Login Register Cart 0
Generic placeholder image

Current Molecular Medicine

Editor-in-Chief

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

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Regenerative Potential of Mesenchymal Stem Cell-Derived Extracellular Vesicles

Author(s): Dineshi Sewvandi Thalakiriyawa , Primali Rukmal Jayasooriya and Waruna Lakmal Dissanayaka*

Volume 22, Issue 2, 2022

Published on: 11 February, 2021

Page: [98 - 119] Pages: 22

DOI: 10.2174/1566524021666210211114453

Price: $65

Abstract

Mesenchymal stem cells (MSCs) are multipotent cells that can differentiate into diverse cell lineages. MSC based therapy has become a widely experimented treatment strategy in regenerative medicine with promising outcomes. Recent reports suggest that much of the therapeutic effects of MSCs are mediated by their secretome that is expressed through extracellular vesicles (EVs). EVs are lipid bilayer bound components that carry cellular proteins, mRNA, lncRNAs, and other molecules in order to mediate intercellular communication and signaling. In fact, MSC-derived EVs have been observed to implement the same therapeutic effects as MSCs with minimal adverse effects and could be used as an alternative treatment method to MSC-based therapy. The regenerative activity of MSC-EVs has been observed in relation to multiple cell/tissue lineages using various animal models. However, further research and clinical trials are essential for the advancement of this novel treatment strategy. This review provides an insight into the available literature on applications of MSC-EVs in relation to angiogenesis, neurogenesis, hepatic and kidney regeneration, and wound healing.

Keywords: Extracellular vesicles, mesenchymal stem cells, regenerative medicine, secretome, paracrine signaling, regeneration.

« Previous Next »
[1]
Mao AS, Mooney DJ. Regenerative medicine: Current therapies and future directions. Proc Natl Acad Sci USA 2015; 112(47): 14452-9.
[http://dx.doi.org/10.1073/pnas.1508520112] [PMID: 26598661]
[2]
Tatullo M, Gargiulo IC, Dipalma G, et al. Stem Cells and Regenerative Medicine. Translational Systems Medicine and Oral Disease 2019.
[3]
Fathi E, Farahzadi R. Isolation, Culturing, Characterization and Aging of Adipose Tissue-Derived Mesenchymal Stem Cells: A Brief Overview. Braz Arch Biol Technol 2016.
[http://dx.doi.org/10.1590/1678-4324-2016150383]
[4]
Seifrtová M, Havelek R, Cmielová J, et al. The response of human ectomesenchymal dental pulp stem cells to cisplatin treatment. Int Endod J 2012; 45(5): 401-12.
[http://dx.doi.org/10.1111/j.1365-2591.2011.01990.x] [PMID: 22142405]
[5]
Mrozik KM, Zilm PS, Bagley CJ, et al. Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: analysis of differentially expressed proteins. Stem Cells Dev 2010; 19(10): 1485-99.
[http://dx.doi.org/10.1089/scd.2009.0446] [PMID: 20050811]
[6]
Koch TG, Heerkens T, Thomsen PD, Betts DH. Isolation of mesenchymal stem cells from equine umbilical cord blood. BMC Biotechnol 2007; 7: 26.
[http://dx.doi.org/10.1186/1472-6750-7-26] [PMID: 17537254]
[7]
Kisiel AH, McDuffee LA, Masaoud E, Bailey TR, Esparza Gonzalez BP, Nino-Fong R. Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Am J Vet Res 2012; 73(8): 1305-17.
[http://dx.doi.org/10.2460/ajvr.73.8.1305] [PMID: 22849692]
[8]
Wagner W, Wein F, Seckinger A, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33(11): 1402-16.
[http://dx.doi.org/10.1016/j.exphem.2005.07.003] [PMID: 16263424]
[9]
Schüring AN, Schulte N, Kelsch R, Röpke A, Kiesel L, Götte M. Characterization of endometrial mesenchymal stem-like cells obtained by endometrial biopsy during routine diagnostics. Fertil Steril 2011; 95(1): 423-6.
[http://dx.doi.org/10.1016/j.fertnstert.2010.08.035] [PMID: 20864098]
[10]
Morito T, Muneta T, Hara K, et al. Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans. Rheumatology (Oxford) 2008; 47(8): 1137-43.
[http://dx.doi.org/10.1093/rheumatology/ken114] [PMID: 18390894]
[11]
Janderová L, McNeil M, Murrell AN, Mynatt RL, Smith SR. Human mesenchymal stem cells as an in vitro model for human adipogenesis. Obes Res 2003; 11(1): 65-74.
[http://dx.doi.org/10.1038/oby.2003.11] [PMID: 12529487]
[12]
Hanna H, Mir LM, Andre FM. In vitro osteoblastic differentiation of mesenchymal stem cells generates cell layers with distinct properties. Stem Cell Res Ther 2018; 9(1): 203.
[http://dx.doi.org/10.1186/s13287-018-0942-x] [PMID: 30053888]
[13]
Du M. qing; Huang, Y. qin; Lu, N. S.; Shu, G.; Zhu, X. tong; Wang, L. na; Gao, P.; Xi, Q. yun; Zhang, Y. liang; Wang, S. bo; Jiang, Q. yan. Characterization and Differentiation into Adipocytes and Myocytes of Porcine Bone Marrow Mesenchymal Stem Cells. J Integr Agric 2014; 13(14): 837-48.
[http://dx.doi.org/10.1016/S2095-3119(13)60497-9]
[14]
Solchaga LA, Penick KJ, Welter JF. Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells: tips and tricks. Methods Mol Biol 2011; 698: 253-78.
[http://dx.doi.org/10.1007/978-1-60761-999-4_20] [PMID: 21431525]
[15]
Naghdi M, Tiraihi T, Namin SAM, Arabkheradmand J. Transdifferentiation of bone marrow stromal cells into cholinergic neuronal phenotype: a potential source for cell therapy in spinal cord injury. Cytotherapy 2009; 11(2): 137-52.
[http://dx.doi.org/10.1080/14653240802716582] [PMID: 19253075]
[16]
Lee KD, Kuo TKC, Whang-Peng J, et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 2004; 40(6): 1275-84.
[http://dx.doi.org/10.1002/hep.20469] [PMID: 15562440]
[17]
Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105(4): 1815-22.
[http://dx.doi.org/10.1182/blood-2004-04-1559] [PMID: 15494428]
[18]
Qin Y, Guan J, Zhang C. Mesenchymal stem cells: mechanisms and role in bone regeneration. Postgrad Med J 2014; 90(1069): 643-7.
[http://dx.doi.org/10.1136/postgradmedj-2013-132387] [PMID: 25335795]
[19]
Morishita T, Honoki K, Ohgushi H, Kotobuki N, Matsushima A, Takakura Y. Tissue Engineering Approach to the Treatment of Bone Tumors: Three Cases of Cultured Bone Grafts Derived from Patients’ Mesenchymal Stem Cells. Artifcial Organs 2006.
[20]
Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair--current views Stem Cells 2007; (11): 2896-902; 30 (2): 115-8
[http://dx.doi.org/10.1634/stemcells.2007-0637] [PMID: 17901396]
[21]
Yamada Y, Boo JS, Ozawa R, et al. Bone regeneration following injection of mesenchymal stem cells and fibrin glue with a biodegradable scaffold. J Craniomaxillofac Surg 2003; 31(1): 27-33.
[http://dx.doi.org/10.1016/S1010-5182(02)00143-9] [PMID: 12553923]
[22]
Liu P, Song J. Sulfobetaine as a zwitterionic mediator for 3D hydroxyapatite mineralization. Biomaterials 2013; 34(10): 2442-54.
[http://dx.doi.org/10.1016/j.biomaterials.2012.12.029] [PMID: 23332320]
[23]
Lin W, Xu L, Zwingenberger S, Gibon E, Goodman SB, Li G. Mesenchymal stem cells homing to improve bone healing. J Orthop Translat 2017; 9: 19-27.
[http://dx.doi.org/10.1016/j.jot.2017.03.002] [PMID: 29662796]
[24]
Guo X, Wang C, Zhang Y, et al. Repair of large articular cartilage defects with implants of autologous mesenchymal stem cells seeded into β-tricalcium phosphate in a sheep model. Tissue Eng 2004; 10(11-12): 1818-29.
[http://dx.doi.org/10.1089/ten.2004.10.1818] [PMID: 15684690]
[25]
Cooney DS, Wimmers EG, Ibrahim Z, et al. Mesenchymal Stem Cells Enhance Nerve Regeneration in a Rat Sciatic Nerve Repair and Hindlimb Transplant Model. Sci Rep 2016; 6: 31306.
[http://dx.doi.org/10.1038/srep31306] [PMID: 27510321]
[26]
Lipinski MJ, Biondi-Zoccai GGL, Abbate A, et al. Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials. J Am Coll Cardiol 2007; 50(18): 1761-7.
[http://dx.doi.org/10.1016/j.jacc.2007.07.041] [PMID: 17964040]
[27]
Schächinger V, Erbs S, Elsässer A, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006; 355(12): 1210-21.
[http://dx.doi.org/10.1056/NEJMoa060186] [PMID: 16990384]
[28]
Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell 2011; 9(1): 11-5.
[http://dx.doi.org/10.1016/j.stem.2011.06.008] [PMID: 21726829]
[29]
Gnecchi M, He H, Noiseux N, et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006; 20(6): 661-9.
[http://dx.doi.org/10.1096/fj.05-5211com] [PMID: 16581974]
[30]
Lee RH, Pulin AA, Seo MJ, et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009; 5(1): 54-63.
[http://dx.doi.org/10.1016/j.stem.2009.05.003] [PMID: 19570514]
[31]
Herberts CA, Kwa MSG, Hermsen HPH. Risk factors in the development of stem cell therapy. J Transl Med 2011; 9: 29.
[http://dx.doi.org/10.1186/1479-5876-9-29] [PMID: 21418664]
[32]
Aguilar S, Nye E, Chan J, et al. Murine but not human mesenchymal stem cells generate osteosarcoma-like lesions in the lung. Stem Cells 2007; 25(6): 1586-94.
[http://dx.doi.org/10.1634/stemcells.2006-0762] [PMID: 17363552]
[33]
Sundin M, Örvell C, Rasmusson I, Sundberg B, Ringdén O, Le Blanc K. Mesenchymal stem cells are susceptible to human herpesviruses, but viral DNA cannot be detected in the healthy seropositive individual. Bone Marrow Transplant 2006; 37(11): 1051-9.
[http://dx.doi.org/10.1038/sj.bmt.1705368] [PMID: 16604097]
[34]
Lin L, Du L. The role of secreted factors in stem cells-mediated immune regulation. Cell Immunol 2018; 326: 24-32.
[http://dx.doi.org/10.1016/j.cellimm.2017.07.010] [PMID: 28778535]
[35]
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.
[http://dx.doi.org/10.1016/j.scr.2009.12.003] [PMID: 20138817]
[36]
Hsieh JY, Wang HW, Chang SJ, et al. Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One 2013; 8(8)e72604
[http://dx.doi.org/10.1371/journal.pone.0072604] [PMID: 23991127]
[37]
Gowen A, Shahjin F, Chand S, Odegaard KE, Yelamanchili SV. Mesenchymal Stem Cell-Derived Extracellular Vesicles: Challenges in Clinical Applications. Front Cell Dev Biol 2020; 8: 149.
[http://dx.doi.org/10.3389/fcell.2020.00149] [PMID: 32226787]
[38]
Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011; 2: 282.
[http://dx.doi.org/10.1038/ncomms1285] [PMID: 21505438]
[39]
Bukong TN, Momen-Heravi F, Kodys K, Bala S, Szabo G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog 2014; 10(10)e1004424
[http://dx.doi.org/10.1371/journal.ppat.1004424] [PMID: 25275643]
[40]
Heng BC, Cao T, Lee EH. Directing stem cell differentiation into the chondrogenic lineage in vitro. Stem Cells 2004; 22(7): 1152-67.
[http://dx.doi.org/10.1634/stemcells.2004-0062] [PMID: 15579636]
[41]
Wang S, Guo L, Ge J, et al. Excess Integrins Cause Lung Entrapment of Mesenchymal Stem Cells. Stem Cells 2015; 33(11): 3315-26.
[http://dx.doi.org/10.1002/stem.2087] [PMID: 26148841]
[42]
Lee M, Ban JJ, Yang S. The Exosome of Adipose-Derived Stem Cells Reduces β-Amyloid Pathology and Apoptosis of Neuronal Cells Derived from the Transgenic Mouse Model of Alzheimer’s Disease. Brain Res 2018.
[43]
Bai L, Shao H, Wang H, et al. Effects of Mesenchymal Stem Cell-Derived Exosomes on Experimental Autoimmune Uveitis. Sci Rep 2017; 7(1): 4323.
[http://dx.doi.org/10.1038/s41598-017-04559-y] [PMID: 28659587]
[44]
Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200(4): 373-83.
[http://dx.doi.org/10.1083/jcb.201211138] [PMID: 23420871]
[45]
Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30(1): 255-89.
[http://dx.doi.org/10.1146/annurev-cellbio-101512-122326] [PMID: 25288114]
[46]
Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13(3): 269-88.
[http://dx.doi.org/10.1111/j.1365-2141.1967.tb08741.x] [PMID: 6025241]
[47]
Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluidsCurr Protoc Cell Biol 2006; Chapter 3: unit 322.
[http://dx.doi.org/10.1002/0471143030.cb0322s30] [PMID: 18228490]
[48]
Yuana Y, Böing AN, Grootemaat AE, et al. Handling and storage of human body fluids for analysis of extracellular vesicles. J Extracell Vesicles 2015; 4(1): 29260.
[http://dx.doi.org/10.3402/jev.v4.29260] [PMID: 26563735]
[49]
Morrison EE, Bailey MA, Dear JW. Renal extracellular vesicles: from physiology to clinical application. J Physiol 2016; 594(20): 5735-48.
[http://dx.doi.org/10.1113/JP272182] [PMID: 27104781]
[50]
Allen TM, Austin GA, Chonn A, Lin L, Lee KC. Uptake of Liposomes by Cultured Mouse Bone Marrow Macrophages: Influence of Liposome Composition and Size. BBA - Biomembr 1991.
[51]
Ramstedt B, Slotte JP. Membrane properties of sphingomyelins. FEBS Lett 2002; 531(1): 33-7.
[http://dx.doi.org/10.1016/S0014-5793(02)03406-3] [PMID: 12401199]
[52]
Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK, Gho YS. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002; 62(21): 6312-7.
[PMID: 12414662]
[53]
Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 1998; 273(32): 20121-7.
[http://dx.doi.org/10.1074/jbc.273.32.20121] [PMID: 9685355]
[54]
Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 2013; 13(10-11): 1554-71.
[http://dx.doi.org/10.1002/pmic.201200329] [PMID: 23401200]
[55]
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 2009; 11(9): 1143-9.
[http://dx.doi.org/10.1038/ncb1929] [PMID: 19684575]
[56]
Fevrier B, Vilette D, Archer F, et al. Cells release prions in association with exosomes. Proc Natl Acad Sci USA 2004; 101(26): 9683-8.
[http://dx.doi.org/10.1073/pnas.0308413101] [PMID: 15210972]
[57]
Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9(8): 581-93.
[http://dx.doi.org/10.1038/nri2567] [PMID: 19498381]
[58]
Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009; 10(9): 597-608.
[http://dx.doi.org/10.1038/nrm2755] [PMID: 19696797]
[59]
Morelli AE, Larregina AT, Shufesky WJ, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004; 104(10): 3257-66.
[http://dx.doi.org/10.1182/blood-2004-03-0824] [PMID: 15284116]
[60]
van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018; 19(4): 213-28.
[http://dx.doi.org/10.1038/nrm.2017.125] [PMID: 29339798]
[61]
Wollert T, Hurley JH. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 2010; 464(7290): 864-9.
[http://dx.doi.org/10.1038/nature08849] [PMID: 20305637]
[62]
Henne WM, Stenmark H, Emr SD. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol 2013; 5(9)a016766
[http://dx.doi.org/10.1101/cshperspect.a016766] [PMID: 24003212]
[63]
Savina A, Furlán M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 2003; 278(22): 20083-90.
[http://dx.doi.org/10.1074/jbc.M301642200] [PMID: 12639953]
[64]
Muralidharan-Chari V, Clancy J, Plou C, et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 2009; 19(22): 1875-85.
[http://dx.doi.org/10.1016/j.cub.2009.09.059] [PMID: 19896381]
[65]
Bucki R, Bachelot-Loza C, Zachowski A, Giraud F, Sulpice JC. Calcium induces phospholipid redistribution and microvesicle release in human erythrocyte membranes by independent pathways. Biochemistry 1998; 37(44): 15383-91.
[http://dx.doi.org/10.1021/bi9805238] [PMID: 9799499]
[66]
Wang T, Gilkes DM, Takano N, et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci USA 2014; 111(31): E3234-42.
[http://dx.doi.org/10.1073/pnas.1410041111] [PMID: 24938788]
[67]
Maguire G. Stem cell therapy without the cells. Commun Integr Biol 2013; 6(6)e26631
[http://dx.doi.org/10.4161/cib.26631] [PMID: 24567776]
[68]
Vishnubhatla I, Corteling R, Stevanato L, Hicks C, Sinden J. The Development of Stem Cell-Derived Exosomes as a Cell-Free Regenerative Medicine. J Circul Biomark 2014; 3: 2014.
[69]
Lu J, Yang J, Zheng Y, Chen X, Fang S. Extracellular vesicles from endothelial progenitor cells prevent steroid-induced osteoporosis by suppressing the ferroptotic pathway in mouse osteoblasts based on bioinformatics evidence. Sci Rep 2019; 9(1): 16130.
[http://dx.doi.org/10.1038/s41598-019-52513-x] [PMID: 31695092]
[70]
Hao D, Swindell HS, Ramasubramanian L, et al. Extracellular Matrix Mimicking Nanofibrous Scaffolds Modified With Mesenchymal Stem Cell-Derived Extracellular Vesicles for Improved Vascularization. Front Bioeng Biotechnol 2020; 8: 633.
[http://dx.doi.org/10.3389/fbioe.2020.00633] [PMID: 32671037]
[71]
Karlsson M, Lundin S, Dahlgren U, Kahu H, Pettersson I, Telemo E. “Tolerosomes” are produced by intestinal epithelial cells. Eur J Immunol 2001; 31(10): 2892-900.
[http://dx.doi.org/10.1002/1521-4141(2001010)31:10<2892:AID-IMMU2892>3.0.CO;2-I] [PMID: 11592064]
[72]
Anderson HC. Vesicles associated with calcification in the matrix of epiphyseal cartilage. J Cell Biol 1969; 41(1): 59-72.
[http://dx.doi.org/10.1083/jcb.41.1.59] [PMID: 5775794]
[73]
Stegmayr B, Ronquist G. Promotive effect on human sperm progressive motility by prostasomes. Urol Res 1982; 10(5): 253-7.
[http://dx.doi.org/10.1007/BF00255932] [PMID: 6219486]
[74]
Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 2015; 25(6): 364-72.
[http://dx.doi.org/10.1016/j.tcb.2015.01.004] [PMID: 25683921]
[75]
Stein JM, Luzio JP. Ectocytosis caused by sublytic autologous complement attack on human neutrophils. The sorting of endogenous plasma-membrane proteins and lipids into shed vesicles. Biochem J 1991; 274(Pt 2): 381-6.
[http://dx.doi.org/10.1042/bj2740381] [PMID: 1848755]
[76]
Xu R, Greening DW, Rai A, Ji H, Simpson RJ. Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods 2015; 87: 11-25.
[http://dx.doi.org/10.1016/j.ymeth.2015.04.008] [PMID: 25890246]
[77]
Minciacchi VR, You S, Spinelli C, et al. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget 2015; 6(13): 11327-41.
[http://dx.doi.org/10.18632/oncotarget.3598] [PMID: 25857301]
[78]
Keerthikumar S, Gangoda L, Liem M, et al. Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget 2015; 6(17): 15375-96.
[http://dx.doi.org/10.18632/oncotarget.3801] [PMID: 25944692]
[79]
Haraszti RA, Didiot MC, Sapp E, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles 2016; 5(1): 32570.
[http://dx.doi.org/10.3402/jev.v5.32570] [PMID: 27863537]
[80]
Murray LMA, Krasnodembskaya AD. Concise Review: Intercellular Communication Via Organelle Transfer in the Biology and Therapeutic Applications of Stem Cells. Stem Cells 2019; 37(1): 14-25.
[http://dx.doi.org/10.1002/stem.2922] [PMID: 30353966]
[81]
Théry C, Witwer KW, Aikawa E, et al. 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 2018.
[http://dx.doi.org/10.1080/20013078.2018.1535750] [PMID: 30637094]
[82]
Vagner T, Spinelli C, Minciacchi VR, et al. Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. J Extracell Vesicles 2018; 7(1)1505403
[http://dx.doi.org/10.1080/20013078.2018.1505403] [PMID: 30108686]
[83]
Yekula A, Minciacchi VR, Morello M, et al. Large and Small Extracellular Vesicles Released by Glioma Cells in Vitro and in Vivo. J Extracell Vesicles 2020.
[http://dx.doi.org/10.1080/20013078.2019.1689784] [PMID: 31839905]
[84]
D’Souza-Schorey C, Clancy JW. Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 2012; 26(12): 1287-99.
[http://dx.doi.org/10.1101/gad.192351.112] [PMID: 22713869]
[85]
Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014; 14(3): 195-208.
[http://dx.doi.org/10.1038/nri3622] [PMID: 24566916]
[86]
Igami K, Uchiumi T, Ueda S, et al. Characterization and Function of Medium and Large Extracellular Vesicles from Plasma and Urine by Surface Antigens and Annexin V. Peer. J Anal Chem 2020.
[http://dx.doi.org/10.7717/peerj-achem.4]
[87]
Rojas A. The Imperative Authentication of Cell Lines. Antimicrob Agents Chemother 2017; 61(11): e01823-17.
[http://dx.doi.org/10.1128/AAC.01823-17] [PMID: 29066454]
[88]
Enabling a Robust Scalable Manufacturing Process for Therapeutic Exosomes through Oncogenic Immortalization of Human ESC-Derived MSCs. J Transl Med 2011; 9: 47.elinks.library.upenn.edu/sfx_local?sid=EMBASE&issn=14795876&id=doi:10.1186%2F1479-5876-9-47&atitle=Enabling+a+robust+scalable+manufacturing+process+for+therapeutic+exosomes+through+oncogenic+immortalization+of+human+ESC-derived+MSCs&stitle=J.+Transl.+Med.&title=Journal+of+Translational+Medicine&volume=9&issue=&spage=&epage=&aulast=Chen&aufirst=Tian+S.&auinit=T.S.&aufull=Chen+T.S.&coden=&isbn=&pages=-&date=2011&auinit1=T&auinitm=S
[89]
Frey B, Gaipl US. The immune functions of phosphatidylserine in membranes of dying cells and microvesicles. Semin Immunopathol 2011; 33(5): 497-516.
[http://dx.doi.org/10.1007/s00281-010-0228-6] [PMID: 20941495]
[90]
Roseblade A, Luk F, Ung A, Bebawy M. Targeting microparticle biogenesis: a novel approach to the circumvention of cancer multidrug resistance. Curr Cancer Drug Targets 2015; 15(3): 205-14.
[http://dx.doi.org/10.2174/1568009615666150225121508] [PMID: 25714701]
[91]
Takasugi M. Emerging roles of extracellular vesicles in cellular senescence and aging. Aging Cell 2018; 17(2)e12734
[http://dx.doi.org/10.1111/acel.12734] [PMID: 29392820]
[92]
Shao H. New Technologies for Analysis of Extracellular Vesicles 2018; 118
[93]
Tamkovich S, Tutanov O, Efimenko A, et al. Blood Circulating Exosomes Contain Distinguishable Fractions of Free and Cell-Surface-Associated Vesicles. Curr Mol Med 2019; 19(4): 273-85.
[http://dx.doi.org/10.2174/1566524019666190314120532] [PMID: 30868953]
[94]
Mincheva-Nilsson L, Baranov V, Nagaeva O, Dehlin E. Isolation and Characterization of Exosomes from Cultures of Tissue Explants and Cell Lines. Curr Protoc Immunol 2016; 115: 1-21.
[http://dx.doi.org/10.1002/cpim.17] [PMID: 27801511]
[95]
Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E. The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J Biol Chem 2012; 287(51): 43108-15.
[http://dx.doi.org/10.1074/jbc.M112.404467] [PMID: 23129776]
[96]
Deng ZB, Poliakov A, Hardy RW, et al. Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes 2009; 58(11): 2498-505.
[http://dx.doi.org/10.2337/db09-0216] [PMID: 19675137]
[97]
Vella LJ, Scicluna BJ, Cheng L, et al. A rigorous method to enrich for exosomes from brain tissue. J Extracell Vesicles 2017; 6(1)1348885
[http://dx.doi.org/10.1080/20013078.2017.1348885] [PMID: 28804598]
[98]
Roura S, Vives J. Extracellular vesicles: Squeezing every drop of regenerative potential of umbilical cord blood. Metabolism 2019; 95: 102-4.
[http://dx.doi.org/10.1016/j.metabol.2019.02.006] [PMID: 30831143]
[99]
Konoshenko MY, Lekchnov EA, Vlassov AV, Laktionov PP. Isolation of Extracellular Vesicles: General Methodologies and Latest Trends. BioMed Res Int 2018; 20188545347
[http://dx.doi.org/10.1155/2018/8545347] [PMID: 29662902]
[100]
Witwer KW, Buza EI, Bernis LT, Lo J. Nolte-, E. N.; Bora, A.; La, C.; Piper, M. G.; Sivaraman, S.; The, C.; Hochberg, F. Standardization of Sample Collection, Isolation and Analysis Methods in Extracellular Vesicle Research. J Extracell Vesicles 2013.
[http://dx.doi.org/10.3402/jev.v2i0.20360]
[101]
Gardiner C, Di Vizio D, Sahoo S, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles 2016; 5: 32945.
[http://dx.doi.org/10.3402/jev.v5.32945] [PMID: 27802845]
[102]
Cvjetkovic A, Lötvall J, Lässer C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J Extracell Vesicles 2014; 3(1): 1-11.
[http://dx.doi.org/10.3402/jev.v3.23111] [PMID: 24678386]
[103]
Carnino JM, Lee H, Jin Y. Isolation and characterization of extracellular vesicles from Broncho-alveolar lavage fluid: a review and comparison of different methods. Respir Res 2019; 20(1): 240.
[http://dx.doi.org/10.1186/s12931-019-1210-z] [PMID: 31666080]
[104]
Yamamoto KR, Alberts BM, Benzinger R, Lawhorne L, Treiber G. Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 1970; 40(3): 734-44.
[http://dx.doi.org/10.1016/0042-6822(70)90218-7] [PMID: 4908735]
[105]
Böing AN, van der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles 2014; 3(1)
[http://dx.doi.org/10.3402/jev.v3.23430] [PMID: 25279113]
[106]
Gámez-Valero A, Monguió-Tortajada M, Carreras-Planella L. Franquesa Ml, Beyer K, Borràs FE. Size-Exclusion Chromatography-based isolation minimally alters Extracellular Vesicles’ characteristics compared to precipitating agents. Sci Rep 2016; 6: 33641.
[http://dx.doi.org/10.1038/srep33641] [PMID: 27640641]
[107]
Kosaka N, Kogure A, Yamamoto T, et al. Exploiting the message from cancer: the diagnostic value of extracellular vesicles for clinical applications. Exp Mol Med 2019; 51(3): 1-9.
[http://dx.doi.org/10.1038/s12276-019-0219-1] [PMID: 30872565]
[108]
Brownlee Z, Lynn KD, Thorpe PE, Schroit AJA. A novel “salting-out” procedure for the isolation of tumor-derived exosomes. J Immunol Methods 2014; 407: 120-6.
[http://dx.doi.org/10.1016/j.jim.2014.04.003] [PMID: 24735771]
[109]
Rider MA, Hurwitz SN, Meckes DG Jr. ExtraPEG: A Polyethylene Glycol-Based Method for Enrichment of Extracellular Vesicles. Sci Rep 2016; 6: 23978.
[http://dx.doi.org/10.1038/srep23978] [PMID: 27068479]
[110]
Heath N, Grant L, De Oliveira TM, et al. Rapid isolation and enrichment of extracellular vesicle preparations using anion exchange chromatography. Sci Rep 2018; 8(1): 5730.
[http://dx.doi.org/10.1038/s41598-018-24163-y] [PMID: 29636530]
[111]
Merchant ML, Powell DW, Wilkey DW, et al. Microfiltration isolation of human urinary exosomes for characterization by MS. Proteomics Clin Appl 2010; 4(1): 84-96.
[http://dx.doi.org/10.1002/prca.200800093] [PMID: 21137018]
[112]
Lucchetti D, Fattorossi A, Sgambato A. Extracellular Vesicles in Oncology: Progress and Pitfalls in the Methods of Isolation and Analysis. Biotechnol J 2019; 14(1)e1700716
[http://dx.doi.org/10.1002/biot.201700716] [PMID: 29878510]
[113]
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.
[http://dx.doi.org/10.3171/2014.11.JNS14770] [PMID: 25594326]
[114]
Martins M, Ribeiro D, Martins A, Reis RL, Neves NM. Extracellular Vesicles Derived from Osteogenically Induced Human Bone Marrow Mesenchymal Stem Cells Can Modulate Lineage Commitment. Stem Cell Reports 2016; 6(3): 284-91.
[http://dx.doi.org/10.1016/j.stemcr.2016.01.001] [PMID: 26923821]
[115]
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.
[http://dx.doi.org/10.7150/thno.20746] [PMID: 29463990]
[116]
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
[http://dx.doi.org/10.14814/phy2.14172] [PMID: 31325249]
[117]
Grange C, Tritta S, Tapparo M, et al. Stem cell-derived extracellular vesicles inhibit and revert fibrosis progression in a mouse model of diabetic nephropathy. Sci Rep 2019; 9(1): 4468.
[http://dx.doi.org/10.1038/s41598-019-41100-9] [PMID: 30872726]
[118]
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.
[http://dx.doi.org/10.1111/jcmm.14190] [PMID: 30772948]
[119]
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
[http://dx.doi.org/10.3390/cells8080855] [PMID: 31398924]
[120]
Liang YC, Wu YP, Li XD, et al. TNF-α-induced exosomal miR-146a mediates mesenchymal stem cell-dependent suppression of urethral stricture. J Cell Physiol 2019; 234(12): 23243-55.
[http://dx.doi.org/10.1002/jcp.28891] [PMID: 31144307]
[121]
Pascucci L, Coccè V, Bonomi A, et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Control Release 2014; 192: 262-70.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.042] [PMID: 25084218]
[122]
Gomari H, Forouzandeh Moghadam M, Soleimani M, Ghavami M, Khodashenas S. Targeted delivery of doxorubicin to HER2 positive tumor models. Int J Nanomedicine 2019; 14: 5679-90.
[http://dx.doi.org/10.2147/IJN.S210731] [PMID: 31413568]
[123]
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.
[http://dx.doi.org/10.1038/srep32993] [PMID: 27615560]
[124]
Chen S, Tang Y, Liu Y, et al. Exosomes derived from miR-375-overexpressing human adipose mesenchymal stem cells promote bone regeneration. Cell Prolif 2019; 52(5)e12669
[http://dx.doi.org/10.1111/cpr.12669] [PMID: 31380594]
[125]
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.
[http://dx.doi.org/10.1186/s13287-018-0939-5] [PMID: 29996938]
[126]
Pittenger MF, Mackay AM, Beck SC, et al. Multilineage Potential of Adult Human Mesenchymal Stem Cells. Science 1999; 284(5411): 143-7.
[127]
Embryonic . Stem Cell-Derived Mesenchymal Stem Cells (MSCs) Have a Superior Neuroprotective Capacity Over Fetal MSCs in the Hypoxic-Ischemic Mouse Brain. Stem Cells Transl Med 2018; 7(5): 439-49.findit.library.jhu.edu/resolve?sid=EMBASE&issn=21576580&id=doi:10.1002%2Fsctm.17-0260& atitle=Embryonic+Stem+Cell-Derived+Mesenchymal+Stem+Cells+%28MSCs%29+Have+a+Superior+Neuroprotective+Capacity+Over+Fetal+MSCs+in+the+Hypoxic-Ischemic+Mouse+Brain&stitle=Stem+Cells+Transl.+Med.&title=Stem+Cells+Translational+Medicine&volume=7&issue=5&spage=439&epage=449&aulast=Hawkins&aufirst=Kate+E.&auinit=K.E.&aufull=Hawkins+K.E.&coden=&isbn=&pages=439-449 & date=2018 & auinit1=K&
[128]
Zhang S, Chuah SJ, Lai RC, Hui JHP, Lim SK, Toh WS. MSC exosomes mediate cartilage repair by enhancing proliferation, attenuating apoptosis and modulating immune reactivity. Biomaterials 2018; 156: 16-27.
[http://dx.doi.org/10.1016/j.biomaterials.2017.11.028] [PMID: 29182933]
[129]
Zhang B, Yin Y, Lai RC, Tan SS, Choo ABH, Lim SK. Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev 2014; 23(11): 1233-44.
[http://dx.doi.org/10.1089/scd.2013.0479] [PMID: 24367916]
[130]
Hollands P, Aboyeji D, Orcharton M. Dental pulp stem cells in regenerative medicine. Br Dent J 2018; 224(9): 747-50.
[http://dx.doi.org/10.1038/sj.bdj.2018.348] [PMID: 29725075]
[131]
Miura M, Gronthos S, Zhao M, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100(10): 5807-12.
[http://dx.doi.org/10.1073/pnas.0937635100] [PMID: 12716973]
[132]
Stanko P, Altanerova U, Jakubechova J, Repiska V, Altaner C. Dental Mesenchymal Stem/Stromal Cells and Their Exosomes. Stem Cells Int 2018; 20188973613
[http://dx.doi.org/10.1155/2018/8973613] [PMID: 29760738]
[133]
Rasulov MF, Vasilchenkov AV, Onishchenko NA, et al. First experience of the use bone marrow mesenchymal stem cells for the treatment of a patient with deep skin burns. Bull Exp Biol Med 2005; 139(1): 141-4.
[http://dx.doi.org/10.1007/s10517-005-0232-3] [PMID: 16142297]
[134]
Kadar K, Kiraly M, Porcsalmy B, et al. Differentiation potential of stem cells from human dental origin - promise for tissue engineering. J Physiol Pharmacol 2009; 60(Suppl. 7): 167-75.
[PMID: 20388961]
[135]
Clarke D L, Johansson C B, Wilbertz J, et al. Generalized Potential of Adult Neural Stem Cells Science (80- ) 2000.
[136]
Mortada I, Mortada R, Al Bazzal M. Dental Pulp Stem Cells and Neurogenesis. Advances in Experimental Medicine and Biology 2018; 1083: 63-75.
[137]
Angulski ABB, Capriglione LG, Batista M, et al. The Protein Content of Extracellular Vesicles Derived from Expanded Human Umbilical Cord Blood-Derived CD133+ and Human Bone Marrow-Derived Mesenchymal Stem Cells Partially Explains Why Both Sources Are Advantageous for Regenerative Medicine. Stem Cell Rev Reports 2017; 13(2): 244-57.
[http://dx.doi.org/10.1007/s12015-016-9715-z]
[138]
Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007; 8(6): 464-78.
[http://dx.doi.org/10.1038/nrm2183] [PMID: 17522591]
[139]
Ribeiro MF, Zhu H, Millard RW, Fan GC. Exosomes Function in Pro- and Anti-Angiogenesis. Curr Angiogenes 2013; 2(1): 54-9.
[http://dx.doi.org/10.2174/22115528113020020001] [PMID: 25374792]
[140]
Adair TH, Montani J-P. Angiogenesis 2010.
[141]
Zhang HC, Liu XB, Huang S, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells Dev 2012; 21(18): 3289-97.
[http://dx.doi.org/10.1089/scd.2012.0095] [PMID: 22839741]
[142]
Nazari-Shafti TZ, Neuber S, Garcia Duran A, et al. Human mesenchymal stromal cells and derived extracellular vesicles: Translational strategies to increase their proangiogenic potential for the treatment of cardiovascular disease. Stem Cells Transl Med 2020; 9(12): 1558-69.
[http://dx.doi.org/10.1002/sctm.19-0432] [PMID: 32761804]
[143]
Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005; 438(7070): 937-45.
[http://dx.doi.org/10.1038/nature04479] [PMID: 16355211]
[144]
Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006; 7(5): 359-71.
[http://dx.doi.org/10.1038/nrm1911] [PMID: 16633338]
[145]
Chade AR, Stewart N. Angiogenic cytokines in renovascular disease: do they have potential for therapeutic use? J Am Soc Hypertens 2013; 7(2): 180-90.
[http://dx.doi.org/10.1016/j.jash.2013.01.004] [PMID: 23428409]
[146]
Tan CY, Lai RC, Wong W, Dan YY, Lim SK, Ho HK. Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res Ther 2014; 5(3): 76.
[http://dx.doi.org/10.1186/scrt465] [PMID: 24915963]
[147]
Li W, Xu H, Qian C. c-Kit-Positive Adipose Tissue-Derived Mesenchymal Stem Cells Promote the Growth and Angiogenesis of Breast Cancer. BioMed Res Int 2017; 20177407168
[http://dx.doi.org/10.1155/2017/7407168] [PMID: 28573141]
[148]
Lopatina T, Bruno S, Tetta C, Kalinina N, Porta M, Camussi G. Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential. Cell Commun Signal 2014; 12: 26.
[http://dx.doi.org/10.1186/1478-811X-12-26] [PMID: 24725987]
[149]
Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008; 79(4): 581-8.
[http://dx.doi.org/10.1093/cvr/cvn156] [PMID: 18550634]
[150]
Chen TS, Lai RC, Lee MM, Choo ABH, Lee CN, Lim SK. Mesenchymal Stem Cell Secretes Microparticles Enriched in Pre-MicroRNAs. Nucleic Acids Res 2009.
[http://dx.doi.org/10.1093/nar/gkp857] [PMID: 19850715]
[151]
Baglio SR, Rooijers K, Koppers-Lalic D, et al. Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species. Stem Cell Res Ther 2015; 6: 127.
[http://dx.doi.org/10.1186/s13287-015-0116-z] [PMID: 26129847]
[152]
Yoo JK, Kim J, Choi SJ, et al. Discovery and characterization of novel microRNAs during endothelial differentiation of human embryonic stem cells. Stem Cells Dev 2012; 21(11): 2049-57.
[http://dx.doi.org/10.1089/scd.2011.0500] [PMID: 22142236]
[153]
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.
[http://dx.doi.org/10.1159/000438594] [PMID: 26646808]
[154]
Ma Y, Bao-Han W, Lv X, et al. MicroRNA-34a mediates the autocrine signaling of PAR2-activating proteinase and its role in colonic cancer cell proliferation. PLoS One 2013; 8(8)e72383
[http://dx.doi.org/10.1371/journal.pone.0072383] [PMID: 23991105]
[155]
Gong XH, Liu H, Wang SJ, Liang SW, Wang GG. Exosomes derived from SDF1-overexpressing mesenchymal stem cells inhibit ischemic myocardial cell apoptosis and promote cardiac endothelial microvascular regeneration in mice with myocardial infarction. J Cell Physiol 2019; 234(8): 13878-93.
[http://dx.doi.org/10.1002/jcp.28070] [PMID: 30720220]
[156]
Zhang Z, Yang J, Yan W, Li Y, Shen Z, Asahara T. Pretreatment of Cardiac Stem Cells With Exosomes Derived From Mesenchymal Stem Cells Enhances Myocardial Repair. J Am Heart Assoc 2016; 5(1)e002856
[http://dx.doi.org/10.1161/JAHA.115.002856] [PMID: 26811168]
[157]
Ma T, Chen Y, Chen Y, et al. MicroRNA-132, Delivered by Mesenchymal Stem Cell-Derived Exosomes, Promote Angiogenesis in Myocardial Infarction. Stem Cells Int 2018; 20183290372
[http://dx.doi.org/10.1155/2018/3290372] [PMID: 30271437]
[158]
Fan ZG, Qu XL, Chu P, et al. MicroRNA-210 promotes angiogenesis in acute myocardial infarction. Mol Med Rep 2018; 17(4): 5658-65.
[http://dx.doi.org/10.3892/mmr.2018.8620] [PMID: 29484401]
[159]
Jakob P, Doerries C, Briand S, et al. Loss of angiomiR-126 and 130a in angiogenic early outgrowth cells from patients with chronic heart failure: role for impaired in vivo neovascularization and cardiac repair capacity. Circulation 2012; 126(25): 2962-75.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.093906] [PMID: 23136161]
[160]
Gross JC, Chaudhary V, Bartscherer K, Boutros M. Active Wnt proteins are secreted on exosomes. Nat Cell Biol 2012; 14(10): 1036-45.
[http://dx.doi.org/10.1038/ncb2574] [PMID: 22983114]
[161]
Pate KT, Stringari C, Sprowl-Tanio S, et al. Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer. EMBO J 2014; 33(13): 1454-73.
[http://dx.doi.org/10.15252/embj.201488598] [PMID: 24825347]
[162]
Zhang B, Wu X, Zhang X, et al. Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the Wnt4/β-catenin pathway. Stem Cells Transl Med 2015; 4(5): 513-22.
[http://dx.doi.org/10.5966/sctm.2014-0267] [PMID: 25824139]
[163]
Lee JK, Park SR, Jung BK, et al. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One 2013; 8(12)e84256
[http://dx.doi.org/10.1371/journal.pone.0084256] [PMID: 24391924]
[164]
Nishida N, Yano H, Nishida T, Kamura T, Kojiro M. Angiogenesis in cancer. Vasc Health Risk Manag 2006; 2(3): 213-9.
[http://dx.doi.org/10.2147/vhrm.2006.2.3.213] [PMID: 17326328]
[165]
Taraboletti G, D’Ascenzo S, Borsotti P, Giavazzi R, Pavan A, Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 2002; 160(2): 673-80.
[http://dx.doi.org/10.1016/S0002-9440(10)64887-0] [PMID: 11839588]
[166]
Millimaggi D, Mari M, D’Ascenzo S, et al. Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 2007; 9(4): 349-57.
[http://dx.doi.org/10.1593/neo.07133] [PMID: 17460779]
[167]
Boni R, Ali A, Shavandi A, Clarkson AN. Current and novel polymeric biomaterials for neural tissue engineering. J Biomed Sci 2018; 25(1): 90.
[http://dx.doi.org/10.1186/s12929-018-0491-8] [PMID: 30572957]
[168]
Faroni A, Mobasseri SA, Kingham PJ, Reid AJ. Peripheral nerve regeneration: experimental strategies and future perspectives. Adv Drug Deliv Rev 2015; 82-83: 160-7.
[http://dx.doi.org/10.1016/j.addr.2014.11.010] [PMID: 25446133]
[169]
Bailey SB, Eichler ME, Villadiego A, Rich KM. The influence of fibronectin and laminin during Schwann cell migration and peripheral nerve regeneration through silicon chambers. J Neurocytol 1993; 22(3): 176-84.
[http://dx.doi.org/10.1007/BF01246356] [PMID: 8478639]
[170]
Frostick SP, Yin Q, Kemp GJ. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 1998; 18(7): 397-405.
[http://dx.doi.org/10.1002/(SICI)1098-2752(1998)18:7<397: AID-MICR2>3.0.CO;2-F] [PMID: 9880154]
[171]
Mao Q, Nguyen PD, Shanti RM, et al. Gingiva-Derived Mesenchymal Stem Cell-Extracellular Vesicles Activate Schwann Cell Repair Phenotype and Promote Nerve Regeneration. Tissue Eng Part A 2019; 25(11-12): 887-900.
[http://dx.doi.org/10.1089/ten.tea.2018.0176] [PMID: 30311853]
[172]
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 Reports 2017.
[http://dx.doi.org/10.1007/s12015-016-9713-1]
[173]
Qing L, Chen H, Tang J, Jia X. Exosomes and Their MicroRNA Cargo: New Players in Peripheral Nerve Regeneration. Neurorehabil Neural Repair 2018; 32(9): 765-76.
[http://dx.doi.org/10.1177/1545968318798955] [PMID: 30223738]
[174]
Verma P, Augustine GJ, Ammar MR, Tashiro A, Cohen SM. A neuroprotective role for microRNA miR-1000 mediated by limiting glutamate excitotoxicity. Nat Neurosci 2015; 18(3): 379-85.
[http://dx.doi.org/10.1038/nn.3935] [PMID: 25643297]
[175]
Vallabhaneni KC, Penfornis P, Dhule S, et al. Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget 2015; 6(7): 4953-67.
[http://dx.doi.org/10.18632/oncotarget.3211] [PMID: 25669974]
[176]
Pusic AD, Kraig RP. Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination. Glia 2014; 62(2): 284-99.
[http://dx.doi.org/10.1002/glia.22606] [PMID: 24339157]
[177]
Xin H, Li Y, Liu Z, et al. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. Stem Cells 2013; 31(12): 2737-46.
[http://dx.doi.org/10.1002/stem.1409] [PMID: 23630198]
[178]
Ma Y, Ge S, Zhang J, et al. Mesenchymal stem cell-derived extracellular vesicles promote nerve regeneration after sciatic nerve crush injury in rats. Int J Clin Exp Pathol 2017; 10(9): 10032-9.
[PMID: 31966893]
[179]
Lopez-Verrilli MA, Caviedes A, Cabrera A, Sandoval S, Wyneken U, Khoury M. Mesenchymal stem cell-derived exosomes from different sources selectively promote neuritic outgrowth. Neuroscience 2016; 320: 129-39.
[http://dx.doi.org/10.1016/j.neuroscience.2016.01.061] [PMID: 26851773]
[180]
Lopez-Verrilli MA, Picou F, Court FA. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia 2013; 61(11): 1795-806.
[http://dx.doi.org/10.1002/glia.22558] [PMID: 24038411]
[181]
Court FA, Midha R, Cisterna BA, et al. Morphological evidence for a transport of ribosomes from Schwann cells to regenerating axons. Glia 2011; 59(10): 1529-39.
[http://dx.doi.org/10.1002/glia.21196] [PMID: 21656857]
[182]
Farinazzo A, Turano E, Marconi S, Bistaffa E, Bazzoli E, Bonetti B. Murine adipose-derived mesenchymal stromal cell vesicles: in vitro clues for neuroprotective and neuro-regenerative approaches. Cytotherapy 2015; 17(5): 571-8.
[http://dx.doi.org/10.1016/j.jcyt.2015.01.005] [PMID: 25743633]
[183]
Bucan V, Vaslaitis D, Peck CT, Strauß S, Vogt PM, Radtke C. Effect of Exosomes from Rat Adipose-Derived Mesenchymal Stem Cells on Neurite Outgrowth and Sciatic Nerve Regeneration After Crush Injury. Mol Neurobiol 2019; 56(3): 1812-24.
[http://dx.doi.org/10.1007/s12035-018-1172-z] [PMID: 29931510]
[184]
Zhang H, Qiu X, Shindel AW, et al. Adipose tissue-derived stem cells ameliorate diabetic bladder dysfunction in a type II diabetic rat model. Stem Cells Dev 2012; 21(9): 1391-400.
[http://dx.doi.org/10.1089/scd.2011.0244] [PMID: 22008016]
[185]
Haertinger M, Weiss T, Mann A, Tabi A, Brandel V, Radtke C. Adipose Stem Cell-Derived Extracellular Vesicles Induce Proliferation of Schwann Cells via Internalization. Cells 2020; 9(1)E163
[http://dx.doi.org/10.3390/cells9010163] [PMID: 31936601]
[186]
Clark K, Zhang S, Barthe S, et al. Placental Mesenchymal Stem Cell-Derived Extracellular Vesicles Promote Myelin Regeneration in an Animal Model of Multiple Sclerosis. Cells 2019; 8(12)E1497
[http://dx.doi.org/10.3390/cells8121497] [PMID: 31771176]
[187]
Li C, Jiao G, Wu W, et al. Exosomes from Bone Marrow Mesenchymal Stem Cells Inhibit Neuronal Apoptosis and Promote Motor Function Recovery via the Wnt/β-catenin Signaling Pathway. Cell Transplant 2019; 28(11): 1373-83.
[http://dx.doi.org/10.1177/0963689719870999] [PMID: 31423807]
[188]
Riazifar M, Mohammadi MR, Pone EJ, et al. Stem Cell-Derived Exosomes as Nanotherapeutics for Autoimmune and Neurodegenerative Disorders. ACS Nano 2019; 13(6): 6670-88.
[http://dx.doi.org/10.1021/acsnano.9b01004] [PMID: 31117376]
[189]
Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372(9648): 1502-17.
[http://dx.doi.org/10.1016/S0140-6736(08)61620-7] [PMID: 18970977]
[190]
Junker A, Krumbholz M, Eisele S, et al. MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 2009; 132(Pt 12): 3342-52.
[http://dx.doi.org/10.1093/brain/awp300] [PMID: 19952055]
[191]
Katsuda T, Tsuchiya R, Kosaka N, et al. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Sci Rep 2013; 3: 1197.
[http://dx.doi.org/10.1038/srep01197] [PMID: 23378928]
[192]
Murphy MP, LeVine H III. Alzheimer’s disease and the amyloid-β peptide. J Alzheimers Dis 2010; 19(1): 311-23.
[http://dx.doi.org/10.3233/JAD-2010-1221] [PMID: 20061647]
[193]
Yasojima K, Akiyama H, McGeer EG, McGeer PL. Reduced neprilysin in high plaque areas of Alzheimer brain: a possible relationship to deficient degradation of β-amyloid peptide. Neurosci Lett 2001; 297(2): 97-100.
[http://dx.doi.org/10.1016/S0304-3940(00)01675-X] [PMID: 11121879]
[194]
Jarmalavičiūtė A, Tunaitis V, Pivoraitė U, Venalis A, Pivoriūnas A. Exosomes from dental pulp stem cells rescue human dopaminergic neurons from 6-hydroxy-dopamine-induced apoptosis. Cytotherapy 2015; 17(7): 932-9.
[http://dx.doi.org/10.1016/j.jcyt.2014.07.013] [PMID: 25981557]
[195]
Chen KH, Chen CH, Wallace CG, et al. Intravenous administration of xenogenic adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes markedly reduced brain infarct volume and preserved neurological function in rat after acute ischemic stroke. Oncotarget 2016; 7(46): 74537-56.
[http://dx.doi.org/10.18632/oncotarget.12902] [PMID: 27793019]
[196]
Perugorria MJ, Olaizola P, Banales JM. Cholangiocyte-to-Hepatocyte Differentiation: A Context-Dependent Process and an Opportunity for Regenerative Medicine. Hepatology 2019; 69(2): 480-3.
[http://dx.doi.org/10.1002/hep.30305] [PMID: 30296341]
[197]
Nojima H, Freeman CM, Schuster RM, et al. Hepatocyte exosomes mediate liver repair and regeneration via sphingosine-1-phosphate. J Hepatol 2016; 64(1): 60-8.
[http://dx.doi.org/10.1016/j.jhep.2015.07.030] [PMID: 26254847]
[198]
HucMSC Exosome-Derived GPX1 Is Required for the Recovery of Hepatic Oxidant Injury. Mol Ther 2017.http://sfx.metabib.ch/sfx_locater?sid=EMBASE&issn=15250024&id=doi:10.1016%2Fj.ymthe.2016.11.019&atitle=hucMSC+Exosome-Derived+GPX1+Is+Required+for+the+Recovery+of+Hepatic+Oxidant+Injury&stitle=Mol.+Ther.&title=Molecular+Therapy&volume=25&issue=2&spage=465&epage=479&aulast=Yan&aufirst=Yongmin&auinit=Y.&aufull=Yan+Y.&coden=MTOHC&isbn=&pages=465-479&date=2017&auinit1=Y&auinitm=
[199]
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.
[http://dx.doi.org/10.1089/scd.2012.0395] [PMID: 23002959]
[200]
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.
[http://dx.doi.org/10.1002/sctm.16-0226] [PMID: 28213967]
[201]
Mullet J, and Thoene J. Human Adipose Stem Cells Originated Exosomes Improving Survival Rate of Rats with Acute Liver Failure Probably by Releasing IncRNA H19. J Extracell Vesicles 2017.
[http://dx.doi.org/10.1080/20013078.2017.1310414]
[202]
Cho NH, Shaw JE, Karuranga S, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 2018; 138: 271-81.
[http://dx.doi.org/10.1016/j.diabres.2018.02.023] [PMID: 29496507]
[203]
Abecassis M, Bartlett ST, Collins AJ, et al. Kidney transplantation as primary therapy for end-stage renal disease: a National Kidney Foundation/Kidney Disease Outcomes Quality Initiative (NKF/KDOQITM) conference. Clin J Am Soc Nephrol 2008; 3(2): 471-80.
[http://dx.doi.org/10.2215/CJN.05021107] [PMID: 18256371]
[204]
Bruno S, Grange C, Deregibus MC, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 2009; 20(5): 1053-67.
[http://dx.doi.org/10.1681/ASN.2008070798] [PMID: 19389847]
[205]
Alzahrani FA. Melatonin improves therapeutic potential of mesenchymal stem cells-derived exosomes against renal ischemia-reperfusion injury in rats. Am J Transl Res 2019; 11(5): 2887-907.
[PMID: 31217862]
[206]
Reis LA, Borges FT, Simões MJ, Borges AA, Sinigaglia-Coimbra R, Schor N. Bone marrow-derived mesenchymal stem cells repaired but did not prevent gentamicin-induced acute kidney injury through paracrine effects in rats. PLoS One 2012; 7(9)e44092
[http://dx.doi.org/10.1371/journal.pone.0044092] [PMID: 22970165]
[207]
Zhao L, Hu C, Zhang P, Jiang H, Chen J. Genetic communication by extracellular vesicles is an important mechanism underlying stem cell-based therapy-mediated protection against acute kidney injury. Stem Cell Res Ther 2019; 10(1): 119.
[http://dx.doi.org/10.1186/s13287-019-1227-8] [PMID: 30995947]
[208]
Tomasoni S, Longaretti L, Rota C, et al. Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev 2013; 22(5): 772-80.
[http://dx.doi.org/10.1089/scd.2012.0266] [PMID: 23082760]
[209]
Herrera Sanchez MB, Bruno S, Grange C, et al. Human liver stem cells and derived extracellular vesicles improve recovery in a murine model of acute kidney injury. Stem Cell Res Ther 2014; 5(6): 124.
[http://dx.doi.org/10.1186/scrt514] [PMID: 25384729]
[210]
Ranghino A, Bruno S, Bussolati B, et al. The effects of glomerular and tubular renal progenitors and derived extracellular vesicles on recovery from acute kidney injury. Stem Cell Res Ther 2017; 8(1): 24.
[http://dx.doi.org/10.1186/s13287-017-0478-5] [PMID: 28173878]
[211]
Choi HY, Moon SJ, Ratliff BB, et al. Microparticles from kidney-derived mesenchymal stem cells act as carriers of proangiogenic signals and contribute to recovery from acute kidney injury. PLoS One 2014; 9(2)e87853
[http://dx.doi.org/10.1371/journal.pone.0087853] [PMID: 24504266]
[212]
Zhou Y, Xu H, Xu W, et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res Ther 2013; 4(2): 34.
[http://dx.doi.org/10.1186/scrt194] [PMID: 23618405]
[213]
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.
[http://dx.doi.org/10.1186/scrt428] [PMID: 24646750]
[214]
Gu D, Zou X, Ju G, Zhang G, Bao E, Zhu Y. Mesenchymal Stromal Cells Derived Extracellular Vesicles Ameliorate Acute Renal Ischemia Reperfusion Injury by Inhibition of Mitochondrial Fission through miR-30. Stem Cells Int 2016; 20162093940
[http://dx.doi.org/10.1155/2016/2093940] [PMID: 27799943]
[215]
Eirin A, Zhu XY, Puranik AS, et al. Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int 2017; 92(1): 114-24.
[http://dx.doi.org/10.1016/j.kint.2016.12.023] [PMID: 28242034]
[216]
Jiang ZZ, Liu YM, Niu X, et al. Exosomes secreted by human urine-derived stem cells could prevent kidney complications from type I diabetes in rats. Stem Cell Res Ther 2016; 7: 24.
[http://dx.doi.org/10.1186/s13287-016-0287-2] [PMID: 26852014]
[217]
Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature 2008; 453(7193): 314-21.
[http://dx.doi.org/10.1038/nature07039] [PMID: 18480812]
[218]
Badiavas EV, Falanga V. Treatment of chronic wounds with bone marrow-derived cells. Arch Dermatol 2003; 139(4): 510-6.
[http://dx.doi.org/10.1001/archderm.139.4.510] [PMID: 12707099]
[219]
Whitfield ML, George LK, Grant GD, Perou CM. Common markers of proliferation. Nat Rev Cancer 2006; 6(2): 99-106.
[http://dx.doi.org/10.1038/nrc1802] [PMID: 16491069]
[220]
Zhang W, Bai X, Zhao B, et al. Cell-free therapy based on adipose tissue stem cell-derived exosomes promotes wound healing via the PI3K/Akt signaling pathway. Exp Cell Res 2018; 370(2): 333-42.
[http://dx.doi.org/10.1016/j.yexcr.2018.06.035] [PMID: 29964051]
[221]
Merjaneh M, Langlois A, Larochelle S, Cloutier CB, Ricard-Blum S, Moulin VJ. Pro-angiogenic capacities of microvesicles produced by skin wound myofibroblasts. Angiogenesis 2017; 20(3): 385-98.
[http://dx.doi.org/10.1007/s10456-017-9554-9] [PMID: 28391377]
[222]
Ren S, Chen J, Duscher D, et al. Microvesicles from human adipose stem cells promote wound healing by optimizing cellular functions via AKT and ERK signaling pathways. Stem Cell Res Ther 2019; 10(1): 47.
[http://dx.doi.org/10.1186/s13287-019-1152-x] [PMID: 30704535]
[223]
Duscher D, Rennert RC, Januszyk M, et al. Aging disrupts cell subpopulation dynamics and diminishes the function of mesenchymal stem cells. Sci Rep 2014; 4: 7144.
[http://dx.doi.org/10.1038/srep07144] [PMID: 25413454]
[224]
Zhang S, Chu WC, Lai RC, Lim SK, Hui JHP, Toh WS. Exosomes Derived from Human Embryonic Mesenchymal Stem Cells Promote Osteochondral Regeneration. Osteoarthr Cartil 2016.
[225]
Mead B, Tomarev S. Bone Marrow-Derived Mesenchymal Stem Cells-Derived Exosomes Promote Survival of Retinal Ganglion Cells Through miRNA-Dependent Mechanisms. Stem Cells Transl Med 2017; 6(4): 1273-85.
[http://dx.doi.org/10.1002/sctm.16-0428] [PMID: 28198592]
[226]
Mead B, Ahmed Z, Tomarev S. Mesenchymal Stem Cell-Derived Small Extracellular Vesicles Promote Neuroprotection in a Genetic DBA/2J Mouse Model of Glaucoma. Invest Ophthalmol Vis Sci 2018; 59(13): 5473-80.
[http://dx.doi.org/10.1167/iovs.18-25310] [PMID: 30452601]
[227]
Yu B, Shao H, Su C, et al. Exosomes derived from MSCs ameliorate retinal laser injury partially by inhibition of MCP-1. Sci Rep 2016; 6: 34562.
[http://dx.doi.org/10.1038/srep34562] [PMID: 27686625]
[228]
Zhu LP, Tian T, Wang JY, et al. Hypoxia-elicited mesenchymal stem cell-derived exosomes facilitates cardiac repair through miR-125b-mediated prevention of cell death in myocardial infarction. Theranostics 2018; 8(22): 6163-77.
[http://dx.doi.org/10.7150/thno.28021] [PMID: 30613290]
[229]
Toh WS, Lai RC, Hui JHP, Lim SK. MSC exosome as a cell-free MSC therapy for cartilage regeneration: Implications for osteoarthritis treatment. Semin Cell Dev Biol 2017; 67: 56-64.
[http://dx.doi.org/10.1016/j.semcdb.2016.11.008] [PMID: 27871993]
[230]
Katagiri W, Osugi M, Kawai T, Hibi H. First-in-human study and clinical case reports of the alveolar bone regeneration with the secretome from human mesenchymal stem cells. Head Face Med 2016; 12: 5.
[http://dx.doi.org/10.1186/s13005-016-0101-5] [PMID: 26772731]
[231]
Fukuoka H, Suga H. Hair Regeneration Treatment Using Adipose-Derived Stem Cell Conditioned Medium: Follow-up With Trichograms. Eplasty 2015; 15e10
[PMID: 25834689]
[232]
Shin H, Ryu HH, Kwon O, Park BS, Jo SJ. Clinical use of conditioned media of adipose tissue-derived stem cells in female pattern hair loss: a retrospective case series study. Int J Dermatol 2015; 54(6): 730-5.
[http://dx.doi.org/10.1111/ijd.12650] [PMID: 25777970]
[233]
Ono M, Kosaka N, Tominaga N, et al. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal 2014; 7(332): ra63.
[http://dx.doi.org/10.1126/scisignal.2005231] [PMID: 24985346]

Rights & Permissions Print Cite
Article Metrics
54
3
© 2024 Bentham Science Publishers | Privacy Policy