Concise review: MSC-derived exosomes for cell-free therapy
Abstract
Mesenchymal stem cell transplantation is undergoing extensive evaluation as a cellular therapy in human clinical trials. Because MSCs are easily isolated and amenable to culture expansion in vitro there is a natural desire to test MSCs in many diverse clinical indications. This is exemplified by the rapidly expanding literature base that includes many in vivo animal models. More recently, MSC-derived extracellular vesicles (EVs), which include exosomes and microvesicles (MV), are being examined for their role in MSC-based cellular therapy. These vesicles are involved in cell-to-cell communication, cell signaling, and altering cell or tissue metabolism at short or long distances in the body. The exosomes and MVs can influence tissue responses to injury, infection, and disease. MSC-derived exosomes have a content that includes cytokines and growth factors, signaling lipids, mRNAs, and regulatory miRNAs. To the extent that MSC exosomes can be used for cell-free regenerative medicine, much will depend on the quality, reproducibility, and potency of their production, in the same manner that these parameters dictate the development of cell-based MSC therapies. However, the MSC exosome's contents are not static, but rather a product of the MSC tissue origin, its activities and the immediate intercellular neighbors of the MSCs. As such, the exosome content produced by MSCs appears to be altered when MSCs are cultured with tumor cells or in the in vivo tumor microenvironment. Therefore, careful attention to detail in producing MSC exosomes may provide a new therapeutic paradigm for cell-free MSC-based therapies with decreased risk. Stem Cells 2017;35:851-858.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
The anti-inflammatory potential of MSC-Exos relies on the effects of MSC-sourced bioactive molecules which efficiently modulated immune responses and promoted tissue repair and regeneration.
“The anti-inflammatory potential of MSC-Exos was shown to rely on the effects of MSC-sourced bioactive molecules (lipids, enzymes, cytokines, chemokines, immunoregulatory proteins, trophic and growth factors, and microRNAs) which efficiently modulated immune responses and promoted tissue repair and regeneration [78].”
Cites
Marrow Stromal Cells as Stem Cells for Nonhematopoietic Tissues
Prockop, D. J. (1997) · Science · doi:10.1126/science.276.5309.71 · Cited by 4,629 · see citing works
Human mesenchymal stem cells modulate allogeneic immune cell responses
Aggarwal, S., & Pittenger, M. F. (2005) · Blood · doi:10.1182/blood-2004-04-1559 · Cited by 4,511 · see citing works
Self-citationCommunication by Extracellular Vesicles: Where We Are and Where We Need to Go
Tkach, M., & Théry, C. (2016) · Cell · doi:10.1016/j.cell.2016.01.043 · Cited by 3,444 · see citing works
Mesenchymal stem cells as trophic mediators
Caplan, A. I., & Dennis, J. E. (2006) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20886 · Cited by 2,992 · see citing works
Lötvall, J. O., Hill, A. F., Hochberg, F. H., Buzás, E. I., Vizio, D. D., Gardiner, C., Gho, Y. S., Kurochkin, I. V., Mathivanan, S., Quesenberry, P. J., et al. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.26913 · Cited by 2,710 · see citing works
Bartholomew, A. M., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K. R., Patil, S., Hardy, W., Devine, S. M., Ucker, D. S., Deans, R., et al. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(01)00769-x · Cited by 2,296 · see citing works
Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury
Lai, R. C., Arslan, F., Lee, M. M., Sze, N. S. K., Choo, A., Chen, T. S., Salto-Tellez, M., Timmers, L., Lee, C. N., El Oakley, R. M., et al. (2010) · Stem Cell Research · doi:10.1016/j.scr.2009.12.003 · Cited by 2,215 · see citing works
Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues.
Friedenstein, A. J., Kv, P., KUROLESOVA, A. I., & Frolova, G. P. (1968) · PubMed · Cited by 1,921 · see citing works
HETEROTOPIC TRANSPLANTS OF BONE MARROW
Friedenstein, A. J., Kv, P., KUROLESOVA, A. I., & Frolova, G. P. (1968) · Transplantation · doi:10.1097/00007890-196803000-00009 · Cited by 1,703 · see citing works
Caplan, A. I., & Correa, D. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2011.06.008 · Cited by 1,682 · see citing works
Gnecchi, M., He, H., Liang, O. D., Melo, L. G., Morello, F., Mu, H., Noiseux, N., Zhang, L., Pratt, R. E., Ingwall, J. S., et al. (2005) · Nature Medicine · doi:10.1038/nm0405-367 · Cited by 1,677 · see citing works
Horwitz, E. M., Gordon, P. L., Koo, W. K. K., Marx, J. C., Neel, M. D., McNall, R. Y., Muul, L., & Hofmann, T. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132252399 · Cited by 1,650 · see citing works
Kopen, G. C., Prockop, D. J., & Phinney, D. G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.19.10711 · Cited by 1,643 · see citing works
Self-citationOrtiz, L. A., Gambelli, F., McBride, C., Gaupp, D., Baddoo, M., Kaminski, N., & Phinney, D. G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1432929100 · Cited by 1,448 · see citing works
Self-citationMesenchymal Stem Cells and Their Potential as Cardiac Therapeutics
Pittenger, M. F., & Martin, B. J. (2004) · Circulation Research · doi:10.1161/01.res.0000135902.99383.6f · Cited by 1,434 · see citing works
Self-citationMesenchymal Stem Cell-Derived Microvesicles Protect Against Acute Tubular Injury
Bruno, S., Grange, C., Deregibus, M. C., Calogero, R., Saviozzi, S., Collino, F., Morando, L., Busca, A., Falda, M., Bussolati, B., et al. (2009) · Journal of the American Society of Nephrology · doi:10.1681/asn.2008070798 · Cited by 1,332 · see citing works
Arslan, F., Lai, R. C., Smeets, M. B., Akeroyd, L., Choo, A. B. H., Aguor, E. N. E., Timmers, L., van Rijen, H. V. M., Doevendans, P. A., Pasterkamp, G., et al. (2013) · Stem Cell Research · doi:10.1016/j.scr.2013.01.002 · Cited by 1,108 · see citing works
Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs
Phinney, D. G., Di Giuseppe, M., Njah, J., Sala, E., Shiva, S., St Croix, C. M., Stolz, D. B., Watkins, S. C., Di, Y. P., Leikauf, G. D., et al. (2015) · Nature Communications · doi:10.1038/ncomms9472 · Cited by 1,007 · see citing works
Self-citationXin, H., Li, Y., Cui, Y., Yang, J. J., Zhang, Z. G., & Chopp, M. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.152 · Cited by 985 · see citing works
Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy
Lee, Y., Andaloussi, S. E., & Wood, M. J. A. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds317 · Cited by 936 · see citing works
Shake, J. G., Gruber, P. J., Baumgartner, W. A., Sénéchal, G., Meyers, J., Redmond, J. M., Pittenger, M. F., & Martin, B. J. (2002) · The Annals of Thoracic Surgery · doi:10.1016/s0003-4975(02)03517-8 · Cited by 901 · see citing works
Self-citationExtracellular vesicle isolation and characterization: toward clinical application
Xu, R., Greening, D. W., Zhu, H., Takahashi, N., & Simpson, R. J. (2016) · Journal of Clinical Investigation · doi:10.1172/jci81129 · Cited by 879 · see citing works
Exosomes Derived from Human Umbilical Cord Mesenchymal Stem Cells Alleviate Liver Fibrosis
Li, T., Yan, Y., Wang, B., Qian, H., Zhang, X., Shen, L., Wang, M., Zhou, Y., Zhu, W. Z., Li, W., et al. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0395 · Cited by 853 · see citing works
Bone Marrow–Derived Mesenchymal Stem Cells in Repair of the Injured Lung
Rojas, M., Xu, J., Woods, C. R., Mora, A. L., Spears, W., Roman, J., & Brigham, K. L. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2004-0330oc · Cited by 849 · see citing works
BM mesenchymal stromal cell–derived exosomes facilitate multiple myeloma progression
Roccaro, A. M., Sacco, A., Maiso, P., Azab, A. K., Tai, Y., Reagan, M. R., Azab, F., Flores, L. M., Campigotto, F., Weller, E. A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66517 · Cited by 794 · see citing works
Zhang, J., Guan, J., Niu, X., Hu, G., Guo, S., Li, Q., Xie, Z., Zhang, C., & Wang, Y. (2015) · Journal of Translational Medicine · doi:10.1186/s12967-015-0417-0 · Cited by 786 · see citing works
Lee, C., Mitsialis, S. A., Aslam, M., Vitali, S. H., Vergadi, E., Konstantinou, G., Sdrimas, K., Fernandez‐Gonzalez, A., & Kourembanas, S. (2012) · Circulation · doi:10.1161/circulationaha.112.114173 · Cited by 784 · see citing works
Doeppner, T. R., Herz, J., Görgens, A., Schlechter, J., Ludwig, A., Radtke, S., de Miroschedji, K., Horn, P. A., Giebel, B., & Hermann, D. M. (2015) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0078 · Cited by 773 · see citing works
Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth
Katakowski, M., Buller, B., Zheng, X., Lü, Y., Rogers, T., Osobamiro, O. O., Shu, W., Jiang, F., & Chopp, M. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.02.019 · Cited by 748 · see citing works
HucMSC‐Exosome Mediated‐Wnt4 Signaling Is Required for Cutaneous Wound Healing
Zhang, B., Wang, M., Gong, A.-H., Zhang, X., Wu, X., Zhu, Y.-H., Shi, H., Wu, L.-J., Zhu, W., Qian, H., et al. (2015) · Stem Cells · doi:10.1002/stem.1771 · Cited by 746 · see citing works
Zhang, Y., Chopp, M., Meng, Y., Katakowski, M., Xin, H., Mahmood, A., & Xiong, Y. (2015) · Journal of neurosurgery · doi:10.3171/2014.11.jns14770 · Cited by 737 · see citing works
Xin, H., Li, Y., Liu, Z., Wang, X., Shang, X., Cui, Y., Zhang, Z. G., & Chopp, M. (2013) · Stem Cells · doi:10.1002/stem.1409 · Cited by 724 · see citing works
Shabbir, A., Cox, A., Rodriguez-Menocal, L., Salgado, M., & Badiavas, E. V. (2015) · Stem Cells and Development · doi:10.1089/scd.2014.0316 · Cited by 721 · see citing works
Bian, S., Zhang, L., Duan, L., Wang, X., Min, Y., & Yu, H. (2013) · Journal of Molecular Medicine · doi:10.1007/s00109-013-1110-5 · Cited by 711 · see citing works
Mesenchymal Stem Cells Secrete Immunologically Active Exosomes
Zhang, B., Yin, Y., Lai, R. C., Tan, S. S., Choo, A. B. H., & Lim, S. K. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0479 · Cited by 698 · see citing works
Zhu, Y.-G., Feng, X.-M., Abbott, J., Fang, X.-H., Hao, Q., Monsel, A., Qu, J.-M., Matthay, M. A., & Lee, J. W. (2014) · Stem Cells · doi:10.1002/stem.1504 · Cited by 688 · see citing works
Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration
Zhang, S., Chu, W. C., Lai, R. C., Lim, S. K., Hui, J. H. P., & Toh, W. S. (2016) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2016.06.022 · Cited by 673 · see citing works
Ono, M., Kosaka, N., Tominaga, N., Yoshioka, Y., Takeshita, F., Takahashi, R.-U., Yoshida, M., Tsuda, H., Tamura, K., & Ochiya, T. (2014) · Science Signaling · doi:10.1126/scisignal.2005231 · Cited by 663 · see citing works
Zhou, Y., Xu, H., Xu, W., Wang, B., Wu, H., Tao, Y., Zhang, B., Wang, M., Mao, F., Yan, Y., et al. (2013) · Stem Cell Research & Therapy · doi:10.1186/scrt194 · Cited by 647 · see citing works
Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium.
Timmers, L., Lim, S. K., Arslan, F., Armstrong, J., Hoefer, I., Doevendans, P., Piek, J., Oakley, R. E., Choo, A., Lee, C. N., et al. (2008) · Stem Cell Research · doi:10.1016/j.scr.2008.02.002 · Cited by 622 · see citing works
Bruno, S., Grange, C., Collino, F., Deregibus, M. C., Cantaluppi, V., Biancone, L., Tetta, C., & Camussi, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033115 · Cited by 613 · see citing works
Dynamic Imaging of Allogeneic Mesenchymal Stem Cells Trafficking to Myocardial Infarction
Kraitchman, D. L., Tatsumi, M., Gilson, W. D., Ishimori, T., Kedziorek, D., Walczak, P., Segars, W. P., Chen, H. H., Fritzges, D., Izbudak, I., et al. (2005) · Circulation · doi:10.1161/circulationaha.105.537480 · Cited by 602 · see citing works
Self-citationFang, S., Xu, C., Zhang, Y., Xue, C., Yang, C., Bi, H., Qian, X., Wu, M., Ji, K., Zhao, Y., et al. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0367 · Cited by 579 · see citing works
Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes
Katsuda, T., Tsuchiya, R., Kosaka, N., Yoshioka, Y., Takagaki, K., Oki, K., Takeshita, F., Sakai, Y., Kuroda, M., & Ochiya, T. (2013) · Scientific Reports · doi:10.1038/srep01197 · Cited by 565 · see citing works
Tan, C. Y., Lai, R. C., Wong, W., Dan, Y. Y., Lim, S.-K., & Ho, H. K. (2014) · Stem Cell Research & Therapy · doi:10.1186/scrt465 · Cited by 548 · see citing works
Qi, X., Zhang, J., Yuan, H., Xu, Z., Li, Q., Niu, X., Hu, B., Wang, Y., & Li, X. (2016) · International Journal of Biological Sciences · doi:10.7150/ijbs.14809 · Cited by 541 · see citing works
Galipeau, J., Krampera, M., Barrett, J., Dazzi, F., Deans, R., de Bruijn, J. D., Dominici, M., Fibbe, W. E., Gee, A. P., Gimble, J. M., et al. (2015) · Cytotherapy · doi:10.1016/j.jcyt.2015.11.008 · Cited by 521 · see citing works
Self-citationLiang, X.-L., Zhang, L.-N., Wang, S.-H., Han, Q., & Zhao, R. (2016) · Journal of Cell Science · doi:10.1242/jcs.170373 · Cited by 521 · see citing works
Mesenchymal‐stem‐cell‐derived exosomes accelerate skeletal muscle regeneration
Nakamura, Y., Miyaki, S., Ishitobi, H., Matsuyama, S., Nakasa, T., Kamei, N., Akimoto, T., Higashi, Y., & Ochi, M. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.03.031 · Cited by 511 · see citing works
Bone Marrow Stromal Cells Attenuate Lung Injury in a Murine Model of Neonatal Chronic Lung Disease
Aslam, M., Baveja, R., Liang, O. D., Fernandez‐Gonzalez, A., Lee, C., Mitsialis, S. A., & Kourembanas, S. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200902-0242oc · Cited by 510 · see citing works
ALLOGENEIC MESENCHYMAL STEM CELLS REGENERATE BONE IN A CRITICAL-SIZED CANINE SEGMENTAL DEFECT
Arinzeh, T. L., Peter, S. J., Archambault, M., van den Bos, C., GORDON, S., Kraus, K. H., SMITH, A., & Kadiyala, S. (2003) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-200310000-00010 · Cited by 503 · see citing works
Feng, Y., Huang, W. C., Mashhood, W., Yu, X., & Ashraf, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088685 · Cited by 476 · see citing works
Paggetti, J., Haderk, F., Seiffert, M., Janji, B., Distler, U., Ammerlaan, W., Kim, Y. J., Adam, J., Lichter, P., Solary, É., et al. (2015) · Blood · doi:10.1182/blood-2014-12-618025 · Cited by 475 · see citing works
Yu, B., Kim, H. W., Gong, M., Wang, J., Millard, R. W., Wang, Y., Ashraf, M., & Xu, M. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.12.043 · Cited by 473 · see citing works
Teng, X.-M., Chen, L., Chen, W., Yang, J., Yang, Z., & Shen, Z. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000438594 · Cited by 470 · see citing works
Therapeutic Effects of Human Mesenchymal Stem Cell–derived Microvesicles in Severe Pneumonia in Mice
Monsel, A., Zhu, Y., Gennai, S., Qi, H., Hu, S., Rouby, J., Rosenzwajg, M., Matthay, M. A., & Lee, J. W. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201410-1765oc · Cited by 458 · see citing works
Mesenchymal Stem Cell-Derived Exosomes Promote Fracture Healing in a Mouse Model
Furuta, T., Miyaki, S., Ishitobi, H., Ogura, T., Kato, Y., Kamei, N., Miyado, K., Higashi, Y., & Ochi, M. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0285 · Cited by 444 · see citing works
Kim, D.-K., Nishida, H., An, S. Y., Shetty, A. K., Bartosh, T. J., & Prockop, D. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1522297113 · Cited by 434 · see citing works
Zhang, B., Wu, X., Zhang, X., Sun, Y., Yan, Y.-M., Shi, H., Zhu, Y.-H., Wu, L.-J., Pan, Z.-J., Zhu, W., et al. (2015) · Stem Cells Translational Medicine · doi:10.5966/sctm.2014-0267 · Cited by 433 · see citing works
Cyrne, L., Guerreiro, P., Cardoso, A. C., Rodrigues‐Pousada, C., & Soares, H. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00240-2 · Cited by 432 · see citing works
Normal and Leukemic Stem Cell Niches: Insights and Therapeutic Opportunities
Schepers, K., Campbell, T., & Passegué, E. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.02.014 · Cited by 416 · see citing works
Hu, G., Li, Q., Niu, X., Hu, B., Liu, J., Zhou, S.-M., Guo, S., Lang, H., Zhang, C., Wang, Y., et al. (2015) · Stem Cell Research & Therapy · doi:10.1186/scrt546 · Cited by 394 · see citing works
Blázquez, R., Sanchez-Margallo, F. M., de la Rosa, O., Dalemans, W., Álvarez, V., Tarazona, R., & Casado, J. G. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00556 · Cited by 377 · see citing works
François, S., Bensidhoum, M., Mouiseddine, M., Mazurier, C., Allenet, B., Sémont, A., Frick, J., Saché, A., Bouchet, S., Thierry, D., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0260 · Cited by 377 · see citing works
Fate Of Culture-Expanded Mesenchymal Stem Cells in The Microvasculature
Toma, C., Wagner, W. R., Bowry, S., Schwartz, A., & Villanueva, F. S. (2008) · Circulation Research · doi:10.1161/circresaha.108.187724 · Cited by 366 · see citing works
Tomasoni, S., Longaretti, L., Rota, C., Morigi, M., Conti, S., Gotti, E., Capelli, C., Introna, M., Remuzzi, G., & Benigni, A. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0266 · Cited by 340 · see citing works
Wang, X., Gu, H., Qin, D., Yang, L., Huang, W. C., Essandoh, K., Wang, Y., Caldwell, C. C., Peng, T., Zingarelli, B., et al. (2015) · Scientific Reports · doi:10.1038/srep13721 · Cited by 337 · see citing works
Exosomes Derived from Mesenchymal Stromal Cells Promote Axonal Growth of Cortical Neurons
Zhang, Y., Chopp, M., Liu, X., Katakowski, M., Wang, X., Tian, X., Wu, D., & Zhang, Z. G. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9851-0 · Cited by 302 · see citing works
Regulation of hematopoietic stem cells by bone marrow stromal cells
Anthony, B. A., & Link, D. C. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.10.002 · Cited by 301 · see citing works
Ophelders, D. R. M. G., Wolfs, T. G. A. M., Jellema, R. K., Zwanenburg, A., Andriessen, P., Delhaas, T., Ludwig, A., Radtke, S., Peters, V. B. M., Janssen, L. E. W., et al. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0197 · Cited by 278 · see citing works
Reis, L. A., Borges, F. T., Simões, M. D. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044092 · Cited by 277 · see citing works
Yang, J., Liu, X., Fan, H., Tang, Q., Shou, Z., Zuo, D.-M., Zou, Z., Xu, M., Chen, Q.-Y., Peng, Y., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140551 · Cited by 277 · see citing works
Tremain, N., Körkkö, J., Ibberson, D., Kopen, G. C., DiGirolamo, C. M., & Phinney, D. G. (2001) · Stem Cells · doi:10.1634/stemcells.19-5-408 · Cited by 271 · see citing works
Self-citationStem Cell-Derived Extracellular Vesicles and Immune-Modulation
Burrello, J., Monticone, S., Gai, C., Gomez, Y., Kholia, S., & Camussi, G. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00083 · Cited by 266 · see citing works
Exosomes induce and reverse monocrotaline-induced pulmonary hypertension in mice
Aliotta, J. M., Pereira, M. G., Wen, S., et al. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw054 · Cited by 249 · see citing works
Wen, S., Dooner, M. S., Cheng, Y., Papa, E. F., Tatto, M. D., Pereira, M. G., Deng, Y., Goldberg, L. R., Aliotta, J. M., Chatterjee, D., et al. (2016) · Leukemia · doi:10.1038/leu.2016.107 · Cited by 217 · see citing works
Mesenchymal stem cell-derived exosomes from different sources selectively promote neuritic outgrowth
Lopez‐Verrilli, M. A., Caviedes, A., Cabrera, A. J. H., Sandoval, S., Wyneken, Ú., & Khoury, M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.061 · Cited by 208 · see citing works
van Koppen, A., Joles, J. A., van Balkom, B. W. M., Lim, S. K., de Kleijn, D. P. V., Giles, R. H., & Verhaar, M. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038746 · Cited by 204 · see citing works
Al-Khaldi, A., Al-Sabti, H. A., Galipeau, J., & Lachapelle, K. J. (2003) · The Annals of Thoracic Surgery · doi:10.1016/s0003-4975(02)04291-1 · Cited by 203 · see citing works
Bonafede, R., Scambi, I., Peroni, D., Potrich, V., Boschi, F., Benati, D., Bonetti, B., & Mariotti, R. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.12.009 · Cited by 198 · see citing works
Fattore, A. D., Luciano, R., Saracino, R., Battafarano, G., Rizzo, C., Pascucci, L., Alessandri, G., Pessina, A., Perrotta, A., Fierabracci, A., et al. (2014) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2015.997706 · Cited by 185 · see citing works
OSTEOGENIC PRECURSOR CELLS OF BONE MARROW IN RADIATION CHIMERAS
Friedenstein, A. J., & Kuralesova, A. I. (1971) · Transplantation · doi:10.1097/00007890-197108000-00001 · Cited by 168 · see citing works
Unraveling the Mesenchymal Stromal Cells' Paracrine Immunomodulatory Effects
Fontaine, M. J., Shih, H., Schäfer, R., & Pittenger, M. F. (2016) · Transfusion Medicine Reviews · doi:10.1016/j.tmrv.2015.11.004 · Cited by 162 · see citing works
Self-citationGennai, S., Monsel, A., Hao, Q., Park, J. J., Matthay, M. A., & Lee, J. W. (2015) · American Journal of Transplantation · doi:10.1111/ajt.13271 · Cited by 155 · see citing works
Complex N-Linked Glycans Serve as a Determinant for Exosome/Microvesicle Cargo Recruitment
Liang, Y., Eng, W. S., Colquhoun, D. R., Dinglasan, R. R., Graham, D. R. M., & Mahal, L. K. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.606269 · Cited by 154 · see citing works
Goolaerts, A., Randrianarison, N., Larghero, J., Vanneaux, V., Uzunhan, Y., Gille, T., Dard, N., Planès, C., Matthay, M. A., & Clérici, C. (2014) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00242.2013 · Cited by 149 · see citing works
Nonunions and the Potential of Stem Cells in Fracture-Healing
Tseng, S., Lee, M. A., & Reddi, A. H. (2008) · Journal of Bone and Joint Surgery · doi:10.2106/jbjs.g.01192 · Cited by 144 · see citing works
Rager, T. M., Olson, J. K., Zhou, Y., et al. (2016) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2016.02.061 · Cited by 143 · see citing works
Veirman, K. D., Wang, J., Xu, S., Leleu, X. P., Himpe, E., Maes, K., Bruyne, E. D., Valckenborgh, E. V., Vanderkerken, K., Menu, E., et al. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.04.024 · Cited by 138 · see citing works
Amarnath, S., Foley, J., Farthing, D. E., Gress, R. E., Laurence, A. D. J., Eckhaus, M., Métais, J., Rose, J. J., Hakim, F. T., Felizardo, T. C., et al. (2014) · Stem Cells · doi:10.1002/stem.1934 · Cited by 117 · see citing works
Quantifying levels of transplanted murine and human mesenchymal stem cells in vivo by realtime PCR
McBride, C., Gaupp, D., & Phinney, D. G. (2003) · Cytotherapy · doi:10.1080/14653240310000038 · Cited by 114 · see citing works
Self-citationMobilization and homing of bone marrow stromal cells in myocardial infarction
Bittira, B. (2003) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/s1010-7940(03)00325-7 · Cited by 109 · see citing works
Choi, M., Ban, T., & Rhim, T. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.2317 · Cited by 103 · see citing works
Corrado, C., Saieva, L., Raimondo, S., Santoro, A., Leo, G. D., & Alessandro, R. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12873 · Cited by 103 · see citing works
Exosomes: mediators of communication in eukaryotes
Lopez‐Verrilli, M. A., & Court, F. A. (2013) · Biological Research · doi:10.4067/s0716-97602013000100001 · Cited by 98 · see citing works
Phinney, D. G., Hill, K., Michelson, C. A., Dutreil, M. F., Hughes, C., Humphries, S., Wilkinson, R., Baddoo, M., & Bayly, E. E. (2005) · Stem Cells · doi:10.1634/stemcells.2004-0236 · Cited by 96 · see citing works
Self-citationViola, S. A., Traer, E. A., Huan, J., Hornick, N. I., Tyner, J. W., Agarwal, A., Loriaux, M., Johnstone, B., & Kurre, P. (2015) · British Journal of Haematology · doi:10.1111/bjh.13551 · Cited by 92 · see citing works
Muntión, S., Ramos, T. L., Díez‐Campelo, M., Rosón, B., Sánchez‐Abarca, L. I., Misiewicz-Krzemińska, I., Preciado, S., Sarasquete, M. E., Rivas, J. D. L., González, M., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146722 · Cited by 91 · see citing works
Iglesias, D. M., El-Kares, R., Taranta, A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042840 · Cited by 79 · see citing works
Ren, J., Jin, P., Sabatino, M., Balakumaran, A., Feng, J., Kuznetsov, S. A., Klein, H. G., Robey, P. G., & Stroncek, D. F. (2011) · Cytotherapy · doi:10.3109/14653249.2010.548379 · Cited by 72 · see citing works
Tharin, S. A., Hamel, P. A., Conway, E. M., Michalak, M., & Opas, M. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199603)166:3 · Cited by 24 · see citing works
Collins (1998) · doi:10.1002/(sici)1097-4652(199807)176:1
Flagged first, then by citations
Cited by
Sorted by citations
Mesenchymal stem cell perspective: cell biology to clinical progress
Pittenger, M. F., Discher, D. E., Péault, B. M., Phinney, D. G., Hare, J. M., & Caplan, A. I. (2019) · npj Regenerative Medicine · doi:10.1038/s41536-019-0083-6 · Cited by 2,008 · see citing works
Self-citationZhao, H., Shang, Q., Pan, Z., Bai, Y., Li, Z., Zhang, H., Zhang, Q., Guo, C., Zhang, L., & Wang, Q. (2018) · Diabetes · doi:10.2337/db17-0356 · Cited by 657 · see citing works
Mesenchymal stem/stromal cells in cancer therapy
Lan, T., Luo, M., & Wei, X. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01208-w · Cited by 374 · see citing works
Zhang, W., Bai, X., Zhao, B., Li, Y., Zhang, Y., Li, Z., Wang, X., Luo, L., Han, F., Zhang, J., et al. (2018) · Experimental Cell Research · doi:10.1016/j.yexcr.2018.06.035 · Cited by 361 · see citing works
Paracrine Mechanisms of Mesenchymal Stromal Cells in Angiogenesis
Maacha, S., Sidahmed, H., Jacob, S., Gentilcore, G., Calzone, R., Grivel, J.-C., & Cugno, C. (2020) · Stem Cells International · doi:10.1155/2020/4356359 · Cited by 259 · see citing works
Reza-Zaldivar, E. E., Hernández-Sapiéns, M. A., Gutiérrez-Mercado, Y. K., Sandoval-Ávila, S., Gomez-Pinedo, U., Márquez-Aguirre, A. L., Vázquez-Méndez, E., Padilla-Camberos, E., & Canales-Aguirre, A. A. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.255978 · Cited by 256 · see citing works
Kang, Y., Xu, C., Meng, L., Dong, X., Qi, M., & Jiang, D. (2022) · Bioactive materials · doi:10.1016/j.bioactmat.2022.02.012 · Cited by 253 · see citing works
Immunomodulatory properties of mesenchymal stromal cells: an update
Müller, L., Tunger, A., Wobus, M., von Bonin, M., Towers, R., Bornhäuser, M., Dazzi, F., Wehner, R., & Schmitz, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.637725 · Cited by 205 · see citing works
Liu, Q., Li, D., Pan, X., & Liang, Y. (2023) · Journal of Nanobiotechnology · doi:10.1186/s12951-023-02081-0 · Cited by 201 · see citing works
Chen, Y.-A., Lu, C.-H., Ke, C.-C., Chiu, S.-J., Jeng, F.-S., Chang, C.-W., Yang, B.-H., & Liu, R.-S. (2021) · Biomedicines · doi:10.3390/biomedicines9060594 · Cited by 167 · see citing works
Galland, S., & Stamenkovic, I. (2020) · The Journal of Pathology · doi:10.1002/path.5357 · Cited by 165 · see citing works
Mesenchymal Stromal Cell Therapies for Neurodegenerative Diseases
Staff, N. P., Jones, D. T., & Singer, W. (2019) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2019.01.001 · Cited by 150 · see citing works
Bastos, R., Mathias, M., Andrade, R., Amaral, R. J. F. C., Schott, V., Balduino, A., Bastos, R., Miguel Oliveira, J., Reis, R. L., Rodeo, S., et al. (2020) · Knee Surgery, Sports Traumatology, Arthroscopy · doi:10.1007/s00167-019-05732-8 · Cited by 117 · see citing works
Oligodendrocyte progenitor cells in Alzheimer's disease: from physiology to pathology
Zou, P., Wu, C., Liu, T. C.-Y., Duan, R., & Yang, L. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00385-7 · Cited by 97 · see citing works
Bari, E., Ferrarotti, I., Di Silvestre, D., Grisoli, P., Barzon, V., Balderacchi, A., Torre, M. L., Rossi, R., Mauri, P., Corsico, A. G., et al. (2019) · Cells · doi:10.3390/cells8090965 · Cited by 70 · see citing works
Stroncek, D. F., Jin, P., McKenna, D. H., Takanashi, M., Fontaine, M. J., Pati, S., Schäfer, R., Peterson, E., Benedetti, E., & Reems, J.-A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00458 · Cited by 59 · see citing works
Techniques for increasing the yield of stem cell-derived exosomes: What factors may be involved?
Feng, Z.-Y., Zhang, Q.-Y., Tan, J., & Xie, H.-Q. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-1997-2 · Cited by 40 · see citing works
Matrix-Bound Nanovesicles: The Effects of Isolation Method upon Yield, Purity, and Function
Quijano, L. M., Naranjo, J. D., El-Mossier, S. O., Turner, N. J., Pineda Molina, C., Bartolacci, J., Zhang, L., White, L., Li, H., & Badylak, S. F. (2020) · Tissue Engineering Part C: Methods · doi:10.1089/ten.tec.2020.0243 · Cited by 38 · see citing works
Production and quality testing of multipotent mesenchymal stromal cell therapeutics for clinical use
Bieback, K., Kuçi, S., & Schäfer, R. (2019) · Transfusion · doi:10.1111/trf.15252 · Cited by 24 · see citing works
Exosomes and Biomaterials: In Search of a New Therapeutic Strategy for Multiple Sclerosis
Ojeda-Hernández, D. D., Hernández-Sapiéns, M. A., Reza-Zaldívar, E. E., Canales-Aguirre, A., Matías-Guiu, J. A., Matías-Guiu, J., Mateos-Díaz, J. C., Gómez-Pinedo, U., & Sancho-Bielsa, F. (2022) · Life · doi:10.3390/life12091417 · Cited by 25 · see citing works
Su, G., Lei, X., Wang, Z., Xie, W., Wen, D., & Wu, Y. (2023) · Current Molecular Medicine · doi:10.2174/1566524022666220511123625 · Cited by 10 · see citing works
- Authors
- Phinney, D. G., & Pittenger, M. F.
- Affiliations
- Scripps Research Institute (US)
- b Longevity Therapeutics, Inc, La Jolla, California, USA
- Corresponding author
- Phinney, Donald G.
- Venue
- Stem Cells
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-03-10
- Volume
- 35
- Issue
- 4
- Pages
- 851-858
- ISSN
- 1066-5099 (ISSN-L)
- 1549-4918
- OpenAlex
- W2605484523
- Cited by
- 1,834
- References
- 102
- Citations by year
- 2026: 189 · 2025: 198 · 2024: 224 · 2023: 198 · 2022: 251 · 2021: 263 · 2020: 244 · 2019: 145 · 2018: 87 · 2017: 33 · 2012: 1
- FWCI
- 13.04
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Stem Cells (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
- Keywords
- mesenchymal stem cells, exosomes, extracellular vesicles, microvesicles, cell-free therapy, tumor microenvironment, cell-to-cell communication, microRNA, cytokines and growth factors
- MeSH terms
- Animals, Humans, Wound Healing, Paracrine Communication, Stem Cell Niche, Exosomes, Mesenchymal Stem Cells
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