RNA delivery by extracellular vesicles in mammalian cells and its applications
Open accessAbstract
The term 'extracellular vesicles' refers to a heterogeneous population of vesicular bodies of cellular origin that derive either from the endosomal compartment (exosomes) or as a result of shedding from the plasma membrane (microvesicles, oncosomes and apoptotic bodies). Extracellular vesicles carry a variety of cargo, including RNAs, proteins, lipids and DNA, which can be taken up by other cells, both in the direct vicinity of the source cell and at distant sites in the body via biofluids, and elicit a variety of phenotypic responses. Owing to their unique biology and roles in cell-cell communication, extracellular vesicles have attracted strong interest, which is further enhanced by their potential clinical utility. Because extracellular vesicles derive their cargo from the contents of the cells that produce them, they are attractive sources of biomarkers for a variety of diseases. Furthermore, studies demonstrating phenotypic effects of specific extracellular vesicle-associated cargo on target cells have stoked interest in extracellular vesicles as therapeutic vehicles. There is particularly strong evidence that the RNA cargo of extracellular vesicles can alter recipient cell gene expression and function. During the past decade, extracellular vesicles and their RNA cargo have become better defined, but many aspects of extracellular vesicle biology remain to be elucidated. These include selective cargo loading resulting in substantial differences between the composition of extracellular vesicles and source cells; heterogeneity in extracellular vesicle size and composition; and undefined mechanisms for the uptake of extracellular vesicles into recipient cells and the fates of their cargo. Further progress in unravelling the basic mechanisms of extracellular vesicle biogenesis, transport, and cargo delivery and function is needed for successful clinical implementation. This Review focuses on the current state of knowledge pertaining to packaging, transport and function of RNAs in extracellular vesicles and outlines the progress made thus far towards their clinical applications.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Two primary approaches can accomplish the loading of specific cargoes into exosomes: endogenous loading and exogenous loading.
“Two primary approaches can accomplish the loading of specific cargoes into exosomes.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [15]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
3 retracted
Zhang, H., Deng, T., Ge, S., Liu, Y., Bai, M., Zhu, K., Fan, Q., Li, J., Ning, T., Tian, F., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0619-z · Cited by 303 · see citing works
RetractedZhang, H., Zhu, L., Bai, M., Liu, Y., Zhan, Y., Deng, T., Yang, H., Sun, W., Wang, X., Zhu, K., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31977 · Cited by 210 · see citing works
RetractedOtero‐Ortega, L., Frutos, M. C. G.-D., Laso-García, F., Rodríguez‐Frutos, B., Medina-Gutiérrez, E., López, J. A., Vázquez, J., Díez‐Tejedor, E., & Gutiérrez‐Fernández, M. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17708917 · Cited by 144 · see citing works
RetractedValadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007) · Nature Cell Biology · doi:10.1038/ncb1596 · Cited by 12,834 · see citing works
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin‐Smith, G. K., et al. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1535750 · Cited by 11,099 · see citing works
Self-citationShedding light on the cell biology of extracellular vesicles
van Niel, G., D'Angelo, G., & Raposo, G. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.125 · Cited by 8,369 · see citing works
Tumour exosome integrins determine organotropic metastasis
Hoshino, A., Costa-Silva, B., Shen, T.-L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., et al. (2015) · Nature · doi:10.1038/nature15756 · Cited by 5,101 · see citing works
Skog, J., Würdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Curry, W. T., Carter, B. S., Krichevsky, A. M., & Breakefield, X. O. (2008) · Nature Cell Biology · doi:10.1038/ncb1800 · Cited by 5,001 · see citing works
Self-citationDelivery 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 · see citing works
Mathieu, M., Jaular, L. M., Lavieu, G., & Théry, C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0250-9 · Cited by 3,776 · see citing works
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 · see citing works
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 · see citing works
Reassessment of exosome composition
Jeppesen, D. K., Fenix, A. M., Franklin, J. L., Higginbotham, J. N., Zhang, Q., Zimmerman, L. J., Liebler, D. C., Ping, J., Liu, Q., Evans, R., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.029 · Cited by 2,975 · see citing works
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 · see citing works
MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins
Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., & Remaley, A. T. (2011) · Nature Cell Biology · doi:10.1038/ncb2210 · Cited by 2,741 · see citing works
Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer
Kamerkar, S., LeBleu, V. S., Sugimoto, H., Yang, S., Ruivo, C. F., Melo, S. A., Lee, J. J., & Kalluri, R. (2017) · Nature · doi:10.1038/nature22341 · Cited by 2,639 · see citing works
Nanotubular Highways for Intercellular Organelle Transport
Rustom, A., Saffrich, R., Markovic, I., Walther, P., & Gerdes, H.-H. (2004) · Science · doi:10.1126/science.1093133 · Cited by 2,038 · see citing works
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 · see citing works
Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs
Villarroya-Beltri, C., Gutiérrez-Vázquez, C., Sánchez-Cabo, F., Perez-Hernandez, D., Vázquez, J., Martín-Cófreces, N., Martínez-Herrera, D. J., Pascual-Montano, A., Mittelbrunn, M., & Sánchez-Madrid, F. (2013) · Nature Communications · doi:10.1038/ncomms3980 · Cited by 1,907 · see citing works
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 1,768 · see citing works
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 · see citing works
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 1,672 · see citing works
Self-citationSystemically 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 · see citing works
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 1,623 · see citing works
Microenvironmental pH Is a Key Factor for Exosome Traffic in Tumor Cells
Parolini, I., Federici, C., Raggi, C., Lugini, L., Palleschi, S., Milito, A. D., Coscia, C., Iessi, E., Logozzi, M., Molinari, A., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.041152 · Cited by 1,561 · see citing works
MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response
Fabbri, M., Paone, A., Calore, F., Galli, R., Gaudio, E., Santhanam, R., Lovat, F., Fadda, P., Mao, C., Nuovo, G. J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209414109 · Cited by 1,558 · see citing works
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 · see citing works
Intracellular Toll-like Receptors
Blasius, A. L., & Beutler, B. (2010) · Immunity · doi:10.1016/j.immuni.2010.03.012 · Cited by 1,329 · see citing works
Escudier, B. J., 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 1,285 · see citing works
Use of resonance energy transfer to monitor membrane fusion
Struck, D. K., Hoekstra, D., & Pagano, R. E. (1981) · Biochemistry · doi:10.1021/bi00517a023 · Cited by 1,281 · see citing works
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 1,262 · see citing works
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 1,261 · see citing works
Iversen, T., Skotland, T., & Sandvig, K. (2011) · Nano Today · doi:10.1016/j.nantod.2011.02.003 · Cited by 1,235 · see citing works
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 · see citing works
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 · see citing works
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 1,105 · see citing works
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 1,080 · see citing works
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 1,069 · see citing works
A Novel Role for 3-O-Sulfated Heparan Sulfate in Herpes Simplex Virus 1 Entry
Shukla, D., Liu, J., Blaiklock, P., Shworak, N. W., Bai, X., Esko, J. D., Cohen, G. H., Eisenberg, R. J., ROSENBERG, R. D., & Spear, P. G. (1999) · Cell · doi:10.1016/s0092-8674(00)80058-6 · Cited by 1,053 · see citing works
Characterization of human plasma-derived exosomal RNAs by deep sequencing
Huang, X., Yuan, T., Tschannen, M., Sun, Z., Jacob, H. J., Du, M., Liang, M., Dittmar, R. L., Liu, Y. U., Liang, M., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-319 · Cited by 1,046 · see citing works
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 · see citing works
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 · see citing works
Self-citationJang, 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 1,023 · see citing works
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 1,000 · see citing works
Crescitelli, R., Lässer, C., Szabó, T. G., Kittel, Á., Eldh, M., Dianzani, I., Buzás, E. I., & Lötvall, J. O. (2013) · Journal of Extracellular Vesicles · doi:10.3402/jev.v2i0.20677 · Cited by 996 · see citing works
Gibbings, D., Ciaudo, C., Erhardt, M., & Voinnet, O. (2009) · Nature Cell Biology · doi:10.1038/ncb1929 · Cited by 990 · see citing works
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 · see citing works
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 941 · see citing works
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 · see citing works
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 919 · see citing works
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 · see citing works
Extracellular Vesicles in Cancer: Exosomes, Microvesicles and the Emerging Role of Large Oncosomes
Minciacchi, V. R., Freeman, M., & Vizio, D. D. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.02.010 · Cited by 900 · see citing works
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 894 · see citing works
Self-citationExosome 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 · see citing works
In Vivo Imaging Reveals Extracellular Vesicle-Mediated Phenocopying of Metastatic Behavior
Zomer, A., Maynard, C., Verweij, F., Kamermans, A., Schäfer, R., Beerling, E., Schiffelers, R., de Wit, E., Berenguer, J., Ellenbroek, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.042 · Cited by 815 · see citing works
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 795 · see citing works
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 784 · see citing works
Exosome Transfer from Stromal to Breast Cancer Cells Regulates Therapy Resistance Pathways
Boelens, M., Wu, T. J., Nabet, B., Xu, B.-H., Qiu, Y., Yoon, T., Azzam, D. J., Victor, C. T.-S., Wiemann, B., Ishwaran, H., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.051 · Cited by 768 · see citing works
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 766 · see citing works
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 756 · see citing works
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 · see citing works
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 741 · see citing works
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 729 · see citing works
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 715 · see citing works
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 · see citing works
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 712 · see citing works
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 707 · see citing works
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 697 · see citing works
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 · see citing works
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 688 · see citing works
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 · see citing works
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 682 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction
Shurtleff, M. J., Karfilis, K. V., Temoche-Diaz, M. M., Ri, S., & Schekman, R. W. (2016) · eLife · doi:10.7554/elife.19276 · Cited by 648 · see citing works
Pastuzyn, E. D., Day, C. E., Kearns, R. B., Kyrke‐Smith, M., Taibi, A. V., McCormick, J. F., Yoder, N., Belnap, D. M., Erlendsson, S., Morado, D. R., et al. (2018) · Cell · doi:10.1016/j.cell.2017.12.024 · Cited by 642 · see citing works
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 629 · see citing works
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 · see citing works
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 · see citing works
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 605 · see citing works
Exosomes and Exosome-Inspired Vesicles for Targeted Drug Delivery
Antimisiaris, S. G., Mourtas, S., & Marazioti, A. (2018) · Pharmaceutics · doi:10.3390/pharmaceutics10040218 · Cited by 605 · see citing works
Plasma exosome microRNAs are indicative of breast cancer
Hannafon, B. N., Trigoso, Y. D., Calloway, C. L., Zhao, Y. D., Lum, D. H., Welm, A. L., Zhao, Z. J., Blick, K. E., Dooley, W. C., & Ding, W. (2016) · Breast Cancer Research · doi:10.1186/s13058-016-0753-x · Cited by 603 · see citing works
Santangelo, L., Giurato, G., Cicchini, C., Montaldo, C., Mancone, C., Tarallo, R., Battistelli, C., Alonzi, T., Weisz, A., & Tripodi, M. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.031 · Cited by 600 · see citing works
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 591 · see citing works
Zhu, X., Badawi, M. A., Pomeroy, S. M., Sutaria, D. S., Xie, Z., Baek, A., Jiang, J., Elgamal, O. A., Mo, X. M., Perle, K. L., et al. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1324730 · Cited by 588 · see citing works
Selective Release of MicroRNA Species from Normal and Malignant Mammary Epithelial Cells
Pigati, L., Yaddanapudi, S. C., Iyengar, R., Kim, D.-J., Hearn, S., Danforth, D. N., Hastings, M. L., & Duelli, D. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013515 · Cited by 583 · see citing works
Lai, C. P., Kim, E. Y., Badr, C. E., Weissleder, R., Mempel, T. R., Tannous, B. A., & Breakefield, X. O. (2015) · Nature Communications · doi:10.1038/ncomms8029 · Cited by 574 · see citing works
Self-citationEndogenous 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 565 · see citing works
Exosome Secretion Is Enhanced by Invadopodia and Drives Invasive Behavior
Hoshino, D., Kirkbride, K. C., Costello, K., Clark, E. S., Sinha, S., Grega‐Larson, N. E., Tyska, M. J., & Weaver, A. M. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.050 · Cited by 561 · see citing works
Guduric‐Fuchs, J., O’Connor, A., Camp, B., O’Neill, C. L., Medina, R. J., & Simpson, D. A. C. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-357 · Cited by 554 · see citing works
Apoptotic Cell-Derived Extracellular Vesicles: More Than Just Debris
Caruso, S., & Poon, I. K. H. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01486 · Cited by 541 · see citing works
Elucidation of Exosome Migration Across the Blood–Brain Barrier Model In Vitro
Chen, C. C., Liu, L., Ma, F., Wong, C. W., Guo, X. E., Chacko, J. V., Farhoodi, H. P., Zhang, S. X., Zimak, J., Ségaliny, A., et al. (2016) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-016-0458-3 · Cited by 537 · see citing works
Coding and noncoding landscape of extracellular RNA released by human glioma stem cells
Wei, Z., Batagov, A. O., Schinelli, S., Wang, J., Wang, Y., Fatimy, R. E., Rabinovsky, R., Balaj, L., Chen, C. C., Hochberg, F. H., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01196-x · Cited by 532 · see citing works
Self-citationTherapeutic Applications of Extracellular Vesicles: Clinical Promise and Open Questions
György, B., Hung, M. E., Breakefield, X. O., & Leonard, J. N. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124630 · Cited by 512 · see citing works
Self-citationThe cell biology of receptor-mediated virus entry
Grove, J., & Marsh, M. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201108131 · Cited by 506 · see citing works
Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells
Ramakrishnaiah, V., Thumann, C., Fofana, I., Habersetzer, F., Pan, Q., de Ruiter, P. E., Willemsen, R., Demmers, J., Raj, V. S., Jenster, G. W., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221899110 · Cited by 503 · see citing works
Exosomes are natural carriers of exogenous siRNA to human cells in vitro
Shtam, T. A., Kovalev, R. A., Varfolomeeva, E. Y., Makarov, E. M., Kil, Y. V., & Filatov, M. V. (2013) · Cell Communication and Signaling · doi:10.1186/1478-811x-11-88 · Cited by 499 · see citing works
Extracellular vesicles and viruses: Are they close relatives?
Hoen, E. N. M. N., Cremer, T., Gallo, R. C., & Margolis, L. B. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1605146113 · Cited by 495 · see citing works
Pi, F., Binzel, D. W., Lee, T. J., Li, Z., Sun, M., Rychahou, P. G., Li, H., Haque, F., Wang, S., Croce, C. M., et al. (2017) · Nature Nanotechnology · doi:10.1038/s41565-017-0012-z · Cited by 495 · see citing works
Retrovirus-like Gag Protein Arc1 Binds RNA and Traffics across Synaptic Boutons
Ashley, J., Cordy, B., Lucia, D., Fradkin, L. G., Budnik, V., & Thomson, T. (2018) · Cell · doi:10.1016/j.cell.2017.12.022 · Cited by 488 · see citing works
Exosome-mediated delivery of hydrophobically modified siRNA for huntingtin mRNA silencing
Didiot, M.-C., Hall, L. M., Coles, A. H., Haraszti, R. A., Godinho, B. M., Chase, K., Sapp, E., Ly, S., Alterman, J. F., Hassler, M. R., et al. (2016) · Molecular Therapy · doi:10.1038/mt.2016.126 · Cited by 483 · see citing works
Kim, S. M., Yang, Y., Oh, S. J., Hong, Y., Seo, M., & Jang, M. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.09.013 · Cited by 481 · see citing works
Leidal, A. M., Huang, H. H., Marsh, T., Solvik, T. A., Zhang, D., Ye, J., Kai, F., Goldsmith, J., Liu, J. Y., Huang, Y.-H., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-019-0450-y · Cited by 480 · see citing works
MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression
Teng, Y., Ren, Y., Hu, X., Mu, J., Samykutty, A. K., Zhuang, X., Deng, Z., Kumar, A., Zhang, L., Merchant, M. L., et al. (2017) · Nature Communications · doi:10.1038/ncomms14448 · Cited by 479 · see citing works
Cholesterol-Dependent Cytolysins, a Family of Versatile Pore-Forming Toxins
Tweten, R. K. (2005) · Infection and Immunity · doi:10.1128/iai.73.10.6199-6209.2005 · Cited by 464 · see citing works
Visualizing of the cellular uptake and intracellular trafficking of exosomes by live‐cell microscopy
Tian, T., Wang, Y., Wang, H., Zhu, Z., & Xiao, Z. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22733 · Cited by 457 · see citing works
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., Perelman, L., Melo, C., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.09.005 · Cited by 453 · see citing works
Nabet, B. Y., Qiu, Y., Shabason, J. E., Wu, T. J., Yoon, T., Kim, B. C., Benci, J. L., DeMichele, A. M., Tchou, J. C., Marcotrigiano, J., et al. (2017) · Cell · doi:10.1016/j.cell.2017.06.031 · Cited by 453 · see citing works
Heusermann, W., Hean, J., Trojer, D., Steib, E., von Bueren, S., Graff-Meyer, A., Genoud, C., Martin, K., Pizzato, N., Voshol, J., et al. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201506084 · Cited by 447 · see citing works
Kooijmans, S. A. A., Gomez‐Aleza, C., Roffler, S. R., van Solinge, W. W., Vader, P., & Schiffelers, R. M. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.31053 · Cited by 429 · see citing works
Linkage between endosomal escape of LNP-mRNA and loading into EVs for transport to other cells
Maugeri, M., Nawaz, M., Papadimitriou, A., Angerfors, A., Camponeschi, A., Na, M., Hölttä, M., Skantze, P., Johansson, S., Sundqvist, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12275-6 · Cited by 428 · see citing works
Anchor peptide captures, targets, and loads exosomes of diverse origins for diagnostics and therapy
Gao, X., Ran, N., Dong, X., Zuo, B., Yang, R., Zhou, Q., Moulton, H. M., Seow, Y., & Yin, H. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aat0195 · Cited by 426 · see citing works
KRAS-MEK Signaling Controls Ago2 Sorting into Exosomes
McKenzie, A. J., Hoshino, D., Hong, N. H., Cha, D. J., Franklin, J. L., Coffey, R. J., Patton, J. G., & Weaver, A. M. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.085 · Cited by 423 · see citing works
Exosome removal as a therapeutic adjuvant in cancer
Marleau, A. M., Chen, C.-S., Joyce, J. A., & Tullis, R. H. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-134 · Cited by 412 · see citing works
Ridder, K., Keller, S., Dams, M., Rupp, A.-K., Schlaudraff, J., Del Turco, D., Starmann, J., Macas, J., Karpova, D., Devraj, K., et al. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001874 · Cited by 412 · see citing works
Bukong, T. N., Momen‐Heravi, F., Kodys, K., Bala, S., & Szabó, G. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004424 · Cited by 407 · see citing works
Pseudotyping exosomes for enhanced protein delivery in mammalian cells
Meyer, C. C., Losacco, J., Stickney, Z., Li, L., Marriott, G., & Lü, B. (2017) · International Journal of Nanomedicine · doi:10.2147/ijn.s133430 · Cited by 405 · see citing works
Mechanisms of RNA loading into exosomes
Janas, T., Janas, M. M., Sapoń, K., & Janas, T. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.04.036 · Cited by 397 · see citing works
Neuronal Exosomal miRNA-dependent Translational Regulation of Astroglial Glutamate Transporter GLT1
Morel, L., Regan, M., Higashimori, H., Ng, S. K., Esau, C., Vidensky, S., Rothstein, J., & Yang, Y. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.410944 · Cited by 390 · see citing works
Burgos, K., Malenica, I., Metpally, R., Courtright, A., Rakela, B., Beach, T., Shill, H., Adler, C., Sabbagh, M., Villa, S., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094839 · Cited by 385 · see citing works
Exosomes from mesenchymal stem/stromal cells: a new therapeutic paradigm
Yin, K., Wang, S., & Zhao, R. C. (2019) · Biomarker Research · doi:10.1186/s40364-019-0159-x · Cited by 383 · see citing works
Li, M., Zeringer, E., Barta, T. J., Schageman, J. J., Cheng, A., & Vlassov, A. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0502 · Cited by 382 · see citing works
Tkach, M., Kowal, J., Zucchetti, A. E., Enserink, L. N. F. L., Jouve, M. J., Lankar, D., Saitakis, M., Jaular, L. M., & Théry, C. (2017) · The EMBO Journal · doi:10.15252/embj.201696003 · Cited by 381 · see citing works
Transfer of Functional Cargo in Exomeres
Zhang, Q., Higginbotham, J. N., Jeppesen, D. K., Yang, Y., Li, W., McKinley, E. T., Graves‐Deal, R., Ping, J., Britain, C. M., Dorsett, K. A., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.009 · Cited by 374 · see citing works
Liu, J., Chang, J., Jiang, Y., Meng, X., Sun, T., Mao, L., Xu, Q., & Wang, M. (2019) · Advanced Materials · doi:10.1002/adma.201902575 · Cited by 373 · see citing works
Geoffroy, C., Gaillard, J. L., Alouf, J. E., et al. (1987) · Infection and Immunity · doi:10.1128/iai.55.7.1641-1646.1987 · Cited by 372 · see citing works
Oncogene Knockdown via Active Loading of Small RNAs into Extracellular Vesicles by Sonication
Lamichhane, T. N., Jeyaram, A., Patel, D. B., Parajuli, B., Livingston, N. K., Arumugasaamy, N., Schardt, J. S., & Jay, S. M. (2016) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-016-0457-4 · Cited by 371 · see citing works
Wang, Q., Ren, Y., Mu, J., Egilmez, N. K., Zhuang, X., Deng, Z., Zhang, L., Yan, J., Miller, D. M., & Zhang, H. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3095 · Cited by 368 · see citing works
Grange, C., Tapparo, M., Bruno, S., Chatterjee, D., Quesenberry, P. J., Tetta, C., & Camussi, G. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.1663 · Cited by 362 · see citing works
Multiplexed Profiling of Single Extracellular Vesicles
Lee, K., Fraser, K. B., Ghaddar, B., Yang, K. S., Kim, E., Balaj, L., Chiocca, E. A., Breakefield, X. O., Lee, H., & Weissleder, R. (2017) · ACS Nano · doi:10.1021/acsnano.7b07060 · Cited by 362 · see citing works
Self-citationChen, S., Tang, Y., Liu, Y., Zhang, P., Lv, L., Zhang, X., Jia, L., & Zhou, Y. (2019) · Cell Proliferation · doi:10.1111/cpr.12669 · Cited by 344 · see citing works
Broad role for YBX1 in defining the small noncoding RNA composition of exosomes
Shurtleff, M. J., Yao, J., Qin, Y., Nottingham, R. M., Temoche-Diaz, M. M., Schekman, R. W., & Lambowitz, A. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712108114 · Cited by 333 · see citing works
An improved MS2 system for accurate reporting of the mRNA life cycle
Tutucci, E., Vera, M., Biswas, J., Garcia, J. F., Parker, R., & Singer, R. H. (2017) · Nature Methods · doi:10.1038/nmeth.4502 · Cited by 332 · see citing works
Cortactin promotes exosome secretion by controlling branched actin dynamics
Sinha, S., Hoshino, D., Hong, N. H., Kirkbride, K. C., Grega‐Larson, N. E., Seiki, M., Tyska, M. J., & Weaver, A. M. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201601025 · Cited by 330 · see citing works
Reátegui, E., van der Vos, K. E., Lai, C. P., Zeinali, M., Atai, N. A., Aldikacti, B., Floyd, F. P., Khankhel, A. H., Thapar, V., Hochberg, F. H., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02261-1 · Cited by 330 · see citing works
Self-citationEnhancing Endosomal Escape for Intracellular Delivery of Macromolecular Biologic Therapeutics
Lönn, P., Kacsinta, A. D., Cui, X.-S., Hamil, A. S., Kaulich, M., Gogoi, K., & Dowdy, S. F. (2016) · Scientific Reports · doi:10.1038/srep32301 · Cited by 325 · see citing works
Manufacturing of Human Extracellular Vesicle-Based Therapeutics for Clinical Use
Gimona, M., Pachler, K., Laner‐Plamberger, S., Schallmoser, K., & Rohde, E. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061190 · Cited by 323 · see citing works
Heparanase Regulates Secretion, Composition, and Function of Tumor Cell-derived Exosomes
Thompson, C. A., Purushothaman, A., Ramani, V. C., Vlodavsky, I., & Sanderson, R. D. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.c112.444562 · Cited by 322 · see citing works
A live cell reporter of exosome secretion and uptake reveals pathfinding behavior of migrating cells
Sung, B. H., von Lersner, A. K., Guerrero, J. F., Krystofiak, E., Inman, D. R., Pelletier, R., Zijlstra, A., Ponik, S. M., & Weaver, A. M. (2020) · Nature Communications · doi:10.1038/s41467-020-15747-2 · Cited by 313 · see citing works
Hu, Y., Litwin, T. R., Nagaraja, A. R., Kwong, B., Katz, J. S., Watson, N., & Irvine, D. J. (2007) · Nano Letters · doi:10.1021/nl071542i · Cited by 306 · see citing works
Loss of EpCAM expression in breast cancer derived serum exosomes: Role of proteolytic cleavage
Rupp, A.-K., Rupp, C., Keller, S., Brase, J. C., Ehehalt, R., Fogel, M., Moldenhauer, G., Marmé, F., Sültmann, H., & Altevogt, P. (2011) · Gynecologic Oncology · doi:10.1016/j.ygyno.2011.04.035 · Cited by 301 · see citing works
Murillo, O. D., Thistlethwaite, W., Rozowsky, J. S., Subramanian, S. L., Lucero, R., Shah, N., Jackson, A. R., Srinivasan, S., Chung, A. Y., Laurent, C. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.018 · Cited by 300 · see citing works
Self-citationNakase, I., & Futaki, S. (2015) · Scientific Reports · doi:10.1038/srep10112 · Cited by 297 · see citing works
Datta, A., Kim, H., McGee, L. E., Johnson, A. E., Talwar, S., Marugán, J., Southall, N. T., Hu, X., Lal, M. A., Mondal, D., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-26411-7 · Cited by 297 · see citing works
Small RNA Sequencing across Diverse Biofluids Identifies Optimal Methods for exRNA Isolation
Srinivasan, S., Yeri, A., Cheah, P.-S., Chung, A. Y., Danielson, K., Hoff, P. L. D., Filant, J., Laurent, C. D., Laurent, L. D., Magee, R. G., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.024 · Cited by 296 · see citing works
Self-citationvan Balkom, B. W. M., Eisele, A. S., Pegtel, D. M., Bervoets, S., & Verhaar, M. C. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.26760 · Cited by 294 · see citing works
miR-1289 and “Zipcode”-like Sequence Enrich mRNAs in Microvesicles
Bolukbasi, M. F., Mizrak, A., Ozdener, G. B., Madlener, S., Ströbel, T., Erkan, E. P., Fan, J., Breakefield, X. O., & Saydam, O. (2012) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2011.2 · Cited by 290 · see citing works
Self-citationMcKiernan, J., Donovan, M. J., Margolis, E., Partin, A. W., Carter, B., Brown, G. A., Torkler, P., Noerholm, M., Skog, J., Shore, N. D., et al. (2018) · European Urology · doi:10.1016/j.eururo.2018.08.019 · Cited by 286 · see citing works
Protein Targeting to Exosomes/Microvesicles by Plasma Membrane Anchors
Shen, B., Wu, N., Yang, J.-M., & Gould, S. J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.208660 · Cited by 283 · see citing works
Luo, Z.-W., Li, F.-X.-Z., Liu, Y.-W., Rao, S.-S., Yin, H., Huang, J., Chen, C.-Y., Hu, Y., Zhang, Y., Tan, Y.-J., et al. (2019) · Nanoscale · doi:10.1039/c9nr02791b · Cited by 281 · see citing works
ARMMs as a versatile platform for intracellular delivery of macromolecules
Wang, Q., Yu, J., Kadungure, T., Beyene, J., Zhang, H., & Lu, Q. (2018) · Nature Communications · doi:10.1038/s41467-018-03390-x · Cited by 275 · see citing works
Nakase, I., Kobayashi, N. B., Takatani‐Nakase, T., & Yoshida, T. (2015) · Scientific Reports · doi:10.1038/srep10300 · Cited by 271 · see citing works
Xu, R., Greening, D. W., Rai, A., Ji, H. L., & Simpson, R. J. (2015) · Methods · doi:10.1016/j.ymeth.2015.04.008 · Cited by 267 · see citing works
Binding and Fusion of Extracellular Vesicles to the Plasma Membrane of Their Cell Targets
Prada, I., & Meldolesi, J. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17081296 · Cited by 265 · see citing works
Extracellular Vesicles Exploit Viral Entry Routes for Cargo Delivery
van Dongen, H. M., Masoumi, N., Witwer, K. W., & Pegtel, D. M. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00063-15 · Cited by 264 · see citing works
Statello, L., Maugeri, M., Garré, E., Nawaz, M., Wahlgren, J., Papadimitriou, A., Lundqvist, C., Lindfors, L., Collén, A., Sunnerhagen, P., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0195969 · Cited by 262 · see citing works
Glycosylation of extracellular vesicles: current knowledge, tools and clinical perspectives
Williams, C., Royo, F., Aizpurua‐Olaizola, O., Pazos, R., Boons, G., Reichardt, N., & Falcón‐Pérez, J. M. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1442985 · Cited by 260 · see citing works
Atomic structure of anthrax protective antigen pore elucidates toxin translocation
Jiang, J., Pentelute, B. L., Collier, R. J., & Zhou, Z. H. (2015) · Nature · doi:10.1038/nature14247 · Cited by 255 · see citing works
Targeting extracellular vesicles to injured tissue using membrane cloaking and surface display
Antes, T. J., Middleton, R., Luther, K. M., Ijichi, T., Peck, K. A., Liu, W. J., Valle, J., Echavez, A. K., & Marbán, E. (2018) · Journal of Nanobiotechnology · doi:10.1186/s12951-018-0388-4 · Cited by 255 · see citing works
A platform for actively loading cargo RNA to elucidate limiting steps in EV‐mediated delivery
Hung, M. E., & Leonard, J. N. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.31027 · Cited by 251 · see citing works
Extracellular vesicle-mediated transfer of functional RNA in the tumor microenvironment
Ridder, K., Sevko, A., Heide, J., Dams, M., Rupp, A.-K., Macas, J., Starmann, J., Tjwa, M., Plate, K., Sültmann, H., et al. (2015) · Oncoimmunology · doi:10.1080/2162402x.2015.1008371 · Cited by 243 · see citing works
Rescue of hearing by gene delivery to inner-ear hair cells using exosome-associated AAV
György, B., Sage, C., Indzhykulian, A. A., Scheffer, D. I., Brisson, A. R., Tan, S., Wu, X., Volak, A., Mu, D., Tamvakologos, P. I., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2016.12.010 · Cited by 243 · see citing works
Self-citationImproved Loading of Plasma-Derived Extracellular Vesicles to Encapsulate Antitumor miRNAs
Pomatto, M. A. C., Bussolati, B., D’Antico, S., Ghiotto, S., Tetta, C., Brizzi, M. F., & Camussi, G. (2019) · Molecular Therapy - Methods & Clinical Development · doi:10.1016/j.omtm.2019.01.001 · Cited by 243 · see citing works
Purification, characterization and biological significance of tumor-derived exosomes.
Koga, K., Matsumoto, K., Akiyoshi, T., Kubo, M., Yamanaka, N., Tasaki, A., Nakashima, H., Nakamura, M., Kuroki, S., Tanaka, M., et al. (2005) · PubMed · Cited by 240 · see citing works
Large Differences in Small RNA Composition Between Human Biofluids
Godoy, P. M., Bhakta, N. R., Barczak, A. J., Çakmak, H., Fisher, S. J., MacKenzie, T. C., Patel, T. C., Price, R. W., Smith, J. F., Woodruff, P. G., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.014 · Cited by 239 · see citing works
Selective Export into Extracellular Vesicles and Function of tRNA Fragments during T Cell Activation
Chiou, N.-T., Kageyama, R., & Ansel, K. M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.073 · Cited by 234 · see citing works
Rohde, E., Pachler, K., & Gimona, M. (2019) · Cytotherapy · doi:10.1016/j.jcyt.2018.12.006 · Cited by 234 · see citing works
Atienzar‐Aroca, S., Flores‐Bellver, M., Serrano‐Heras, G., Martínez‐Gil, N., Barcia, J. M., Aparicio, S. F., Pérez‐Cremades, D., García‐Verdugo, J. M., Díaz-Llopis, M., Romero, F. J., et al. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12834 · Cited by 232 · see citing works
Ying, W., Riopel, M., Bandyopadhyay, G. K., Dong, Y., Birmingham, A., Bae Seo, J., Ofrecio, J. M., Wollam, J., Hernández-Carretero, A., Fu, W., et al. (2018) · Yearbook of pediatric endocrinology · doi:10.1530/ey.15.11.14 · Cited by 229 · see citing works
Distinct mechanisms of microRNA sorting into cancer cell-derived extracellular vesicle subtypes
Temoche-Diaz, M. M., Shurtleff, M. J., Nottingham, R. M., Yao, J., Fadadu, R. P., Lambowitz, A. M., & Schekman, R. W. (2019) · eLife · doi:10.7554/elife.47544 · Cited by 225 · see citing works
Das, S., Abdel‐Mageed, A. B., Adamidi, C., Adelson, P. D., Akat, K. M., Alsop, E. B., Ansel, K. M., Arango, J. I., D, N. A. M., Kilinc, S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.023 · Cited by 223 · see citing works
Self-citationLiu, C., Song, J., Zhang, Y., & Wang, P. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2484 · Cited by 221 · see citing works
Serotonin stimulates secretion of exosomes from microglia cells
Glebov, K., Löchner, M., Jabs, R., Lau, T., Merkel, O., Schloss, P., Steinhäuser, C., & Walter, J. (2015) · Glia · doi:10.1002/glia.22772 · Cited by 221 · see citing works
Zou, J., Shi, M., Liu, X., Jin, C. Y., Xing, X., Qiu, L., & Tan, W. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.8b05204 · Cited by 214 · see citing works
Pastuzyn, E. D., Day, C. E., Kearns, R. B., Kyrke-Smith, M., Taibi, A. V., McCormick, J., Yoder, N., Belnap, D. M., Erlendsson, S., Morado, D. R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.024 · Cited by 213 · see citing works
Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein
Wahlberg, J. M., Bron, R., Wilschut, J., et al. (1992) · Journal of Virology · doi:10.1128/jvi.66.12.7309-7318.1992 · Cited by 212 · see citing works
Im, E.-J., Lee, C., Moon, P., Gunassekaran, G. R., Lee, B.-H., Lee, J. M., Lee, J.-C., Jee, J., Bae, J., Kwon, T., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09387-4 · Cited by 212 · see citing works
Extracellular Vesicle RNA: A Universal Mediator of Microbial Communication?
Tsatsaronis, J. A., Franch-Arroyo, S., Resch, U., & Charpentier, E. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2018.02.009 · Cited by 210 · see citing works
Diverse human extracellular RNAs are widely detected in human plasma
Freedman, J. E., Gerstein, M., Mick, E., Rozowsky, J., Levy, D., Kitchen, R., Das, S., Shah, R., Danielson, K., Beaulieu, L., et al. (2016) · Nature Communications · doi:10.1038/ncomms11106 · Cited by 202 · see citing works
Ekström, K., Valadi, H., Sjöstrand, M., Malmhäll, C., Bossios, A., Eldh, M., & Lötvall, J. (2012) · Journal of Extracellular Vesicles · doi:10.3402/jev.v1i0.18389 · Cited by 201 · see citing works
Ragelle, H., Riva, R., Vandermeulen, G., et al. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.12.026 · Cited by 200 · see citing works
Modification of the glycosylation of extracellular vesicles alters their biodistribution in mice
Royo, F., Cossío, U., Ruiz‐de‐Angulo, A., et al. (2019) · Nanoscale · doi:10.1039/c8nr03900c · Cited by 199 · see citing works
Abels, E. R., Maas, S. L. N., Nieland, L., Wei, Z., Cheah, P. S., Tai, E., Kolsteeg, C.-J., Dusoswa, S. A., Ting, D. T., Hickman, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.036 · Cited by 199 · see citing works
Self-citationSoares, A. R., Martins‐Marques, T., Ribeiro‐Rodrigues, T., Ferreira, J. V., Catarino, S., Pinho, M. J., Zuzarte, M., Anjo, S. I., Manadas, B. J., Sluijter, J. P. G., et al. (2015) · Scientific Reports · doi:10.1038/srep13243 · Cited by 198 · see citing works
Varcianna, A., Myszczynska, M. A., Castelli, L. M., O'Neill, B., Kim, Y., Talbot, J., Nyberg, S., Nyamali, I., Heath, P. R., Stopford, M. J., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2018.11.067 · Cited by 194 · see citing works
Oncosomes – large and small: what are they, where they came from?
Meehan, B., Rak, J. W., & Vizio, D. D. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.33109 · Cited by 189 · see citing works
Extracellular vesicles induce minimal hepatotoxicity and immunogenicity
Saleh, A. F. A., Lázaro‐Ibáñez, E., Forsgard, M., Shatnyeva, O., Osteikoetxea, X., Karlsson, F. H., Heath, N., Ingelsten, M., Rose, J., Harris, J., et al. (2019) · Nanoscale · doi:10.1039/c8nr08720b · Cited by 185 · see citing works
The Small Non-coding Vault RNA1-1 Acts as a Riboregulator of Autophagy
Horos, R., Büscher, M., Kleinendorst, R., Alleaume, A.-M., Tarafder, A. K., Schwarzl, T., Dziuba, D., Tischer, C., Zielonka, E. M., Adak, A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.030 · Cited by 183 · see citing works
Assessing the role of surface glycans of extracellular vesicles on cellular uptake
Williams, C., Pazos, R., Royo, F., González, E., Roura‐Ferrer, M., Martinez, A., Gamiz, J., Reichardt, N., & Falcón‐Pérez, J. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-48499-1 · Cited by 181 · see citing works
Nakase, I., Noguchi, K., Aoki, A., Takatani‐Nakase, T., Fujii, I., & Futaki, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-02014-6 · Cited by 180 · see citing works
Fanale, D., Taverna, S., Russo, A. D., & Bazan, V. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_9 · Cited by 178 · see citing works
Shen, M., Dong, C., Ruan, X., Yan, W., Cao, M., Pizzo, D. P., Wu, X., Yang, L., Liu, L., Ren, X., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-4055 · Cited by 178 · see citing works
Comprehensive multi-center assessment of small RNA-seq methods for quantitative miRNA profiling
Giraldez, M. D., Spengler, R. M., Etheridge, A., Godoy, P. M., Barczak, A. J., Srinivasan, S., De Hoff, P. L., Tanriverdi, K., Courtright, A., Lu, S., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4183 · Cited by 177 · see citing works
Self-citationRole of Alix in miRNA packaging during extracellular vesicle biogenesis
IAVELLO, A., FRECH, V. S. L., GAI, C., DEREGIBUS, M. C., QUESENBERRY, P. J., & CAMUSSI, G. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2488 · Cited by 175 · see citing works
Long non-coding RNAs harboring miRNA seed regions are enriched in prostate cancer exosomes
Ahadi, A., Brennan, S. E., Kennedy, P. J., Hutvágner, G., & Tran, N. (2016) · Scientific Reports · doi:10.1038/srep24922 · Cited by 175 · see citing works
Persson, H., Kvist, A., Vallon‐Christersson, J., Medstrand, P., Borg, Å., & Rovira, C. (2009) · Nature Cell Biology · doi:10.1038/ncb1972 · Cited by 173 · see citing works
Muscle-enriched microRNA miR-486 decreases in circulation in response to exercise in young men
Aoi, W., Ichikawa, H., Mune, K., Tanimura, Y., Mizushima, K., Naito, Y., & Yoshikawa, T. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00080 · Cited by 172 · see citing works
Mukherjee, K., Ghoshal, B., Ghosh, S., Chakrabarty, Y., Shivaprasad, S., Das, S., & Bhattacharyya, S. N. (2016) · EMBO Reports · doi:10.15252/embr.201541930 · Cited by 171 · see citing works
Kooijmans, S. A. A., Gitz-Francois, J. J., Schiffelers, R. M., & Vader, P. (2018) · Nanoscale · doi:10.1039/c7nr06966a · Cited by 163 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [131]Schorey J Cheng Y Extracellular vesicles promote host immunity during an M. tuberculosis infection through RNA sensing bioRxiv 2018 10.1101/346254 · DOI
Cited by
Sorted by citations
Challenges and directions in studying cell–cell communication by extracellular vesicles
van Niel, G., Carter, D. R. F., Clayton, A., Lambert, D. W., Raposo, G., & Vader, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00460-3 · Cited by 1,229 · see citing works
Extracellular Vesicles and Nanoparticles: Emerging Complexities
Jeppesen, D. K., Zhang, Q., Franklin, J. L., & Coffey, R. J. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.01.002 · Cited by 705 · see citing works
Clinical applications of stem cell-derived exosomes
Tan, F., Li, X., Wang, Z., Li, J., Shahzad, K., & Zheng, J. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01704-0 · Cited by 708 · see citing works
Exosome Processing and Characterization Approaches for Research and Technology Development
Lai, J. J., Chau, Z. L., Chen, S., Hill, J. J., Korpany, K. V., Liang, N., Lin, L., Lin, Y., Liu, J. K., Liu, Y., et al. (2022) · Advanced Science · doi:10.1002/advs.202103222 · Cited by 623 · see citing works
Engineered Extracellular Vesicles for Cancer Therapy
Zhang, X., Zhang, H., Gu, J., Zhang, J., Shi, H., Qian, H., Wang, D., Xu, W., Pan, J., & Santos, H. A. (2021) · Advanced Materials · doi:10.1002/adma.202005709 · Cited by 428 · see citing works
Intradermally delivered mRNA-encapsulating extracellular vesicles for collagen-replacement therapy
You, Y., Tian, Y., Yang, Z., Shi, J., Kwak, K. J., Tong, Y., Estania, A. P., Cao, J., Hsu, W.-H., Liu, Y., et al. (2023) · Nature Biomedical Engineering · doi:10.1038/s41551-022-00989-w · Cited by 258 · see citing works
Xu, M., Feng, T., Liu, B., Qiu, F., Xu, Y., Zhao, Y., & Zheng, Y. (2021) · Theranostics · doi:10.7150/thno.62330 · Cited by 229 · see citing works
Adipose-derived stem cells secretome and its potential application in “stem cell-free therapy”
Trzyna, A., & Banaś-Ząbczyk, A. (2021) · Biomolecules · doi:10.3390/biom11060878 · Cited by 201 · see citing works
Exosome as drug delivery system: Current advancements
Sharma, V., & Mukhopadhyay, C. D. (2024) · Extracellular Vesicle · doi:10.1016/j.vesic.2023.100032 · Cited by 156 · see citing works
Alzahrani, F. A., Khan, M. I., Kameli, N., Alsahafi, E., & Riza, Y. M. (2023) · Biomolecules · doi:10.3390/biom13050839 · Cited by 143 · see citing works
“These categories are exosomes (50–150 nm), microvesicles (100–1000 nm), large oncosomes (1000–10,000 nm), and apoptotic bodies (100–5000 nm) [2].”
BackgroundExosome for mRNA delivery: Strategies and therapeutic applications
Iqbal, Z., Rehman, K., Mahmood, A., Shabbir, M., Liang, Y., Duan, L., & Zeng, H. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-02634-x · Cited by 144 · see citing works
Plant-Derived Nanovesicles: Further Exploration of Biomedical Function and Application Potential
Li, A., Li, D., Gu, Y., Liu, R., Tang, X., Zhao, Y., Qi, F., Wei, J., & Liu, J. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2022.12.022 · Cited by 137 · see citing works
Ramirez-Garrastacho, M., Bajo-Santos, C., Line, A., Martens-Uzunova, E. S., de la Fuente, J. M., Moros, M., Soekmadji, C., Tasken, K. A., & Llorente, A. (2022) · British Journal of Cancer · doi:10.1038/s41416-021-01610-8 · Cited by 130 · see citing works
Extracellular Vesicles as an Emerging Frontier in Spinal Cord Injury Pathobiology and Therapy
Dutta, D., Khan, N., Wu, J., & Jay, S. M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.01.003 · Cited by 112 · see citing works
Therapeutic reversal of Huntington’s disease by <i>in vivo</i> self-assembled siRNAs
Zhang, L., Wu, T., Shan, Y., Li, G., Ni, X., Chen, X., Hu, X., Lin, L., Li, Y., Guan, Y., et al. (2021) · Brain · doi:10.1093/brain/awab354 · Cited by 97 · see citing works
Lee, E. J., Choi, Y., Lee, H. J., Hwang, D. W., & Lee, D. S. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01356-2 · Cited by 89 · see citing works
Current advances in non‐viral gene delivery systems: Liposomes versus extracellular vesicles
Belhadj, Z., Qie, Y., Carney, R. P., Li, Y., & Nie, G. (2023) · BMEMat · doi:10.1002/bmm2.12018 · Cited by 79 · see citing works
Engineered extracellular vesicles as brain therapeutics
Lino, M. M., Simões, S., Tomatis, F., Albino, I., Barrera, A., Vivien, D., Sobrino, T., & Ferreira, L. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.08.037 · Cited by 68 · see citing works
Extracellular Vesicles as Novel Diagnostic and Prognostic Biomarkers for Parkinson’s Disease
Leggio, L., Paternò, G., Vivarelli, S., Falzone, G. G., Giachino, C., Marchetti, B., & Iraci, N. (2021) · Aging and disease · doi:10.14336/ad.2021.0527 · Cited by 55 · see citing works
Selective Encapsulation of Therapeutic mRNA in Engineered Extracellular Vesicles by DNA Aptamer
Zhang, S., Dong, Y., Wang, Y., Sun, W., Wei, M., Yuan, L., & Yang, G. (2021) · Nano Letters · doi:10.1021/acs.nanolett.1c01817 · Cited by 50 · see citing works
- Authors
- O’Brien, K., Breyne, K., Ughetto, S., Laurent, L. C., & Breakefield, X. O.
- Affiliations
- Harvard University (US)
- University of California San Diego (US)
- Corresponding author
- Laurent, Louise C.
- Breakefield, Xandra O.
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2020-05-26
- Volume
- 21
- Issue
- 10
- Pages
- 585-606
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- PMC
- PMC7249041
- OpenAlex
- W3028960763
- Cited by
- 1,811
- References
- 301
- Citations by year
- 2026: 217 · 2025: 282 · 2024: 315 · 2023: 329 · 2022: 338 · 2021: 255 · 2020: 70 · 2019: 2
- FWCI
- 23.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Associazione Italiana per la Ricerca sul Cancro (IG20210, 20210)
- National Institutes of Health (CA069246)
- National Heart, Lung, and Blood Institute (U01HL126494)
- National Cancer Institute (P01CA069246, CA069246, CA232103, R35CA232103)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Keywords
- extracellular vesicles, RNA delivery, exosomes, microvesicles, oncosomes, apoptotic bodies, RNA cargo, vesicle biogenesis, vesicle uptake, intercellular communication, biomarkers, gene expression regulation
- MeSH terms
- Extracellular Vesicles, Animals, Biological Transport, Cell Communication, Humans, Mammals, RNA
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review