RESEARCH PROGRESS OF MECHANISMS OF MESENCHYMAL STEM CELLS-DERIVED EXOSOMES IN TISSUE REPAIR_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHANGGuowei ^1,2 , WANGYang ³ ,  DENGZhifeng ²

1. Taishan Medical University, Taian Shandong, 271000, P. R. China;
2. Department of Neurosurgery, the Sixth People's Hospital of Shanghai, Shanghai Jiaotong University;
3. Institute of Microsurgery on Extremities, the Sixth People's Hospital of Shanghai, Shanghai Jiaotong University;

Corresponding author：

DENGZhifeng, Email: dengzf63@126.com

Keywords：

Mesenchymal stem cells; Exosomes; Bioactive substance; Tissue repair

DOI：

10.7507/1002-1892.20160099

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the mechanisms of bioactive substances of mesenchymal stem cells-derived exosomes (MEX) in tissue repair and analyze the therapeutic values of MEX. Method Recent relevant literature about MEX for tissue repair was extensively reviewed and analyzed. Results The diameter of exosomes ranges from 30 to 100 nm which contain an abundance of bioactive substances, such as mRNA, microRNA, and protein. The majority of the exact bioactive substances in MEX, which are therapeutically beneficial to a wide range of diseases, are still unclear. Conclusions Bioactive substances contained in the MEX have repairing effect in tissue injury, which could provide a new insight for the clinical treatment of tissue damage. However, further studies are required to investigate the individual differences of MEX and the possible risk of accelerating cancer progression of MEX.

Citation： ZHANGGuowei, WANGYang, DENGZhifeng. RESEARCH PROGRESS OF MECHANISMS OF MESENCHYMAL STEM CELLS-DERIVED EXOSOMES IN TISSUE REPAIR. Chinese Journal of Reparative and Reconstructive Surgery, 2016, 30(4): 499-503. doi: 10.7507/1002-1892.20160099 Copy

1.	Katsha AM, Ohkouchi S, Xin H, et al. Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model. Mol Ther, 2011, 19(1) :196-203.
2.	Spees JL, Olson SD, Ylostalo J, et al. Differentia-tion, cell fusion, and nuclear fusion during ex vivo repair of epithelium byhuman adult stem cells from bone marrow stroma. Proc Natl Acad Sci U S A, 2003, 100(5) :2397-2402.
3.	Iso Y, Spees JL, Serrano C, et al. Multipotent human stromal cells improve cardiac function after myocardial infarctionin mice without long-term engraftment. Biochem Biophys Res Commun, 2007, 354(3) :700-706.
4.	da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity ofmesenchymal stem cells. Stem Cells, 2008, 26(9) :2287-2299.
5.	Dai W, Hale SL, Martin BJ, et al. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium:short-and long-term effects. Circulation, 2005, 112(2) :214-223.
6.	Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J CellBiochem, 2006, 98(5) :1076-1084.
7.	Camussi G, Deregibus MC, Bruno S, et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int, 2010, 78(9) :838-848.
8.	Théry C. Exosomes:secreted vesicles and intercellular communications. F1000 Biol Rep, 2011, 3:15.
9.	Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro:Selective externalization of the receptor. Cell, 1983, 33(3) :967-978.
10.	Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19) :9412-9420.
11.	Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med, 1996, 183(3) :1161-1172.
12.	Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors:evidence for horizontal transfer of mRNA and protein delivery. Leukemia, 2006, 20(5) :847-856.
13.	Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6) :654-659.
14.	Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A, 2010, 107(14) :6328-6333.
15.	Zhang Y, Liu D, Chen X, et al. Secreted monocyticmiR-150 enhances targeted endothelial cellmigration. Mol Cell, 2010, 39(1) :133-144.
16.	Kosaka N, Iguchi H, Yoshioka Y, et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem, 2010, 285(23) :17442-17452.
17.	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) :1053-1067.
18.	Bruno S, Grange C, Collino F, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethalmodel of acute kidney injury. PLoS One, 2012, 7(3) :e33115.
19.	Gatti S, Bruno S, Deregibus MC, et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant, 2011, 26(5) :1474-1483.
20.	Zhu Y, Feng X, Abbott J, et al. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells, 2014, 32(1) :116-125.
21.	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) :2737-2746.
22.	Bonafede R, Scambi I, Peroni D, et al. Exosome derived from murine adipose-derived stromal cells:Neuroprotective effect on in vitro model of amyotrophic lateral sclerosis. Exp Cell Res, 2016, 340(1) :150-158.
23.	Feng Y, Huang W, Wani M, et al. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One, 2014, 9(2) :e88685.
24.	Yu B, Kim HW, Gong M, et al. Exosomessecreted from GATA-4 overexpressing mesenchymal stem cells serve as areservoir of anti-apoptotic microRNAs for cardioprotection. Int J Cardiol, 2015, 182:349-360.
25.	Nakamura Y, Miyaki S, Ishitobi H, et al. Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett, 2015, 589(11) :1257-1265.
26.	Wang X, Gu H, Qin D, et al. Exosomal mir-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis. Sci Rep, 2015, 5:13721.
27.	Bobrie A, Colombo M, Raposo G, et al. Exosome secretion:molecular mechanisms and roles in immune responses. Traffic, 2011, 12(12) :1659-1668.
28.	Wolfers J, Lozier A, Raposo G, et al. Tumor-derived exosomes are a source of shared tumor rejection antigensfor CTL cross-priming. Nat Med, 2001, 7(3) :297-303.
29.	Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology:toward the development of novel cancer biomarkers. Proteomics, 2014, 14(4-5) :412-425.
30.	Medina M, Avila J. The role of extracellular Tau in the spreading of neurofibrillary pathology. Front Cell Neurosci, 2014, 8:113.
31.	Lai RC, Arslan F, Lee MM, et al. Exosomesecreted by MSCs reduces myocardial ischemia/reperfusion injury. Stem Cell Res, 2010, 4(3) :214-222.
32.	Lai RC, Arslan F, Tan SS, et al. Derivation and characterization of human fetal MSCs:an alternative cell source forlarge-scale production of cardioprotective microparticles. J Mol Cell Cardiol, 2010, 48(6) :1215-1224.
33.	Arslan F, Lai RC, Smeets MB, et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res, 2013, 10(3) :301-312.
34.	Zhang B, Wu X, Zhang X, et al. Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the wnt4/beta-catenin pathway. Stem Cells Transl Med, 2015, 4(5) :513-522.
35.	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.
36.	Fierabracci A, Del Fattore A, Luciano R, et al. Recent advances in mesenchymal stem cell immunomodulation:the role of microvesicles. Cell Transplant, 2015, 24(2) :133-149.
37.	Amarnath S, Foley JE, Farthing DE, et al. Bone marrow derived mesenchymal stromal cells harness purinergenic signaling to tolerize human Th1 cells in vivo. Stem Cells, 2015, 33(4) :1200-1212.
38.	He J, Wang Y, Sun S, et al. Bone marrow stemcells-derived microvesicles protect against renal injury in the mouseremnant kidney model. Nephrology (Carlton), 2012, 17(5) :493-500.
39.	Lee C, Mitsialis SA, Aslam M, et al. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation, 2012, 126(22) :2601-2611.
40.	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) :856-867.
41.	Farinazzo A, Turano E, Marconi S, et al. Murine adipose-derived mesenchymal stromal cell vesicles:in vitro clues for neuroprotective and neuroregenerative approaches. Cytotherapy, 2015, 17(5) :571-578.
42.	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) :3289-3297.
43.	Tan CY, Lai RC, Wong W, et al. Mesenchymal stemcell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res Ther, 2014, 5(3) :76.
44.	Teng X, Chen L, Chen W, et al. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem, 2015, 37(6) :2415-2424.
45.	Zhao Y, Sun X, Cao W, et al. Exosomes derived from human umbilical cord mesenchymal stem cells relieve acute myocardial ischemic injury. Stem Cells Int, 2015, 2015:761643.
46.	Shabbir A, Cox A, Rodriguez-Menocal L, et al. Mesenchymal stem cell exosomes induce proliferation and migration of normal and chronic wound fibroblasts, and enhance angiogenesis in vitro. Stem Cells Dev, 2015, 24(14) :1635-1647.
47.	Zhang J, Guan J, Niu X, et al. Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J Transl Med, 2015, 13:49.
48.	Lai RC, Yeo RW, Tan KH, et al. Exosomes for drug delivery-a novel application for the mesenchymal stem cell. Biotechnol, 2013, 31(5) :543-551.
49.	Kim SH, Bianco NR, Shufesky WJ, et al. Effective treatment of inflammatory disease models with exosomes derived from dendritic cells genetically modified to express IL-4. J Immunol, 2007, 179(4) :2242-2249.
50.	Yu L, Yang F, Jiang L, et al. Exosomes with membrane-associated TGF-beta1 from gene-modified dendritic cells inhibit murine EAE independently of MHC restriction. Eur J Immunol, 2013, 43(9) :2461-2472.
51.	Pollock K, Dahlenburg H, Nelson H, et al. Human mesenchymal stem cells genetically engineered to overexpress brain-derived neurotrophic factor improve outcomes in huntington's disease mouse models. Mol Ther, 2016.[Epub ahead of print].
52.	Teoh HK, Chong PP, Abdullah M, et al. Small interfering rna silencing of interleukin-6 in mesenchymal stromal cells inhibits multiple myeloma cell growth. Leuk Res, 2016, 40:44-53.
53.	Xie Q, Wang Z, Zhou H, et al. The role of mir-135-modified adipose-derived mesenchymal stem cells in bone regeneration. Biomaterials, 2016, 75:279-294.
54.	Ménard C, Tarte K. Immunoregulatory properties of clinical grade mesenchymal stromal cells:evidence, uncertainties, and clinical application. Stem Cell Res Ther, 2013, 4(3) :64.
55.	Siegel G, Kluba T, Hermanutz-Klein U, et al. Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Med, 2013, 11:146.
56.	Wu S, Ju GQ, Du T, et al. Microvesicles derived from human umbilical cord Wharton's jelly mesenchymal stem cells attenuate bladder tumor cell growth in vitro and in vivo. PLoS One, 2013, 8(4) :e61366.
57.	Du T, Ju G, Wu S, et al. Microvesicles derived from human Wharton's jelly mesenchymal stem cells promote human renal cancer cell growth and aggressiveness through induction of hepatocyte growth factor. PLoS One, 2014, 9(5) :e96836.

1. Katsha AM, Ohkouchi S, Xin H, et al. Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model. Mol Ther, 2011, 19(1) :196-203.
2. Spees JL, Olson SD, Ylostalo J, et al. Differentia-tion, cell fusion, and nuclear fusion during ex vivo repair of epithelium byhuman adult stem cells from bone marrow stroma. Proc Natl Acad Sci U S A, 2003, 100(5) :2397-2402.
3. Iso Y, Spees JL, Serrano C, et al. Multipotent human stromal cells improve cardiac function after myocardial infarctionin mice without long-term engraftment. Biochem Biophys Res Commun, 2007, 354(3) :700-706.
4. da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity ofmesenchymal stem cells. Stem Cells, 2008, 26(9) :2287-2299.
5. Dai W, Hale SL, Martin BJ, et al. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium:short-and long-term effects. Circulation, 2005, 112(2) :214-223.
6. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J CellBiochem, 2006, 98(5) :1076-1084.
7. Camussi G, Deregibus MC, Bruno S, et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int, 2010, 78(9) :838-848.
8. Théry C. Exosomes:secreted vesicles and intercellular communications. F1000 Biol Rep, 2011, 3:15.
9. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro:Selective externalization of the receptor. Cell, 1983, 33(3) :967-978.
10. Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19) :9412-9420.
11. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med, 1996, 183(3) :1161-1172.
12. Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors:evidence for horizontal transfer of mRNA and protein delivery. Leukemia, 2006, 20(5) :847-856.
13. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6) :654-659.
14. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A, 2010, 107(14) :6328-6333.
15. Zhang Y, Liu D, Chen X, et al. Secreted monocyticmiR-150 enhances targeted endothelial cellmigration. Mol Cell, 2010, 39(1) :133-144.
16. Kosaka N, Iguchi H, Yoshioka Y, et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem, 2010, 285(23) :17442-17452.
17. 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) :1053-1067.
18. Bruno S, Grange C, Collino F, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethalmodel of acute kidney injury. PLoS One, 2012, 7(3) :e33115.
19. Gatti S, Bruno S, Deregibus MC, et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant, 2011, 26(5) :1474-1483.
20. Zhu Y, Feng X, Abbott J, et al. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells, 2014, 32(1) :116-125.
21. 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) :2737-2746.
22. Bonafede R, Scambi I, Peroni D, et al. Exosome derived from murine adipose-derived stromal cells:Neuroprotective effect on in vitro model of amyotrophic lateral sclerosis. Exp Cell Res, 2016, 340(1) :150-158.
23. Feng Y, Huang W, Wani M, et al. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One, 2014, 9(2) :e88685.
24. Yu B, Kim HW, Gong M, et al. Exosomessecreted from GATA-4 overexpressing mesenchymal stem cells serve as areservoir of anti-apoptotic microRNAs for cardioprotection. Int J Cardiol, 2015, 182:349-360.
25. Nakamura Y, Miyaki S, Ishitobi H, et al. Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett, 2015, 589(11) :1257-1265.
26. Wang X, Gu H, Qin D, et al. Exosomal mir-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis. Sci Rep, 2015, 5:13721.
27. Bobrie A, Colombo M, Raposo G, et al. Exosome secretion:molecular mechanisms and roles in immune responses. Traffic, 2011, 12(12) :1659-1668.
28. Wolfers J, Lozier A, Raposo G, et al. Tumor-derived exosomes are a source of shared tumor rejection antigensfor CTL cross-priming. Nat Med, 2001, 7(3) :297-303.
29. Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology:toward the development of novel cancer biomarkers. Proteomics, 2014, 14(4-5) :412-425.
30. Medina M, Avila J. The role of extracellular Tau in the spreading of neurofibrillary pathology. Front Cell Neurosci, 2014, 8:113.
31. Lai RC, Arslan F, Lee MM, et al. Exosomesecreted by MSCs reduces myocardial ischemia/reperfusion injury. Stem Cell Res, 2010, 4(3) :214-222.
32. Lai RC, Arslan F, Tan SS, et al. Derivation and characterization of human fetal MSCs:an alternative cell source forlarge-scale production of cardioprotective microparticles. J Mol Cell Cardiol, 2010, 48(6) :1215-1224.
33. Arslan F, Lai RC, Smeets MB, et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res, 2013, 10(3) :301-312.
34. Zhang B, Wu X, Zhang X, et al. Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the wnt4/beta-catenin pathway. Stem Cells Transl Med, 2015, 4(5) :513-522.
35. 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.
36. Fierabracci A, Del Fattore A, Luciano R, et al. Recent advances in mesenchymal stem cell immunomodulation:the role of microvesicles. Cell Transplant, 2015, 24(2) :133-149.
37. Amarnath S, Foley JE, Farthing DE, et al. Bone marrow derived mesenchymal stromal cells harness purinergenic signaling to tolerize human Th1 cells in vivo. Stem Cells, 2015, 33(4) :1200-1212.
38. He J, Wang Y, Sun S, et al. Bone marrow stemcells-derived microvesicles protect against renal injury in the mouseremnant kidney model. Nephrology (Carlton), 2012, 17(5) :493-500.
39. Lee C, Mitsialis SA, Aslam M, et al. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation, 2012, 126(22) :2601-2611.
40. 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) :856-867.
41. Farinazzo A, Turano E, Marconi S, et al. Murine adipose-derived mesenchymal stromal cell vesicles:in vitro clues for neuroprotective and neuroregenerative approaches. Cytotherapy, 2015, 17(5) :571-578.
42. 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) :3289-3297.
43. Tan CY, Lai RC, Wong W, et al. Mesenchymal stemcell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res Ther, 2014, 5(3) :76.
44. Teng X, Chen L, Chen W, et al. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem, 2015, 37(6) :2415-2424.
45. Zhao Y, Sun X, Cao W, et al. Exosomes derived from human umbilical cord mesenchymal stem cells relieve acute myocardial ischemic injury. Stem Cells Int, 2015, 2015:761643.
46. Shabbir A, Cox A, Rodriguez-Menocal L, et al. Mesenchymal stem cell exosomes induce proliferation and migration of normal and chronic wound fibroblasts, and enhance angiogenesis in vitro. Stem Cells Dev, 2015, 24(14) :1635-1647.
47. Zhang J, Guan J, Niu X, et al. Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J Transl Med, 2015, 13:49.
48. Lai RC, Yeo RW, Tan KH, et al. Exosomes for drug delivery-a novel application for the mesenchymal stem cell. Biotechnol, 2013, 31(5) :543-551.
49. Kim SH, Bianco NR, Shufesky WJ, et al. Effective treatment of inflammatory disease models with exosomes derived from dendritic cells genetically modified to express IL-4. J Immunol, 2007, 179(4) :2242-2249.
50. Yu L, Yang F, Jiang L, et al. Exosomes with membrane-associated TGF-beta1 from gene-modified dendritic cells inhibit murine EAE independently of MHC restriction. Eur J Immunol, 2013, 43(9) :2461-2472.
51. Pollock K, Dahlenburg H, Nelson H, et al. Human mesenchymal stem cells genetically engineered to overexpress brain-derived neurotrophic factor improve outcomes in huntington's disease mouse models. Mol Ther, 2016.[Epub ahead of print].
52. Teoh HK, Chong PP, Abdullah M, et al. Small interfering rna silencing of interleukin-6 in mesenchymal stromal cells inhibits multiple myeloma cell growth. Leuk Res, 2016, 40:44-53.
53. Xie Q, Wang Z, Zhou H, et al. The role of mir-135-modified adipose-derived mesenchymal stem cells in bone regeneration. Biomaterials, 2016, 75:279-294.
54. Ménard C, Tarte K. Immunoregulatory properties of clinical grade mesenchymal stromal cells:evidence, uncertainties, and clinical application. Stem Cell Res Ther, 2013, 4(3) :64.
55. Siegel G, Kluba T, Hermanutz-Klein U, et al. Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Med, 2013, 11:146.
56. Wu S, Ju GQ, Du T, et al. Microvesicles derived from human umbilical cord Wharton's jelly mesenchymal stem cells attenuate bladder tumor cell growth in vitro and in vivo. PLoS One, 2013, 8(4) :e61366.
57. Du T, Ju G, Wu S, et al. Microvesicles derived from human Wharton's jelly mesenchymal stem cells promote human renal cancer cell growth and aggressiveness through induction of hepatocyte growth factor. PLoS One, 2014, 9(5) :e96836.

Chinese Journal of Reparative and Reconstructive Surgery

RESEARCH PROGRESS OF MECHANISMS OF MESENCHYMAL STEM CELLS-DERIVED EXOSOMES IN TISSUE REPAIR

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