Stem cell Derived Extracellular Vesicles to Alleviate ischemia-reperfusion Injury of Transplantable Organs. A Systematic Review

Blondeel, J; Gilbo, NICHOLAS; De Bondt, S; Monbaliu, D

doi:10.1007/s12015-023-10573-7

Article (Scientific journals)

Stem cell Derived Extracellular Vesicles to Alleviate ischemia-reperfusion Injury of Transplantable Organs. A Systematic Review

Blondeel, J; Gilbo, NICHOLAS; De Bondt, S et al.

2023 • In Stem Cell Reviews and Reports, 19 (7), p. 2225 - 2250

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10.1007/s12015-023-10573-7

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37548807

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Abstract :

[en] Background: The possible beneficial effects of stem cell-derived EV on ischemia-reperfusion injury (IRI) in organ transplantation have been frequently investigated; however, the source of EV, as well as the methods of isolation and administration vary widely. We conducted a systematic review to summarize current pre-clinical evidence on stem cell-derived EV therapy for IRI of transplantable organs. Methods: PubMed, Embase and Web of Science were searched from inception until August 19th, 2022, for studies on stem cell-derived EV therapy for IRI after heart, kidney, liver, pancreas, lung and intestine transplantation. The Systematic Review Center for Laboratory animal Experiments (SYRCLE) guidelines were followed to assess potential risk of bias. Results: The search yielded 4153 unique articles, of which 96 were retained. We identified 32 studies on cardiac IRI, 38 studies on renal IRI, 21 studies on liver IRI, four studies on lung IRI and one study on intestinal IRI. Most studies used rodent models of transient ischemic injury followed by in situ reperfusion. In all studies, EV therapy was associated with improved outcome albeit to a variable degree. EV-therapy reduced organ injury and improved function while displaying anti-inflammatory-, immunomodulatory- and pro-regenerative properties. Conclusion: A multitude of animal studies support the potential of stem cell-derived EV-therapy to alleviate IRI after solid organ transplantation but suffer from low reporting quality and wide methodological variability. Future studies should focus on determining optimal stem cell source, dosage, and timing of treatment, as well as long-term efficacy in transplant models. © 2023, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Disciplines :

Surgery

Author, co-author :

Blondeel, J; Department of Microbiology, Immunology and Transplantation, Laboratory of Abdominal Transplantation, KU Leuven, Leuven, Belgium, Department of Abdominal Transplant Surgery and Coordination, University Hospitals Leuven, Herestraat 49, Leuven, 3000, Belgium

Gilbo, NICHOLAS ; Université de Liège - ULiège > Département des sciences cliniques > Pathologie chirurgicale abdominale et endocrinienne ; Centre Hospitalier Universitaire de Liège - CHU > > Service de chirurgie abdo, sénologique, endocrine et de transplantation

De Bondt, S; Faculty of Medicine, KU Leuven, Leuven, Belgium

Monbaliu, D; Department of Microbiology, Immunology and Transplantation, Laboratory of Abdominal Transplantation, KU Leuven, Leuven, Belgium, Department of Abdominal Transplant Surgery and Coordination, University Hospitals Leuven, Herestraat 49, Leuven, 3000, Belgium

Language :

English

Title :

Stem cell Derived Extracellular Vesicles to Alleviate ischemia-reperfusion Injury of Transplantable Organs. A Systematic Review

Publication date :

2023

Journal title :

Stem Cell Reviews and Reports

ISSN :

2629-3269

eISSN :

2629-3277

Publisher :

Springer

Volume :

Issue :

Pages :

2225 - 2250

Peer reviewed :

Peer Reviewed verified by ORBi

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since 25 January 2024

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Bibliography

Lomero, M., et al. (2020). Donation after circulatory death today: An updated overview of the european landscape. Transplant International, 33(1), 76–88. 10.1111/tri.13506. DOI: 10.1111/tri.13506
M. S et al., ‘Outcome after heart transplantation from donation after circulatory-determined death donors’, Journal Of Heart And Lung Transplantation, vol. 36, no. 12, pp. 1311–1318, doi: https://doi.org/10.1016/J.HEALUN.2017.10.021.
Monbaliu, D., Pirenne, J., & Talbot, D. (2012). ‘Liver transplantation using Donation after Cardiac Death donors’, Journal of Hepatology, vol. 56, no. 2. Elsevier B.V., pp. 474–485, doi: https://doi.org/10.1016/j.jhep.2011.07.004.
Meurisse, N. (Nov. 2012). ‘Outcomes of liver transplantations using donations after circulatory death: A single-center experience’, in Transplantation Proceedings, pp. 2868–2873. doi: 10.1016/j.transproceed.2012.09.077.
Barreda Monteoliva, P., Redondo-Pachón, D., Miñambres García, E., & Rodrigo Calabia, E. (2022). ‘Kidney transplant outcome of expanded criteria donors after circulatory death’, Nefrologia, vol. 42, no. 2, pp. 135–144, Mar. doi: https://doi.org/10.1016/J.NEFROE.2021.01.005.
van Rijn, R. (Apr. 2021). ‘Hypothermic Machine Perfusion in Liver Transplantation — A Randomized Trial’, New England Journal of Medicine, vol. 384, no. 15, pp. 1391–1401, doi: 10.1056/nejmoa2031532.
Nasralla, D., et al. (May 2018). A randomized trial of normothermic preservation in liver transplantation. Nature, 557(7703), 50–56. 10.1038/s41586-018-0047-9.
Jochmans, I. (Nov. 2020). ‘Oxygenated versus standard cold perfusion preservation in kidney transplantation (COMPARE): a randomised, double-blind, paired, phase 3 trial’, Lancet, vol. 396, no. 10263, pp. 1653–1662, doi: 10.1016/S0140-6736(20)32411-9.
Langmuur, S. J. J., Amesz, J. H., Veen, K. M., Bogers, A. J. J. C., Manintveld, O. C., & Taverne, Y. J. H. J. (2022). ‘Normothermic Ex Situ Heart Perfusion With the Organ Care System for Cardiac Transplantation: A Meta-analysis’, Transplantation, vol. 106, no. 9, pp. 1745–1753, Sep. doi: https://doi.org/10.1097/TP.0000000000004167.
Mergental, H., et al. (Dec. 2020). Transplantation of discarded livers following viability testing with normothermic machine perfusion. Nature Communications, 11(1), 10.1038/s41467-020-16251-3.
Sasajima, H. (Nov. 2018). ‘Cytoprotective Effects of Mesenchymal Stem Cells During Liver Transplantation from Donors After Cardiac Death in Rats’, Transplant Proc, vol. 50, no. 9, pp. 2815–2820, doi: 10.1016/J.TRANSPROCEED.2018.02.180.
McAuley, D. F., et al. (May 2014). Clinical grade allogeneic human mesenchymal stem cells restore alveolar fluid clearance in human lungs rejected for transplantation. American Journal Of Physiology. Lung Cellular And Molecular Physiology, 306(9), 10.1152/AJPLUNG.00358.2013.
Sun, D., Yang, L., Zheng, W., Cao, H., Wu, L., & Song, H. (2021). Protective Effects of Bone Marrow Mesenchymal Stem cells (BMMSCS) combined with normothermic machine perfusion on liver grafts donated after circulatory death via reducing the ferroptosis of hepatocytes. Medical Science Monitor, 27, 10.12659/MSM.930258.
Thompson, E. R. (Apr. 2021). ‘Novel delivery of cellular therapy to reduce ischemia reperfusion injury in kidney transplantation’, Am J Transplant, vol. 21, no. 4, pp. 1402–1414, doi: 10.1111/AJT.16100.
Brasile, L., Henry, N., Orlando, G., & Stubenitsky, B. (2019). ‘Potentiating Renal Regeneration Using Mesenchymal Stem Cells’, Transplantation, vol. 103, no. 2, pp. 307–313, Feb. doi: https://doi.org/10.1097/TP.0000000000002455.
Rowart, P., et al. (2015). Mesenchymal stromal cell therapy in Ischemia/Reperfusion Injury. J Immunol Res, 2015, 10.1155/2015/602597.
Eggenhofer, E., Luk, F., Dahlke, M. H., & Hoogduijn, M. J. (2014). ‘The life and fate of mesenchymal stem cells’, Front Immunol, vol. 5, no. MAY, doi: https://doi.org/10.3389/FIMMU.2014.00148.
Laing, R. W., et al. (Jun. 2020). The delivery of Multipotent Adult Progenitor cells to extended Criteria human donor livers using Normothermic Machine Perfusion. Frontiers In Immunology, 11, 10.3389/FIMMU.2020.01226.
Mordant, P., et al. (Oct. 2016). Mesenchymal stem cell treatment is associated with decreased perfusate concentration of interleukin-8 during ex vivo perfusion of donor lungs after 18-hour preservation. Journal Of Heart And Lung Transplantation, 35(10), 1245–1254. 10.1016/J.HEALUN.2016.04.017.
Pool, M. (Jul. 2019). ‘Infusing Mesenchymal Stromal Cells into Porcine Kidneys during Normothermic Machine Perfusion: Intact MSCs Can Be Traced and Localised to Glomeruli’, Int J Mol Sci, vol. 20, no. 14, doi: https://doi.org/10.3390/IJMS20143607.
Nawaz, M. (2016). ‘Extracellular Vesicles: Evolving Factors in Stem Cell Biology’, Stem Cells International, vol. Hindawi Publishing Corporation, 2016. doi: https://doi.org/10.1155/2016/1073140.
van Niel, G., D’Angelo, G., & Raposo, G. (2018). Shedding light on the cell biology of extracellular vesicles. Nature Reviews Molecular Cell Biology, 19(01), 213–228. 10.1038/nrm.2017.125. no. 4Nature Publishing Group. DOI: 10.1038/nrm.2017.125
Colombo, M., Raposo, G., & Théry, C. (2014). Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annual Review Of Cell And Developmental Biology, 30, 255–289. 10.1146/ANNUREV-CELLBIO-101512-122326. DOI: 10.1146/ANNUREV-CELLBIO-101512-122326
lo Cicero, A., Stahl, P. D., & Raposo, G. (2015). ‘Extracellular vesicles shuffling intercellular messages: for good or for bad’, Curr Opin Cell Biol, vol. 35, pp. 69–77, Aug. doi: https://doi.org/10.1016/J.CEB.2015.04.013.
Martins, P. N., Del Turco, S., Gilbo, N., & ‘ORGAN THERAPEUTICS DURING EX-SITU DYNAMIC (2023). PRESERVATION. A LOOK INTO THE FUTURE’, European Journal of Transplantation, vol. 1, no. 1, pp. 63–78, Oct. doi: https://doi.org/10.57603/EJT-010.
Leenaars, M. (Jan. 2012). ‘A step-by-step guide to systematically identify all relevant animal studies’, Lab Anim, vol. 46, no. 1, pp. 24–31, doi: 10.1258/la.2011.011087.
Bramer, W. M., Giustini, D., de Jong, G. B., Holland, L., & Bekhuis, T. (Jul. 2016). De-duplication of database search results for systematic reviews in EndNote. Journal Of The Medical Library Association: Jmla, 104(3), 240–243. 10.3163/1536-5050.104.3.014.
Ouzzani, M., Hammady, H., Fedorowicz, Z., & Elmagarmid, A. (Dec. 2016). Rayyan-a web and mobile app for systematic reviews. Syst Rev, 5(1), 10.1186/S13643-016-0384-4.
Hooijmans, C. R., Rovers, M. M., de Vries, R. B. M., Leenaars, M., Ritskes-Hoitinga, M., & Langendam, M. W. (2014). ‘SYRCLE’s risk of bias tool for animal studies’, BMC Med Res Methodol, vol. 14, no. 1, Mar. doi: https://doi.org/10.1186/1471-2288-14-43.
Adamiak, M., et al. (Jan. 2018). Induced Pluripotent Stem cell (iPSC)-derived extracellular vesicles are safer and more effective for cardiac repair than iPSCs. Circ Res, 122(2), 296–309. 10.1161/CIRCRESAHA.117.311769.
Agarwal, U., et al. (Feb. 2017). Experimental, systems, and computational approaches to understanding the MicroRNA-mediated reparative potential of cardiac progenitor cell-derived exosomes from pediatric patients. Circ Res, 120(4), 701–712. 10.1161/CIRCRESAHA.116.309935.
Arslan, F., et al. (May 2013). Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res, 10(3), 301–312. 10.1016/j.scr.2013.01.002.
Barile, L. (Jun. 2018). ‘Cardioprotection by cardiac progenitor cell-secreted exosomes: Role of pregnancy-associated plasma protein-A’, Cardiovasc Res, vol. 114, no. 7, pp. 992–1005, doi: https://doi.org/10.1093/cvr/cvy055.
Chai, H. T. (2019). ‘Early administration of cold water and adipose derived mesenchymal stem cell derived exosome effectively protects the heart from ischemia-reperfusion injury’, [Online]. Available: www.ajtr.org.
Chen, L., et al. (Feb. 2013). Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury. Biochemical And Biophysical Research Communications, 431(3), 566–571. 10.1016/j.bbrc.2013.01.015.
Chen, G., Wang, M., Ruan, Z., Zhu, L., & Tang, C. (Sep. 2021). Mesenchymal stem cell-derived exosomal mir-143-3p suppresses myocardial ischemia-reperfusion injury by regulating autophagy. Life Sciences, 280, 119742. 10.1016/J.LFS.2021.119742.
Cui, X., He, Z., Liang, Z., Chen, Z., Wang, H., & Zhang, J. (2017). ‘Exosomes from adipose-derived mesenchymal stem cells protect the myocardium against ischemia/Reperfusion Injury Through Wnt/b-Catenin Signaling Pathway’, [Online]. Available: www.jcvp.org.
De Couto, G. (Jul. 2017). ‘Exosomal MicroRNA Transfer into Macrophages Mediates Cellular Postconditioning’, Circulation, vol. 136, no. 2, pp. 200–214, doi: https://doi.org/10.1161/CIRCULATIONAHA.116.024590.
De Couto, G., et al. (Oct. 2019). Mechanism of enhanced MerTK-Dependent macrophage efferocytosis by extracellular vesicles. Arteriosclerosis, Thrombosis, And Vascular Biology, 39(10), 2082–2096. 10.1161/ATVBAHA.119.313115.
de Pedro, M. (May 2022). ‘Intrapericardial Administration of Secretomes from Menstrual Blood-Derived Mesenchymal Stromal Cells: Effects on Immune-Related Genes in a Porcine Model of Myocardial Infarction’, Biomedicines, vol. 10, no. 5, p. 1117, doi: https://doi.org/10.3390/BIOMEDICINES10051117/S1.
Du, W., Wang, X., Maimaitiyiming, D., Sai, Q., Zhao, G., & Tuerxun, G. (2021). Exosomes from adipose-derived mesenchymal stem cells alleviates rat myocardial Ischemia/Reperfusion Injury by inhibiting oxidative stress and inflammatory response. J Biomater Tissue Eng, 11(1), 38–43. 10.1166/jbt.2021.2533. DOI: 10.1166/jbt.2021.2533
Gallet, R. (Jan. 2017). ‘Exosomes secreted by cardiosphere-derived cells reduce scarring, attenuate adverse remodelling, and improve function in acute and chronic porcine myocardial infarction’, Eur Heart J, vol. 38, no. 3, pp. 201–211, doi: 10.1093/eurheartj/ehw240.
Gray, W. D. (Jan. 2015). ‘Identification of therapeutic covariant microRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology’, Circ Res, vol. 116, no. 2, pp. 255–263, doi: 10.1161/CIRCRESAHA.116.304360.
Katsur, M., He, Z., Vinokur, V., Corteling, R., Yellon, D. M., & Davidson, S. M. (May 2021). Exosomes from neuronal stem cells may protect the heart from ischaemia/reperfusion injury via JAK1/2 and gp130. Journal Of Cellular And Molecular Medicine, 25(9), 4455. https://doi.org/10.1111/JCMM.16515.
Li, T., Gu, J., Yang, O., Wang, J., Wang, Y., & Kong, J. (2020). ‘Bone Marrow Mesenchymal Stem Cell-Derived Exosomal miRNA-29c Decreases Cardiac Ischemia/Reperfusion Injury Through Inhibition of Excessive Autophagy via the PTEN/Akt/mTOR Signaling Pathway’, Circulation Journal, vol. 84, no. 8, pp. 1304–1311, Jul. doi: https://doi.org/10.1253/CIRCJ.CJ-19-1060.
Liu, L., Jin, X., Hu, C. F., Li, R., Zhou, Z., & Shen, C. X. (2017). ‘Exosomes Derived from Mesenchymal Stem Cells Rescue Myocardial Ischaemia/Reperfusion Injury by Inducing Cardiomyocyte Autophagy Via AMPK and Akt Pathways’, Cellular Physiology and Biochemistry, vol. 43, no. 1, pp. 52–68, Oct. doi: https://doi.org/10.1159/000480317.
Luther, K. M., et al. (Jun. 2018). Exosomal miR-21a-5p mediates cardioprotection by mesenchymal stem cells. Journal Of Molecular And Cellular Cardiology, 119, 125–137. 10.1016/j.yjmcc.2018.04.012.
Mao, C., et al. (Feb. 2021). Extracellular vesicles from anoxia preconditioned mesenchymal stem cells alleviate myocardial ischemia/reperfusion injury. Aging (Albany NY), 13(4), 6156. 10.18632/AGING.202611.
Park, H., et al. (Aug. 2018). Extracellular vesicles derived from hypoxic human mesenchymal stem cells attenuate GSK3β expression via miRNA-26a in an ischemia-reperfusion injury model. Yonsei Medical Journal, 59(6), 736–745. 10.3349/ymj.2018.59.6.736.
Schena, G. J. (Dec. 2021). ‘Cortical bone stem cell-derived exosomes’ therapeutic effect on myocardial ischemia-reperfusion and cardiac remodeling’, Am J Physiol Heart Circ Physiol, vol. 231, no. 6, pp. H1–H16, doi: https://doi.org/10.1152/AJPHEART.00197.2021/ASSET/IMAGES/LARGE/AJPHEART.00197.2021_F008.JPEG.
Scott, S. R. (Mar. 2022). ‘Bone marrow- or adipose-mesenchymal stromal cell secretome preserves myocardial transcriptome profile and ameliorates cardiac damage following ex vivo cold storage’, J Mol Cell Cardiol, vol. 164, pp. 1–12, doi: 10.1016/J.YJMCC.2021.11.002.
Sun, X. H., Wang, X., Zhang, Y., & Hui, J. (May 2019). Exosomes of bone-marrow stromal cells inhibit cardiomyocyte apoptosis under ischemic and hypoxic conditions via mir-486-5p targeting the PTEN/PI3K/AKT signaling pathway. Thrombosis Research, 177, 23–32. 10.1016/j.thromres.2019.02.002.
Takov, K., et al. (May 2020). Small extracellular vesicles secreted from human amniotic fluid mesenchymal stromal cells possess cardioprotective and promigratory potential. Basic Research In Cardiology, 115(3), 10.1007/s00395-020-0785-3.
Vandergriff, A. (2018). ‘Targeting regenerative exosomes to myocardial infarction using cardiac homing peptide’, Theranostics, vol. 8, no. 7, pp. 1869–1878, doi: 10.7150/thno.20524.
Wang, M., et al. (Apr. 2022). Mesenchymal stem cell secretions improve donor heart function following ex vivo cold storage. Journal Of Thoracic And Cardiovascular Surgery, 163(4), e277–e292. 10.1016/J.JTCVS.2020.08.095.
Wang, X., et al. (Dec. 2021). Extruded mesenchymal stem cell nanovesicles are equally potent to natural extracellular vesicles in Cardiac Repair. Acs Applied Materials & Interfaces, 13(47), 55767–55779. https://doi.org/10.1021/ACSAMI.1C08044/ASSET/IMAGES/LARGE/AM1C08044_0008.JPEG.
Wang, X. (Dec. 2021). ‘Cardiac microvascular functions improved by MSC-derived exosomes attenuate cardiac fibrosis after ischemia–reperfusion via PDGFR-β modulation’, Int J Cardiol, vol. 344, pp. 13–24, doi: https://doi.org/10.1016/J.IJCARD.2021.09.017.
Wei, Z., et al. (Sep. 2019). miRNA-181a over-expression in mesenchymal stem cell-derived exosomes influenced inflammatory response after myocardial ischemia-reperfusion injury. Life Sciences, 232, 10.1016/j.lfs.2019.116632.
Yue, R., et al. (Dec. 2022). Mesenchymal stem cell-derived exosomal microRNA-182-5p alleviates myocardial ischemia/reperfusion injury by targeting GSDMD in mice. Cell Death Discov, 8(1), 10.1038/S41420-022-00909-6.
Zhang, L., et al. (Dec. 2021). Exosomal microRNA-98-5p from hypoxic bone marrow mesenchymal stem cells inhibits myocardial ischemia–reperfusion injury by reducing TLR4 and activating the PI3K/Akt signaling pathway. International Immunopharmacology, 101, 107592. 10.1016/J.INTIMP.2021.107592.
Zhao, J. (Jun. 2019). ‘Mesenchymal stromal cell-derived exosomes attenuate myocardial ischaemia-reperfusion injury through miR-182-regulated macrophage polarization’, Cardiovasc Res, vol. 115, no. 7, pp. 1205–1216, doi: https://doi.org/10.1093/cvr/cvz040.
Burger, D. (Aug. 2015). ‘Human Endothelial Colony-Forming Cells Protect against Acute Kidney Injury Role of Exosomes’, American Journal of Pathology, vol. 185, no. 8, pp. 2309–2323, doi: 10.1016/j.ajpath.2015.04.010.
Cantaluppi, V., et al. (Aug. 2012). Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney International, 82(4), 412–427. 10.1038/ki.2012.105.
Cao, H. (Apr. 2020). ‘In Vivo Tracking of Mesenchymal Stem Cell-Derived Extracellular Vesicles Improving Mitochondrial Function in Renal Ischemia-Reperfusion Injury’, ACS Nano, vol. 14, no. 4, pp. 4014–4026, doi: 10.1021/acsnano.9b08207.
Chen, W., Yan, Y., Song, C., Ding, Y., & Du, T. (2017). ‘Microvesicles derived from human Wharton’s Jelly mesenchymal stem cells ameliorate ischemia-reperfusion-induced renal fibrosis by releasing from G2/M cell cycle arrest’, Biochemical Journal, vol. 474, no. 24, pp. 4207–4218, Dec. doi: https://doi.org/10.1042/BCJ20170682.
Choi, H. Y., et al. (Feb. 2014). Microparticles from kidney-derived mesenchymal stem cells act as carriers of proangiogenic signals and contribute to recovery from acute kidney injury. PLoS One, 9(2), 10.1371/journal.pone.0087853.
Collino, F., et al. (2019). Adipose-derived mesenchymal stromal cells under hypoxia: Changes in extracellular vesicles secretion and improvement of renal recovery after ischemic injury. Cellular Physiology and Biochemistry, 52(6), 1463–1483. 10.33594/000000102. DOI: 10.33594/000000102
Collino, F. (Feb. 2020). ‘Extracellular Vesicles Derived from Induced Pluripotent Stem Cells Promote Renoprotection in Acute Kidney Injury Model’, Cells, vol. 9, no. 2, p. 453, doi: 10.3390/CELLS9020453.
Gao, Z., et al. (Dec. 2022). Hypoxic mesenchymal stem cell-derived extracellular vesicles ameliorate renal fibrosis after ischemia–reperfusion injure by restoring CPT1A mediated fatty acid oxidation. Stem Cell Research & Therapy, 13(1), 10.1186/S13287-022-02861-9.
Gatti, S., et al. (May 2011). Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrology Dialysis Transplantation, 26(5), 1474–1483. 10.1093/ndt/gfr015.
Gu, D., Zou, X., Ju, G., Zhang, G., Bao, E., & Zhu, Y. (2016). ‘Mesenchymal Stromal Cells Derived Extracellular Vesicles Ameliorate Acute Renal Ischemia Reperfusion Injury by Inhibition of Mitochondrial Fission through miR-30.’, Stem Cells Int, vol. p. 2093940, 2016, doi: https://doi.org/10.1155/2016/2093940.
Huang, J., et al. (May 2022). Mesenchymal stem cells-derived Exosomes Ameliorate Ischemia/Reperfusion Induced Acute kidney Injury in a Porcine Model. Front Cell Dev Biol, 10, 1. 10.3389/FCELL.2022.899869.
Ju, G. Q., et al. (Mar. 2015). Microvesicles derived from human umbilical cord mesenchymal stem cells facilitate tubular epithelial cell dedifferentiation and growth via hepatocyte growth factor induction. PLoS One, 10(3), 10.1371/journal.pone.0121534.
Li, L., Wang, R., Jia, Y., Rong, R., Xu, M., & Zhu, T. (2019). ‘Exosomes Derived From Mesenchymal Stem Cells Ameliorate Renal Ischemic-Reperfusion Injury Through Inhibiting Inflammation and Cell Apoptosis’, Front Med (Lausanne), vol. 6, Nov. doi: https://doi.org/10.3389/fmed.2019.00269.
Li, X., et al. (2020). Human urine-derived stem cells protect against renal ischemia/reperfusion injury in a rat model via exosomal miR-146a-5p which targets IRAK1. Theranostics, 10(21), 9561. 10.7150/THNO.42153. DOI: 10.7150/THNO.42153
Lim, S. W., et al. (Mar. 2022). Alleviation of renal ischemia/reperfusion injury by exosomes from induced pluripotent stem cell-derived mesenchymal stem cells. Korean Journal Of Internal Medicine, 37(2), 411. 10.3904/KJIM.2020.438.
Lin, K. C., et al. (Aug. 2016). Combination of adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes for protecting kidney from acute ischemia-reperfusion injury. International Journal Of Cardiology, 216, 173–185. 10.1016/j.ijcard.2016.04.061.
Liu, Y., et al. (Apr. 2020). Enhanced therapeutic effects of MSC-derived extracellular vesicles with an injectable collagen matrix for experimental acute kidney injury treatment. Stem Cell Research & Therapy, 11(1), 10.1186/S13287-020-01668-W.
Lopes, J. A., et al. (Mar. 2022). Early Effects of Extracellular vesicles secreted by adipose tissue mesenchymal cells in renal ischemia followed by reperfusion: Mechanisms rely on a decrease in mitochondrial anion superoxide production. International Journal Of Molecular Sciences, 23(6), 2906. 10.3390/IJMS23062906/S1.
Ranghino, A., et al. (Feb. 2017). The effects of glomerular and tubular renal progenitors and derived extracellular vesicles on recovery from acute kidney injury. Stem Cell Research & Therapy, 8(1), 1–15. 10.1186/s13287-017-0478-5.
Shen, B. (2016). ‘CCR2 Positive Exosome Released by Mesenchymal Stem Cells Suppresses Macrophage Functions and Alleviates Ischemia/Reperfusion-Induced Renal Injury’, Stem Cells Int, vol. 2016, doi: https://doi.org/10.1155/2016/1240301.
Sun, Z., Gao, Z., Wu, J., Zheng, X., Jing, S., & Wang, W. (2022). ‘MSC-Derived Extracellular Vesicles Activate Mitophagy to Alleviate Renal Ischemia/Reperfusion Injury via the miR-223-3p/NLRP3 Axis’, Stem Cells Int, vol. 2022, doi: https://doi.org/10.1155/2022/6852661.
Sun, Z., Wu, J., Bi, Q., & Wang, W. (2022). ‘Exosomal lncRNA TUG1 derived from human urine-derived stem cells attenuates renal ischemia/reperfusion injury by interacting with SRSF1 to regulate ASCL4-mediated ferroptosis’, Stem Cell Res Ther, vol. 13, no. 1, p. 297, Dec. doi: https://doi.org/10.1186/S13287-022-02986-X.
Viñas, J. L., et al. (Dec. 2018). Receptor-ligand Interaction mediates targeting of endothelial colony forming cell-derived Exosomes to the kidney after ischemic Injury. Scientific Reports, 8(1), 10.1038/s41598-018-34557-7.
Viñas, J. L., et al. (2016). Transfer of microRNA-486-5p from human endothelial colony forming cell-derived exosomes reduces ischemic kidney injury. Kidney International, 90, 1238–1250. 10.1016/j.kint.2016.07.015. DOI: 10.1016/j.kint.2016.07.015
Wang, C., et al. (2019). BMSCs protect against renal ischemia-reperfusion injury by secreting exosomes loaded with miR-199a-5p that target BIP to inhibit endoplasmic reticulum stress at the very early reperfusion stages. FASEB Journal, 33(4), 5440–5456. 10.1096/fj.201801821R. DOI: 10.1096/fj.201801821R
Wu, X., et al. (Feb. 2018). Micro-vesicles derived from human Wharton’s jelly mesenchymal stromal cells mitigate renal ischemia-reperfusion injury in rats after cardiac death renal transplantation. Journal Of Cellular Biochemistry, 119(2), 1879–1888. 10.1002/jcb.26348.
Yu, L., et al. (Dec. 2021). Embryonic stem cell-derived extracellular vesicles promote the recovery of kidney injury. Stem Cell Research & Therapy, 12(1), 10.1186/S13287-021-02460-0.
Yuan, X. (Dec. 2017). ‘Extracellular vesicles from human-induced pluripotent stem cell-derived mesenchymal stromal cells (hiPSC-MSCs) protect against renal ischemia/reperfusion injury via delivering specificity protein (SP1) and transcriptional activating of sphingosine kinase 1 and inhibiting necroptosis’, Cell Death Dis, vol. 8, no. 12, doi: 10.1038/s41419-017-0041-4.
Zahran, R., Ghozy, A., Elkholy, S. S., El-Taweel, F., & El-Magd, M. A. (2020). ‘Combination therapy with melatonin, stem cells and extracellular vesicles is effective in limiting renal ischemia–reperfusion injury in a rat model’, International Journal of Urology, vol. 27, no. 11, pp. 1039–1049, Nov. doi: https://doi.org/10.1111/IJU.14345.
Zhang, G. (Mar. 2016). ‘Mesenchymal stromal cell-derived extracellular vesicles protect against acute kidney injury through anti-oxidation by enhancing Nrf2/ARE activation in rats’, Kidney Blood Press Res, vol. 41, no. 2, pp. 119–128, doi: 10.1159/000443413.
Zhang, Z. Y. (Jan. 2020). ‘Oct-4 enhanced the therapeutic effects of mesenchymal stem cell-derived extracellular vesicles in acute kidney injury’, Kidney Blood Press Res, vol. 45, no. 1, pp. 95–108, doi: 10.1159/000504368.
Zhang, G. (Mar. 2014). ‘The anti-oxidative role of micro-vesicles derived from human wharton-jelly mesenchymal stromal cells through NOX2/gp91(phox) suppression in alleviating renal ischemia-reperfusion injury in rats’, PLoS One, vol. 9, no. 3, doi: 10.1371/journal.pone.0092129.
Zhang, X. (Feb. 2022). ‘Extracellular vesicles from three dimensional culture of human placental mesenchymal stem cells ameliorated renal ischemia/reperfusion injury’, International Journal of Artificial Organs, vol. 45, no. 2, pp. 181–192, doi: 10.1177/0391398820986809.
Zhou, Y., et al. (Dec. 2019). Injectable extracellular vesicle-released self-assembling peptide nanofiber hydrogel as an enhanced cell-free therapy for tissue regeneration. Journal of Controlled Release, 316, 93–104. 10.1016/j.jconrel.2019.11.003.
Zhu, G. (Jun. 2019). ‘Exosomes from human-bone‐marrow‐derived mesenchymal stem cells protect against renal ischemia/reperfusion injury via transferring miR‐199a‐3p’, J Cell Physiol, doi: 10.1002/jcp.28941. DOI: 10.1002/jcp.28941
Zou, X. ‘Human mesenchymal stromal cell-derived extracellular vesicles alleviate renal ischemic reperfusion injury and enhance angiogenesis in rats.’, Am J Transl Res, vol. 8, no. 10, pp. 4289–4299, 2016, Accessed: Aug. 26, 2019. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/27830012.
Zou, X. (Mar. 2014). ‘Microvesicles derived from human Wharton’s Jelly mesenchymal stromal cells ameliorate renal ischemia-reperfusion injury in rats by suppressing CX3CL1’, Stem Cell Res Ther, vol. 5, no. 2, doi: 10.1186/scrt428.
Zou, X., et al. (Nov. 2016). NK cell regulatory property is involved in the protective role of MSC-derived extracellular vesicles in renal ischemic reperfusion injury. Human Gene Therapy, 27(11), 926–935. 10.1089/hum.2016.057.
Anger, F. (Nov. 2019). ‘Human Mesenchymal Stromal Cell-Derived Extracellular Vesicles Improve Liver Regeneration after Ischemia Reperfusion Injury in Mice’, Stem Cells Dev, vol. 28, no. 21, pp. 1451–1462, doi: 10.1089/scd.2019.0085.
De Stefano, N., et al. (Sep. 2021). Human liver stem cell-derived extracellular vesicles reduce injury in a model of normothermic machine perfusion of rat livers previously exposed to a prolonged warm ischemia. Transplant International, 34(9), 1607. 10.1111/TRI.13980.
Du, Y., et al. (2017). Exosomes from Human-Induced Pluripotent Stem cell–derived mesenchymal stromal cells (hiPSC-MSCs) protect liver against hepatic Ischemia/ reperfusion Injury via activating sphingosine kinase and sphingosine-1-Phosphate signaling pathway. Cellular Physiology and Biochemistry, 43(2), 611–625. 10.1159/000480533. DOI: 10.1159/000480533
Haga, H. (Jun. 2017). ‘Extracellular vesicles from bone marrow–derived mesenchymal stem cells protect against murine hepatic ischemia/reperfusion injury’, Liver Transplantation, vol. 23, no. 6, pp. 791–803, doi: 10.1002/lt.24770.
Jiao, Z., et al. (Dec. 2021). The adipose-derived mesenchymal stem cell secretome promotes hepatic regeneration in miniature pigs after liver ischaemia-reperfusion combined with partial resection. Stem Cell Research & Therapy, 12(1), 10.1186/S13287-021-02284-Y.
Khosravi-Farsani, S., Zaminy, A., Kazemi, S., & Hashemzadeh-Chaleshtori, M. (Jul. 2022). Mesenchymal stem cells versus their conditioned medium in the treatment of ischemia/reperfusion injury: Evaluation of efficacy and hepatic specific gene expression in mice. Iran J Basic Med Sci, 25(7), 799. 10.22038/IJBMS.2022.62642.13860.
Lee, S. C., Kim, J. O., & Kim, S. J. (May 2015). Secretome from human adipose-derived stem cells protects mouse liver from hepatic ischemia-reperfusion injury. Surgery (United States), 157(5), 934–943. 10.1016/j.surg.2014.12.016.
Lu, T. (May 2022). ‘Extracellular vesicles derived from mesenchymal stromal cells as nanotherapeutics for liver ischaemia–reperfusion injury by transferring mitochondria to modulate the formation of neutrophil extracellular traps’, Biomaterials, vol. 284, p. 121486, doi: 10.1016/J.BIOMATERIALS.2022.121486.
Nong, K. (Dec. 2016). ‘Hepatoprotective effect of exosomes from human-induced pluripotent stem cell–derived mesenchymal stromal cells against hepatic ischemia-reperfusion injury in rats’, Cytotherapy, vol. 18, no. 12, pp. 1548–1559, doi: 10.1016/j.jcyt.2016.08.002.
Rigo, F. (May 2018). ‘Extracellular Vesicles from Human Liver Stem Cells Reduce Injury in an Ex Vivo Normothermic Hypoxic Rat Liver Perfusion Model’, Transplantation, vol. 102, no. 5, pp. e205–e210, doi: 10.1097/TP.0000000000002123.
Sun, C. K. ‘Melatonin treatment enhances therapeutic effects of exosomes against acute liver ischemia-reperfusion injury’, 2017. [Online]. Available: www.ajtr.org.
Wei, X. (Oct. 2020). ‘Administration of glycyrrhetinic acid reinforces therapeutic effects of mesenchymal stem cell-derived exosome against acute liver ischemia‐reperfusion injury’, J Cell Mol Med, vol. 24, no. 19, p. 11211, doi: 10.1111/JCMM.15675.
Wu, L., et al. (Dec. 2022). Mir-124-3p delivered by exosomes from heme oxygenase-1 modified bone marrow mesenchymal stem cells inhibits ferroptosis to attenuate ischemia–reperfusion injury in steatotic grafts. J Nanobiotechnology, 20(1), 10.1186/S12951-022-01407-8.
Xie, K., Liu, L., Chen, J., & Liu, F. (Dec. 2019). Exosomal miR-1246 derived from human umbilical cord blood mesenchymal stem cells attenuates hepatic ischemia reperfusion injury by modulating T helper 17/regulatory T balance. Iubmb Life, 71(12), 2020–2030. 10.1002/iub.2147.
Xie, K., Liu, L., Chen, J., & Liu, F. (2019). ‘Exosomes derived from human umbilical cord blood mesenchymal stem cells improve hepatic ischemia reperfusion injury via delivering miR-1246’, Cell Cycle, vol. 18, no. 24, pp. 3491–3501, Dec. doi: https://doi.org/10.1080/15384101.2019.1689480.
Yang, B. (Mar. 2020). ‘Bone Marrow Mesenchymal Stem Cell-Derived Hepatocyte-Like Cell Exosomes Reduce Hepatic Ischemia/Reperfusion Injury by Enhancing Autophagy’, Stem Cells Dev, vol. 29, no. 6, pp. 372–379, doi: 10.1089/scd.2019.0194.
Yao, J., et al. (2019). Extracellular vesicles derived from human umbilical cord mesenchymal stem cells alleviate rat hepatic ischemia-reperfusion injury by suppressing oxidative stress and neutrophil inflammatory response. FASEB Journal, 33(2), 1695–1710. 10.1096/fj.201800131RR. DOI: 10.1096/fj.201800131RR
Zhang, L. (Apr. 2020). ‘MiR-20a-containing exosomes from umbilical cord mesenchymal stem cells alleviates liver ischemia/reperfusion injury’, J Cell Physiol, vol. 235, no. 4, pp. 3698–3710, doi: 10.1002/jcp.29264.
Zhang, Q., et al. (Nov. 2021). Exosomes from adipose-derived mesenchymal stem cells alleviate liver ischaemia reperfusion injury subsequent to hepatectomy in rats by regulating mitochondrial dynamics and biogenesis. Journal Of Cellular And Molecular Medicine, 25(21), 10152. 10.1111/JCMM.16952.
Zhang, Y., et al. (Feb. 2022). Attenuation of hepatic ischemia-reperfusion injury by adipose stem cell-derived exosome treatment via ERK1/2 and GSK-3β signaling pathways. International Journal Of Molecular Medicine, 49(2), 10.3892/IJMM.2021.5068.
Zheng, J. (Sep. 2020). ‘Extracellular Vesicles Derived from Human Umbilical Cord Mesenchymal Stem Cells Protect Liver Ischemia/Reperfusion Injury by Reducing CD154 Expression on CD4 + T Cells via CCT2’, Advanced Science, vol. 7, no. 18, doi: 10.1002/ADVS.201903746.
Gennai, S., Monsel, A., Hao, Q., Park, J., Matthay, M. A., & Lee, J. W. (2015). ‘Microvesicles Derived from Human Mesenchymal Stem Cells Restore Alveolar Fluid Clearance in Human Lungs Rejected for Transplantation’, American Journal of Transplantation, vol. 15, no. 9, pp. 2404–2412, Sep. doi: https://doi.org/10.1111/ajt.13271.
Li, J., Wei, L., Han, Z., & Chen, Z. (Jun. 2019). Mesenchymal stromal cells-derived exosomes alleviate ischemia/reperfusion injury in mouse lung by transporting anti-apoptotic miR-21-5p. European Journal Of Pharmacology, 852, 68–76. 10.1016/j.ejphar.2019.01.022.
Lonati, C. (Dec. 2019). ‘Mesenchymal stem cell–derived extracellular vesicles improve the molecular phenotype of isolated rat lungs during ischemia/reperfusion injury’, Journal of Heart and Lung Transplantation, vol. 38, no. 12, pp. 1306–1316, doi: 10.1016/j.healun.2019.08.016.
Stone, M. L., et al. (Dec. 2017). Mesenchymal stromal cell-derived extracellular vesicles attenuate lung ischemia-reperfusion injury and enhance reconditioning of donor lungs after circulatory death. Respiratory Research, 18(1), 10.1186/s12931-017-0704-9.
Zhang, G., Wan, Z., Liu, Z., Liu, D., Zhao, Z., & Leng, Y. (May 2022). Exosomes Derived from BMSCs ameliorate intestinal ischemia–reperfusion Injury by regulating mir-144-3p-Mediated oxidative stress. Digestive Diseases And Sciences, 1, 1–17. 10.1007/S10620-022-07546-0/FIGURES/8.
Camussi, G., Deregibus, M. C., & Cantaluppi, V. (2013). ‘Role of stem-cell-derived microvesicles in the paracrine action of stem cells’, in Biochemical Society Transactions, Feb. pp. 283–287. doi: https://doi.org/10.1042/BST20120192.
Quesenberry, P. J., Aliotta, J., Deregibus, M. C., & Camussi, G. (Dec. 2015). Role of extracellular RNA-carrying vesicles in cell differentiation and reprogramming. Stem Cell Research & Therapy, 6(1), 10.1186/s13287-015-0150-x.
Théry, C., et al. (Jan. 2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles, 7(1), 10.1080/20013078.2018.1535750.
Zhang, Q., et al. (Dec. 2021). Supermeres are functional extracellular nanoparticles replete with disease biomarkers and therapeutic targets. Nature Cell Biology, 23(12), 1240–1254. 10.1038/s41556-021-00805-8.
van Deun, J. (Feb. 2017). ‘EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research’, Nature Methods 2017 14:3, vol. 14, no. 3, pp. 228–232, doi: 10.1038/nmeth.4185.