu, C., Barnes, S., Grizzle, W., Miller, D., & Zhang, H.-G. (2010) · Molecular Therapy · doi:10.1038/mt.2010.105 · Cited by 1,572
Self-citationCancer Exosomes Perform Cell-Independent MicroRNA Biogenesis and Promote Tumorigenesis
Melo, S. A., Sugimoto, H., O’Connell, J. T., Kato, N., Villanueva, A., Vidal, A., Qiu, L., Vitkin, E., Perelman, L. T., Melo, C. A., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.09.005 · Cited by 1,531
Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells
Kim, M. S., Haney, M. J., Zhao, Y., Mahajan, V., Deygen, I., Klyachko, N. L., Inskoe, E., Piroyan, A., Sokolsky, M., Okolie, O., et al. (2016) · Nanomedicine: Nanotechnology, Biology and Medicine · doi:10.1016/j.nano.2015.10.012 · Cited by 1,410
Extracellular vesicles for drug delivery.
Vader, P., Mol, E. A., Pasterkamp, G., & Schiffelers, R. M. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2016.02.006 · Cited by 1,319
Escudier, B., Dorval, T., Chaput, N., André, F., Caby, M.-P., Novault, S., Flament, C., Leboulaire, C., Borg, C., Amigorena, S., et al. (2005) · Journal of Translational Medicine · doi:10.1186/1479-5876-3-10 · Cited by 1,280
The Smart Drug Delivery System and Its Clinical Potential
Liu, D., Yang, F., Xiong, F., & Gu, N. (2016) · Theranostics · doi:10.7150/thno.14858 · Cited by 1,066
Using exosomes, naturally-equipped nanocarriers, for drug delivery
Batrakova, E. V., & Kim, M. S. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.07.030 · Cited by 1,041
Indirect activation of naïve CD4+ T cells by dendritic cell–derived exosomes
Théry, C., Duban, L., Segura, E., Véron, P., Lantz, O., & Amigorena, S. (2002) · Nature Immunology · doi:10.1038/ni854 · Cited by 960
Bovine milk-derived exosomes for drug delivery
Munagala, R., Aqil, F., Jeyabalan, J., & Gupta, R. C. (2016) · Cancer Letters · doi:10.1016/j.canlet.2015.10.020 · Cited by 931
Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter
Lai, C. P., Mardini, O., Ericsson, M., Prabhakar, S., Maguire, C. A., Chen, J. W., Tannous, B. A., & Breakefield, X. O. (2014) · ACS Nano · doi:10.1021/nn404945r · Cited by 902
In Vivo Imaging Reveals Extracellular Vesicle-Mediated Phenocopying of Metastatic Behavior
Zomer, A., Maynard, C., Verweij, F. J., Kamermans, A., Schäfer, R., Beerling, E., Schiffelers, R. M., de Wit, E., Berenguer, J., Ellenbroek, S. I. J., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.042 · Cited by 869
Ju, S., Mu, J., Dokland, T., Zhuang, X., Wang, Q., Jiang, H., Xiang, X., Deng, Z.-B., Wang, B., Zhang, L., et al. (2013) · Molecular Therapy · doi:10.1038/mt.2013.64 · Cited by 862
Pascucci, L., Coccè, V., Bonomi, A., Ami, D., Ceccarelli, P., Ciusani, E., Viganò, L., Locatelli, A., Sisto, F., Doglia, S. M., et al. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.07.042 · Cited by 846
Tumor-Derived Exosomes and Their Role in Cancer Progression
(2016) · Advances in Clinical Chemistry · doi:10.1016/bs.acc.2015.12.005 · Cited by 755
Engineering hybrid exosomes by membrane fusion with liposomes
Sato, Y. T., Umezaki, K., Sawada, S., Mukai, S.-A., Sasaki, Y., Harada, N., Shiku, H., & Akiyoshi, K. (2016) · Scientific Reports · doi:10.1038/srep21933 · Cited by 744
Fuhrmann, G., Serio, A., Mazo, M., Nair, R., & Stevens, M. M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.11.029 · Cited by 742
Exosome mediated communication within the tumor microenvironment
Milane, L., Singh, A., Mattheolabakis, G., Suresh, M., & Amiji, M. M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.06.029 · Cited by 742
Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes
Wahlgren, J., Karlson, T. D. L., Brisslert, M., Vaziri Sani, F., Telemo, E., Sunnerhagen, P., & Valadi, H. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks463 · Cited by 715
Saponins as cytotoxic agents: a review
Podolak, I., Galanty, A., & Sobolewska, D. (2010) · Phytochemistry Reviews · doi:10.1007/s11101-010-9183-z · Cited by 704
Production and characterization of clinical grade exosomes derived from dendritic cells
Lamparski, H. G., Metha-Damani, A., Yao, J.-Y., Patel, S., Hsu, D.-H., Ruegg, C., & Le Pecq, J.-B. (2002) · Journal of Immunological Methods · doi:10.1016/s0022-1759(02)00330-7 · Cited by 700
Re-Engineering Extracellular Vesicles as Smart Nanoscale Therapeutics
Armstrong, J. P. K., Holme, M. N., & Stevens, M. M. (2017) · ACS Nano · doi:10.1021/acsnano.6b07607 · Cited by 602
Exosomes and tumor-mediated immune suppression
Whiteside, T. L. (2016) · Journal of Clinical Investigation · doi:10.1172/jci81136 · Cited by 569
Surface Functionalization of Exosomes Using Click Chemistry
Smyth, T., Petrova, K., Payton, N. M., Persaud, I., Redzic, J. S., Graner, M. W., Smith-Jones, P., & Anchordoquy, T. J. (2014) · Bioconjugate Chemistry · doi:10.1021/bc500291r · Cited by 532
Exosomes: New players in cell–cell communication
Bang, C., & Thum, T. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.08.007 · Cited by 505
Kim, J. W., Wieckowski, E., Taylor, D. D., Reichert, T. E., Watkins, S., & Whiteside, T. L. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.1010.11.3 · Cited by 497
Turturici, G., Tinnirello, R., Sconzo, G., & Geraci, F. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00228.2013 · Cited by 483
Extracellular vesicles as drug delivery systems: Lessons from the liposome field
van der Meel, R., Fens, M. H. A. M., Vader, P., van Solinge, W. W., Eniola-Adefeso, O., & Schiffelers, R. M. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.07.049 · Cited by 482
Blood Exosomes Endowed with Magnetic and Targeting Properties for Cancer Therapy
Qi, H., Liu, C., Long, L., Ren, Y., Zhang, S., Chang, X., Qian, X., Jia, H., Zhao, J., Sun, J., et al. (2016) · ACS Nano · doi:10.1021/acsnano.5b06939 · Cited by 459
Viaud, S., Terme, M., Flament, C., Taieb, J., André, F., Novault, S., Escudier, B., Robert, C., Caillat-Zucman, S., Tursz, T., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004942 · Cited by 437
Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments
Taylor, D. D., & Gercel-Taylor, C. (2011) · Seminars in Immunopathology · doi:10.1007/s00281-010-0234-8 · Cited by 383
Hinde, E., Thammasiraphop, K., Duong, H. T. T., Yeow, J., Karagoz, B., Boyer, C., Gooding, J. J., & Gaus, K. (2017) · Nature Nanotechnology · doi:10.1038/nnano.2016.160 · Cited by 374
Morishita, M., Takahashi, Y., Matsumoto, A., Nishikawa, M., & Takakura, Y. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.09.031 · Cited by 369
A review of nanocarriers for the delivery of small interfering RNA
Kesharwani, P., Gajbhiye, V., & Jain, N. K. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.06.068 · Cited by 368
Thomas, M., Lu, J. J., Ge, Q., Zhang, C., Chen, J., & Klibanov, A. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502067102 · Cited by 366
Wang, Q., Ren, Y., Mu, J., Egilmez, N. K., Zhuang, X., Deng, Z., Zhang, L., Yan, J., Miller, D., & Zhang, H.-G. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3095 · Cited by 366
Nakase, I., & Futaki, S. (2015) · Scientific Reports · doi:10.1038/srep10112 · Cited by 295
Cationic liposome-mediated delivery of siRNAs in adult mice
Sioud, M., & Sørensen, D. R. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.11.057 · Cited by 286
Simhadri, V. R., Reiners, K. S., Hansen, H. P., Topolar, D., Simhadri, V. L., Nohroudi, K., Kufer, T. A., Engert, A., & Pogge von Strandmann, E. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003377 · Cited by 262
Antitumor Activity of Small Interfering RNA/Cationic Liposome Complex in Mouse Models of Cancer
Yano, J., Hirabayashi, K., Nakagawa, S.-I., Yamaguchi, T., Nogawa, M., Kashimori, I., Naito, H., Kitagawa, H., Ishiyama, K., Ohgi, T., et al. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-1049 · Cited by 238
Dendrimer nanoarchitectures for cancer diagnosis and anticancer drug delivery
Sharma, A. K., Gothwal, A., Kesharwani, P., Alsaab, H., Iyer, A. K., & Gupta, U. (2017) · Drug Discovery Today · doi:10.1016/j.drudis.2016.09.013 · Cited by 226
Patil, M. L., Zhang, M., Taratula, O., Garbuzenko, O. B., He, H., & Minko, T. (2009) · Biomacromolecules · doi:10.1021/bm8009973 · Cited by 213
Rupert, D. L. M., Claudio, V., Lässer, C., & Bally, M. (2017) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2016.07.028 · Cited by 212
Evaluation of electroporation-induced adverse effects on adipose-derived stem cell exosomes
Johnsen, K. B., Gudbergsson, J. M., Skov, M. N., Christiansen, G., Gurevich, L., Moos, T., & Duroux, M. (2016) · Cytotechnology · doi:10.1007/s10616-016-9952-7 · Cited by 210
Exosomes – Structure, Biogenesis and Biological Role in Non‐Small‐Cell Lung Cancer
Frydrychowicz, M., Kolecka‐Bednarczyk, A., Madejczyk, M., Yasar, S., & Dworacki, G. (2015) · Scandinavian Journal of Immunology · doi:10.1111/sji.12247 · Cited by 209
Post Isolation Modification of Exosomes for Nanomedicine Applications
Hood, J. L. (2016) · Nanomedicine · doi:10.2217/nnm-2016-0102 · Cited by 201
Quantification of human urinary exosomes by nanoparticle tracking analysis
Oosthuyzen, W., Sime, N. E. L., Ivy, J. R., Turtle, E. J., Street, J. M., Pound, J., Bath, L. E., Webb, D. J., Gregory, C. D., Bailey, M. A., et al. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.264069 · Cited by 197
Extracellular Vesicles: Satellites of Information Transfer in Cancer and Stem Cell Biology
Desrochers, L. M., Antonyak, M. A., & Cerione, R. A. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.04.019 · Cited by 178
Exosomes Released from Breast Cancer Carcinomas Stimulate Cell Movement
Harris, D. A., Patel, S. H., Gucek, M., Hendrix, A., Westbroek, W., & Taraska, J. W. (2015) · PLOS ONE · doi:10.1371/journal.pone.0117495 · Cited by 169
Wang, M., Altinoglu, S., Takeda, Y. S., & Xu, Q. (2015) · PLOS ONE · doi:10.1371/journal.pone.0141860 · Cited by 164
Romagnoli, G. G., Zelante, B. B., Toniolo, P. A., Migliori, I. K., & Barbuto, J. A. M. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00692 · Cited by 152
Higginbotham, J. N., Zhang, Q., Jeppesen, D. K., Scott, A. M., Manning, H. C., Ochieng, J., Franklin, J. L., & Coffey, R. J. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.29254 · Cited by 135
The potential of protein–nanomaterial interaction for advanced drug delivery
Peng, Q., & Mu, H. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.01.041 · Cited by 134
Mahaweni, N. M., Kaijen-Lambers, M. E. H., Dekkers, J., Aerts, J. G. J. V., & Hegmans, J. P. (2013) · Journal of Extracellular Vesicles · doi:10.3402/jev.v2i0.22492 · Cited by 119
Malhotra, H., Sheokand, N., Kumar, S., Chauhan, A. S., Kumar, M., Jakhar, P., Boradia, V. M., Raje, C. I., & Raje, M. (2016) · Journal of Biomedical Nanotechnology · doi:10.1166/jbn.2016.2229 · Cited by 114
Modulation of Immune Responses by Exosomes Derived from Antigen-Presenting Cells
Shenoda, B. B., & Ajit, S. K. (2016) · Clinical Medicine Insights Pathology · doi:10.4137/cpath.s39925 · Cited by 106
Wang, C., Mäkilä, E. M., Kaasalainen, M. H., Liu, D., Sarparanta, M. P., Airaksinen, A. J., Salonen, J., Hirvonen, J. J., & Santos, H. A. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.10.065 · Cited by 105
Strategies of polymeric nanoparticles for enhanced internalization in cancer therapy
Sun, L., Wu, Q., Peng, F., Liu, L., & Gong, C. (2015) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2015.07.013 · Cited by 102
A systematic approach to exosome‐based translational nanomedicine
Hood, J. L., & Wickline, S. A. (2012) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1174 · Cited by 98
Myeloid suppressor cells regulate the adaptive immune response to cancer
Frey, A. B. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29906 · Cited by 94
Controllable mineral coatings on PCL scaffolds as carriers for growth factor release
Suárez-González, D., Barnhart, K., Migneco, F., Flanagan, C. L., Hollister, S. J., & Murphy, W. L. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.09.095 · Cited by 92
The functions and clinical applications of tumor-derived exosomes
Shao, Y., Shen, Y., Chen, T., Xu, F., Chen, X., & Zheng, S. S. (2016) · Oncotarget · doi:10.18632/oncotarget.11177 · Cited by 90
Disposition and safety of inhaled biodegradable nanomedicines: Opportunities and challenges
Haque, S., Whittaker, M. R., McIntosh, M. P., Pouton, C. W., & Kaminskas, L. M. (2016) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2016.03.002 · Cited by 87
Tomihari, M., Chung, J., Akiyoshi, H., Cruz, P. D., & Ariizumi, K. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-2538 · Cited by 85
The Drug Discovery by NanoMedicine and its Clinical Experience
Matsumura, Y. (2014) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyu046 · Cited by 82
Wang, J., Guo, R., Yang, Y., Jacobs, B. S., Chen, S., Iwuchukwu, I. O., Gaines, K. J., Chen, Y., Simman, R., Lv, G., et al. (2016) · Stem Cells International · doi:10.1155/2016/2639728 · Cited by 63
Tumor priming using metronomic chemotherapy with neovasculature-targeted, nanoparticulate paclitaxel
Luan, X., Guan, Y., Lovell, J. F., Zhao, M., Lu, Q., Liu, Y., Liu, H.-J., Gao, Y., Dong, X., Yang, S., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.04.008 · Cited by 63
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Metadata
- Authors
- Luan, X., Sansanaphongpricha, K., Myers, I., Chen, H., Yuan, H., & Sun, D.
- Venue
- Acta Pharmacologica Sinica
- Published
- 2017-04-10
- Volume
- 38
- Issue
- 6
- Pages
- 754-763
- ISSN
- 0253-9756 (ISSN-L)
- 1671-4083
- 1745-7254
- OpenAlex
- W2607411382
- Cited by
- 1,163
- References
- 72
- FWCI
- 24.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
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