Login Register Cart 0
Generic placeholder image

Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

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

Roles of Stem Cell Exosomes and their MicroRNA Carrier in Bone and Cartilage Regeneration

Author(s): Dazhi Yang*, Zecai Chen, Zhen Xu, Lei Qin, Weihong Yi and Yufeng Long

Volume 18, Issue 7, 2023

Published on: 15 September, 2022

Page: [917 - 925] Pages: 9

DOI: 10.2174/1574888X17666220817093305

Price: $65

Abstract

Bone and cartilage regeneration is a dynamic and complex process involving multiple cell types, such as osteoblasts, osteoclasts, endothelial cells, etc. Stem cells have been proved to have an efficient capability to promote bone and cartilage regeneration and repair, but the usage of cells harbors some important safety issues, such as immune rejection and carcinogenicity. Exosomes are non-cell structures secreted from various cells. The content of exosomes is enriched with proteins, such as cytoskeleton proteins, adhesion factors, transcription factors, etc., and a variety of nucleic acids, such as mRNA (Messenger RNA), long-chain non-coding RNA, microRNA (miRNA), etc. Exosomes can deliver a variety of contents from the parent cells to the recipient cells in different tissue backgrounds, influencing the phenotype and function of the recipient cells. Recent studies have demonstrated that miRNAs play significant roles in bone formation, suggesting that miRNAs may be novel therapeutic targets for bone and cartilage diseases. Exosomes have been shown with low/no immune rejection in vivo, no carcinogenic risk of infection, nor other side effects. In recent years, stem cell exosomes have been utilized to promote bone and cartilage regeneration processes during bone defect, bone fracture, cartilage repair, osteoporosis, and osteoarthritis. In this review, we discuss different exosomes derived from stem cells and their interactions with target cells, including osteoblasts, chondrocytes and osteoclasts. We also highlight the various signaling pathways involved in stem cell exosome-related bone and cartilage regeneration.

Keywords: Stem cells, Bone regeneration, Exosomes, Osteoblasts, Osteoclasts, Cartilage

« Previous Next »
Graphical Abstract

[1]
Dimitriou R, Jones E, McGonagle D, Giannoudis PV. Bone regeneration: Current concepts and future directions. BMC Med 2011; 9(1): 66.
[http://dx.doi.org/10.1186/1741-7015-9-66] [PMID: 21627784]
[2]
Oryan A, Alidadi S, Moshiri A, Maffulli N. Bone regenerative medicine: Classic options, novel strategies, and future directions. J Orthop Surg Res 2014; 9(1): 18.
[http://dx.doi.org/10.1186/1749-799X-9-18] [PMID: 24628910]
[3]
Baldwin P, Li DJ, Auston DA, Mir HS, Yoon RS, Koval KJ. Autograft, allograft, and bone graft substitutes: Clinical evidence and indications for use in the setting of orthopaedic trauma surgery. J Orthop Trauma 2019; 33(4): 203-13.
[http://dx.doi.org/10.1097/BOT.0000000000001420] [PMID: 30633080]
[4]
Hegde C, Shetty V, Wasnik S, Ahammed I, Shetty V. Use of bone graft substitute in the treatment for distal radius fractures in elderly. Eur J Orthop Surg Traumatol 2013; 23(6): 651-6.
[http://dx.doi.org/10.1007/s00590-012-1057-1] [PMID: 23412190]
[5]
Stahl A, Yang YP. Regenerative approaches for the treatment of large bone defects. Tissue Eng Part B Rev 2021; 27(6): 539-47.
[http://dx.doi.org/10.1089/ten.teb.2020.0281] [PMID: 33138705]
[6]
Sohn HS, Oh JK. Review of bone graft and bone substitutes with an emphasis on fracture surgeries. Biomater Res 2019; 23(1): 9.
[http://dx.doi.org/10.1186/s40824-019-0157-y] [PMID: 30915231]
[7]
Walmsley GG, Ransom RC, Zielins ER, et al. Stem cells in bone regeneration. Stem Cell Rev Rep 2016; 12(5): 524-9.
[http://dx.doi.org/10.1007/s12015-016-9665-5] [PMID: 27250635]
[8]
Sharma P, Kumar P, Sharma R, Bhatt VD, Dhot PS. Tissue engineering; current status & futuristic scope. J Med Life 2019; 12(3): 225-9.
[http://dx.doi.org/10.25122/jml-2019-0032] [PMID: 31666821]
[9]
Ekeland AG, Bowes A, Flottorp S. Effectiveness of telemedicine: A systematic review of reviews. Int J Med Inform 2010; 79(11): 736-71.
[http://dx.doi.org/10.1016/j.ijmedinf.2010.08.006] [PMID: 20884286]
[10]
Wu X, Showiheen SAA, Sun AR, et al. Exosomes extraction and identification. Methods Mol Biol 2019; 2054: 81-91.
[http://dx.doi.org/10.1007/978-1-4939-9769-5_4] [PMID: 31482448]
[11]
Kusuma GD, Carthew J, Lim R, Frith JE. Effect of the microenvironment on mesenchymal stem cell paracrine signaling: Opportunities to engineer the therapeutic effect. Stem Cells Dev 2017; 26(9): 617-31.
[http://dx.doi.org/10.1089/scd.2016.0349] [PMID: 28186467]
[12]
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(1): 127.
[http://dx.doi.org/10.1186/s13287-015-0116-z] [PMID: 26129847]
[13]
Qin Y, Wang L, Gao Z, Chen G, Zhang C. Bone marrow stromal/stem cell-derived extracellular vesicles regulate osteoblast activity and differentiation in vitro and promote bone regeneration in vivo. Sci Rep 2016; 6(1): 21961.
[http://dx.doi.org/10.1038/srep21961] [PMID: 26911789]
[14]
Chen C, Wang D, Moshaverinia A, et al. Mesenchymal stem cell transplantation in tight-skin mice identifies miR-151-5p as a therapeutic target for systemic sclerosis. Cell Res 2017; 27(4): 559-77.
[http://dx.doi.org/10.1038/cr.2017.11] [PMID: 28106077]
[15]
Tan SHS, Wong JRY, Sim SJY, et al. Mesenchymal stem cell exosomes in bone regenerative strategies-a systematic review of preclinical studies. Mater Today Bio 2020; 7: 100067.
[http://dx.doi.org/10.1016/j.mtbio.2020.100067] [PMID: 32695985]
[16]
Cui Y, Luan J, Li H, Zhou X, Han J. Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microRNA expression. FEBS Lett 2016; 590(1): 185-92.
[http://dx.doi.org/10.1002/1873-3468.12024] [PMID: 26763102]
[17]
Yin K, Wang S, Zhao RC. Exosomes from mesenchymal stem/stromal cells: A new therapeutic paradigm. Biomark Res 2019; 7(1): 8.
[http://dx.doi.org/10.1186/s40364-019-0159-x] [PMID: 30992990]
[18]
Phinney DG, Pittenger MF. Concise review: MSC-derived exosomes for cell-free therapy. Stem Cells 2017; 35(4): 851-8.
[http://dx.doi.org/10.1002/stem.2575] [PMID: 28294454]
[19]
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]
[20]
Ren L, Song ZJ, Cai QW, et al. Adipose mesenchymal stem cell-derived exosomes ameliorate hypoxia/serum deprivation-induced osteocyte apoptosis and osteocyte-mediated osteoclastogenesis in vitro. Biochem Biophys Res Commun 2019; 508(1): 138-44.
[http://dx.doi.org/10.1016/j.bbrc.2018.11.109] [PMID: 30473217]
[21]
Zhang Y, Hao Z, Wang P, et al. Exosomes from human umbilical cord mesenchymal stem cells enhance fracture healing through HIF-1α-mediated promotion of angiogenesis in a rat model of stabilized fracture. Cell Prolif 2019; 52(2): e12570.
[http://dx.doi.org/10.1111/cpr.12570] [PMID: 30663158]
[22]
Yin B, Ma Q, Song C, et al. Exosome-derived noncoding RNAs as a promising treatment of bone regeneration. Stem Cells Int 2021; 2021: 6696894.
[http://dx.doi.org/10.1155/2021/6696894] [PMID: 33542737]
[23]
Pittenger MF, Discher DE, Péault BM, Phinney DG, Hare JM, Caplan AI. Mesenchymal stem cell perspective: Cell biology to clinical progress. NPJ Regen Med 2019; 4(1): 22.
[http://dx.doi.org/10.1038/s41536-019-0083-6] [PMID: 31815001]
[24]
Kaneko T, Sone PP, Zaw SYM, et al. In vivo fate of bone marrow mesenchymal stem cells implanted into rat pulpotomized molars. Stem Cell Res (Amst) 2019; 38: 101457.
[http://dx.doi.org/10.1016/j.scr.2019.101457] [PMID: 31082676]
[25]
Paspaliaris V, Kolios G. Stem cells in Osteoporosis: From biology to new therapeutic approaches. Stem Cells Int 2019; 2019: 1730978.
[http://dx.doi.org/10.1155/2019/1730978] [PMID: 31281368]
[26]
Murphy MP, Koepke LS, Lopez MT, et al. Articular cartilage regeneration by activated skeletal stem cells. Nat Med 2020; 26(10): 1583-92.
[http://dx.doi.org/10.1038/s41591-020-1013-2] [PMID: 32807933]
[27]
Baba S, Yamada Y, Komuro A, et al. Phase I/II trial of autologous bone marrow stem cell transplantation with a three-dimensional woven-fabric scaffold for periodontitis. Stem Cells Int 2016; 2016: 6205910.
[http://dx.doi.org/10.1155/2016/6205910] [PMID: 27990164]
[28]
Okano H, Nakamura M, Yoshida K, et al. Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 2013; 112(3): 523-33.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.256149] [PMID: 23371901]
[29]
Tan Y, Ooi S, Wang L. Immunogenicity and tumorigenicity of pluripotent stem cells and their derivatives: Genetic and epigenetic perspectives. Curr Stem Cell Res Ther 2014; 9(1): 63-72.
[http://dx.doi.org/10.2174/1574888X113086660068] [PMID: 24160683]
[30]
Charron D, Suberbielle-Boissel C, Al-Daccak R. Immunogenicity and allogenicity: A challenge of stem cell therapy. J Cardiovasc Transl Res 2009; 2(1): 130-8.
[http://dx.doi.org/10.1007/s12265-008-9062-9] [PMID: 20559977]
[31]
Lee AS, Tang C, Rao MS, Weissman IL, Wu JC. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med 2013; 19(8): 998-1004.
[http://dx.doi.org/10.1038/nm.3267] [PMID: 23921754]
[32]
Ni Z, Zhou S, Li S, et al. Exosomes: roles and therapeutic potential in osteoarthritis. Bone Res 2020; 8(1): 25.
[http://dx.doi.org/10.1038/s41413-020-0100-9] [PMID: 32596023]
[33]
He X, Dong Z, Cao Y, et al. MSC-derived exosome promotes M2 polarization and enhances cutaneous wound healing. Stem Cells Int 2019; 2019: 7132708.
[http://dx.doi.org/10.1155/2019/7132708] [PMID: 31582986]
[34]
Yaghoubi Y, Movassaghpour A, Zamani M, Talebi M, Mehdizadeh A, Yousefi M. Human umbilical cord mesenchymal stem cells derived-exosomes in diseases treatment. Life Sci 2019; 233: 116733.
[http://dx.doi.org/10.1016/j.lfs.2019.116733] [PMID: 31394127]
[35]
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.
[http://dx.doi.org/10.1186/s13287-017-0632-0] [PMID: 28807034]
[36]
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.
[http://dx.doi.org/10.1016/j.joca.2016.06.022] [PMID: 27390028]
[37]
Jeon OH, Panicker LM, Lu Q, Chae JJ, Feldman RA, Elisseeff JH. Human iPSC-derived osteoblasts and osteoclasts together promote bone regeneration in 3D biomaterials. Sci Rep 2016; 6(1): 26761.
[http://dx.doi.org/10.1038/srep26761] [PMID: 27225733]
[38]
Zhao P, Xiao L, Peng J, Qian YQ, Huang CC. Exosomes derived from bone marrow mesenchymal stem cells improve osteoporosis through promoting osteoblast proliferation via MAPK pathway. Eur Rev Med Pharmacol Sci 2018; 22(12): 3962-70.
[http://dx.doi.org/10.26355/eurrev_201806_15280] [PMID: 29949171]
[39]
Qi X, Zhang J, Yuan H, et al. Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells repair critical-sized bone defects through enhanced angiogenesis and osteogenesis in osteoporotic rats. Int J Biol Sci 2016; 12(7): 836-49.
[http://dx.doi.org/10.7150/ijbs.14809] [PMID: 27313497]
[40]
Lu Z, Wang G, Dunstan CR, Zreiqat H. Short-term exposure to tumor necrosis factor-alpha enables human osteoblasts to direct adipose tissue-derived mesenchymal stem cells into osteogenic differentiation. Stem Cells Dev 2012; 21(13): 2420-9.
[http://dx.doi.org/10.1089/scd.2011.0589] [PMID: 22296271]
[41]
Lu Z, Chen Y, Dunstan C, Roohani-Esfahani S, Zreiqat H. Priming adipose stem cells with tumor necrosis factor-alpha preconditioning potentiates their exosome efficacy for bone regeneration. Tissue Eng Part A 2017; 23(21-22): 1212-20.
[http://dx.doi.org/10.1089/ten.tea.2016.0548] [PMID: 28346798]
[42]
Liu W, Li L, Rong Y, et al. Hypoxic mesenchymal stem cell-derived exosomes promote bone fracture healing by the transfer of miR-126. Acta Biomater 2020; 103: 196-212.
[http://dx.doi.org/10.1016/j.actbio.2019.12.020] [PMID: 31857259]
[43]
Wu L, Leijten JC, Georgi N, Post JN, van Blitterswijk CA, Karperien M. Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation. Tissue Eng Part A 2011; 17(9-10): 1425-36.
[http://dx.doi.org/10.1089/ten.tea.2010.0517] [PMID: 21247341]
[44]
Cosenza S, Ruiz M, Toupet K, Jorgensen C, Noël D. Mesenchymal stem cells derived exosomes and microparticles protect cartilage and bone from degradation in osteoarthritis. Sci Rep 2017; 7(1): 16214.
[http://dx.doi.org/10.1038/s41598-017-15376-8] [PMID: 29176667]
[45]
Cosenza S, Toupet K, Maumus M, et al. Mesenchymal stem cells-derived exosomes are more immunosuppressive than microparticles in inflammatory arthritis. Theranostics 2018; 8(5): 1399-410.
[http://dx.doi.org/10.7150/thno.21072] [PMID: 29507629]
[46]
Wu L, Prins HJ, Helder MN, van Blitterswijk CA, Karperien M. Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources. Tissue Eng Part A 2012; 18(15-16): 1542-51.
[http://dx.doi.org/10.1089/ten.tea.2011.0715] [PMID: 22429306]
[47]
Mianehsaz E, Mirzaei HR, Mahjoubin-Tehran M, et al. Mesenchymal stem cell-derived exosomes: A new therapeutic approach to osteoarthritis? Stem Cell Res Ther 2019; 10(1): 340.
[http://dx.doi.org/10.1186/s13287-019-1445-0] [PMID: 31753036]
[48]
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]
[49]
Mao G, Zhang Z, Hu S, et al. Exosomes derived from miR-92a-3p-overexpressing human mesenchymal stem cells enhance chondrogenesis and suppress cartilage degradation via targeting WNT5A. Stem Cell Res Ther 2018; 9(1): 247.
[http://dx.doi.org/10.1186/s13287-018-1004-0] [PMID: 30257711]
[50]
Qi H, Liu DP, Xiao DW, Tian DC, Su YW, Jin SF. Exosomes derived from mesenchymal stem cells inhibit mitochondrial dysfunction-induced apoptosis of chondrocytes via p38, ERK, and Akt pathways. In Vitro Cell Dev Biol Anim 2019; 55(3): 203-10.
[http://dx.doi.org/10.1007/s11626-019-00330-x] [PMID: 30783864]
[51]
He L, Chen Y, Ke Z, et al. Exosomes derived from miRNA-210 overexpressing bone marrow mesenchymal stem cells protect lipopolysaccharide induced chondrocytes injury via the NF-κB pathway. Gene 2020; 751: 144764.
[http://dx.doi.org/10.1016/j.gene.2020.144764] [PMID: 32428694]
[52]
Liu Y, Zou R, Wang Z, Wen C, Zhang F, Lin F. Exosomal KLF3-AS1 from hMSCs promoted cartilage repair and chondrocyte proliferation in osteoarthritis. Biochem J 2018; 475(22): 3629-38.
[http://dx.doi.org/10.1042/BCJ20180675] [PMID: 30341166]
[53]
Zhang Z, Huang G, Mao G, Hu S. Characterization of exosomal long non-coding RNAs in chondrogenic differentiation of human adipose-derived stem cells. Mol Cell Biochem 2021; 476(3): 1411-20.
[http://dx.doi.org/10.1007/s11010-020-04003-2] [PMID: 33389494]
[54]
Wang X, Thomsen P. Mesenchymal stem cell-derived small extracellular vesicles and bone regeneration. Basic Clin Pharmacol Toxicol 2021; 128(1): 18-36.
[http://dx.doi.org/10.1111/bcpt.13478] [PMID: 32780530]
[55]
Otsuru S, Desbourdes L, Guess AJ, et al. Extracellular vesicles released from mesenchymal stromal cells stimulate bone growth in osteogenesis imperfecta. Cytotherapy 2018; 20(1): 62-73.
[http://dx.doi.org/10.1016/j.jcyt.2017.09.012] [PMID: 29107738]
[56]
Xu R, Shen X, Si Y, et al. MicroRNA-31a-5p from aging BMSCs links bone formation and resorption in the aged bone marrow microenvironment. Aging Cell 2018; 17(4): e12794.
[http://dx.doi.org/10.1111/acel.12794] [PMID: 29896785]
[57]
Rather HA, Jhala D, Vasita R. Dual functional approaches for osteogenesis coupled angiogenesis in bone tissue engineering. Mater Sci Eng C 2019; 103: 109761.
[http://dx.doi.org/10.1016/j.msec.2019.109761] [PMID: 31349418]
[58]
Furuta T, Miyaki S, Ishitobi H, et al. Mesenchymal stem cell-derived exosomes promote fracture healing in a mouse model. Stem Cells Transl Med 2016; 5(12): 1620-30.
[http://dx.doi.org/10.5966/sctm.2015-0285] [PMID: 27460850]
[59]
Zuo R, Kong L, Wang M, et al. Exosomes derived from human CD34+ stem cells transfected with miR-26a prevent glucocorticoid-induced osteonecrosis of the femoral head by promoting angiogenesis and osteogenesis. Stem Cell Res Ther 2019; 10(1): 321.
[http://dx.doi.org/10.1186/s13287-019-1426-3] [PMID: 31730486]
[60]
Liu L, Yu F, Li L, et al. Bone marrow stromal cells stimulated by strontium-substituted calcium silicate ceramics: Release of exosomal miR-146a regulates osteogenesis and angiogenesis. Acta Biomater 2021; 119: 444-57.
[http://dx.doi.org/10.1016/j.actbio.2020.10.038] [PMID: 33129987]
[61]
Gu C, Feng J, Waqas A, et al. Technological advances of 3D scaffold-based stem cell/exosome therapy in tissues and organs. Front Cell Dev Biol 2021; 9: 709204.
[http://dx.doi.org/10.3389/fcell.2021.709204] [PMID: 34568322]
[62]
Swanson WB, Zhang Z, Xiu K, et al. Scaffolds with controlled release of pro-mineralization exosomes to promote craniofacial bone healing without cell transplantation. Acta Biomater 2020; 118: 215-32.
[http://dx.doi.org/10.1016/j.actbio.2020.09.052] [PMID: 33065285]
[63]
Li W, Liu Y, Zhang P, et al. Tissue-engineered bone immobilized with human adipose stem cells-derived exosomes promotes bone regeneration. ACS Appl Mater Interfaces 2018; 10(6): 5240-54.
[http://dx.doi.org/10.1021/acsami.7b17620] [PMID: 29359912]
[64]
Liu X, Yang Y, Li Y, et al. Integration of stem cell-derived exosomes with in situ hydrogel glue as a promising tissue patch for articular cartilage regeneration. Nanoscale 2017; 9(13): 4430-8.
[http://dx.doi.org/10.1039/C7NR00352H] [PMID: 28300264]
[65]
Yoon SJ, Yoo Y, Nam SE, et al. The cocktail effect of BMP-2 and TGF-β1 loaded in visible light-cured glycol chitosan hydrogels for the enhancement of bone formation in a rat tibial defect model. Mar Drugs 2018; 16(10): 16.
[http://dx.doi.org/10.3390/md16100351] [PMID: 30257482]
[66]
Chen P, Zheng L, Wang Y, et al. Desktop-stereolithography 3D printing of a radially oriented extracellular matrix/mesenchymal stem cell exosome bioink for osteochondral defect regeneration. Theranostics 2019; 9(9): 2439-59.
[http://dx.doi.org/10.7150/thno.31017] [PMID: 31131046]
[67]
Shang F, Yu Y, Liu S, et al. Advancing application of mesenchymal stem cell-based bone tissue regeneration. Bioact Mater 2020; 6(3): 666-83.
[http://dx.doi.org/10.1016/j.bioactmat.2020.08.014] [PMID: 33005830]
[68]
Brennan MÁ, Layrolle P, Mooney DJ. Biomaterials functionalized with MSC secreted extracellular vesicles and soluble factors for tissue regeneration. Adv Funct Mater 2020; 30(37): 30.
[http://dx.doi.org/10.1002/adfm.201909125] [PMID: 32952493]
[69]
Hade MD, Suire CN, Suo Z. Mesenchymal stem cell-derived exosomes: Applications in regenerative medicine. Cells 2021; 10(8): 10.
[http://dx.doi.org/10.3390/cells10081959] [PMID: 34440728]
[70]
Huang J, Xiong J, Yang L, Zhang J, Sun S, Liang Y. Cell-free exosome-laden scaffolds for tissue repair. Nanoscale 2021; 13(19): 8740-50.
[http://dx.doi.org/10.1039/D1NR01314A] [PMID: 33969373]
[71]
Sun Y, Liu G, Zhang K, Cao Q, Liu T, Li J. Mesenchymal stem cells-derived exosomes for drug delivery. Stem Cell Res Ther 2021; 12(1): 561.
[http://dx.doi.org/10.1186/s13287-021-02629-7] [PMID: 34717769]
[72]
Lu GD, Cheng P, Liu T, Wang Z. BMSC-derived exosomal miR-29a promotes angiogenesis and osteogenesis. Front Cell Dev Biol 2020; 8: 608521.
[http://dx.doi.org/10.3389/fcell.2020.608521] [PMID: 33363169]
[73]
Jia Y, Qiu S, Xu J, Kang Q, Chai Y. Exosomes secreted by young mesenchymal stem cells promote new bone formation during distraction osteogenesis in older rats. Calcif Tissue Int 2020; 106(5): 509-17.
[http://dx.doi.org/10.1007/s00223-019-00656-4] [PMID: 32103287]
[74]
Ying C, Wang R, Wang Z, et al. BMSC-exosomes carry mutant HIF-1α for improving angiogenesis and osteogenesis in critical-sized calvarial defects. Front Bioeng Biotechnol 2020; 8: 565561.
[http://dx.doi.org/10.3389/fbioe.2020.565561] [PMID: 33330411]
[75]
Bei HP, Hung PM, Yeung HL, Wang S, Zhao X. Bone-a-Petite: Engineering exosomes towards bone, osteochondral, and cartilage repair. Small 2021; 17(50): e2101741.
[http://dx.doi.org/10.1002/smll.202101741] [PMID: 34288410]
[76]
Pendse S, Kale V, Vaidya A. Extracellular vesicles isolated from mesenchymal stromal cells primed with hypoxia: Novel strategy in regenerative medicine. Curr Stem Cell Res Ther 2021; 16(3): 243-61.
[http://dx.doi.org/10.2174/1574888X15999200918110638] [PMID: 32957892]
[77]
Mitchell R, Mellows B, Sheard J, et al. Secretome of adipose-derived mesenchymal stem cells promotes skeletal muscle regeneration through synergistic action of extracellular vesicle cargo and soluble proteins. Stem Cell Res Ther 2019; 10(1): 116.
[http://dx.doi.org/10.1186/s13287-019-1213-1] [PMID: 30953537]
[78]
Nikfarjam S, Rezaie J, Zolbanin NM, Jafari R. Mesenchymal stem cell derived-exosomes: A modern approach in translational medicine. J Transl Med 2020; 18(1): 449.
[http://dx.doi.org/10.1186/s12967-020-02622-3] [PMID: 33246476]
[79]
Huang CC, Kang M, Lu Y, et al. Functionally engineered extracellular vesicles improve bone regeneration. Acta Biomater 2020; 109: 182-94.
[http://dx.doi.org/10.1016/j.actbio.2020.04.017] [PMID: 32305445]
[80]
Li P, Kaslan M, Lee SH, Yao J, Gao Z. Progress in exosome isolation techniques. Theranostics 2017; 7(3): 789-804.
[http://dx.doi.org/10.7150/thno.18133] [PMID: 28255367]
[81]
Marote A, Teixeira FG, Mendes-Pinheiro B, Salgado AJ. MSCs-derived exosomes: Cell-secreted nanovesicles with regenerative potential. Front Pharmacol 2016; 7: 231.
[http://dx.doi.org/10.3389/fphar.2016.00231] [PMID: 27536241]
[82]
González-González A, García-Sánchez D, Dotta M, Rodríguez-Rey JC, Pérez-Campo FM. Mesenchymal stem cells secretome: The cornerstone of cell-free regenerative medicine. World J Stem Cells 2020; 12(12): 1529-52.
[http://dx.doi.org/10.4252/wjsc.v12.i12.1529] [PMID: 33505599]
[83]
Xie Y, Chen Y, Zhang L, Ge W, Tang P. The roles of bone-derived exosomes and exosomal microRNAs in regulating bone remodelling. J Cell Mol Med 2017; 21(5): 1033-41.
[http://dx.doi.org/10.1111/jcmm.13039] [PMID: 27878944]
[84]
Jin Z, Ren J, Qi S. Human bone mesenchymal stem cells-derived exosomes overexpressing microRNA-26a-5p alleviate osteoarthritis via down-regulation of PTGS2. Int Immunopharmacol 2020; 78: 105946.
[http://dx.doi.org/10.1016/j.intimp.2019.105946] [PMID: 31784400]

Rights & Permissions Print Cite
Article Metrics
6
© 2024 Bentham Science Publishers | Privacy Policy