The DOI matches its Crossref record; 11 of the 11 references it cites were found in a registry or an index.
Exosome-Mediated Transfer of miR-133b from Multipotent Mesenchymal Stromal Cells to Neural Cells Contributes to Neurite Outgrowth
Open accessAbstract
Multipotent mesenchymal stromal cells (MSCs) have potential therapeutic benefit for the treatment of neurological diseases and injury. MSCs interact with and alter brain parenchymal cells by direct cell-cell communication and/or by indirect secretion of factors and thereby promote functional recovery. In this study, we found that MSC treatment of rats subjected to middle cerebral artery occlusion (MCAo) significantly increased microRNA 133b (miR-133b) level in the ipsilateral hemisphere. In vitro, miR-133b levels in MSCs and in their exosomes increased after MSCs were exposed to ipsilateral ischemic tissue extracts from rats subjected to MCAo. miR-133b levels were also increased in primary cultured neurons and astrocytes treated with the exosome-enriched fractions released from these MSCs. Knockdown of miR-133b in MSCs confirmed that the increased miR-133b level in astrocytes is attributed to their transfer from MSCs. Further verification of this exosome-mediated intercellular communication was performed using a cel-miR-67 luciferase reporter system and an MSC-astrocyte coculture model. Cel-miR-67 in MSCs was transferred to astrocytes via exosomes between 50 and 100 nm in diameter. Our data suggest that the cel-miR-67 released from MSCs was primarily contained in exosomes. A gap junction intercellular communication inhibitor arrested the exosomal microRNA communication by inhibiting exosome release. Cultured neurons treated with exosome-enriched fractions from MSCs exposed to 72 hours post-MCAo brain extracts significantly increased the neurite branch number and total neurite length. This study provides the first demonstration that MSCs communicate with brain parenchymal cells and may regulate neurite outgrowth by transfer of miR-133b to neural cells via exosomes.
Overview
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
Verification
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714
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
Yang, M., Chen, J., Su, F., Yu, B., Su, F., Lin, L., Liu, Y., Huang, J.-D., & Song, E. (2011) · Molecular Cancer · doi:10.1186/1476-4598-10-117 · Cited by 693
Qu, Y., Franchi, L., Nunez, G., & Dubyak, G. R. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1913 · Cited by 563
Pakkenberg, B. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00151-1 · Cited by 485
MicroRNA‐21 protects neurons from ischemic death
Buller, B., Liu, X., Wang, X., Zhang, R. L., Zhang, L., Hozeska‐Solgot, A., Chopp, M., & Zhang, Z. G. (2010) · The FEBS Journal · doi:10.1111/j.1742-4658.2010.07818.x · Cited by 242
Self-citationLiu, Z., Li, Y., Zhang, X., Savant-Bhonsale, S., & Chopp, M. (2008) · Stroke · doi:10.1161/strokeaha.107.511659 · Cited by 115
Self-citationLiu, Z., Li, Y., Zhang, Z. G., Cui, X., Cui, Y., Lu, M., Savant-Bhonsale, S., & Chopp, M. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.8 · Cited by 111
Self-citationXin, H., Li, Y., Shen, L. H., Liu, X., Wang, X., Zhang, J., Pourabdollah-Nejad D, S., Zhang, C., Zhang, L., Jiang, H., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009027 · Cited by 101
Self-citationLiu, Z., Zhang, R. L., Li, Y., Cui, Y., & Chopp, M. (2009) · Stroke · doi:10.1161/strokeaha.109.547265 · Cited by 81
Self-citation
Cited by
Exosomes: biogenesis, biologic function and clinical potential
Zhang, Y., Liu, Y., Liu, H., & Tang, W. H. (2019) · Cell & Bioscience · doi:10.1186/s13578-019-0282-2 · Cited by 2,119
Self-citationExosomes: Vehicles of Intercellular Signaling, Biomarkers, and Vectors of Cell Therapy
Kourembanas, S. (2015) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021014-071641 · Cited by 761
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
Self-citationJohnsen, K. B., Gudbergsson, J. M., Skov, M. N., Pilgaard, L., Moos, T., & Duroux, M. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.04.005 · Cited by 704
MiRNA Biogenesis and Regulation of Diseases: An Overview
Vishnoi, A., & Rani, S. (2017) · Methods in Molecular Biology · doi:10.1007/978-1-4939-6524-3_1 · Cited by 689
Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth
Katakowski, M., Buller, B., Zheng, X., Lu, Y., Rogers, T., Osobamiro, O., Shu, W., Jiang, F., & Chopp, M. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.02.019 · Cited by 681
Self-citationLou, G., Song, X., Yang, F., Wu, S., Wang, J., Chen, Z., & Liu, Y. (2015) · Journal of Hematology & Oncology · doi:10.1186/s13045-015-0220-7 · Cited by 651
Exosomes and Exosome-Inspired Vesicles for Targeted Drug Delivery
Antimisiaris, S. G., Mourtas, S., & Marazioti, A. (2018) · doi:10.20944/preprints201810.0507.v1 · Cited by 605
Exosome Mediated Delivery of miR-124 Promotes Neurogenesis after Ischemia
Yang, J., Zhang, X., Chen, X., Wang, L., & Yang, G. (2017) · Molecular Therapy - Nucleic Acids · doi:10.1016/j.omtn.2017.04.010 · Cited by 547
Xin, H., Katakowski, M., Wang, F., Qian, J.-Y., Liu, X. S., Ali, M. M., Buller, B., Zhang, Z. G., & Chopp, M. (2017) · Stroke · doi:10.1161/strokeaha.116.015204 · Cited by 533
Self-citationMesenchymal‐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
Exosomes — beyond stem cells for restorative therapy in stroke and neurological injury
Zhang, Z. G., Buller, B., & Chopp, M. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-018-0126-4 · Cited by 503
Self-citationSchwann cell‐derived exosomes enhance axonal regeneration in the peripheral nervous system
Lopez‐Verrilli, M. A., Picou, F., & Court, F. A. (2013) · Glia · doi:10.1002/glia.22558 · Cited by 453
Exosome Biochemistry and Advanced Nanotechnology for Next‐Generation Theranostic Platforms
Yang, B., Chen, Y., & Shi, J. (2019) · Advanced Materials · doi:10.1002/adma.201802896 · Cited by 435
Guo, S., Perets, N., Betzer, O., Ben-Shaul, S., Sheinin, A., Michaelevski, I., Popovtzer, R., Offen, D., & Levenberg, S. (2019) · ACS Nano · doi:10.1021/acsnano.9b01892 · Cited by 424
Extracellular vesicles: novel promising delivery systems for therapy of brain diseases.
Rufino-Ramos, D., Albuquerque, P. R., Carmona, V., Perfeito, R., Nobre, R. J., & Pereira de Almeida, L. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.07.001 · Cited by 418
Cui, G., Wu, J., Mou, F., Xie, W., Wang, F., Wang, Q., Fang, J., Xu, Y., Dong, Y., Liu, J., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201700600r · Cited by 387
Huang, S., Ge, X., Yu, J., Han, Z., Yin, Z., Li, Y., Chen, F., Wang, H., Zhang, J., & Lei, P. (2018) · The FASEB Journal · doi:10.1096/fj.201700673r · Cited by 388
Self-citationPerets, N., Betzer, O., Shapira, R., Brenstein, S., Angel, A., Sadan, T., Ashery, U., Popovtzer, R., & Offen, D. (2019) · Nano Letters · doi:10.1021/acs.nanolett.8b04148 · Cited by 382
Yang, L., Han, B., Zhang, Z., Wang, S., Bai, Y., Zhang, Y., Tang, Y., Du, L., Xu, L., Wu, F., et al. (2020) · Circulation · doi:10.1161/circulationaha.120.045765 · Cited by 376
Self-citationChivet, M., Javalet, C., Laulagnier, K., Blot, B., Hemming, F. J., & Sadoul, R. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.24722 · Cited by 340
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 319
Sun, G., Li, G., Li, D., Huang, W., Zhang, R., Zhang, H., Duan, Y., & Wang, B. (2018) · Materials Science and Engineering C · doi:10.1016/j.msec.2018.04.006 · Cited by 314
Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020171 · Cited by 301
Dabrowska, S., Andrzejewska, A., Lukomska, B., & Janowski, M. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1571-8 · Cited by 298
Long, X., Yao, X., Jiang, Q., Yang, Y., He, X., Tian, W., Zhao, K., & Zhang, H. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01761-0 · Cited by 294
Cui, Y., Luan, J., Li, H., Zhou, X., & Han, J. (2016) · FEBS Letters · doi:10.1002/1873-3468.12024 · Cited by 292
Huang, J.-H., Yin, X.-M., Xu, Y., Xu, C.-C., Lin, X., Ye, F.-B., Cao, Y., & Lin, F.-Y. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5063 · Cited by 292
Xin, H., Wang, F., Li, Y., Lu, Q.-E., Cheung, W. L., Zhang, Y., Zhang, Z. G., & Chopp, M. (2017) · Cell Transplantation · doi:10.3727/096368916x693031 · Cited by 267
Self-citationTakahashi, K., Yan, I. K., Wood, J., Haga, H., & Patel, T. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0636 · Cited by 258
Liu, W.-Z., Ma, Z.-J., Li, J.-R., & Kang, X.-W. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02153-8 · Cited by 252
Host Matrix Modulation by Tumor Exosomes Promotes Motility and Invasiveness
Mu, W., Rana, S., & Zöller, M. (2013) · Neoplasia · doi:10.1593/neo.13786 · Cited by 248
de Godoy, M. A., Saraiva, L. M., de Carvalho, L. R. P., Vasconcelos-dos-Santos, A., Beiral, H. J. V., Ramos, A. B., Silva, L. R. D. P., Leal, R. B., Monteiro, V. H. S., Braga, C. V., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.807180 · Cited by 214
Increased Circulating Exosomal miRNA-223 Is Associated with Acute Ischemic Stroke
Chen, Y., Song, Y., Huang, J., Qu, M., Zhang, Y., Geng, J., Zhang, Z., Liu, J., & Yang, G.-Y. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00057 · Cited by 207
Self-citationPeng, H., Li, Y., Ji, W., Zhao, R., Lu, Z., Shen, J., Wu, Y., Wang, J., Hao, Q., Wang, J., et al. (2022) · ACS Nano · doi:10.1021/acsnano.1c08473 · Cited by 205
Self-citationXia, X., Wang, Y., Huang, Y., Zhang, H., Lu, H., & Zheng, J. C. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.101694 · Cited by 202
Monsel, A., Zhu, Y.-G., Gudapati, V., Lim, H., & Lee, J. W. (2016) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2016.1170804 · Cited by 200
Deng, Y., Chen, D., Gao, F., Lv, H., Zhang, G., Sun, X., Liu, L., Mo, D., Ma, N., Song, L., et al. (2019) · Journal of Biological Engineering · doi:10.1186/s13036-019-0193-0 · Cited by 179
miR-219 Cooperates with miR-338 in Myelination and Promotes Myelin Repair in the CNS
Wang, H., Moyano, A. L., Ma, Z., Deng, Y., Lin, Y., Zhao, C., Zhang, L., Jiang, M., He, X., Ma, Z., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.03.001 · Cited by 174
“We transfected primary rat OPCs with biotinylated miR-219 or cel-miR-67, a negative control, which has minimal sequence identity with miRNAs in mammals (Xin et al., 2012).”
Emerging potential of exosomes for treatment of traumatic brain injury
Xiong, Y., Mahmood, A., & Chopp, M. (2017) · Neural Regeneration Research · doi:10.4103/1673-5374.198966 · Cited by 165
Self-citationExosomes 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
Liang, Y., Iqbal, Z., Lu, J., Wang, J., Zhang, H., Chen, X., Duan, L., & Xia, J. (2023) · Molecular Therapy · doi:10.1016/j.ymthe.2022.10.008 · Cited by 162
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
Chen, J., & Chopp, M. (2018) · Stroke · doi:10.1161/strokeaha.117.018292 · Cited by 152
Self-citationMicroglia-derived extracellular vesicles in Alzheimer’s Disease: A double-edged sword
Trotta, T., Antonietta Panaro, M., Cianciulli, A., Mori, G., Di Benedetto, A., & Porro, C. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.12.020 · Cited by 126
Li, D., Huang, S., Yin, Z., Zhu, J., Ge, X., Han, Z., Tan, J., Zhang, S., Zhao, J., Chen, F., et al. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02825-1 · Cited by 121
Zhang, B., Yan, W., Zhu, Y., Yang, W., Le, W., Chen, B., Zhu, R., & Cheng, L. (2018) · Advanced Materials · doi:10.1002/adma.201705694 · Cited by 113
Chen, Y., Tian, Z., He, L., Liu, C., Wang, N., Rong, L., & Liu, B. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02282-0 · Cited by 106
Optimized Cholesterol-siRNA Chemistry Improves Productive Loading onto Extracellular Vesicles
Haraszti, R. A., Miller, R., Didiot, M.-C., Biscans, A., Alterman, J. F., Hassler, M. R., Roux, L., Echeverria, D., Sapp, E., DiFiglia, M., et al. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.05.024 · Cited by 107
Mendes-Pinheiro, B., Anjo, S. I., Manadas, B., Da Silva, J. D., Marote, A., Behie, L. A., Teixeira, F. G., & Salgado, A. J. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00294 · Cited by 103
Transplanting Mesenchymal Stem Cells for Treatment of Ischemic Stroke
Wang, F., Tang, H., Zhu, J., & Zhang, J. H. (2018) · Cell Transplantation · doi:10.1177/0963689718795424 · Cited by 102
Biogenesis, Isolation, and Detection of Exosomes and Their Potential in Therapeutics and Diagnostics
Sonbhadra, S., Mehak, & Pandey, L. M. (2023) · Biosensors · doi:10.3390/bios13080802 · Cited by 97
Cell secretome: basic insights and therapeutic opportunities for CNS disorders
Pinho, A. G., Cibrão, J. R., Silva, N. A., Monteiro, S., & Salgado, A. J. (2020) · Pharmaceuticals · doi:10.3390/ph13020031 · Cited by 94
Chen, J.-J., Zhao, B., Zhao, J., & Li, S. (2017) · Neural Plasticity · doi:10.1155/2017/7027380 · Cited by 93
Different sourced extracellular vesicles and their potential applications in clinical treatments
Bahmani, L., & Ullah, M. (2022) · Cells · doi:10.3390/cells11131989 · Cited by 83
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
Venkat, P., Chen, J., & Chopp, M. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18782789 · Cited by 65
Self-citationStem cell therapy in Alzheimer’s disease: possible benefits and limiting drawbacks
Alipour, M., Nabavi, S. M., Arab, L., Vosough, M., Pakdaman, H., Ehsani, E., & Shahpasand, K. (2019) · Molecular Biology Reports · doi:10.1007/s11033-018-4499-7 · Cited by 63
Downregulation of exosomal miR-204-5p and miR-632 as a biomarker for FTD: a GENFI study
Schneider, R., McKeever, P., Kim, T., Graff, C., van Swieten, J. C., Karydas, A., Boxer, A., Rosen, H., Miller, B. L., Laforce Jr, R., et al. (2018) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp-2017-317492 · Cited by 62
Self-citationmiR-124: A Promising Therapeutic Target for Central Nervous System Injuries and Diseases
Xu, J., Zheng, Y., Wang, L., Liu, Y., Wang, X., Li, Y., & Chi, G. (2022) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-021-01091-6 · Cited by 55
Self-citationGhosh, S., Garg, S., & Ghosh, S. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00368 · Cited by 43
Segaran, R. C., Chan, L. Y., Wang, H., Sethi, G., & Tang, F. R. (2020) · Current Medicinal Chemistry · doi:10.2174/0929867327666200121122910 · Cited by 42
Genetic Engineering of Mesenchymal Stem Cells for Regenerative Medicine
Nowakowski, A., Walczak, P., Janowski, M., & Lukomska, B. (2015) · Stem Cells and Development · doi:10.1089/scd.2015.0062 · Cited by 38
Small Extracellular Vesicles’ miRNAs: Biomarkers and Therapeutics for Neurodegenerative Diseases
Lim, W. Q., Michelle Luk, K. H., Lee, K. Y., Nurul, N., Loh, S. J., Yeow, Z. X., Wong, Q. X., Daniel Looi, Q. H., Chong, P. P., How, C. W., et al. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15041216 · Cited by 25
Metadata
- Authors
- Xin, H., Li, Y., Buller, B., Katakowski, M., Zhang, Y., Wang, X., Shang, X., Zhang, Z. G., & Chopp, M.
- Venue
- Stem Cells
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-06-18
- Volume
- 30
- Issue
- 7
- Pages
- 1556-1564
- ISSN
- 1066-5099 (ISSN-L)
- 1549-4918
- OpenAlex
- W2058180357
- Cited by
- 895
- References
- 11
- FWCI
- 16.61
- Type
- journal article
- Language
- en
- Open access
- bronze
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
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.