RNA delivery by extracellular vesicles in mammalian cells and its applications

Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells

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Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines

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Shedding light on the cell biology of extracellular vesicles

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Tumour exosome integrins determine organotropic metastasis

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Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers

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Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes

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Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication

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Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes

Kowal, J., Arras, G., Colombo, M., Jouve, M., Morath, J. P., Primdal-Bengtson, B., Dingli, F., Loew, D., Tkach, M., & Théry, C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521230113 · Cited by 3,426

Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma

Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., Mitchell, P. S., Bennett, C. F., Pogosova-Agadjanyan, E. L., Stirewalt, D. L., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019055108 · Cited by 3,294

Reassessment of exosome composition

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Routes and mechanisms of extracellular vesicle uptake

Mulcahy, L. A., Pink, R. C., & Carter, D. R. F. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.24641 · Cited by 2,832

MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins

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Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer

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Nanotubular Highways for Intercellular Organelle Transport

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Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs

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Secretory Mechanisms and Intercellular Transfer of MicroRNAs in Living Cells

Kosaka, N., Iguchi, H., Yoshioka, Y., Takeshita, F., Matsuki, Y., & Ochiya, T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.107821 · Cited by 1,934

Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells

Mittelbrunn, M., Gutiérrez‐Vázquez, C., Villarroya‐Beltri, C., González, S., Sánchez‐Cabo, F., González, M. A., Bernad, A., & Sánchez‐Madrid, F. (2011) · Nature Communications · doi:10.1038/ncomms1285 · Cited by 1,818

Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting

Wiklander, O. P. B., Nordin, J. Z., O'Loughlin, A., Gustafsson, Y., Corso, G., Mäger, I., Vader, P., Lee, Y., Sork, H., Seow, Y., et al. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.26316 · Cited by 1,730

New Technologies for Analysis of Extracellular Vesicles

Shao, H., Im, H., Castro, C. M., Breakefield, X. O., Weissleder, R., & Lee, H. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00534 · Cited by 1,697

Systemically Injected Exosomes Targeted to EGFR Deliver Antitumor MicroRNA to Breast Cancer Cells

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Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation

Zhang, H., Freitas, D. P., Kim, H. S., Fabijanic, K. I., Li, Z., Chen, H., Mark, M. T., Molina, H., Benito‐Martín, A., Bojmar, L., et al. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0040-4 · Cited by 1,666

Microenvironmental pH Is a Key Factor for Exosome Traffic in Tumor Cells

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Cancer 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. I., Perelman, L. T., Melo, C. A., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.09.005 · Cited by 1,565

Adipose-derived circulating miRNAs regulate gene expression in other tissues

Thomou, T., Mori, M. A., Dreyfuss, J. M., Konishi, M., Sakaguchi, M., Wolfrum, C., Rao, T. N., Winnay, J. N., Garcia-Martin, R., Grinspoon, S. K., et al. (2017) · Nature · doi:10.1038/nature21365 · Cited by 1,539

MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response

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Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes.

Montecalvo, A., Larregina, A. T., Shufesky, W. J., Beer Stolz, D., Sullivan, M. L. G., Karlsson, J. M., Baty, C. J., Gibson, G. A., Erdos, G., Wang, Z., et al. (2012) · Blood · doi:10.1182/blood-2011-02-338004 · Cited by 1,429

Intracellular Toll-like Receptors

Blasius, A. L., & Beutler, B. (2010) · Immunity · doi:10.1016/j.immuni.2010.03.012 · Cited by 1,392

lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements

Gong, C., & Maquat, L. E. (2011) · Nature · doi:10.1038/nature09701 · Cited by 1,294

Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial

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Use of resonance energy transfer to monitor membrane fusion

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Endocytosis and intracellular transport of nanoparticles: Present knowledge and need for future studies

Iversen, T., Skotland, T., & Sandvig, K. (2011) · Nano Today · doi:10.1016/j.nantod.2011.02.003 · Cited by 1,267

Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity

Ying, W., Riopel, M., Bandyopadhyay, G., Dong, Y., Birmingham, A., Seo, J. B., Ofrecio, J. M., Wollam, J., Hernandez-Carretero, A., Fu, W., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.035 · Cited by 1,191

Identification of Tim4 as a phosphatidylserine receptor

Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T., & Nagata, S. (2007) · Nature · doi:10.1038/nature06307 · Cited by 1,180

Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth

Zhang, L., Zhang, S., Yao, J., Lowery, F. J., Zhang, Q., Huang, W.-C., Li, P., Li, M., Wang, X., Zhang, C., et al. (2015) · Nature · doi:10.1038/nature15376 · Cited by 1,175

Quantitative and stoichiometric analysis of the microRNA content of exosomes

Chevillet, J. R., Kang, Q., Ruf, I. K., Briggs, H., Vojtech, L. N., Hughes, S. M., Cheng, H. H., Arroyo, J. D., Meredith, E. K., Gallichotte, E. N., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408301111 · Cited by 1,137

Structure and mechanism of the M2 proton channel of influenza A virus

Schnell, J. R., & Chou, J. J. (2008) · Nature · doi:10.1038/nature06531 · Cited by 1,090

A Novel Role for 3-O-Sulfated Heparan Sulfate in Herpes Simplex Virus 1 Entry

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Hypoxic enhancement of exosome release by breast cancer cells

King, H. W., Michael, M. Z., & Gleadle, J. M. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-421 · Cited by 1,045

Advances in therapeutic applications of extracellular vesicles

Wiklander, O. P. B., Brennan, M. Á., Lötvall, J., Breakefield, X. O., & EL Andaloussi, S. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aav8521 · Cited by 1,039

Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity

Gibbings, D., Ciaudo, C., Erhardt, M., & Voinnet, O. (2009) · Nature Cell Biology · doi:10.1038/ncb1929 · Cited by 1,037

Bioinspired Exosome-Mimetic Nanovesicles for Targeted Delivery of Chemotherapeutics to Malignant Tumors

Jang, S. C., Kim, O. Y., Yoon, C. M., Choi, D., Roh, T., Park, J., Nilsson, J. A., Lötvall, J. O., Kim, Y., & Gho, Y. S. (2013) · ACS Nano · doi:10.1021/nn402232g · Cited by 1,037

Extracellular Vesicles in Cancer: Exosomes, Microvesicles and the Emerging Role of Large Oncosomes

Minciacchi, V. R., Freeman, M. R., & Vizio, D. D. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.02.010 · Cited by 1,014

CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer

Wang, J., Liu, X., Wu, H., Ni, P., Gu, Z., Qiao, Y., Chen, N., Sun, F., & Fan, Q. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq285 · Cited by 1,008

The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling

Deun, J. V., Mestdagh, P., Sormunen, R. T., Cocquyt, V., Vermaelen, K., Vandesompele, J., Bracke, M., Wever, O. D., & Hendrix, A. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.24858 · Cited by 987

Endogenous tRNA-Derived Fragments Suppress Breast Cancer Progression via YBX1 Displacement

Goodarzi, H., Liu, X., Nguyen, H. C. B., Zhang, S., Fish, L., & Tavazoie, S. F. (2015) · Cell · doi:10.1016/j.cell.2015.02.053 · Cited by 949

Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing

van der Pol, E., Coumans, F. A. W., Grootemaat, A. E., Gardiner, C., Sargent, I. L., Harrison, P., Sturk, A., van Leeuwen, T. G. J. M., & Nieuwland, R. (2014) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12602 · Cited by 947

Bovine milk-derived exosomes for drug delivery

Munagala, R., Aqil, F., Jeyabalan, J., & Gupta, R. C. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.10.020 · Cited by 936

Characterization of human plasma-derived exosomal RNAs by deep sequencing.

Huang, X., Yuan, T., Tschannen, M., Sun, Z., Jacob, H., Du, M., Liang, M., Dittmar, R. L., Liu, Y., Liang, M., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-319 · Cited by 932

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 915

Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity

Christianson, H. C., Svensson, K. J., van Kuppevelt, T. H., Li, J.-P., & Belting, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304266110 · Cited by 903

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 893

Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes

Crescitelli, R., Lässer, C., Szabó, T. G., Kittel, A., Eldh, M., Dianzani, I., Buzás, E. I., & Lötvall, J. (2013) · Journal of Extracellular Vesicles · doi:10.3402/jev.v2i0.20677 · Cited by 876

Exosome Release Is Regulated by a Calcium-dependent Mechanism in K562 Cells

Savina, A., Furlán, M., Vidal, M., & Colombo, M. I. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301642200 · Cited by 835

Exosome Transfer from Stromal to Breast Cancer Cells Regulates Therapy Resistance Pathways

Boelens, M. C., Wu, T. J., Nabet, B. Y., Xu, B., Qiu, Y., Yoon, T., Azzam, D. J., Victor, C. T.-S., Wiemann, B. Z., Ishwaran, H., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.051 · Cited by 819

Generation and testing of clinical-grade exosomes for pancreatic cancer

Mendt, M. C., Kamerkar, S., Sugimoto, H., McAndrews, K. M., Wu, C.-C., Gagea, M., Yang, S., Blanko, E. V. R., Peng, Q., Ma, X., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.99263 · Cited by 812

Endogenous miRNA Sponge lincRNA-RoR Regulates Oct4, Nanog, and Sox2 in Human Embryonic Stem Cell Self-Renewal

Wang, Y., Xu, Z., Jiang, J., Xu, C., Kang, J., Xiao, L., Wu, M., Xiong, J., Guo, X., & Liu, H. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.03.002 · Cited by 795

An unconventional role for miRNA: let-7 activates toll-like receptor 7 and causes neurodegeneration

Lehmann, S. M., Krüger, C., Park, B., Derkow, K., Rosenberger, K., Baumgart, J., Trimbuch, T., Eom, G., Hinz, M., Kaul, D., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3113 · Cited by 786

Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species

Baglio, S. R., Rooijers, K., Koppers‐Lalic, D., Verweij, F. J., Pérez-Lanzón, M., Zini, N., Naaijkens, B. A., Perut, F., Niessen, H. W. M., Baldini, N., et al. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0116-z · Cited by 776

Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions

Hoen, E. N. M. N., Buermans, H. P. J., Waasdorp, M., Stoorvogel, W., Wauben, M. H. M., & Hoen, P. A. C. ’. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks658 · Cited by 772

Exosome-delivered microRNAs modulate the inflammatory response to endotoxin

Alexander, M., Hu, R., Runtsch, M. C., Kagele, D. A., Mosbruger, T. L., Tolmachova, T., Seabra, M. C., Round, J. L., Ward, D. M., & O’Connell, R. M. (2015) · Nature Communications · doi:10.1038/ncomms8321 · Cited by 769

Circulating Extracellular Vesicles in Human Disease

Shah, R. V., Patel, T. C., & Freedman, J. E. (2018) · New England Journal of Medicine · doi:10.1056/nejmra1704286 · Cited by 765

Obstacles and opportunities in the functional analysis of extracellular vesicle RNA – an ISEV position paper

Mateescu, B., Kowal, E. J. K., van Balkom, B. W. M., Bartel, S., Bhattacharyya, S. N., Buzás, E. I., Buck, A. H., de Candia, P., Chow, F. W., Das, S., et al. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1286095 · Cited by 757

Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment

Kojima, R., Bojar, D., Rizzi, G., Hamri, G. C.-E., El-Baba, M. D., Saxena, P., Ausländer, S., Tan, K. R., & Fussenegger, M. (2018) · Nature Communications · doi:10.1038/s41467-018-03733-8 · Cited by 748

Extracellular vesicle-based therapeutics: natural versus engineered targeting and trafficking

Murphy, D. E., de Jong, O. G., Brouwer, M., Wood, M. J. A., Lavieu, G., Schiffelers, R. M., & Vader, P. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0223-5 · Cited by 740

Extracellular vesicle-packaged HIF-1α-stabilizing lncRNA from tumour-associated macrophages regulates aerobic glycolysis of breast cancer cells

Chen, F., Chen, J., Yang, L., Liu, J., Zhang, X., Zhang, Y., Tu, Q., Yin, D., Lin, D., Wong, P., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0299-0 · Cited by 722

A pathogenic picornavirus acquires an envelope by hijacking cellular membranes

Feng, Z., Hensley, L., McKnight, K. L., Hu, F., Madden, V. J., Ping, L., Jeong, S., Walker, C. M., Lanford, R. E., & Lemon, S. M. (2013) · Nature · doi:10.1038/nature12029 · Cited by 712

How do lncRNAs regulate transcription?

Long, Y., Wang, X., Youmans, D. T., & Cech, T. R. (2017) · Science Advances · doi:10.1126/sciadv.aao2110 · Cited by 701

Defining mesenchymal stromal cell (MSC)‐derived small extracellular vesicles for therapeutic applications

Witwer, K. W., van Balkom, B. W. M., Bruno, S., Choo, A. B. H., Dominici, M., Gimona, M., Hill, A. F., de Kleijn, D. P. V., Koh, M., Lai, R. C., et al. (2019) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2019.1609206 · Cited by 697

Visualizing lipid-formulated siRNA release from endosomes and target gene knockdown

Wittrup, A., Ai, A., Liu, X., Hamar, P., Trifonova, R., Charisse, K., Manoharan, M., Kirchhausen, T., & Lieberman, J. (2015) · Nature Biotechnology · doi:10.1038/nbt.3298 · Cited by 693

HIV Enters Cells via Endocytosis and Dynamin-Dependent Fusion with Endosomes

Miyauchi, K., Kim, Y., Latinovic, O., Va, M., & Melikyan, G. B. (2009) · Cell · doi:10.1016/j.cell.2009.02.046 · Cited by 682

Interaction and uptake of exosomes by ovarian cancer cells

Escrevente, C., Keller, S., Altevogt, P., & Costa, J. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-108 · Cited by 666

Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles

Kooijmans, S. A. A., Stremersch, S., Braeckmans, K., de Smedt, S. C., Hendrix, A., Wood, M. J. A., Schiffelers, R. M., Raemdonck, K., & Vader, P. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.08.014 · Cited by 663

Efficient RNA drug delivery using red blood cell extracellular vesicles

Usman, W. M., Pham, T. C., Kwok, Y. Y., Vu, L. T., Ma, V., Peng, B., Chan, Y. S., Wei, L., Chin, S. M., Azad, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04791-8 · Cited by 663

PEGylated and targeted extracellular vesicles display enhanced cell specificity and circulation time

Kooijmans, S. A. A., Fliervoet, L. A. L., van der Meel, R., Fens, M. H. A. M., Heijnen, H. F. G., Henegouwen, P. M. P. V. B. E., Vader, P., & Schiffelers, R. M. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.01.009 · Cited by 645

Exosomes and Exosome-Inspired Vesicles for Targeted Drug Delivery

Antimisiaris, S. G., Mourtas, S., & Marazioti, A. (2018) · Pharmaceutics · doi:10.3390/pharmaceutics10040218 · Cited by 631

Exosome–Liposome Hybrid Nanoparticles Deliver CRISPR/Cas9 System in MSCs

Lin, Y., Wu, J., Gu, W., Huang, Y., Tong, Z., Huang, L., & Tan, J. (2018) · Advanced Science · doi:10.1002/advs.201700611 · Cited by 625

Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction

Shurtleff, M. J., Temoche-Diaz, M. M., Karfilis, K. V., Ri, S., & Schekman, R. (2016) · eLife · doi:10.7554/elife.19276 · Cited by 621

tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma

Maute, R. L., Schneider, C., Sumazin, P., Holmes, A. B., Califano, A., Basso, K., & Dalla‐Favera, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206761110 · Cited by 616

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 616

Detailed analysis of the plasma extracellular vesicle proteome after separation from lipoproteins

Karimi, N., Cvjetkovic, A., Jang, S. C., Crescitelli, R., Feizi, M. A. H., Nieuwland, R., Lötvall, J. O., & Lässer, C. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2773-4 · Cited by 613

Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells.

Squadrito, M. L., Baer, C., Burdet, F., Maderna, C., Gilfillan, G. D., Lyle, R., Ibberson, M., & De Palma, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.035 · Cited by 604

Plasma exosome microRNAs are indicative of breast cancer

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Selective Release of MicroRNA Species from Normal and Malignant Mammary Epithelial Cells

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