Progress of mesenchymal stem cells derived exosomes in wound repair_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

WANG Jiangwen ,  YI Yangyan , ZHU Yuanzheng

Department of Plastic Surgery, Second Affiliated Hospital of Nanchang University, Nanchang Jiangxi, 330006, P.R.China;

Corresponding author：

YI Yangyan, Email: yyy0218@126.com

Keywords：

Mesenchymal stem cells; exosomes; wound repair; inflammation; angiogenesis

DOI：

10.7507/1002-1892.201901051

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of mesenchymal stem cells derived exosomes (MSCs-EXOs) in wound repair in recent years.Methods The literature about the role of MSCs-EXOs in wound repair at home and abroad was extensively consulted. The mechanism of MSCs-EXOs in wound repair and its clinical application prospects were summarized and analyzed.Results MSCs-EXOs can inhibit early inflammatory reaction, promote angiogenesis, proliferation, and migration of epithelial cells, regulate collagen synthesis, and inhibit scar proliferation in the later stage of wound healing. Compared with MSCs, MSCs-EXOs have many advantages, such as high stability, easy storage, non-tumorigenicity, no proliferation, easy quantitative use, and so on. It has broad clinical application prospects.Conclusion MSCs-EXOs can promote wound repair and hopefully develop into a clinical product to promote the repair of acute or chronic wounds.

Citation： WANG Jiangwen, YI Yangyan, ZHU Yuanzheng. Progress of mesenchymal stem cells derived exosomes in wound repair. Chinese Journal of Reparative and Reconstructive Surgery, 2019, 33(5): 634-639. doi: 10.7507/1002-1892.201901051 Copy

1.	Hamed S, Bennett CL, Demiot C, et al. Erythropoietin, a novel repurposed drug: an innovative treatment for wound healing in patients with diabetes mellitus. Wound Repair Regen, 2014, 22(1): 23-33.
2.	Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell, 2015, 17(1): 11-22.
3.	Gyöngyösi M, Wojakowski W, Lemarchand P, et al. Meta-Analysis of Cell-Based CaRdiac stUdiEs (ACCRUE) in patients with acute myocardial infarction based on individual patient data. Circ Res, 2015, 116(8): 1346-1360.
4.	Swaminathan M, Stafford-Smith M, Chertow GM, et al. Allogeneic mesenchymal stem cells for treatment of AKI after cardiac surgery. J Am Soc Nephrol, 2018, 29(1): 260-267.
5.	Ridiandries A, Tan JTM, Bursill CA. The role of chemokines in wound healing. Int J Mol Sci, 2018, 19(10). pii: E3217.
6.	Taverna S, Pucci M, Alessandro R. Extracellular vesicles: small bricks for tissue repair/regeneration. Ann Transl Med, 2017, 5(4): 83.
7.	Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles, 2015, 4: 27066.
8.	Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol, 1983, 97(2): 329-339.
9.	Pan BT, Teng K, Wu C, et al. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol, 1985, 101(3): 942-948.
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.	Rani S, Ryan AE, Griffin MD, et al. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther, 2015, 23(5): 812-823.
12.	Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics, 2010, 73(10): 1907-1920.
13.	Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol, 2009, 19(2): 43-51.
14.	Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol, 2007, 35(4): 495-516.
15.	Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A, 2016, 113(8): E968-E977.
16.	Kalra H, Drummen GP, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci, 2016, 17(2): 170.
17.	Monaco JL, Lawrence WT. Acute wound healing an overview. Clin Plast Surg, 2003, 30(1): 1-12.
18.	Velnar T, Bailey T, Smrkolj V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res, 2009, 37(5): 1528-1542.
19.	Broughton G 2nd, Janis JE, Attinger CE. The basic science of wound healing. Plast Reconstr Surg, 2006, 117(7 Suppl): 12S-34S.
20.	Guo S, Dipietro LA. Factors affecting wound healing. J Dent Res, 2010, 89(3): 219-229.
21.	Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 2008, 8(12): 958-969.
22.	Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg, 2004, 187(5A): 11S-16S.
23.	Mills RE, Taylor KR, Podshivalova K, et al. Defects in skin gamma delta T cell function contribute to delayed wound repair in rapamycin-treated mice. J Immunol, 2008, 181(6): 3974-3983.
24.	Baum CL, Arpey CJ. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg, 2005, 31(6): 674-686.
25.	Sugimoto MA, Sousa LP, Pinho V, et al. Resolution of inflammation: what controls its onset? Front Immunol, 2016, 7: 160.
26.	Hunt TK. The physiology of wound healing. Ann Emerg Med, 1988, 17(12): 1265-1273.
27.	Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med, 2011, 13: e23.
28.	Lo Sicco C, Reverberi D, Balbi C, et al. Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: endorsement of macrophage polarization. Stem Cells Transl Med, 2017, 6(3): 1018-1028.
29.	Ti D, Hao H, Tong C, et al. LPS-preconditioned mesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b. J Transl Med, 2015, 13: 308.
30.	Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol, 2001, 2(9): 764-766.
31.	Nosbaum A, Prevel N, Truong HA, et al. Cutting edge: regulatory T cells facilitate cutaneous wound healing. J Immunol, 2016, 196(5): 2010-2014.
32.	Monguió-Tortajada M, Roura S, Gálvez-Montón C, et al. Nanosized UCMSC-derived extracellular vesicles but not conditioned medium exclusively inhibit the inflammatory response of stimulated T cells: implications for nanomedicine. Theranostics, 2017, 7(2): 270-284.
33.	Yang J, Liu XX, Fan H, et al. Extracellular vesicles derived from bone marrow mesenchymal stem cells protect against experimental colitis via attenuating colon inflammation, oxidative stress and apoptosis. PLoS One, 2015, 10(10): e0140551.
34.	Li X, Liu L, Yang J, et al. Exosome derived from human umbilical cord mesenchymal stem cell mediates MiR-181c attenuating burn-induced excessive inflammation. EBioMedicine, 2016, 8: 72-82.
35.	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.
36.	Mishra S, Tripathi A, Chaudhari BP, et al. Deoxynivalenol induced mouse skin cell proliferation and inflammation via MAPK pathway. Toxicol Appl Pharmacol, 2014, 279(2): 186-197.
37.	Jeon YJ, Kim BH, Kim S, et al. Rhododendrin ameliorates skin inflammation through inhibition of NF-κB, MAPK, and PI3K/Akt signaling. Eur J Pharmacol, 2013, 714(1-3): 7-14.
38.	Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta, 2010, 1802(4): 396-405.
39.	Eirin A, Zhu XY, Puranik AS, et al. Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int, 2017, 92(1): 114-124.
40.	Ti D, Hao H, Fu X, et al. Mesenchymal stem cells-derived exosomal microRNAs contribute to wound inflammation. Sci China Life Sci, 2016, 59(12): 1305-1312.
41.	Martin P. Wound healing—aiming for perfect skin regeneration. Science, 1997, 276(5309): 75-81.
42.	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): 513-522.
43.	Sahoo S, Klychko E, Thorne T, et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res, 2011, 109(7): 724-728.
44.	张静, 易阳艳, 羊水发, 等. 脂肪干细胞来源外泌体对人脐静脉血管内皮细胞增殖、迁移及管样分化的影响. 中国修复重建外科杂志, 2018, 32(10): 1351-1357.
45.	Liang X, Zhang L, Wang S, et al. Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a. J Cell Sci, 2016, 129(11): 2182-2189.
46.	Kang T, Jones TM, Naddell C, et al. Adipose-derived stem cells induce angiogenesis via microvesicle transport of miRNA-31. Stem Cells Transl Med, 2016, 5(4): 440-450.
47.	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.
48.	Guo SC, Tao SC, Yin WJ, et al. Exosomes derived from platelet-rich plasma promote the re-epithelization of chronic cutaneous wounds via activation of YAP in a diabetic rat model. Theranostics, 2017, 7(1): 81-96.
49.	尹刚, 刘蔡钺, 林耀发, 等. 脂肪干细胞来源外泌体对周围神经损伤后再生作用的实验研究. 中国修复重建外科杂志, 2018, 32(12): 1592-1596.
50.	Geiger A, Walker A, Nissen E. Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochem Biophys Res Commun, 2015, 467(2): 303-309.
51.	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.
52.	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.
53.	Zhang B, Wang M, Gong A, et al. HucMSC-exosome mediated-Wnt4 signaling is required for cutaneous wound healing. Stem Cells, 2015, 33(7): 2158-2168.
54.	Fang S, Xu C, Zhang Y, et al. Umbilical cord-derived mesenchymal stem cell-derived exosomal microRNAs suppress myofibroblast differentiation by inhibiting the transforming growth factor-β/SMAD2 pathway during wound healing. Stem Cells Transl Med, 2016, 5(10): 1425-1439.
55.	Zhao B, Zhang Y, Han S, et al. Exosomes derived from human amniotic epithelial cells accelerate wound healing and inhibit scar formation. J Mol Histol, 2017, 48(2): 121-132.
56.	Zhang B, Shi Y, Gong A, et al. HucMSC exosome-delivered 14-3-3ζ orchestrates self-control of the Wnt response via modulation of YAP during cutaneous regeneration. Stem Cells, 2016, 34(10): 2485-2500.
57.	Théry C, Duban L, Segura E, et al. Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol, 2002, 3(12): 1156-1162.
58.	Laulagnier K, Motta C, Hamdi S, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J, 2004, 380(Pt 1): 161-171.
59.	Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles, 2014, 3.
60.	Cabral J, Ryan AE, Griffin MD, et al. Extracellular vesicles as modulators of wound healing. Adv Drug Deliv Rev, 2018, 129: 394-406.
61.	Lu Z, Chen Y, Dunstan C, et al. 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): 1212-1220.
62.	Park JS, Suryaprakash S, Lao YH, et al. Engineering mesenchymal stem cells for regenerative medicine and drug delivery. Methods, 2015, 84: 3-16.
63.	Tao SC, Guo SC, Li M, et al. Chitosan wound dressings incorporating exosomes derived from microRNA-126-overexpressing synovium mesenchymal stem cells provide sustained release of exosomes and heal full-thickness skin defects in a diabetic rat model. Stem Cells Transl Med, 2017, 6(3): 736-747.
64.	Gilligan KE, Dwyer RM. Engineering exosomes for cancer therapy. Int J Mol Sci, 2017, 18(6): pii: E1122.

1. Hamed S, Bennett CL, Demiot C, et al. Erythropoietin, a novel repurposed drug: an innovative treatment for wound healing in patients with diabetes mellitus. Wound Repair Regen, 2014, 22(1): 23-33.
2. Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell, 2015, 17(1): 11-22.
3. Gyöngyösi M, Wojakowski W, Lemarchand P, et al. Meta-Analysis of Cell-Based CaRdiac stUdiEs (ACCRUE) in patients with acute myocardial infarction based on individual patient data. Circ Res, 2015, 116(8): 1346-1360.
4. Swaminathan M, Stafford-Smith M, Chertow GM, et al. Allogeneic mesenchymal stem cells for treatment of AKI after cardiac surgery. J Am Soc Nephrol, 2018, 29(1): 260-267.
5. Ridiandries A, Tan JTM, Bursill CA. The role of chemokines in wound healing. Int J Mol Sci, 2018, 19(10). pii: E3217.
6. Taverna S, Pucci M, Alessandro R. Extracellular vesicles: small bricks for tissue repair/regeneration. Ann Transl Med, 2017, 5(4): 83.
7. Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles, 2015, 4: 27066.
8. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol, 1983, 97(2): 329-339.
9. Pan BT, Teng K, Wu C, et al. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol, 1985, 101(3): 942-948.
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. Rani S, Ryan AE, Griffin MD, et al. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther, 2015, 23(5): 812-823.
12. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics, 2010, 73(10): 1907-1920.
13. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol, 2009, 19(2): 43-51.
14. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol, 2007, 35(4): 495-516.
15. Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A, 2016, 113(8): E968-E977.
16. Kalra H, Drummen GP, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci, 2016, 17(2): 170.
17. Monaco JL, Lawrence WT. Acute wound healing an overview. Clin Plast Surg, 2003, 30(1): 1-12.
18. Velnar T, Bailey T, Smrkolj V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res, 2009, 37(5): 1528-1542.
19. Broughton G 2nd, Janis JE, Attinger CE. The basic science of wound healing. Plast Reconstr Surg, 2006, 117(7 Suppl): 12S-34S.
20. Guo S, Dipietro LA. Factors affecting wound healing. J Dent Res, 2010, 89(3): 219-229.
21. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 2008, 8(12): 958-969.
22. Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg, 2004, 187(5A): 11S-16S.
23. Mills RE, Taylor KR, Podshivalova K, et al. Defects in skin gamma delta T cell function contribute to delayed wound repair in rapamycin-treated mice. J Immunol, 2008, 181(6): 3974-3983.
24. Baum CL, Arpey CJ. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg, 2005, 31(6): 674-686.
25. Sugimoto MA, Sousa LP, Pinho V, et al. Resolution of inflammation: what controls its onset? Front Immunol, 2016, 7: 160.
26. Hunt TK. The physiology of wound healing. Ann Emerg Med, 1988, 17(12): 1265-1273.
27. Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med, 2011, 13: e23.
28. Lo Sicco C, Reverberi D, Balbi C, et al. Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: endorsement of macrophage polarization. Stem Cells Transl Med, 2017, 6(3): 1018-1028.
29. Ti D, Hao H, Tong C, et al. LPS-preconditioned mesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b. J Transl Med, 2015, 13: 308.
30. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol, 2001, 2(9): 764-766.
31. Nosbaum A, Prevel N, Truong HA, et al. Cutting edge: regulatory T cells facilitate cutaneous wound healing. J Immunol, 2016, 196(5): 2010-2014.
32. Monguió-Tortajada M, Roura S, Gálvez-Montón C, et al. Nanosized UCMSC-derived extracellular vesicles but not conditioned medium exclusively inhibit the inflammatory response of stimulated T cells: implications for nanomedicine. Theranostics, 2017, 7(2): 270-284.
33. Yang J, Liu XX, Fan H, et al. Extracellular vesicles derived from bone marrow mesenchymal stem cells protect against experimental colitis via attenuating colon inflammation, oxidative stress and apoptosis. PLoS One, 2015, 10(10): e0140551.
34. Li X, Liu L, Yang J, et al. Exosome derived from human umbilical cord mesenchymal stem cell mediates MiR-181c attenuating burn-induced excessive inflammation. EBioMedicine, 2016, 8: 72-82.
35. 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.
36. Mishra S, Tripathi A, Chaudhari BP, et al. Deoxynivalenol induced mouse skin cell proliferation and inflammation via MAPK pathway. Toxicol Appl Pharmacol, 2014, 279(2): 186-197.
37. Jeon YJ, Kim BH, Kim S, et al. Rhododendrin ameliorates skin inflammation through inhibition of NF-κB, MAPK, and PI3K/Akt signaling. Eur J Pharmacol, 2013, 714(1-3): 7-14.
38. Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta, 2010, 1802(4): 396-405.
39. Eirin A, Zhu XY, Puranik AS, et al. Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int, 2017, 92(1): 114-124.
40. Ti D, Hao H, Fu X, et al. Mesenchymal stem cells-derived exosomal microRNAs contribute to wound inflammation. Sci China Life Sci, 2016, 59(12): 1305-1312.
41. Martin P. Wound healing—aiming for perfect skin regeneration. Science, 1997, 276(5309): 75-81.
42. 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): 513-522.
43. Sahoo S, Klychko E, Thorne T, et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res, 2011, 109(7): 724-728.
44. 张静, 易阳艳, 羊水发, 等. 脂肪干细胞来源外泌体对人脐静脉血管内皮细胞增殖、迁移及管样分化的影响. 中国修复重建外科杂志, 2018, 32(10): 1351-1357.
45. Liang X, Zhang L, Wang S, et al. Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a. J Cell Sci, 2016, 129(11): 2182-2189.
46. Kang T, Jones TM, Naddell C, et al. Adipose-derived stem cells induce angiogenesis via microvesicle transport of miRNA-31. Stem Cells Transl Med, 2016, 5(4): 440-450.
47. 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.
48. Guo SC, Tao SC, Yin WJ, et al. Exosomes derived from platelet-rich plasma promote the re-epithelization of chronic cutaneous wounds via activation of YAP in a diabetic rat model. Theranostics, 2017, 7(1): 81-96.
49. 尹刚, 刘蔡钺, 林耀发, 等. 脂肪干细胞来源外泌体对周围神经损伤后再生作用的实验研究. 中国修复重建外科杂志, 2018, 32(12): 1592-1596.
50. Geiger A, Walker A, Nissen E. Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochem Biophys Res Commun, 2015, 467(2): 303-309.
51. 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.
52. 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.
53. Zhang B, Wang M, Gong A, et al. HucMSC-exosome mediated-Wnt4 signaling is required for cutaneous wound healing. Stem Cells, 2015, 33(7): 2158-2168.
54. Fang S, Xu C, Zhang Y, et al. Umbilical cord-derived mesenchymal stem cell-derived exosomal microRNAs suppress myofibroblast differentiation by inhibiting the transforming growth factor-β/SMAD2 pathway during wound healing. Stem Cells Transl Med, 2016, 5(10): 1425-1439.
55. Zhao B, Zhang Y, Han S, et al. Exosomes derived from human amniotic epithelial cells accelerate wound healing and inhibit scar formation. J Mol Histol, 2017, 48(2): 121-132.
56. Zhang B, Shi Y, Gong A, et al. HucMSC exosome-delivered 14-3-3ζ orchestrates self-control of the Wnt response via modulation of YAP during cutaneous regeneration. Stem Cells, 2016, 34(10): 2485-2500.
57. Théry C, Duban L, Segura E, et al. Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol, 2002, 3(12): 1156-1162.
58. Laulagnier K, Motta C, Hamdi S, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J, 2004, 380(Pt 1): 161-171.
59. Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles, 2014, 3.
60. Cabral J, Ryan AE, Griffin MD, et al. Extracellular vesicles as modulators of wound healing. Adv Drug Deliv Rev, 2018, 129: 394-406.
61. Lu Z, Chen Y, Dunstan C, et al. 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): 1212-1220.
62. Park JS, Suryaprakash S, Lao YH, et al. Engineering mesenchymal stem cells for regenerative medicine and drug delivery. Methods, 2015, 84: 3-16.
63. Tao SC, Guo SC, Li M, et al. Chitosan wound dressings incorporating exosomes derived from microRNA-126-overexpressing synovium mesenchymal stem cells provide sustained release of exosomes and heal full-thickness skin defects in a diabetic rat model. Stem Cells Transl Med, 2017, 6(3): 736-747.
64. Gilligan KE, Dwyer RM. Engineering exosomes for cancer therapy. Int J Mol Sci, 2017, 18(6): pii: E1122.

Previous Article
Electrospun polycaprolactone/collagen typeⅠnanofibers oriented patch for rotator cuff repairing
Next Article
Clinical application and research status of open wedge high tibial osteotomy

Chinese Journal of Reparative and Reconstructive Surgery

Progress of mesenchymal stem cells derived exosomes in wound repair

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content