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Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells
Open accessAbstract
The immune synapse is an exquisitely evolved means of communication between T cells and antigen-presenting cells (APCs) during antigen recognition. Recent evidence points to the transfer of RNA via exosomes as a novel mode of intercellular communication. Here we show that exosomes of T, B and dendritic immune cells contain microRNA (miRNA) repertoires that differ from those of their parent cells. We investigate whether miRNAs are exchanged during cognate immune interactions, and demonstrate the existence of antigen-driven unidirectional transfer of miRNAs from the T cell to the APC, mediated by the delivery of CD63+ exosomes on immune synapse formation. Inhibition of exosome production by targeting neutral sphingomyelinase-2 impairs transfer of miRNAs to APCs. Moreover, miRNAs transferred during immune synapsis are able to modulate gene expression in recipient cells. Thus, our results support a mechanism of cellular communication involving antigen-dependent, unidirectional intercellular transfer of miRNAs by exosomes during immune synapsis. Exosomes released from cells can transfer RNA to recipient cells. In this study, the authors demonstrate that microRNAs in exosomes from T cells can be transferred to antigen-presenting cells during immune synapsis, and that this can alter gene expression, suggesting a new form of cellular communication.
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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
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829
Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids
Théry, C., Amigorena, S., Raposo, G., & Clayton, A. (2006) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb0322s30 · Cited by 5,766
Huber, W., von Heydebreck, A., Sültmann, H., Poustka, A., & Vingron, M. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.suppl_1.s96 · Cited by 2,440
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
Requirement of bic/microRNA-155 for Normal Immune Function
Rodriguez, A., Vigorito, E., Clare, S., Warren, M. V., Couttet, P., Soond, D. R., van Dongen, S., Grocock, R. J., Das, P. P., Miska, E. A., et al. (2007) · Science · doi:10.1126/science.1139253 · Cited by 1,833
Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., & Ratajczak, M. Z. (2006) · Leukemia · doi:10.1038/sj.leu.2404296 · Cited by 1,340
Trafficking and function of the tetraspanin CD63
Pols, M. S., & Klumperman, J. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.09.020 · Cited by 745
TCR Activation of Human T Cells Induces the Production of Exosomes Bearing the TCR/CD3/ζ Complex
Blanchard, N., Lankar, D., Faure, F., Regnault, A., Dumont, C., Raposo, G., & Hivroz, C. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.7.3235 · Cited by 660
MicroRNAs and immunity: Novel players in the regulation of normal immune function and inflammation
Sonkoly, E., Ståhle, M., & Pivarcsi, A. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.01.005 · Cited by 523 · cited 1×
“The emergence of miRNAs as potent post-transcriptional regulators of gene expression has broad implications in all areas of cell biology, including the immune syste”
Background
Research works printed but not linked: 50
- Monks, C. R. F., Freiberg, B. A., Kupfer, H., Sclaky, N. & Kupfer, A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82–86 (1998). · DOI · Paper page
- Dustin, M. L. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell 94, 667–677 (1998). · DOI
- Kupfer, A. & Dennert, G. Reorientation of the microtubule-organizing center and the Golgi apparatus in cloned cytotoxic lymphocytes triggered by binding to lysable target cells. J. Immunol. 133, 2762–2766 (1984). · DOI
- Sancho, D. et al. Regulation of microtubule-organizing center orientation and actomyosin cytoskeleton rearrangement during immune interactions. Immunol. Rev. 189, 84–97 (2002). · DOI
- Huse, M., Lillemeier, B. F., Kuhns, M. S., Chen, D. S. & Davis, M. M. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7, 247–255 (2006). · DOI · Paper page
- Griffiths, G. M., Tsun, A. & Stinchcombe, J. C. The immunological synapse: a focal point for endocytosis and exocytosis. J. Cell. Biol. 189, 399–406 (2010). · DOI
- Das, V. et al. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 20, 577–588 (2004). · DOI
- Gorska, M. M., Liang, Q., Karim, Z. & Alam, R. Uncoordinated 119 protein controls trafficking of Lck via the Rab11 endosome and is critical for immunological synapse formation. J. Immunol. 183, 1675–1684 (2009). · DOI
- Varma, R., Campi, G., Yokosuka, T., Saito, T. & Dustin, M. L. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25, 117–127 (2006). · DOI
- Alcover, A. & Thoulouze, M. I. Vesicle traffic to the immunological synapse: a multifunctional process targeted by lymphotropic viruses. Curr. Top Microbiol. Immunol. 340, 191–207 (2010).
- Simons, M. & Raposo, G. Exosomes--vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575–581 (2009). · DOI · Paper page
- Thery, C., Ostrowski, M. & Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581–593 (2009). · DOI
- Skog, J. et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470–1476 (2008). · DOI · Paper page
- Deregibus, M. C. et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110, 2440–2448 (2007). · DOI · Paper page
- Ratajczak, J. et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847–856 (2006). · DOI · Paper page
- Zernecke, A. et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal 2, ra81 (2009). · DOI · Paper page
- Pegtel, D. M. et al. Functional delivery of viral miRNAs via exosomes. Proc. Natl Acad. Sci. USA 107, 6328–6333 (2010). · DOI · Paper page
- Carthew, R. W. & Sontheimer, E. J. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655 (2009). · DOI
- O'Connell, R. M., Rao, D. S., Chaudhuri, A. A. & Baltimore, D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111–122 (2010). · DOI · Paper page
- Lodish, H. F., Zhou, B., Liu, G. & Chen, C. Z. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 8, 120–130 (2008). · DOI
- Li, Q. J. et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129, 147–161 (2007). · DOI · Paper page
- Thai, T. H. et al. Regulation of the germinal center response by microRNA-155. Science 316, 604–608 (2007). · DOI · Paper page
- Cobb, B. S. et al. A role for Dicer in immune regulation. J. Exp. Med. 203, 2519–2527 (2006). · DOI · Paper page
- Koralov, S. B. et al. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132, 860–874 (2008). · DOI · Paper page
- Zumaquero, E. et al. Exosomes from human lymphoblastoid B cells express enzymatically active CD38 that is associated with signaling complexes containing CD81, Hsc-70 and Lyn. Exp. Cell Res. 316, 2692–2706 (2010). · DOI
- Valitutti, S., Dessing, M., Aktories, K., Gallati, H. & Lanzavecchia, A. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181, 577–584 (1995). · DOI
- Hume, C. R., Shookster, L. A., Collins, N., O'Reilly, R. & Lee, J. S. Bare lymphocyte syndrome: altered HLA class II expression in B cell lines derived from two patients. Hum. Immunol. 25, 1–11 (1989). · DOI
- Trajkovic, K. et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244–1247 (2008). · DOI
- Islam, A. et al. The brefeldin A-inhibited guanine nucleotide-exchange protein, BIG2, regulates the constitutive release of TNFR1 exosome-like vesicles. J. Biol. Chem. 282, 9591–9599 (2007). · DOI · Paper page
- Ostrowski, M. et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12 Suppl, 1–13 (2010).
- Tavazoie, S. F. et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451, 147–152 (2008). · DOI · Paper page
- Booth, A. M. et al. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923–935 (2006). · DOI · Paper page
- Cocucci, E., Racchetti, G. & Meldolesi, J. Shedding microvesicles: artefacts no more. Trends Cell. Biol. 19, 43–51 (2009). · DOI · Paper page
- Rechavi, O. et al. Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev. 23, 1971–1979 (2009). · DOI
- Davis, D. M. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat. Rev. Immunol. 7, 238–243 (2007). · DOI
- Huse, M., Quann, E. J. & Davis, M. M. Shouts, whispers and the kiss of death: directional secretion in T cells. Nat. Immunol. 9, 1105–1111 (2008). · DOI
- Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452 (2009). · DOI · Paper page
- Zhang, Y. et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell 39, 133–144 (2010). · DOI · Paper page
- Gibbings, D. J., Ciaudo, C., Erhardt, M. & Voinnet, O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell. Biol. 11, 1143–1149 (2009). · DOI · Paper page
- Lee, Y. S. et al. Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell. Biol. 11, 1150–1156 (2009). · DOI
- Xiao, C. & Rajewsky, K. MicroRNA control in the immune system: basic principles. Cell 136, 26–36 (2009). · DOI · Paper page
- Morelli, A. E. et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104, 3257–3266 (2004). · DOI · Paper page
- Feng, D. et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic 11, 675–687 (2010). · DOI · Paper page
- Tian, T., Wang, Y., Wang, H., Zhu, Z. & Xiao, Z. Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J. Cell. Biochem. 111, 488–496 (2010). · DOI
- Parolini, I. et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 284, 34211–34222 (2009). · DOI
- Niedergang, F. et al. The Staphylococcus aureus enterotoxin B superantigen induces specific T cell receptor down-regulation by increasing its internalization. J. Biol. Chem. 270, 12839–12845 (1995). · DOI
- Hewitt, C. R. et al. Major histocompatibility complex independent clonal T cell anergy by direct interaction of Staphylococcus aureus enterotoxin B with the T cell antigen receptor. J. Exp. Med. 175, 1493–1499 (1992). · DOI
- de la Fuente, H. et al. Synaptic clusters of MHC class II molecules induced on DCs by adhesion molecule-mediated initial T-cell scanning. Mol. Biol. Cell 16, 3314–3322 (2005). · DOI
- Robles-Valero, J. et al. Integrin and CD3/TCR activation are regulated by the scaffold protein AKAP450. Blood 115, 4174–4184 (2010). · DOI
- Mittelbrunn, M., Yanez-Mo, M., Sancho, D., Ursa, A. & Sanchez-Madrid, F. Cutting edge: dynamic redistribution of tetraspanin CD81 at the central zone of the immune synapse in both T lymphocytes and APC. J. Immunol. 169, 6691–6695 (2002). · DOI
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Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V. C., Borràs, F. E., Breakefield, X., Budnik, V., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001450 · Cited by 1,367
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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
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Fang, T., Lv, H., Lv, G., Li, T., Wang, C., Han, Q., Yu, L., Su, B., Guo, L., Huang, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02583-0 · Cited by 995
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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
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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
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Bronisz, A., Wang, Y., Nowicki, M. O., Peruzzi, P., Ansari, K. I., Ogawa, D., Balaj, L., De Rienzo, G., Mineo, M., Nakano, I., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2650 · Cited by 222
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Quek, C., & Hill, A. F. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.09.090 · Cited by 213
Sarkar, S., Jun, S., Rellick, S., Quintana, D. D., Cavendish, J. Z., & Simpkins, J. W. (2016) · Brain Research · doi:10.1016/j.brainres.2016.05.026 · Cited by 209
Rodrigues, M., Fan, J., Lyon, C., Wan, M., & Hu, Y. (2018) · Theranostics · doi:10.7150/thno.20576 · Cited by 191
Mukherjee, K., Ghoshal, B., Ghosh, S., Chakrabarty, Y., Shwetha, S., Das, S., & Bhattacharyya, S. N. (2016) · The EMBO Reports · doi:10.15252/embr.201541930 · Cited by 184
MicroRNAs as regulators of brain function and targets for treatment of epilepsy
Brennan, G. P., & Henshall, D. C. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0369-8 · Cited by 169
Exosomes and stem cells in degenerative disease diagnosis and therapy
Chang, Y.-H., Wu, K.-C., Harn, H.-J., Lin, S.-Z., & Ding, D.-C. (2018) · Cell Transplantation · doi:10.1177/0963689717723636 · Cited by 159
Harrison, E. B., Hochfelder, C. G., Lamberty, B. G., Meays, B. M., Morsey, B. M., Kelso, M. L., Fox, H. S., & Yelamanchili, S. V. (2016) · FEBS Open Bio · doi:10.1002/2211-5463.12092 · Cited by 151
Geekiyanage, H., Rayatpisheh, S., Wohlschlegel, J. A., Brown, R., & Ambros, V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008323117 · Cited by 148
Bovy, N., Blomme, B., Frères, P., Dederen, S., Nivelles, O., Lion, M., Carnet, O., Martial, J. A., Noël, A., Thiry, M., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.3520 · Cited by 147
NADPH oxidase deficiency underlies dysfunction of aged CD8+ Tregs
Wen, Z., Shimojima, Y., Shirai, T., Li, Y., Ju, J., Yang, Z., Tian, L., Goronzy, J. J., & Weyand, C. M. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84181 · Cited by 146
MicroRNAs are shaping the hematopoietic landscape
Bissels, U., Bosio, A., & Wagner, W. (2012) · Haematologica · doi:10.3324/haematol.2011.051730 · Cited by 129
Mesenchymal stem cell-derived exosome: A tumor regulator and carrier for targeted tumor therapy
Zhang, F., Guo, J., Zhang, Z., Qian, Y., Wang, G., Duan, M., Zhao, H., Yang, Z., & Jiang, X. (2022) · Cancer Letters · doi:10.1016/j.canlet.2021.11.015 · Cited by 127
Investigation of MicroRNA Expression in Human Serum During the Aging Process
Zhang, H., Yang, H., Zhang, C., Jing, Y., Wang, C., Liu, C., Zhang, R., Wang, J., Zhang, J., Zen, K., et al. (2015) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glu145 · Cited by 123
Monfared, H., Jahangard, Y., Nikkhah, M., Mirnajafi-Zadeh, J., & Mowla, S. J. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00782 · Cited by 123
Feng, Y., Huang, W., Meng, W., Jegga, A. G., Wang, Y., Cai, W., Kim, H. W., Pasha, Z., Wen, Z., Rao, F., et al. (2014) · Stem Cells · doi:10.1002/stem.1571 · Cited by 121
Sources and Functions of Extracellular Small RNAs in Human Circulation
Fritz, J. V., Heintz-Buschart, A., Ghosal, A., Wampach, L., Etheridge, A., Galas, D., & Wilmes, P. (2016) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071715-050711 · Cited by 121
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Takahashi, R.-U., Miyazaki, H., & Ochiya, T. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2013.00295 · Cited by 118
The Roles of MicroRNAs in Breast Cancer
Takahashi, R.-U., Miyazaki, H., & Ochiya, T. (2015) · Cancers · doi:10.3390/cancers7020598 · Cited by 116
Exosomes: Mediators of bone diseases, protection, and therapeutics potential
Behera, J., & Tyagi, N. (2018) · Oncoscience · doi:10.18632/oncoscience.421 · Cited by 101
Revisiting extracellular RNA release, processing, and function
Tosar, J. P., Witwer, K., & Cayota, A. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.12.008 · Cited by 91
Iftikhar, H., & Carney, G. E. (2016) · BioEssays · doi:10.1002/bies.201500130 · Cited by 87
Circulating microRNAs as biomarkers for depression: Many candidates, few finalists
Yuan, H., Mischoulon, D., Fava, M., & Otto, M. W. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.06.058 · Cited by 86
Yuan, D., Xu, J., Wang, J., Pan, Y., Fu, J., Bai, Y., Zhang, J., & Shao, C. (2016) · Oncotarget · doi:10.18632/oncotarget.9017 · Cited by 86
let-7 MicroRNAs Regulate Microglial Function and Suppress Glioma Growth through Toll-Like Receptor 7
Buonfiglioli, A., Efe, I. E., Guneykaya, D., Ivanov, A., Huang, Y., Orlowski, E., Krüger, C., Deisz, R. A., Markovic, D., Flüh, C., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.11.029 · Cited by 86
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Tang, X., Zhang, S., Fu, R., Zhang, L., Huang, K., Peng, H., Dai, L., & Chen, Q. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.01208 · Cited by 69
Matsuzaka, Y., Tanihata, J., Komaki, H., Ishiyama, A., Oya, Y., Rüegg, U., Takeda, S.-I., & Hashido, K. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167811 · Cited by 68
Motor neuron-derived microRNAs cause astrocyte dysfunction in amyotrophic lateral sclerosis
Hoye, M. L., Regan, M. R., Jensen, L. A., Lake, A. M., Reddy, L. V., Vidensky, S., Richard, J.-P., Maragakis, N. J., Rothstein, J. D., Dougherty, J. D., et al. (2018) · Brain · doi:10.1093/brain/awy182 · Cited by 63
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Properzi, F., Ferroni, E., Poleggi, A., & Vinci, R. (2015) · Swiss Medical Weekly · doi:10.4414/smw.2015.14204 · Cited by 62
Pang, T. Y., Short, A. K., Bredy, T. W., & Hannan, A. J. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.02.007 · Cited by 61
Fuller, O. K., Whitham, M., Mathivanan, S., & Febbraio, M. A. (2020) · Cells · doi:10.3390/cells9102182 · Cited by 60
Neckles, V. N., Morton, M. C., Holmberg, J. C., Sokolov, A. M., Nottoli, T., Liu, D., & Feliciano, D. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-39679-0 · Cited by 55
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de Candia, P., De Rosa, V., Casiraghi, M., & Matarese, G. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.708842 · Cited by 53
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Szatmári, T., Hargitai, R., Sáfrány, G., & Lumniczky, K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225527 · Cited by 52
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Fernandes, M., Lopes, I., Teixeira, J., Botelho, C., & Gomes, A. C. (2020) · Current Medicinal Chemistry · doi:10.2174/0929867326666190129142604 · Cited by 51
Baek, A. E., Krawczynska, N., Das Gupta, A., Dvoretskiy, S. V., You, S., Park, J., Deng, Y.-H., Sorrells, J. E., Smith, B. P., Ma, L., et al. (2021) · Endocrinology · doi:10.1210/endocr/bqab095 · Cited by 43
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Huber, J., Griffin, M. F., Longaker, M. T., & Quarto, N. (2022) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2020.0246 · Cited by 41
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Zhao, Y., Liu, L., Sun, R., Cui, G., Guo, S., Han, S., Li, Z., Bai, T., & Teng, L. (2022) · Asian Journal of Pharmaceutical Sciences · doi:10.1016/j.ajps.2021.12.001 · Cited by 39
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Palazzolo, S., Memeo, L., Hadla, M., Duzagac, F., Steffan, A., Perin, T., Canzonieri, V., Tuccinardi, T., Caligiuri, I., & Rizzolio, F. (2020) · Cancers · doi:10.3390/cancers12113165 · Cited by 34
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Gierlikowski, W., & Gierlikowska, B. (2022) · Cells · doi:10.3390/cells11091380 · Cited by 25
Oltra, M., Vidal-Gil, L., Maisto, R., Oltra, S. S., Romero, F. J., Sancho-Pelluz, J., & Barcia, J. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-54373-x · Cited by 24
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White, J. R., Dauros-Singorenko, P., Hong, J., Vanholsbeeck, F., Phillips, A., & Swift, S. (2020) · Medicine in Microecology · doi:10.1016/j.medmic.2020.100005 · Cited by 21
Ghosh, S., & Ghosh, S. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.878058 · Cited by 13
Isolation of Extracellular Vesicles Derived from Mesenchymal Stromal Cells by Ultracentrifugation
Ramirez-Bajo, M., Banon-Maneus, E., Rovira, J., Campistol, J. M., & Diekmann, F. (2020) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3860 · Cited by 10
Metadata
- Authors
- Mittelbrunn, M., Gutiérrez-Vázquez, C., Villarroya-Beltri, C., González, S., Sánchez-Cabo, F., González, M. Á., Bernad, A., & Sánchez-Madrid, F.
- Venue
- Nature Communications
- Published
- 2011-04-19
- Volume
- 2
- Issue
- 1
- Pages
- 282-282
- ISSN
- 2041-1723 (ISSN-L)
- OpenAlex
- W1974035668
- Cited by
- 1,769
- References
- 10
- FWCI
- 37.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- Licence
- creativecommons.org/licenses/by-nc-nd/3.0/ (tdm)
- creativecommons.org/licenses/by-nc-nd/3.0/ (vor)
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.
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Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.