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Current Molecular Medicine


ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Review Article

Molecular and Epigenetic Basis of Extracellular Vesicles Cell Repair Phenotypes in Targeted Organ-specific Regeneration

Author(s): Ismail Muhamad Fareez*, Wu Yuan Seng, Ramli Muhammad Zaki, Aazmi Shafiq and Ismail Mohamad Izwan

Volume 22, Issue 2, 2022

Published on: 10 February, 2021

Page: [132 - 150] Pages: 19

DOI: 10.2174/1566524021666210210121905

Price: $65


Extracellular vesicles (EVs), which are released by most of the cells, constitute a new system of cell-cell communication by transporting DNA, RNA, and proteins in various vesicles namely exosomes, apoptotic bodies, protein complexes, high-density lipid (HDL) microvesicles, among others. To ensure accurate regulation of somatic stem cell activity, EVs function as an independent metabolic unit mediating the metabolic homeostasis and pathophysiological of several diseases such as cardiovascular diseases, metabolic diseases, neurodegenerative diseases, immune diseases, and cancer. Whist examining the EV biomolecules cargos and their microenvironments that lead to epigenetic alteration of the cell in tissue regeneration, studies have gained further insights into the biogenesis of EVs and their potential roles in cell biology and pathogenicity. Due to their small size, non-virulence, flexibility, and ability to cross biological barriers, EVs have promising therapeutic potentials in various diseases. In this review, we describe EV’s mechanism of action in intercellular communication and transfer of biological information as well as some details about EVinduced epigenetic changes in recipient cells that cause phenotypic alteration during tissue regeneration. We also highlight some of the therapeutic potentials of EVs in organ-specific regeneration.

Keywords: Cell communication, cell signalling, cellular therapy, epigenetics, exosomes, extracellular vesicles, microvesicles, regenerative medicine

Meldolesi J. Exosomes and ectosomes in intercellular communication. Curr Biol 2018; 28(8): R435-44.
[] [PMID: 29689228]
Record M, Silvente-Poirot S, Poirot M, Wakelam MJO. Extracellular vesicles: lipids as key components of their biogenesis and functions. J Lipid Res 2018; 59(8): 1316-24.
[] [PMID: 29764923]
Koenen RR, Aikawa E. Editorial: Extracellular Vesicle-Mediated Processes in Cardiovascular Diseases. Front Cardiovasc Med 2018; 5(133): 133.
[] [PMID: 30283791]
Iavello A, Frech VS, Gai C, Deregibus MC, Quesenberry PJ, Camussi G. Role of Alix in miRNA packaging during extracellular vesicle biogenesis. Int J Mol Med 2016; 37(4): 958-66.
[] [PMID: 26935291]
Raposo G, Stahl PD. Extracellular vesicles: a new communication paradigm? Nat Rev Mol Cell Biol 2019; 20(9): 509-10.
[] [PMID: 31324871]
Arraud N, Linares R, Tan S, et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost 2014; 12(5): 614-27.
[] [PMID: 24618123]
Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9(8): 581-93.
[] [PMID: 19498381]
Bang C, Thum T. Exosomes: new players in cell-cell communication. Int J Biochem Cell Biol 2012; 44(11): 2060-4.
[] [PMID: 22903023]
Paolicelli RC, Bergamini G, Rajendran L. Cell-to-cell communication by extracellular vesicles: focus on microglia. Neuroscience 2019; 405(Special Issue): 148-57.
[] [PMID: 29660443]
Hosseini M, Roshangar L, Raeisi S, et al. The Therapeutic Applications of Exosomes in Different Types of Diseases: A Review. Curr Mol Med 2021; 21(2): 87-95.
[] [PMID: 32520687]
Collino F, Pomatto M, Bruno S, et al. Exosome and microvesicle-enriched fractions isolated from mesenchymal stem cells by gradient separation showed different molecular signatures and functions on renal tubular epithelial cells. Stem Cell Rev Rep 2017; 13(2): 226-43.
[] [PMID: 28070858]
Luo W, Dai Y, Chen Z, Yue X, Andrade-Powell KC, Chang J. Spatial and temporal tracking of cardiac exosomes in mouse using a nano-luciferase-CD63 fusion protein. Commun Biol 2020; 3(1): 114.
[] [PMID: 32157172]
Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol 2016; 36(3): 301-12.
[] [PMID: 27053351]
Yáñez-Mó M, Siljander PR-M, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015; 4(1): 27066.
[] [PMID: 25979354]
Armstrong JPK, Stevens MM. Strategic design of extracellular vesicle drug delivery systems. Adv Drug Deliv Rev 2018; 130: 12-6.
[] [PMID: 29959959]
Jansen F, Li Q, Pfeifer A, Werner N. Endothelial-and immune cell-derived extracellular vesicles in the regulation of cardiovascular health and disease. JACC Basic Transl Sci 2017; 2(6): 790-807.
[] [PMID: 30062186]
Gai C, Carpanetto A, Deregibus MC, Camussi G. Extracellular vesicle-mediated modulation of angiogenesis. Histol Histopathol 2016; 31(4): 379-91.
[PMID: 26662176]
Shi Y, Shi H, Nomi A, Lei-Lei Z, Zhang B, Qian H. Mesenchymal stem cell-derived extracellular vesicles: a new impetus of promoting angiogenesis in tissue regeneration. Cytotherapy 2019; 21(5): 497-508.
[] [PMID: 31079806]
Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluidsCurr Prot Cell Biol 2006; chapter 3: unit 322.
Gudbergsson JM, Johnsen KB, Skov MN, Duroux M. Systematic review of factors influencing extracellular vesicle yield from cell cultures. Cytotechnology 2016; 68(4): 579-92.
[] [PMID: 26433593]
Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78(9): 838-48.
[] [PMID: 20703216]
Lee Y, El Andaloussi S, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 2012; 21(R1): R125-34.
[] [PMID: 22872698]
Pluchino S, Smith JA. Explicating exosomes: reclassifying the rising stars of intercellular communication. Cell 2019; 177(2): 225-7.
[] [PMID: 30951665]
Chamberlain CS, Clements AEB, Kink JA, et al. Extracellular vesicle‐educated macrophages promote early Achilles tendon healing. Stem Cells 2019; 37(5): 652-62.
[] [PMID: 30720911]
Rödling L, Schwedhelm I, Kraus S, Bieback K, Hansmann J, Lee-Thedieck C. 3D models of the hematopoietic stem cell niche under steady-state and active conditions. Sci Rep 2017; 7(1): 4625.
[] [PMID: 28676663]
Datta Chaudhuri A, Dasgheyb RM, DeVine LR, Bi H, Cole RN, Haughey NJ. Stimulus-dependent modifications in astrocyte-derived extracellular vesicle cargo regulate neuronal excitability. Glia 2020; 68(1): 128-44.
[] [PMID: 31469478]
French KC, Antonyak MA, Cerione RA. Extracellular vesicle docking at the cellular port: Extracellular vesicle binding and uptake. Semin Cell Dev Biol 2017; 67: 48-55.
[] [PMID: 28104520]
Mulcahy LA, Pink RC, Carter DRF. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 2014; 3: 24641.
Cruz L, Romero JAA, Iglesia RP, Lopes MH. Extracellular vesicles: decoding a new language for cellular communication in early embryonic development. Front Cell Dev Biol 2018; 6(94): 94.
[] [PMID: 30211159]
Riazifar M, Pone EJ, Lötvall J, Zhao W. Stem cell extracellular vesicles: extended messages of regeneration. Annu Rev Pharmacol Toxicol 2017; 57: 125-54.
[] [PMID: 27814025]
Moyes CD, Schulte PM, Eds. Principles of Animal Physiology. 3rd ed. San Francisco, CA, USA: Benjamin Cummings 2005.
Bastida E, Ordinas A, Escolar G, Jamieson GA. Tissue factor in microvesicles shed from U87MG human glioblastoma cells induces coagulation, platelet aggregation, and thrombo-genesis. Blood 1984; 64(1): 177-84.
[] [PMID: 6733271]
Cossetti C, Iraci N, Mercer TR, et al. Extracellular vesicles from neural stem cells transfer IFN-γ via Ifngr1 to activate Stat1 signaling in target cells. Mol Cell 2014; 56(2): 193-204.
[] [PMID: 25242146]
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[] [PMID: 17486113]
Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2(180): 180.
[] [PMID: 21285958]
Dini L, Tacconi S, Carata E, Tata AM, Vergallo C, Panzarini E. Microvesicles and exosomes in metabolic diseases and inflammation. Cytokine Growth Factor Rev 2020; 51: 27-39.
[] [PMID: 31917095]
Müller G. Microvesicles/exosomes as potential novel biomarkers of metabolic diseases. Diabetes Metab Syndr Obes 2012; 5: 247-82.
[] [PMID: 22924003]
Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2010; 4(3): 214-22.
[] [PMID: 20138817]
Iraci N, Gaude E, Leonardi T, et al. Extracellular vesicles are independent metabolic units with asparaginase activity. Nat Chem Biol 2017; 13(9): 951-5.
[] [PMID: 28671681]
Whitham M, Parker BL, Friedrichsen M, Hingst JR, Hjorth M, Hughes WE, et al. Extracellular vesicles provide a means for tissue crosstalk during exercise. Cell Metab 2018; 27(1): 237-51.
Jayachandran M, Litwiller RD, Lahr BD, et al. Alterations in platelet function and cell-derived microvesicles in recently menopausal women: relationship to metabolic syndrome and atherogenic risk. J Cardiovasc Transl Res 2011; 4(6): 811-22.
[] [PMID: 21786187]
Afrisham R, Sadegh-Nejadi S, Meshkani R, Emamgholipour S, Paknejad M. Effect of circulating exosomes derived from normal-weight and obese women on gluconeogenesis, glycogenesis, lipogenesis and secretion of FGF21 and fetuin A in HepG2 cells. Diabetol Metab Syndr 2020; 12(32): 32.
[] [PMID: 32322309]
Barreca MM, Cancemi P, Geraci F. Mesenchymal and induced pluripotent stem cells-derived extracellular vesicles: the new frontier for regenerative medicine? Cells 2020; 9(5)E1163
[] [PMID: 32397132]
Cai J, Wu J, Wang J, et al. Extracellular vesicles derived from different sources of mesenchymal stem cells: therapeutic effects and translational potential. Cell Biosci 2020; 10(69): 69.
[] [PMID: 32483483]
Yang D, Wang W, Li L, et al. The relative contribution of paracine effect versus direct differentiation on adipose-derived stem cell transplantation mediated cardiac repair. PLoS One 2013; 8(3)e59020
[] [PMID: 23527076]
Salgado AJ, Reis RL, Sousa NJ, Gimble JM. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther 2010; 5(2): 103-10.
[] [PMID: 19941460]
Drago D, Cossetti C, Iraci N, et al. The stem cell secretome and its role in brain repair. Biochimie 2013; 95(12): 2271-85.
[] [PMID: 23827856]
Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 2004; 104(8): 2543-8.
[] [PMID: 15213101]
Morel O, Toti F, Hugel B, Freyssinet JM. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol 2004; 11(3): 156-64.
[] [PMID: 15257014]
Janowska-Wieczorek A, Majka M, Kijowski J, et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood 2001; 98(10): 3143-9.
[] [PMID: 11698303]
Doeppner TR, Herz J, Görgens A, et al. Extracellular vesicles improve post-stroke neuroregeneration and prevent postischemic immunosuppression. Stem Cells Transl Med 2015; 4(10): 1131-43.
[] [PMID: 26339036]
Zhang Y, Chopp M, Meng Y, et al. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg 2015; 122(4): 856-67.
[] [PMID: 25594326]
Perets N, Hertz S, London M, Offen D. Intranasal administration of exosomes derived from mesenchymal stem cells ameliorates autistic-like behaviors of BTBR mice. Mol Autism 2018; 9: 57.
[] [PMID: 30479733]
Elia CA, Tamborini M, Rasile M, et al. Intracerebral injection of extracellular vesicles from mesenchymal stem cells exerts reduced Aβ plaque burden in early stages of a preclinical model of alzheimer’s disease. Cells 2019; 8(9)E1059
[] [PMID: 31510042]
Thomi G, Joerger-Messerli M, Haesler V, Muri L, Surbek D, Schoeberlein A. Intranasally administered exosomes from umbilical cord stem cells have preventive neuroprotective effects and contribute to functional recovery after perinatal brain injury. Cells 2019; 8(8)E855
[] [PMID: 31398924]
Wang L, Pei S, Han L, et al. Mesenchymal stem cell-derived exosomes reduce A1 astrocytes via downregulation of phosphorylated NFκB P65 subunit in spinal cord injury. Cell Physiol Biochem 2018; 50(4): 1535-59.
[] [PMID: 30376671]
Sun G, Li G, Li D, et al. hucMSC derived exosomes promote functional recovery in spinal cord injury mice via attenuating inflammation. Mater Sci Eng C 2018; 89: 194-204.
[] [PMID: 29752089]
Farinazzo A, Angiari S, Turano E, et al. Nanovesicles from adipose-derived mesenchymal stem cells inhibit T lymphocyte trafficking and ameliorate chronic experimental autoimmune encephalomyelitis. Sci Rep 2018; 8(1): 7473.
[] [PMID: 29748664]
Li Z, Liu F, He X, Yang X, Shan F, Feng J. Exosomes derived from mesenchymal stem cells attenuate inflammation and demyelination of the central nervous system in EAE rats by regulating the polarization of microglia. Int Immunopharmacol 2019; 67: 268-80.
[] [PMID: 30572251]
Ma Y, Dong L, Zhou D, et al. Extracellular vesicles from human umbilical cord mesenchymal stem cells improve nerve regeneration after sciatic nerve transection in rats. J Cell Mol Med 2019; 23(4): 2822-35.
[] [PMID: 30772948]
Shiue SJ, Rau RH, Shiue HS, et al. Mesenchymal stem cell exosomes as a cell-free therapy for nerve injury-induced pain in rats. Pain 2019; 160(1): 210-23.
[] [PMID: 30188455]
Patel NA, Moss LD, Lee JY, et al. Long noncoding RNA MALAT1 in exosomes drives regenerative function and modulates inflammation-linked networks following traumatic brain injury. J Neuroinflammation 2018; 15(1): 204.
[] [PMID: 30001722]
Yu YM, Gibbs KM, Davila J, et al. MicroRNA miR-133b is essential for functional recovery after spinal cord injury in adult zebrafish. Eur J Neurosci 2011; 33(9): 1587-97.
[] [PMID: 21447094]
Joerger-Messerli MS, Oppliger B, Spinelli M, et al. Extracellular vesicles derived from wharton’s jelly mesenchymal stem cells prevent and resolve programmed cell death mediated by perinatal hypoxia-ischemia in neuronal cells. Cell Transplant 2018; 27(1): 168-80.
[] [PMID: 29562785]
Moon GJ, Sung JH, Kim DH, et al. Application of mesenchymal stem cell-derived extracellular vesicles for stroke: biodistribution and MicroRNA study. Transl Stroke Res 2019; 10(5): 509-21.
[] [PMID: 30341718]
Jiang M, Wang H, Jin M, et al. Exosomes from MiR-30d-5p-ADSCs reverse acute ischemic stroke-induced, autophagy-mediated brain injury by promoting M2 microglial/macrophage polarization. Cell Physiol Biochem 2018; 47(2): 864-78.
[] [PMID: 29807362]
Aliotta JM, Pereira M, Wen S, et al. Exosomes induce and reverse monocrotaline-induced pulmonary hypertension in mice. Cardiovasc Res 2016; 110(3): 319-30.
[] [PMID: 26980205]
Lee C, Mitsialis SA, Aslam M, et al. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 2012; 126(22): 2601-11.
[] [PMID: 23114789]
Tang XD, Shi L, Monsel A, et al. Mesenchymal stem cell microvesicles attenuate acute lung injury in mice partly mediated by ang-1 mRNA. Stem Cells 2017; 35(7): 1849-59.
[] [PMID: 28376568]
Potter DR, Miyazawa BY, Gibb SL, et al. Mesenchymal stem cell-derived extracellular vesicles attenuate pulmonary vascular permeability and lung injury induced by hemorrhagic shock and trauma. J Trauma Acute Care Surg 2018; 84(2): 245-56.
[] [PMID: 29251710]
de Castro LL, Xisto DG, Kitoko JZ, et al. Human adipose tissue mesenchymal stromal cells and their extracellular vesicles act differentially on lung mechanics and inflammation in experimental allergic asthma. Stem Cell Res Ther 2017; 8(1): 151.
[] [PMID: 28646903]
Gazdhar A, Grad I, Tamò L, Gugger M, Feki A, Geiser T. The secretome of induced pluripotent stem cells reduces lung fibrosis in part by hepatocyte growth factor. Stem Cell Res Ther 2014; 5(6): 123.
[] [PMID: 25384638]
Teng X, Chen L, Chen W, Yang J, Yang Z, Shen Z. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem 2015; 37(6): 2415-24.
[] [PMID: 26646808]
Vrijsen KR, Maring JA, Chamuleau SA, et al. Exosomes from cardiomyocyte progenitor cells and mesenchymal stem cells stimulate angiogenesis Via EMMPRIN. Adv Healthc Mater 2016; 5(19): 2555-65.
[] [PMID: 27570124]
Shao L, Zhang Y, Lan B, et al. MiRNA-Sequence indicates that mesenchymal stem cells and exosomes have similar mechanism to enhance cardiac repair. BioMed Res Int 2017; 20174150705
[] [PMID: 28203568]
Wang K, Jiang Z, Webster KA, et al. Enhanced cardioprotection by human endometrium mesenchymal stem cells driven by exosomal MicroRNA-21. Stem Cells Transl Med 2017; 6(1): 209-22.
[] [PMID: 28170197]
Feng Y, Huang W, Wani M, Yu X, Ashraf M. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One 2014; 9(2)e88685
[] [PMID: 24558412]
Luther KM, Haar L, McGuinness M, et al. Exosomal miR-21a-5p mediates cardioprotection by mesenchymal stem cells. J Mol Cell Cardiol 2018; 119: 125-37.
[] [PMID: 29698635]
Wang N, Chen C, Yang D, et al. Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis. Biochim Biophys Acta Mol Basis Dis 2017; 1863(8): 2085-92.
[] [PMID: 28249798]
Liu J, Jiang M, Deng S, et al. miR-93-5p-Containing exosomes treatment attenuates acute myocardial infarction-induced myocardial damage. Mol Ther Nucleic Acids 2018; 11: 103-15.
[] [PMID: 29858047]
Xiao C, Wang K, Xu Y, et al. Transplanted mesenchymal stem cells reduce autophagic flux in infarcted hearts via the exosomal transfer of miR-125b. Circ Res 2018; 123(5): 564-78.
[] [PMID: 29921652]
Arslan F, Lai RC, Smeets MB, et al. 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 (Amst) 2013; 10(3): 301-12.
[] [PMID: 23399448]
Liu H, Sun X, Gong X, Wang G. Human umbilical cord mesenchymal stem cells derived exosomes exert antiapoptosis effect via activating PI3K/Akt/mTOR pathway on H9C2 cells. J Cell Biochem 2019; 120(9): 14455-64.
[] [PMID: 30989714]
Xu R, Zhang F, Chai R, et al. Exosomes derived from pro-inflammatory bone marrow-derived mesenchymal stem cells reduce inflammation and myocardial injury via mediating macrophage polarization. J Cell Mol Med 2019; 23(11): 7617-31.
[] [PMID: 31557396]
Wang Y, Zhang L, Li Y, et al. Exosomes/microvesicles from induced pluripotent stem cells deliver cardioprotective miRNAs and prevent cardiomyocyte apoptosis in the ischemic myocardium. Int J Cardiol 2015; 192: 61-9.
[] [PMID: 26000464]
Xuan W, Wang L, Xu M, Weintraub NL, Ashraf M. miRNAs in Extracellular vesicles from iPS-derived cardiac progenitor cells effectively reduce fibrosis and promote angiogenesis in infarcted heart. Stem Cells Int 2019; 20193726392
[] [PMID: 31814833]
Gatti S, Bruno S, Deregibus MC, et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 2011; 26(5): 1474-83.
[] [PMID: 21324974]
He J, Wang Y, Sun S, et al. Bone marrow stem cells-derived microvesicles protect against renal injury in the mouse remnant kidney model. Nephrology (Carlton) 2012; 17(5): 493-500.
[] [PMID: 22369283]
Shen B, Liu J, Zhang F, et al. CCR2 Positive exosome released by mesenchymal stem cells suppresses macrophage functions and alleviates ischemia/reperfusion-induced renal injury. Stem Cells Int 2016; 20161240301
[] [PMID: 27843457]
Zou X, Zhang G, Cheng Z, et al. Microvesicles derived from human Wharton’s Jelly mesenchymal stromal cells ameliorate renal ischemia-reperfusion injury in rats by suppressing CX3CL1. Stem Cell Res Ther 2014; 5(2): 40.
[] [PMID: 24646750]
Matsukura T, Inaba C, Weygant EA, et al. Extracellular vesicles from human bone marrow mesenchymal stem cells repair organ damage caused by cadmium poisoning in a medaka model. Physiol Rep 2019; 7(14)e14172
[] [PMID: 31325249]
Bruno S, Grange C, Collino F, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 2012; 7(3)e33115
[] [PMID: 22431999]
Wang B, Jia H, Zhang B, et al. Pre-incubation with hucMSC-exosomes prevents cisplatin-induced nephrotoxicity by activating autophagy. Stem Cell Res Ther 2017; 8(1): 75.
[] [PMID: 28388958]
Jia H, Liu W, Zhang B, et al. HucMSC exosomes-delivered 14-3-3ζ enhanced autophagy via modulation of ATG16L in preventing cisplatin-induced acute kidney injury. Am J Transl Res 2018; 10(1): 101-13.
[PMID: 29422997]
Zhang G, Zou X, Huang Y, et al. 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 2016; 41(2): 119-28.
[] [PMID: 26894749]
Zou X, Gu D, Xing X, et al. Human mesenchymal stromal cell-derived extracellular vesicles alleviate renal ischemic reperfusion injury and enhance angiogenesis in rats. Am J Transl Res 2016; 8(10): 4289-99.
[PMID: 27830012]
He J, Wang Y, Lu X, et al. Micro-vesicles derived from bone marrow stem cells protect the kidney both in vivo and in vitro by microRNA-dependent repairing. Nephrology (Carlton) 2015; 20(9): 591-600.
[] [PMID: 25907000]
Bruno S, Tapparo M, Collino F, et al. Renal regenerative potential of different extracellular vesicle populations derived from bone marrow mesenchymal stromal cells. Tissue Eng Part A 2017; 23(21-22): 1262-73.
[] [PMID: 28471327]
Lee PY, Chien Y, Chiou GY, Lin CH, Chiou CH, Tarng DC. Induced pluripotent stem cells without c-Myc attenuate acute kidney injury via downregulating the signaling of oxidative stress and inflammation in ischemia-reperfusion rats. Cell Transplant 2012; 21(12): 2569-85.
[] [PMID: 22507855]
Collino F, Lopes JA, Tapparo M, et al. Extracellular vesicles derived from induced pluripotent stem cells promote renoprotection in acute kidney injury model. Cells 2020; 9(2)E453
[] [PMID: 32079274]
Mardpour S, Hassani SN, Mardpour S, et al. Extracellular vesicles derived from human embryonic stem cell-MSCs ameliorate cirrhosis in thioacetamide-induced chronic liver injury. J Cell Physiol 2018; 233(12): 9330-44.
[] [PMID: 29266258]
Haga H, Yan IK, Takahashi K, Matsuda A, Patel T. Extracellular vesicles from bone marrow-derived mesenchymal stem cells improve survival from lethal hepatic failure in mice. Stem Cells Transl Med 2017; 6(4): 1262-72.
[] [PMID: 28213967]
Rong X, Liu J, Yao X, Jiang T, Wang Y, Xie F. Human bone marrow mesenchymal stem cells-derived exosomes alleviate liver fibrosis through the Wnt/β-catenin pathway. Stem Cell Res Ther 2019; 10(1): 98.
[] [PMID: 30885249]
Yan Y, Jiang W, Tan Y, et al. hucMSC Exosome-derived GPX1 Is required for the recovery of hepatic oxidant injury. Mol Ther 2017; 25(2): 465-79.
[] [PMID: 28089078]
Jiang W, Tan Y, Cai M, et al. Human umbilical cord MSC-derived exosomes suppress the development of CCl4-induced liver injury through antioxidant effect. Stem Cells Int 2018; 20186079642
[] [PMID: 29686713]
Yao J, Zheng J, Cai J, et al. 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 J 2019; 33(2): 1695-710.
[] [PMID: 30226809]
Li T, Yan Y, Wang B, et al. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev 2013; 22(6): 845-54.
[] [PMID: 23002959]
Cross M, Smith E, Hoy D, et al. The global burden of hip and knee osteoarthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis 2014; 73(7): 1323-30.
[] [PMID: 24553908]
Zhang S, Chu WC, Lai RC, Lim SK, Hui JH, Toh WS. Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration. Osteoarthritis Cartilage 2016; 24(12): 2135-40.
[] [PMID: 27390028]
Wang Y, Yu D, Liu Z, et al. Exosomes from embryonic mesenchymal stem cells alleviate osteoarthritis through balancing synthesis and degradation of cartilage extracellular matrix. Stem Cell Res Ther 2017; 8(1): 189.
[] [PMID: 28807034]
Vonk LA, van Dooremalen SFJ, Liv N, et al. Mesenchymal stromal/stem cell-derived extracellular vesicles promote human cartilage regeneration In Vitro. Theranostics 2018; 8(4): 906-20.
[] [PMID: 29463990]
Tofiño-Vian M, Guillén MI, Pérez Del Caz MD, Castejón MA, Alcaraz MJ. Extracellular vesicles from adipose-derived mesenchymal stem cells downregulate senescence features in osteoarthritic osteoblasts. Oxid Med Cell Longev 2017; 20177197598
[] [PMID: 29230269]
Tofiño-Vian M, Guillén MI, Pérez Del Caz MD, Silvestre A, Alcaraz MJ. Microvesicles from human adipose tissue-derived mesenchymal stem cells as a new protective strategy in osteoarthritic chondrocytes. Cell Physiol Biochem 2018; 47(1): 11-25.
[] [PMID: 29763932]
Hu Y, Xu R, Chen CY, et al. Extracellular vesicles from human umbilical cord blood ameliorate bone loss in senile osteoporotic mice. Metabolism 2019; 95: 93-101.
[] [PMID: 30668962]
Hu L, Wang J, Zhou X, et al. Exosomes derived from human adipose mensenchymal stem cells accelerates cutaneous wound healing via optimizing the characteristics of fibroblasts. Sci Rep 2016; 6: 32993.
[] [PMID: 27615560]
Wang L, Hu L, Zhou X, et al. Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep 2017; 7(1): 13321.
[] [PMID: 29042658]
Cho BS, Kim JO, Ha DH, Yi YW. Exosomes derived from human adipose tissue-derived mesenchymal stem cells alleviate atopic dermatitis. Stem Cell Res Ther 2018; 9(1): 187.
[] [PMID: 29996938]
Oh M, Lee J, Kim YJ, Rhee WJ, Park JH. Exosomes derived from human induced pluripotent stem cells ameliorate the aging of skin fibroblasts. Int J Mol Sci 2018; 19(6)E1715
[] [PMID: 29890746]
Shi Z, Wang Q, Jiang D. Extracellular vesicles from bone marrow-derived multipotent mesenchymal stromal cells regulate inflammation and enhance tendon healing. J Transl Med 2019; 17(1): 211.
[] [PMID: 31238964]
Zarovni N, Corrado A, Guazzi P, et al. Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods 2015; 87: 46-58.
[] [PMID: 26044649]
Serrano-Pertierra E, Oliveira-Rodríguez M, Rivas M, et al. Characterization of plasma-derived extracellular vesicles isolated by different methods: a comparison study. Bioengineering (Basel) 2019; 6(1): 8.
[] [PMID: 30658418]
Arab T, Raffo-Romero A, Van Camp C, et al. Proteomic characterisation of leech microglia extracellular vesicles (EVs): comparison between differential ultracentrifugation and Optiprep™ density gradient isolation. J Extracell Vesicles 2019; 8(1)1603048
[] [PMID: 31069026]
Baranyai T, Herczeg K, Onódi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. PLoS One 2015; 10(12)e0145686
[] [PMID: 26690353]
Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods 2015; 87: 3-10.
[] [PMID: 25766927]
Monguió-Tortajada M, Gálvez-Montón C, Bayes-Genis A, Roura S, Borràs FE. Extracellular vesicle isolation methods: rising impact of size-exclusion chromatography. Cell Mol Life Sci 2019; 76(12): 2369-82.
[] [PMID: 30891621]
Nordin JZ, Lee Y, Vader P, et al. Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine (Lond) 2015; 11(4): 879-83.
[] [PMID: 25659648]
Heinemann ML, Ilmer M, Silva LP, et al. Benchtop isolation and characterization of functional exosomes by sequential filtration. J Chromatogr A 2014; 1371: 125-35.
[] [PMID: 25458527]
Hsu H, Black L. Polyethylene glycol for purification of potato yellow dwarf virus. Phytopathology 1973; 63(6): 692-6.
Vlassov AV, Magdaleno S, Setterquist R, Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta 2012; 1820(7): 940-8.
[] [PMID: 22503788]
Nakai W, Yoshida T, Diez D, et al. A novel affinity-based method for the isolation of highly purified extracellular vesicles. Sci Rep 2016; 6: 33935.
[] [PMID: 27659060]
Clayton A, Court J, Navabi H, et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J Immunol Methods 2001; 247(1-2): 163-74.
[] [PMID: 11150547]
Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugetion, density-gradient separation, and immune-affinity capture methods Methods Mol Biol. New York, USA: Humana Press 2015; pp. 179-209.
He M, Zeng Y. Microfluidic exosome analysis toward liquid biopsy for cancer. J Lab Autom 2016; 21(4): 599-608.
[] [PMID: 27215792]
Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 2014; 14(11): 1891-900.
[] [PMID: 24722878]
Liga A, Vliegenthart AD, Oosthuyzen W, Dear JW, Kersaudy-Kerhoas M. Exosome isolation: a microfluidic road-map. Lab Chip 2015; 15(11): 2388-94.
[] [PMID: 25940789]
Thind A, Wilson C. Exosomal miRNAs as cancer biomarkers and therapeutic targets. J Extracell Vesicles 2016; 5(1): 31292.
[] [PMID: 27440105]
Davies RT, Kim J, Jang SC, Choi E-J, Gho YS, Park J. Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip 2012; 12(24): 5202-10.
[] [PMID: 23111789]
Lu M, Xing H, Yang Z, et al. Recent advances on extracellular vesicles in therapeutic delivery: Challenges, solutions, and opportunities. Eur J Pharm Biopharm 2017; 119: 381-95.
[] [PMID: 28739288]
Wang Z, Wu HJ, Fine D, et al. Ciliated micropillars for the microfluidic-based isolation of nanoscale lipid vesicles. Lab Chip 2013; 13(15): 2879-82.
[] [PMID: 23743667]
Agrahari V, Agrahari V, Burnouf P-A, Chew CH, Burnouf T. Extracellular microvesicles as new industrial therapeutic frontiers. Trends Biotechnol 2019; 37(7): 707-29.
[] [PMID: 30638682]
Lee K, Shao H, Weissleder R, Lee H. Acoustic purification of extracellular microvesicles. ACS Nano 2015; 9(3): 2321-7.
[] [PMID: 25672598]
Santana SM, Antonyak MA, Cerione RA, Kirby BJ. Microfluidic isolation of cancer-cell-derived microvesicles from hetergeneous extracellular shed vesicle populations. Biomed Microdevices 2014; 16(6): 869-77.
[] [PMID: 25342569]
Wunsch BH, Smith JT, Gifford SM, et al. Nanoscale lateral displacement arrays for the separation of exosomes and colloids down to 20 nm. Nat Nanotechnol 2016; 11(11): 936-40.
[] [PMID: 27479757]

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