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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Mini-Review Article

Potential Effects of Exosomes and their MicroRNA Carrier on Osteoporosis

Author(s): Qi-Cheng Li, Ci Li, Wei Zhang, Wei Pi and Na Han*

Volume 28, Issue 11, 2022

Published on: 25 March, 2022

Page: [899 - 909] Pages: 11

DOI: 10.2174/1381612828666220128104206

Price: $65

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Abstract

Osteoporosis is a common localized or systemic skeletal illness in the clinic, characterized by bone production weakness and increased bone resorption, resulting in a reduction in bone mineral density (BMD), and affecting mostly postmenopausal women. The risk of osteoporosis or even osteoporotic fracture increases as age increases, putting more pressure on society and families. Although anti-osteoporosis drugs have been developed, some side effects are still observed in the treatment group. Hence the need for more reasonable therapeutic strategies. Exosomes are nanosized extracellular vesicles (EVs) secreted virtually by all types of cells in vivo, which play an important role in intercellular communication. Compared with conventional drugs and stem cells transplantation therapy, exosomes have apparent advantages of lower toxicity and immunogenicity. Exosomes contain many functional molecules, such as proteins, lipids, mRNAs, microRNAs (miRNAs), which can be transferred into recipient cells to regulate a series of signaling pathways and influence physiological and pathological behavior. In this review, we briefly summarize the current knowledge of exosomes and the therapeutic potential of exosomal miRNAs derived from mesenchymal stem cells (MSCs), osteoblasts, osteoclasts, and macrophages in osteoporosis. Finally, a prospect of new treatment strategies for osteoporosis using new biomaterial scaffolds combined with exosomes is also given.

Keywords: Biomaterial scaffolds, bone remodeling, exosomes, intercellular communication, miRNAs, osteoporosis.

[1]
Hadjidakis DJ, Androulakis II. Bone remodeling. Ann N Y Acad Sci 2006; 1092: 385-96.
[http://dx.doi.org/10.1196/annals.1365.035] [PMID: 17308163]
[2]
Michalski MN, McCauley LK. Macrophages and skeletal health. Pharmacol Ther 2017; 174: 43-54.
[http://dx.doi.org/10.1016/j.pharmthera.2017.02.017] [PMID: 28185913]
[3]
Kim JM, Lin C, Stavre Z, Greenblatt MB, Shim JH. Osteoblast-osteoclast communication and bone homeostasis. Cells 2020; 9(9): E2073.
[http://dx.doi.org/10.3390/cells9092073] [PMID: 32927921]
[4]
Jilka RL. Biology of the basic multicellular unit and the pathophysiology of osteoporosis. Med Pediatr Oncol 2003; 41(3): 182-5.
[http://dx.doi.org/10.1002/mpo.10334] [PMID: 12868116]
[5]
Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011; 377(9773): 1276-87.
[http://dx.doi.org/10.1016/S0140-6736(10)62349-5] [PMID: 21450337]
[6]
Curtis EM, Moon RJ, Harvey NC, Cooper C. The impact of fragility fracture and approaches to osteoporosis risk assessment worldwide. Bone 2017; 104: 29-38.
[http://dx.doi.org/10.1016/j.bone.2017.01.024] [PMID: 28119181]
[7]
Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet 2019; 393(10169): 364-76.
[http://dx.doi.org/10.1016/S0140-6736(18)32112-3] [PMID: 30696576]
[8]
Khosla S, Hofbauer LC. Osteoporosis treatment: recent developments and ongoing challenges. Lancet Diabetes Endocrinol 2017; 5(11): 898-907.
[http://dx.doi.org/10.1016/S2213-8587(17)30188-2] [PMID: 28689769]
[9]
Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science 2020; 367(6478): eaau6977.
[http://dx.doi.org/10.1126/science.aau6977] [PMID: 32029601]
[10]
Wang J, Yeung BZ, Cui M. Exosome is a mechanism of intercellular drug transfer: Application of quantitative pharmacology. J Control Release 2017; 268: 147-58.
[11]
Xie X, Xiong Y, Panayi AC, et al. Exosomes as a novel approach to reverse osteoporosis: A review of the literature. Front Bioeng Biotechnol 2020; 8: 594247.
[http://dx.doi.org/10.3389/fbioe.2020.594247] [PMID: 33195163]
[12]
Hu X, Zhong Y, Kong Y, Chen Y, Feng J, Zheng J. Lineage-specific exosomes promote the odontogenic differentiation of human dental pulp stem cells (DPSCs) through TGFβ1/smads signaling pathway via transfer of microRNAs. Stem Cell Res Ther 2019; 10(1): 170.
[http://dx.doi.org/10.1186/s13287-019-1278-x] [PMID: 31196201]
[13]
Liao W, Ning Y, Xu HJ. BMSC-derived exosomes carrying microRNA-122-5p promote proliferation of osteoblasts in osteonecrosis of the femoral head. Clin Sci 2019; 133(18): 1955-75.
[14]
Lan J, Sun L, Xu F, et al. M2 macrophage-derived exosomes promote cell migration and invasion in colon cancer. Cancer Res 2019; 79(1): 146-58.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-0014] [PMID: 30401711]
[15]
Cheng X, Zhang G, Zhang L, et al. Mesenchymal stem cells deliver exogenous miR-21 via exosomes to inhibit nucleus pulposus cell apoptosis and reduce intervertebral disc degeneration. J Cell Mol Med 2018; 22(1): 261-76.
[http://dx.doi.org/10.1111/jcmm.13316] [PMID: 28805297]
[16]
Liu M, Sun Y, Zhang Q. Emerging role of extracellular vesicles in bone remodeling. J Dent Res 2018; 97(8): 859-68.
[http://dx.doi.org/10.1177/0022034518764411] [PMID: 29566346]
[17]
Qiu M, Zhai S, Fu Q, Liu D. Bone marrow mesenchymal stem cells-derived exosomal microRNA-150-3p promotes osteoblast proliferation and differentiation in osteoporosis. Hum Gene Ther 2020.
[PMID: 33107350]
[18]
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]
[19]
Li D, Liu J, Guo B, et al. Osteoclast-derived exosomal miR-214-3p inhibits osteoblastic bone formation. Nat Commun 2016; 7: 10872.
[http://dx.doi.org/10.1038/ncomms10872] [PMID: 26947250]
[20]
Xiong Y, Chen L, Yan C, et al. M2 Macrophagy-derived exosomal miRNA-5106 induces bone mesenchymal stem cells towards osteoblastic fate by targeting salt-inducible kinase 2 and 3. J Nanobiotechnology 2020; 18(1): 66.
[http://dx.doi.org/10.1186/s12951-020-00622-5] [PMID: 32345321]
[21]
Song H, Li X, Zhao Z, et al. Reversal of osteoporotic activity by endothelial cell-secreted bone targeting and biocompatible exosomes. Nano Lett 2019; 19(5): 3040-8.
[http://dx.doi.org/10.1021/acs.nanolett.9b00287] [PMID: 30968694]
[22]
Glaser DL, Kaplan FS. Osteoporosis. Definition and clinical presentation. Spine 1997; 22(24)(Suppl.): 12S-6S.
[http://dx.doi.org/10.1097/00007632-199712151-00003] [PMID: 9431639]
[23]
Chen X, Wang Z, Duan N, Zhu G, Schwarz EM, Xie C. Osteoblast-osteoclast interactions. Connect Tissue Res 2018; 59(2): 99-107.
[http://dx.doi.org/10.1080/03008207.2017.1290085] [PMID: 28324674]
[24]
Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006; 116(5): 1186-94.
[http://dx.doi.org/10.1172/JCI28550] [PMID: 16670759]
[25]
Lambert MNT, Thybo CB, Lykkeboe S, et al. Combined bioavailable isoflavones and probiotics improve bone status and estrogen metabolism in postmenopausal osteopenic women: a randomized controlled trial. Am J Clin Nutr 2017; 106(3): 909-20.
[http://dx.doi.org/10.3945/ajcn.117.153353] [PMID: 28768651]
[26]
Khosla S, Oursler MJ, Monroe DG. Estrogen and the skeleton. Trends Endocrinol Metab 2012; 23(11): 576-81.
[http://dx.doi.org/10.1016/j.tem.2012.03.008] [PMID: 22595550]
[27]
Qadir A, Liang S, Wu Z, Chen Z, Hu L, Qian A. Senile osteoporosis: The involvement of differentiation and senescence of bone marrow stromal cells. Int J Mol Sci 2020; 21(1): E349.
[http://dx.doi.org/10.3390/ijms21010349] [PMID: 31948061]
[28]
Manolagas SC, Parfitt AM. What old means to bone. Trends Endocrinol Metab 2010; 21(6): 369-74.
[http://dx.doi.org/10.1016/j.tem.2010.01.010] [PMID: 20223679]
[29]
Polishuk Z, Kleinhause EM. Treatment of post-menopausal osteoporosis with estrone micro-crystal precipitates. Gynaecologia 1952; 133(1): 1-10.
[PMID: 14927048]
[30]
Bogdonoff MD, Shock NW, Parsons J. The effects of stilbestrol on the retention of nitrogen, calcium, phosphorus, and potassium in aged males with and without osteoporosis. J Gerontol 1954; 9(3): 262-75.
[http://dx.doi.org/10.1093/geronj/9.3.262] [PMID: 13184109]
[31]
Marjoribanks J, Farquhar C, Roberts H, Lethaby A, Lee J. Long-term hormone therapy for perimenopausal and postmenopausal women. Cochrane Database Syst Rev 2017; 1(1): CD004143.
[http://dx.doi.org/10.1002/14651858.CD004143.pub5] [PMID: 28093732]
[32]
Martin TJ. Calcitonin, an update. Bone 1999; 24(5)(Suppl.): 63S-5S.
[http://dx.doi.org/10.1016/S8756-3282(99)00068-X] [PMID: 10321932]
[33]
Silverman SL. Calcitonin. Endocrinol Metab Clin North Am 2003; 32(1): 273-84.
[http://dx.doi.org/10.1016/S0889-8529(02)00060-9] [PMID: 12699303]
[34]
Rodan GA, Fleisch HA. Bisphosphonates: mechanisms of action. J Clin Invest 1996; 97(12): 2692-6.
[http://dx.doi.org/10.1172/JCI118722] [PMID: 8675678]
[35]
Colucci S, Minielli V, Zambonin G, et al. Alendronate reduces adhesion of human osteoclast-like cells to bone and bone protein-coated surfaces. Calcif Tissue Int 1998; 63(3): 230-5.
[http://dx.doi.org/10.1007/s002239900519] [PMID: 9701627]
[36]
Hughes DE, Wright KR, Uy HL. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo. JBMR 1995; 10(10): 1478-87.
[37]
Nguyen PV, Bouin M, Ste-Marie LG. Upper gastrointestinal safety of oral bisphosphonate in hospitalized patients. Osteoporos Int 2021; 32(1): 193-7.
[http://dx.doi.org/10.1007/s00198-020-05498-7]
[38]
Vargas-Franco JW, Castaneda B, Rédiní F, Gómez DF, Heymann D, Lézot F. Paradoxical side effects of bisphosphonates on the skeleton: What do we know and what can we do? J Cell Physiol 2018; 233(8): 5696-715.
[http://dx.doi.org/10.1002/jcp.26465] [PMID: 29323712]
[39]
Vahle JL, Long GG, Sandusky G, Westmore M, Ma YL, Sato M. Bone neoplasms in F344 rats given teriparatide [rhPTH(1-34)] are dependent on duration of treatment and dose. Toxicol Pathol 2004; 32(4): 426-38.
[http://dx.doi.org/10.1080/01926230490462138] [PMID: 15204966]
[40]
Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015; 4: 27066.
[http://dx.doi.org/10.3402/jev.v4.27066] [PMID: 25979354]
[41]
Trams EG, Lauter CJ, Salem N Jr, Heine U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim Biophys Acta 1981; 645(1): 63-70.
[http://dx.doi.org/10.1016/0005-2736(81)90512-5] [PMID: 6266476]
[42]
Simons M, Raposo G. Exosomes--vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009; 21(4): 575-81.
[http://dx.doi.org/10.1016/j.ceb.2009.03.007] [PMID: 19442504]
[43]
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]
[44]
Théry C, Regnault A, Garin J, et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 1999; 147(3): 599-610.
[http://dx.doi.org/10.1083/jcb.147.3.599] [PMID: 10545503]
[45]
Raposo G, Tenza D, Mecheri S, Peronet R, Bonnerot C, Desaymard C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell 1997; 8(12): 2631-45.
[http://dx.doi.org/10.1091/mbc.8.12.2631] [PMID: 9398681]
[46]
Villarroya-Beltri C, Baixauli F, Mittelbrunn M, et al. ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat Commun 2016; 7: 13588.
[http://dx.doi.org/10.1038/ncomms13588] [PMID: 27882925]
[47]
Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009; 10(8): 513-25.
[http://dx.doi.org/10.1038/nrm2728] [PMID: 19603039]
[48]
Jahn R, Scheller RH. SNAREs--engines for membrane fusion. Nat Rev Mol Cell Biol 2006; 7(9): 631-43.
[http://dx.doi.org/10.1038/nrm2002] [PMID: 16912714]
[49]
Dinh PC, Paudel D, Brochu H, et al. Inhalation of lung spheroid cell secretome and exosomes promotes lung repair in pulmonary fibrosis. Nat Commun 2020; 11(1): 1064.
[http://dx.doi.org/10.1038/s41467-020-14344-7] [PMID: 32111836]
[50]
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]
[51]
Jia L, Zhou X, Huang X, et al. Maternal and umbilical cord serum-derived exosomes enhance endothelial cell proliferation and migration. FASEB J 2018; 32(8): 4534-43.
[http://dx.doi.org/10.1096/fj.201701337RR] [PMID: 29570394]
[52]
Gao Y, Xu H, Li N, et al. Renal cancer-derived exosomes induce tumor immune tolerance by MDSCs-mediated antigen-specific immunosuppression. Cell Commun Signal 2020; 18(1): 106.
[http://dx.doi.org/10.1186/s12964-020-00611-z] [PMID: 32641056]
[53]
Hu JL, Wang W, Lan XL, et al. CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer. Mol Cancer 2019; 18(1): 91.
[http://dx.doi.org/10.1186/s12943-019-1019-x] [PMID: 31064356]
[54]
Ankasha SJ, Shafiee MN, Wahab NA, Ali RAR, Mokhtar NM. Post-transcriptional regulation of microRNAs in cancer: From prediction to validation. Oncol Rev 2018; 12(1): 344.
[http://dx.doi.org/10.4081/oncol.2018.344] [PMID: 29989022]
[55]
Sun Z, Shi K, Yang S, et al. Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer 2018; 17(1): 147.
[http://dx.doi.org/10.1186/s12943-018-0897-7] [PMID: 30309355]
[56]
Halkein J, Tabruyn SP, Ricke-Hoch M, et al. MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J Clin Invest 2013; 123(5): 2143-54.
[http://dx.doi.org/10.1172/JCI64365] [PMID: 23619365]
[57]
Yang TT, Liu CG, Gao SC, Zhang Y, Wang PC. The serum exosome derived microRNA-135a, -193b, and -384 were potential Alzheimer’s Disease biomarkers. Biomed Environ Sci 2018; 31(2): 87-96.
[PMID: 29606187]
[58]
Han YD, Bai Y, Yan XL, et al. Co-transplantation of exosomes derived from hypoxia-preconditioned adipose mesenchymal stem cells promotes neovascularization and graft survival in fat grafting. Biochem Biophys Res Commun 2018; 497(1): 305-12.
[http://dx.doi.org/10.1016/j.bbrc.2018.02.076] [PMID: 29428734]
[59]
Han Y, Ren J, Bai Y, Pei X, Han Y. Exosomes from hypoxia-treated human adipose-derived mesenchymal stem cells enhance angiogenesis through VEGF/VEGF-R. Int J Biochem Cell Biol 2019; 109: 59-68.
[http://dx.doi.org/10.1016/j.biocel.2019.01.017] [PMID: 30710751]
[60]
Wang ZG, He ZY, Liang S, Yang Q, Cheng P, Chen AM. Comprehensive proteomic analysis of exosomes derived from human bone marrow, adipose tissue, and umbilical cord mesenchymal stem cells. Stem Cell Res Ther 2020; 11(1): 511.
[http://dx.doi.org/10.1186/s13287-020-02032-8] [PMID: 33246507]
[61]
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]
[62]
Charoenviriyakul C, Takahashi Y, Morishita M, Matsumoto A, Nishikawa M, Takakura Y. Cell type-specific and common characteristics of exosomes derived from mouse cell lines: Yield, physicochemical properties, and pharmacokinetics. Eur J Pharm Sci 2017; 96: 316-22.
[63]
Wang AL, Lukas TJ, Yuan M, Du N, Tso MO, Neufeld AH. Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration. PLoS One 2009; 4(1): e4160.
[http://dx.doi.org/10.1371/journal.pone.0004160] [PMID: 19129916]
[64]
Doyle LM, Wang MZ. Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells 2019; 8(7): E727.
[http://dx.doi.org/10.3390/cells8070727] [PMID: 31311206]
[65]
S ELA. Mäger I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013; 12(5): 347-57.
[http://dx.doi.org/ 10.1038/nrd3978] [PMID: 23584393]
[66]
Akers JC, Gonda D, Kim R, Carter BS, Chen CC. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol 2013; 113(1): 1-11.
[http://dx.doi.org/10.1007/s11060-013-1084-8] [PMID: 23456661]
[67]
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]
[68]
An M, Wu J, Zhu J, Lubman DM. Comparison of an optimized ultracentrifugation method versus size-exclusion chromatography for isolation of exosomes from human serum. J Proteome Res 2018; 17(10): 3599-605.
[http://dx.doi.org/10.1021/acs.jproteome.8b00479] [PMID: 30192545]
[69]
Langevin SM, Kuhnell D, Orr-Asman MA, et al. Balancing yield, purity and practicality: a modified differential ultracentrifugation protocol for efficient isolation of small extracellular vesicles from human serum. RNA Biol 2019; 16(1): 5-12.
[http://dx.doi.org/10.1080/15476286.2018.1564465] [PMID: 30604646]
[70]
Marqués-García F, Isidoro-García M. Protocols for exosome isolation and RNA profiling. Methods Mol Biol 2016; 1434: 153-67.
[http://dx.doi.org/10.1007/978-1-4939-3652-6_11] [PMID: 27300537]
[71]
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.
[http://dx.doi.org/10.1016/j.ymeth.2015.05.028] [PMID: 26044649]
[72]
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]
[73]
Lamparski HG, Metha-Damani A, Yao JY, et al. Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods 2002; 270(2): 211-26.
[http://dx.doi.org/10.1016/S0022-1759(02)00330-7] [PMID: 12379326]
[74]
Escudier B, Dorval T, Chaput N, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 2005; 3(1): 10.
[http://dx.doi.org/10.1186/1479-5876-3-10] [PMID: 15740633]
[75]
Mattes B, Scholpp S. Emerging role of contact-mediated cell communication in tissue development and diseases. Histochem Cell Biol 2018; 150(5): 431-42.
[http://dx.doi.org/10.1007/s00418-018-1732-3] [PMID: 30255333]
[76]
Masaoutis C, Theocharis S. The role of exosomes in bone remodeling: Implications for bone physiology and disease. Dis Markers 2019; 2019: 9417914.
[http://dx.doi.org/10.1155/2019/9417914] [PMID: 31485281]
[77]
Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11(9): 597-610.
[http://dx.doi.org/10.1038/nrg2843] [PMID: 20661255]
[78]
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[79]
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.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[80]
Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 2015; 13(1): 17-24.
[http://dx.doi.org/10.1016/j.gpb.2015.02.001] [PMID: 25724326]
[81]
Ye Z, Zheng Z, Peng L. MicroRNA profiling of serum exosomes in patients with osteosarcoma by high-throughput sequencing. JIM 2020; 68(4): 893-901.
[82]
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]
[83]
Tao SC, Yuan T, Zhang YL, Yin WJ, Guo SC, Zhang CQ. Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model. Theranostics 2017; 7(1): 180-95.
[http://dx.doi.org/10.7150/thno.17133] [PMID: 28042326]
[84]
Chen S, Zheng Y, Zhang S, Jia L, Zhou Y. Promotion effects of miR-375 on the osteogenic differentiation of human adipose-derived mesenchymal stem cells. Stem Cell Reports 2017; 8(3): 773-86.
[http://dx.doi.org/10.1016/j.stemcr.2017.01.028] [PMID: 28262546]
[85]
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]
[86]
Watson EC, Adams RH. Biology of bone: The vasculature of the skeletal system. Cold Spring Harb Perspect Med 2018; 8(7): a031559.
[http://dx.doi.org/10.1101/cshperspect.a031559] [PMID: 28893838]
[87]
Majesky MW. Vascular development. Arterioscler Thromb Vasc Biol 2018; 38(3): e17-24.
[http://dx.doi.org/10.1161/ATVBAHA.118.310223] [PMID: 29467221]
[88]
Jia Y, Zhu Y, Qiu S, Xu J, Chai Y. Exosomes secreted by endothelial progenitor cells accelerate bone regeneration during distraction osteogenesis by stimulating angiogenesis. Stem Cell Res Ther 2019; 10(1): 12.
[http://dx.doi.org/10.1186/s13287-018-1115-7] [PMID: 30635031]
[89]
Wang X, Li X, Li J, et al. Mechanical loading stimulates bone angiogenesis through enhancing type H vessel formation and downregulating exosomal miR-214-3p from bone marrow-derived mesenchymal stem cells. FASEB J 2021; 35(1): e21150.
[http://dx.doi.org/10.1096/fj.202001080RR] [PMID: 33161580]
[90]
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]
[91]
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]
[92]
Sarugaser R, Hanoun L, Keating A, Stanford WL, Davies JE. Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PLoS One 2009; 4(8): e6498.
[http://dx.doi.org/10.1371/journal.pone.0006498] [PMID: 19652709]
[93]
Ding DC, Shyu WC, Lin SZ. Mesenchymal stem cells. Cell Transplant 2011; 20(1): 5-14.
[http://dx.doi.org/10.3727/096368910X] [PMID: 21396235]
[94]
Hu L, Yin C, Zhao F, Ali A, Ma J, Qian A. Mesenchymal stem cells: Cell fate decision to osteoblast or adipocyte and application in osteoporosis treatment. Int J Mol Sci 2018; 19(2): E360.
[http://dx.doi.org/10.3390/ijms19020360] [PMID: 29370110]
[95]
Zhang PX, Li-Ya A, Kou YH, et al. Biological conduit small gap sleeve bridging method for peripheral nerve injury: regeneration law of nerve fibers in the conduit. Neural Regen Res 2015; 10(1): 71-8.
[http://dx.doi.org/10.4103/1673-5374.150709] [PMID: 25788923]
[96]
Volarevic V, Markovic BS, Gazdic M, et al. Ethical and safety issues of stem cell-based therapy. Int J Med Sci 2018; 15(1): 36-45.
[http://dx.doi.org/10.7150/ijms.21666] [PMID: 29333086]
[97]
Che Y, Shi X, Shi Y, et al. Exosomes derived from miR-143-Overexpressing MSCs inhibit cell migration and invasion in human prostate cancer by downregulating TFF3. Mol Ther Nucleic Acids 2019; 18: 232-44.
[http://dx.doi.org/10.1016/j.omtn.2019.08.010] [PMID: 31563120]
[98]
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]
[99]
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.
[http://dx.doi.org/10.1161/CIRCRESAHA.118.312758] [PMID: 29921652]
[100]
Zuo R, Liu M, Wang Y, et al. BM-MSC-derived exosomes alleviate radiation-induced bone loss by restoring the function of recipient BM-MSCs and activating Wnt/β-catenin signaling. Stem Cell Res Ther 2019; 10(1): 30.
[http://dx.doi.org/10.1186/s13287-018-1121-9] [PMID: 30646958]
[101]
Yang X, Yang J, Lei P, Wen T. LncRNA MALAT1 shuttled by bone marrow-derived mesenchymal stem cells-secreted exosomes alleviates osteoporosis through mediating microRNA-34c/SATB2 axis. Aging (Albany NY) 2019; 11(20): 8777-91.
[http://dx.doi.org/10.18632/aging.102264] [PMID: 31659145]
[102]
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.
[PMID: 29949171]
[103]
Zhang L, Ouyang P, He G, et al. Exosomes from microRNA-126 overexpressing mesenchymal stem cells promote angiogenesis by targeting the PIK3R2-mediated PI3K/Akt signalling pathway. J Cell Mol Med 2021; 25(4): 2148-62.
[http://dx.doi.org/10.1111/jcmm.16192] [PMID: 33350092]
[104]
Wu J, Kuang L, Chen C, et al. miR-100-5p-abundant exosomes derived from infrapatellar fat pad MSCs protect articular cartilage and ameliorate gait abnormalities via inhibition of mTOR in osteoarthritis. Biomaterials 2019; 206: 87-100.
[http://dx.doi.org/10.1016/j.biomaterials.2019.03.022] [PMID: 30927715]
[105]
Jin Z, Ren J, Qi S. Exosomal miR-9-5p secreted by bone marrow-derived mesenchymal stem cells alleviates osteoarthritis by inhibiting syndecan-1. Cell Tissue Res 2020; 381(1): 99-114.
[http://dx.doi.org/10.1007/s00441-020-03193-x] [PMID: 32377874]
[106]
Jiang LB, Tian L, Zhang CG. Bone marrow stem cells-derived exosomes extracted from osteoporosis patients inhibit osteogenesis via microRNA-21/SMAD7. Eur Rev Med Pharmacol Sci 2018; 22(19): 6221-9.
[PMID: 30338786]
[107]
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: 21961.
[http://dx.doi.org/10.1038/srep21961] [PMID: 26911789]
[108]
Zhang H, Wang J, Ren T, et al. Bone marrow mesenchymal stem cell-derived exosomal miR-206 inhibits osteosarcoma progression by targeting TRA2B. Cancer Lett 2020; 490: 54-65.
[http://dx.doi.org/10.1016/j.canlet.2020.07.008] [PMID: 32682951]
[109]
Matsuo K, Irie N. Osteoclast-osteoblast communication. Arch Biochem Biophys 2008; 473(2): 201-9.
[http://dx.doi.org/10.1016/j.abb.2008.03.027] [PMID: 18406338]
[110]
Narayanan K, Kumar S, Padmanabhan P, Gulyas B, Wan ACA, Rajendran VM. Lineage-specific exosomes could override extracellular matrix mediated human mesenchymal stem cell differentiation. Biomaterials 2018; 182: 312-22.
[http://dx.doi.org/10.1016/j.biomaterials.2018.08.027] [PMID: 30153612]
[111]
Yang JX, Xie P, Li YS, Wen T, Yang XC. Osteoclast-derived miR-23a-5p-containing exosomes inhibit osteogenic differentiation by regulating Runx2. Cell Signal 2020; 70: 109504.
[http://dx.doi.org/10.1016/j.cellsig.2019.109504] [PMID: 31857240]
[112]
Yang DH, Yang MY. The Role of Macrophage in the Pathogenesis of Osteoporosis. Int J Mol Sci 2019; 20(9): E2093.
[http://dx.doi.org/10.3390/ijms20092093] [PMID: 31035384]
[113]
Yamaguchi T, Movila A, Kataoka S, et al. Proinflammatory M1 macrophages inhibit RANKL-induced osteoclastogenesis. Infect Immun 2016; 84(10): 2802-12.
[http://dx.doi.org/10.1128/IAI.00461-16] [PMID: 27456834]
[114]
Dou C, Ding N. Zhao. Estrogen deficiency-mediated M2 macrophage osteoclastogenesis contributes to M1/M2 ratio alteration in ovariectomized osteoporotic mice. JBMR 2018; 33(5): 899-908.
[115]
Kang M, Huang CC, Lu Y, et al. Bone regeneration is mediated by macrophage extracellular vesicles. Bone 2020; 141: 115627.
[http://dx.doi.org/10.1016/j.bone.2020.115627] [PMID: 32891867]
[116]
Wiklander OP, Nordin JZ, O’Loughlin A, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles 2015; 4: 26316.
[http://dx.doi.org/10.3402/jev.v4.26316] [PMID: 25899407]
[117]
Zhu Y, Li Z, Zhang Y, Lan F, He J, Wu Y. The essential role of osteoclast-derived exosomes in magnetic nanoparticle-infiltrated hydroxyapatite scaffold modulated osteoblast proliferation in an osteoporosis model. Nanoscale 2020; 12(16): 8720-6.
[http://dx.doi.org/10.1039/D0NR00867B] [PMID: 32285072]
[118]
Qayoom I, Teotia AK, Kumar A. Nanohydroxyapatite based ceramic carrier promotes bone formation in a femoral neck canal defect in osteoporotic rats. Biomacromolecules 2020; 21(2): 328-37.
[http://dx.doi.org/10.1021/acs.biomac.9b01327] [PMID: 31637919]
[119]
Wei F, Li M, Crawford R, Zhou Y, Xiao Y. Exosome-integrated titanium oxide nanotubes for targeted bone regeneration. Acta Biomater 2019; 86: 480-92.
[http://dx.doi.org/10.1016/j.actbio.2019.01.006] [PMID: 30630122]
[120]
Sengupta V, Sengupta S, Lazo A, Woods P, Nolan A, Bremer N. Exosomes derived from bone marrow mesenchymal stem cells as treatment for severe COVID-19. Stem Cells Dev 2020; 29(12): 747-54.
[http://dx.doi.org/10.1089/scd.2020.0080] [PMID: 32380908]

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