Reassessment of exosome composition
Open accessAbstract
The heterogeneity of small extracellular vesicles and presence of non-vesicular extracellular matter have led to debate about contents and functional properties of exosomes. Here, we employ high-resolution density gradient fractionation and direct immunoaffinity capture to precisely characterize the RNA, DNA, and protein constituents of exosomes and other non-vesicle material. Extracellular RNA, RNA-binding proteins, and other cellular proteins are differentially expressed in exosomes and non-vesicle compartments. Argonaute 1-4, glycolytic enzymes, and cytoskeletal proteins were not detected in exosomes. We identify annexin A1 as a specific marker for microvesicles that are shed directly from the plasma membrane. We further show that small extracellular vesicles are not vehicles of active DNA release. Instead, we propose a new model for active secretion of extracellular DNA through an autophagy- and multivesicular-endosome-dependent but exosome-independent mechanism. This study demonstrates the need for a reassessment of exosome composition and offers a framework for a clearer understanding of extracellular vesicle heterogeneity.
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?
GAPDH-GFP is predominantly associated with non-EV protein fractions, suggesting non-vesicular routes of GAPDH secretion.
“Analysis of GAPDH-GFP fluorescence from EVs and non-EV protein fractions reflected predominant association of GAPDH-GFP in the non-EV protein fractions, suggesting the existence of non-vesicular routes of GAPDH secretion, consistent with reports from others (Fig. 2g)34,43.”
From GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain (2021) · cites this paper as [43]
In one recent study, GAPDH was identified in non-vesicular aggregates from small EV preparations and was not pulled-down using immunocapture with CD63 beads.
“In one recent study, GAPDH was identified in non-vesicular aggregates from small EV preparations and was not pulled-down using immunocapture with magnetic beads coupled to CD63, employed in this analysis as a putative exosome marker43.”
From GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain (2021) · cites this paper as [43]
Only CD63 was commonly identified among all tetraspanins, likely reflecting protocol variabilities for SkM EV purifications.
“Of note, only CD63 was commonly identified among all tetraspanins (Figure 3) likely reflecting the protocol variabilities for SkM EV purifications (Jeppesen et al., 2019).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Jeppesen et al., 2019
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
Valadi, 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
Shedding 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
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
Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes
Trajković, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brügger, B., & Simons, M. (2008) · Science · doi:10.1126/science.1153124 · Cited by 3,639 · 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
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
Chromosomal instability drives metastasis through a cytosolic DNA response
Bakhoum, S. F., Ngo, B., Laughney, A. M., Cavallo, J.-A., Murphy, C. J., Ly, P., Shah, P., Sriram, R. K., Watkins, T. B. K., Taunk, N. K., et al. (2018) · Nature · doi:10.1038/nature25432 · Cited by 1,638 · 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
ATPase-Modulated Stress Granules Contain a Diverse Proteome and Substructure
Jain, S., Wheeler, J., Walters, R. W., Agrawal, A., Barsic, A. J., & Parker, R. (2016) · Cell · doi:10.1016/j.cell.2015.12.038 · Cited by 1,597 · see citing works
Depletion of microglia and inhibition of exosome synthesis halt tau propagation
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., & Ikezu, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4132 · Cited by 1,591 · see citing works
ExoCarta: A Web-Based Compendium of Exosomal Cargo
Keerthikumar, S., Chisanga, D., Ariyaratne, D., Saffar, H. A., Anand, S., Zhao, K., Samuel, M., Pathan, M., Jois, M., Chilamkurti, N., et al. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.09.019 · Cited by 1,447 · 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
van Niel, G., Charrin, S., Simoes, S., Romao, M., Rochin, L., Säftig, P., Marks, M. S., Rubinstein, E., & Raposo, G. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.019 · Cited by 955 · see citing works
ARF6-Regulated Shedding of Tumor Cell-Derived Plasma Membrane Microvesicles
Muralidharan-Chari, V., Clancy, J., Plou, C., Romao, M., Chavrier, P., Raposo, G., & D'Souza-Schorey, C. (2009) · Current Biology · doi:10.1016/j.cub.2009.09.059 · Cited by 912 · 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
P-Body Purification Reveals the Condensation of Repressed mRNA Regulons
Hubstenberger, A., Courel, M., Bénard, M., Souquère, S., Ernoult‐Lange, M., Chouaib, R., Zhou, Y., Morlot, J.-B., Munier, A., Fradet, M., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.003 · Cited by 793 · see citing works
Exosomes maintain cellular homeostasis by excreting harmful DNA from cells
Takahashi, A., Okada, R., Nagao, K., Kawamata, Y., Hanyu, A., Yoshimoto, S., Takasugi, M., Watanabe, S., Kanemaki, M. T., Obuse, C., et al. (2017) · Nature Communications · doi:10.1038/ncomms15287 · Cited by 761 · 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
Multivesicular Endosome Biogenesis in the Absence of ESCRTs
Stuffers, S., Wegner, C. S., Stenmark, H., & Brech, A. (2009) · Traffic · doi:10.1111/j.1600-0854.2009.00920.x · Cited by 731 · 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 726 · see citing works
Nabhan, J. F., Hu, R., Oh, R. S., Cohen, S. N., & Lu, Q. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200448109 · Cited by 722 · see citing works
Autophagy mediates degradation of nuclear lamina
Dou, Z., Xu, C., Donahue, G., Shimi, T., Pan, J.-A., Zhu, J., Ivanov, A., Capell, B. C., Drake, A. M., Shah, P. P., et al. (2015) · Nature · doi:10.1038/nature15548 · Cited by 655 · 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
Maturation of Autophagic Vacuoles in Mammalian Cells
Eskelinen, E.-L. (2005) · Autophagy · doi:10.4161/auto.1.1.1270 · Cited by 626 · see citing works
Mathivanan, S., Lim, J. W. E., Tauro, B. J., Ji, H. L., Moritz, R. L., & Simpson, R. J. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900152-mcp200 · Cited by 593 · see citing works
High‐speed centrifugation induces aggregation of extracellular vesicles
Linares, R., Tan, S., Gounou, C., Arraud, N., & Brisson, A. R. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.29509 · Cited by 572 · see citing works
Hristov, M., Erl, W., Linder, S., & Weber, P. C. (2004) · Blood · doi:10.1182/blood-2003-10-3614 · Cited by 485 · 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
Fader, C. M., Sánchez‐Martínez, D., Furlán, M., & Colombo, M. I. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00677.x · Cited by 470 · 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
Isolation and Characterization of Rat Liver Amphisomes
Berg, T. O., Fengsrud, M., Strømhaug, P. E., Berg, T., & Seglen, P. O. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.34.21883 · Cited by 385 · 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
Self-citationComparative analysis of discrete exosome fractions obtained by differential centrifugation
Jeppesen, D. K., Hvam, M. L., Primdal-Bengtson, B., Boysen, A. T., Whitehead, B. J., Dyrskjøt, L., Orntoft, T. F., Howard, K. A., & Ostenfeld, M. S. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.25011 · Cited by 369 · see citing works
Self-citationBroad 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
A rigorous method to enrich for exosomes from brain tissue
Vella, L. J., Scicluna, B. J., Cheng, L., Bawden, E., Masters, C. L., Ang, C., Williamson, N. A., McLean, C., Barnham, K. J., & Hill, A. F. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1348885 · Cited by 312 · see citing works
PIKfyve inhibition increases exosome release and induces secretory autophagy
Hessvik, N. P., Øverbye, A., Brech, A., Torgersen, M. L., Jakobsen, I. S., Sandvig, K., & Llorente, A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2309-8 · Cited by 269 · see citing works
Differential detergent sensitivity of extracellular vesicle subpopulations
Osteikoetxea, X., Sódar, B. W., Nemeth, A. H., Szabó-Taylor, K., Pálóczi, K., Vukman, K. V., Tamási, V., Balogh, A., Kittel, Á., Pállinger, É., et al. (2015) · Organic & Biomolecular Chemistry · doi:10.1039/c5ob01451d · Cited by 245 · see citing works
The role of extracellular vesicles in COVID-19 virus infection
Hassanpour, M., Rezaie, J., Nouri, M., & Panahi, Y. (2020) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2020.104422 · Cited by 229 · see citing works
Hrs‐ and CD63 ‐Dependent Competing Mechanisms Make Different Sized Endosomal Intraluminal Vesicles
Edgar, J. R., Eden, E. R., & Futter, C. E. (2013) · Traffic · doi:10.1111/tra.12139 · Cited by 224 · see citing works
Autoantigens are translocated into small apoptotic bodies during early stages of apoptosis
Schiller, M. R., Bekeredjian‐Ding, I., Heyder, P., Blank, N., Ho, A. D., & Lorenz, H.-M. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402239 · Cited by 210 · see citing works
Autophagosomes, phagosomes, autolysosomes, phagolysosomes, autophagolysosomes… Wait, I’m confused
Klionsky, D. J., Eskelinen, E., & Deretic, V. P. (2014) · Autophagy · doi:10.4161/auto.28448 · Cited by 210 · see citing works
Jeppesen, D. K., Nawrocki, A., Jensen, S. G., Thorsen, K., Whitehead, B. J., Howard, K. A., Dyrskjøt, L., Orntoft, T. F., Larsen, M. R., & Ostenfeld, M. S. (2013) · PROTEOMICS · doi:10.1002/pmic.201300452 · Cited by 177 · see citing works
Self-citationMYC Mediates Large Oncosome-Induced Fibroblast Reprogramming in Prostate Cancer
Minciacchi, V. R., Spinelli, C., Reis-Sobreiro, M., Cavallini, L., You, S., Zandian, M., Li, X., Mishra, R., Chiarugi, P., Adam, R. M., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2942 · Cited by 166 · see citing works
Tumor‐Derived Exosomes in Immunosuppression and Immunotherapy
Olejarz, W., Dominiak, A., Żołnierzak, A., Kubiak-Tomaszewska, G., & Lorenc, T. (2020) · Journal of Immunology Research · doi:10.1155/2020/6272498 · Cited by 165 · see citing works
Wang, Q., & Lu, Q. (2017) · Nature Communications · doi:10.1038/s41467-017-00767-2 · Cited by 141 · see citing works
Increased exosome production from tumour cell cultures using the Integra CELLine Culture System
Mitchell, J. P., Court, J., Mason, M. D., Tabi, Z., & Clayton, A. (2008) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.03.001 · Cited by 137 · see citing works
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 133 · see citing works
Self-citationMontermini, L., Meehan, B., Garnier, D., Lee, W.-J., Lee, T., Guha, A., Al-Nedawi, K., & Rak, J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.679217 · Cited by 121 · see citing works
Fenix, A. M., Taneja, N., Buttler, C. A., Lewis, J. H., van Engelenburg, S. B., Ohi, R., & Burnette, D. T. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-10-0725 · Cited by 118 · see citing works
Self-citationExophagy of annexin A2 via RAB11, RAB8A and RAB27A in IFN-γ-stimulated lung epithelial cells
Chen, Y.-D., Fang, Y.-T., Cheng, Y., Lin, C., Hsu, L., Wang, S., Anderson, R., Chang, C., & Lin, Y.-S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06076-4 · Cited by 110 · see citing works
Comparative Shotgun Proteomics Using Spectral Count Data and Quasi-Likelihood Modeling
Li, M., Gray, W., Zhang, H., Chung, C. H., Billheimer, D. D., Yarbrough, W. G., Liebler, D. C., Shyr, Y., & Slebos, R. J. C. (2010) · Journal of Proteome Research · doi:10.1021/pr100527g · Cited by 102 · see citing works
Self-citationCommitment of Annexin A2 in recruitment of microRNAs into extracellular vesicles
Hagiwara, K., Katsuda, T., Gailhouste, L., Kosaka, N., & Ochiya, T. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.11.036 · Cited by 98 · see citing works
Toda, H., Díaz-Varela, M., Seguí-Barber, J., Roobsoong, W., Baró, B., Garcı́a-Silva, S., Galiano, A., Gualdrón‐López, M., de Almeida, A. C. G., Brito, M. A. M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16337-y · Cited by 92 · see citing works
Development of the Vault Particle as a Platform Technology
Rome, L. H., & Kickhoefer, V. A. (2012) · ACS Nano · doi:10.1021/nn3052082 · Cited by 90 · see citing works
Self-citationExtracellular vesicle-mediated transfer of processed and functional RNY5 RNA
Chakrabortty, S. K., Prakash, A., Nechooshtan, G., Hearn, S., & Gingeras, T. (2015) · RNA · doi:10.1261/rna.053629.115 · Cited by 86 · see citing works
Choi, D., Go, G., Kim, D., Lee, J., Park, S., Vizio, D. D., & Gho, Y. S. (2020) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2020.1757209 · Cited by 57 · see citing works
Deep-Sequencing Identification of MicroRNA Biomarkers in Serum Exosomes for Early Pig Pregnancy
Zhou, C., Cai, G., Meng, F., et al. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00536 · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The biology <b>,</b> function <b>,</b> and biomedical applications of exosomes
Kalluri, R., & LeBleu, V. S. (2020) · Science · doi:10.1126/science.aau6977 · Cited by 10,770 · see citing works
RNA delivery by extracellular vesicles in mammalian cells and its applications
O’Brien, K., Breyne, K., Ughetto, S., Laurent, L. C., & Breakefield, X. O. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0251-y · Cited by 1,811 · see citing works
Engineering exosomes for targeted drug delivery
Liang, Y., Duan, L., Lu, J., & Xia, J. (2021) · Theranostics · doi:10.7150/thno.52570 · Cited by 1,547 · see citing works
Zhang, Y., Bi, J., Huang, J., Tang, Y., Du, S., & Li, P. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s264498 · Cited by 1,323 · see citing works
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
Mathieu, M., Névo, N., Jouve, M., Valenzuela, J. I., Maurin, M., Verweij, F. J., Palmulli, R., Lankar, D., Dingli, F., Loew, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24384-2 · Cited by 910 · see citing works
Therapeutically harnessing extracellular vesicles
Cheng, L., & Hill, A. F. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00410-w · Cited by 737 · 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
Self-citationApplication of exosomes as liquid biopsy in clinical diagnosis
Zhou, B., Xu, K., Zheng, X., Chen, T., Wang, J., Song, Y., Shao, Y., & Zheng, S. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00258-9 · Cited by 685 · see citing works
Macrophage-derived exosome-mimetic hybrid vesicles for tumor targeted drug delivery
Rayamajhi, S., Nguyen, T. D. T., Marasini, R., & Aryal, S. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.05.054 · Cited by 429 · see citing works
Todkar, K., Chikhi, L., Desjardins, V., El-Mortada, F., Pépin, G., & Germain, M. (2021) · Nature Communications · doi:10.1038/s41467-021-21984-w · Cited by 382 · see citing works
The function and clinical application of extracellular vesicles in innate immune regulation
Zhou, X., Xie, F., Wang, L., Zhang, L., Zhang, S., Fang, M., & Zhou, F. (2020) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-0391-1 · Cited by 294 · see citing works
Neural stem cells traffic functional mitochondria via extracellular vesicles
Peruzzotti-Jametti, L., Bernstock, J. D., Willis, C. M., Manferrari, G., Rogall, R., Fernandez-Vizarra, E., Williamson, J. C., Braga, A., van den Bosch, A., Leonardi, T., et al. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001166 · Cited by 263 · see citing works
Hou, J., Zhang, J., Cui, P., Zhou, Y., Liu, C., Wu, X., Ji, Y., Wang, S., Cheng, B., Ye, H., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci135197 · Cited by 239 · see citing works
The crosstalk: exosomes and lipid metabolism
Wang, W., Zhu, N., Yan, T., Shi, Y.-N., Chen, J., Zhang, C.-J., Xie, X.-J., Liao, D.-F., & Qin, L. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00581-2 · Cited by 203 · see citing works
Lei, Q., Gao, F., Liu, T., Ren, W., Chen, L., Cao, Y., Chen, W., Guo, S., Zhang, Q., Chen, W., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.aaz8697 · Cited by 170 · see citing works
Self-citationThe tissue origin effect of extracellular vesicles on cartilage and bone regeneration
Li, Q., Yu, H., Sun, M., Yang, P., Hu, X., Ao, Y., & Cheng, J. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.02.039 · Cited by 172 · see citing works
Exosome-mediated mRNA delivery in vivo is safe and can be used to induce SARS-CoV-2 immunity
Tsai, S. J., Atai, N. A., Cacciottolo, M., Nice, J., Salehi, A., Guo, C., Sedgwick, A., Kanagavelu, S., & Gould, S. J. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101266 · Cited by 142 · see citing works
The role of extracellular vesicles in skeletal muscle and systematic adaptation to exercise
Vechetti, I. J., Valentino, T., Mobley, C. B., & McCarthy, J. J. (2021) · The Journal of Physiology · doi:10.1113/jp278929 · Cited by 141 · see citing works
Skeletal Muscle-Released Extracellular Vesicles: State of the Art
Rome, S., Forterre, A., Mizgier, M. L., & Bouzakri, K. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00929 · Cited by 139 · see citing works
The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System
Li, T., Li, X., Han, G., Liang, M., Yang, Z., Zhang, C., Huang, S., Tai, S., & Yu, S. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics15010021 · Cited by 110 · see citing works
Dar, G. H., Mendes, C. C., Kuan, W.-L., Speciale, A. A., Conceição, M., Görgens, A., Uliyakina, I., Lobo, M. J., Lim, W. F., EL Andaloussi, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27056-3 · Cited by 100 · see citing works
Miyata, K., Imai, Y., Hori, S., Nishio, M., Loo, T. M., Okada, R., Yang, L., Nakadai, T., Maruyama, R., Fujii, R., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025647118 · Cited by 74 · see citing works
Exosome-mediated delivery of siRNA molecules in cancer therapy: triumphs and challenges
Ubanako, P., Mirza, S., Ruff, P., & Penny, C. (2024) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2024.1447953 · Cited by 68 · see citing works
Fuller, O. K., Whitham, M., Mathivanan, S., & Febbraio, M. A. (2020) · Cells · doi:10.3390/cells9102182 · Cited by 60 · see citing works
Lee, S., Kim, S., Chung, H., Moon, J. H., Kang, S. J., & Park, C.-G. (2020) · Immunology Letters · doi:10.1016/j.imlet.2020.06.006 · Cited by 57 · 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
The functional impact of nuclear reorganization in cellular senescence
Rocha, A., Dalgarno, A., & Neretti, N. (2022) · Briefings in Functional Genomics · doi:10.1093/bfgp/elab012 · Cited by 38 · see citing works
Han, S., Xue, L., Wei, Y., Yong, T., Jia, W., Qi, Y., Luo, Y., Liang, J., Wen, J., Bie, N., et al. (2023) · Advanced Science · doi:10.1002/advs.202207080 · Cited by 24 · see citing works
Self-citationExtracellular vesicle therapy for obesity-induced NAFLD: a comprehensive review of current evidence
Zhang, J., Ma, B., Wang, Z., Chen, Y., Li, C., & Dong, Y. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-023-01292-0 · Cited by 17 · see citing works
Extracellular DNA as potential contributors to pathological calcification
Niu, L., Zhu, Y., Wan, M., Wang, C., Hao, X., Song, J., Lei, C., Qin, Z., Tay, F., & Niu, L. (2024) · Interdisciplinary Medicine · doi:10.1002/inmd.20230061 · Cited by 16 · see citing works
- Authors
- 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., Fissell, W. H., Patton, J. G., Rome, L. H., Burnette, D. T., & Coffey, R. J.
- Affiliations
- Vanderbilt University Medical Center (US)
- Vanderbilt University (US)
- California NanoSystems Institute (US)
- Corresponding author
- Coffey, Robert J.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2019-04
- Volume
- 177
- Issue
- 2
- Pages
- 428-445.e18
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6664447
- OpenAlex
- W2933304441
- Cited by
- 2,975
- References
- 61
- Citations by year
- 2026: 317 · 2025: 422 · 2024: 491 · 2023: 447 · 2022: 433 · 2021: 426 · 2020: 334 · 2019: 100 · 2013: 2
- FWCI
- 107.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Vanderbilt-Ingram Cancer Center (CA68485)
- National Institutes of Health (R35 CA197570, F31 HL136081, U01-EB021214, R35 GM125028, U19 CA179514, DK20593, EY08126, DK59637, P30 DK058404, CA68485)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Keywords
- exosomes, small extracellular vesicles, extracellular RNA, extracellular DNA, exosome composition, microvesicles, annexin A1, autophagy, multivesicular bodies, RNA-binding proteins, density gradient fractionation, immunoaffinity capture
- MeSH terms
- Extracellular Vesicles, Cell Membrane, DNA, Female, Humans, Lysosomes, Male, Proteins, RNA, Annexin A1, Cell Line, Tumor, Cell-Derived Microparticles, Exosomes, Argonaute Proteins
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
