Human endothelial progenitor cells-derived exosomes accelerate cutaneous wound healing in diabetic rats by promoting endothelial function

Journal of Diabetes and its Complications

Volumn 30, Issue 6, 2016, Pages 986-992

  Li, Xiaocong ^a   Jiang, Chunyu ^a   Zhao, Jungong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

Angiogenesis; Diabetes; Endothelial progenitor cells; Exosomes; Wound healing

Indexed keywords

ANGIOPOIETIN 1; CXCL16 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR 1; INTERLEUKIN 8; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIAL PROGENITOR CELL; EXOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKIN INJURY; STEM CELL TRANSPLANTATION; WOUND HEALING; ANGIOGENESIS; ANIMAL; CYTOLOGY; EXPERIMENTAL DIABETES MELLITUS; MALE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL PROLIFERATION; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL PROGENITOR CELLS; EXOSOMES; HUMANS; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, SPRAGUE-DAWLEY; WOUND HEALING;

EID: 84969677326     PISSN: 10568727     EISSN: 1873460X     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2016.05.009     Document Type: Article

References (28)

1. Al-Nedawi, K., Meehan, B., Rak, J., Microvesicles: Messengers and mediators of tumor progression. Cell Cycle 8:13 (2009), 2014–2018.
2. Baglio, S.R., Pegtel, D.M., Baldini, N., Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Frontiers in Physiology, 3, 2012, 359.
3. Baker, C.D., Seedorf, G.J., Wisniewski, B.L., Black, C.P., Ryan, S.L., Balasubramaniam, V., Abman, S.H., Endothelial colony-forming cell conditioned media promote angiogenesis in vitro and prevent pulmonary hypertension in experimental bronchopulmonary dysplasia. American Journal of Physiology. Lung Cellular and Molecular Physiology 305:1 (2013), L73–L81.
4. Cantaluppi, V., Biancone, L., Figliolini, F., Beltramo, S., Medica, D., Deregibus, M.C.,.. Camussi, G., Microvesicles derived from endothelial progenitor cells enhance neoangiogenesis of human pancreatic islets. Cell Transplantation 21:6 (2012), 1305–1320.
5. Cantaluppi, V., Gatti, S., Medica, D., Figliolini, F., Bruno, S., Deregibus, M.C.,.. Camussi, G., Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney International 82:4 (2012), 412–427.
6. Crosby, J.R., Kaminski, W.E., Schatteman, G., Martin, P.J., Raines, E.W., Seifert, R.A., Bowen-Pope, D.F., Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circulation Research 87:9 (2000), 728–730.
7. De Jong, O.G., Van Balkom, B.W., Schiffelers, R.M., Bouten, C.V., Verhaar, M.C., Extracellular vesicles: Potential roles in regenerative medicine. Frontiers in Immunology, 5, 2014, 608.
8. Dittmer, J., Leyh, B., Paracrine effects of stem cells in wound healing and cancer progression (Review). International Journal of Oncology 44:6 (2014), 1789–1798.
9. Gu, S., Zhang, W., Chen, J., Ma, R., Xiao, X., Ma, X.,.. Chen, Y., EPC-derived microvesicles protect cardiomyocytes from Ang II-induced hypertrophy and apoptosis. PloS One, 9(1), 2014, e85396.
10. Hagensen, M.K., Raarup, M.K., Mortensen, M.B., Thim, T., Nyengaard, J.R., Falk, E., Bentzon, J.F., Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovascular Research 93:2 (2012), 223–231.
11. Ingram, D.A., Mead, L.E., Tanaka, H., Meade, V., Fenoglio, A., Mortell, K.,.. Yoder, M.C., Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104:9 (2004), 2752–2760.
12. Kim, J.Y., Song, S.H., Kim, K.L., Ko, J.J., Im, J.E., Yie, S.W.,.. Suh, W., Human cord blood-derived endothelial progenitor cells and their conditioned media exhibit therapeutic equivalence for diabetic wound healing. Cell Transplantation 19:12 (2010), 1635–1644.
13. King, A., Balaji, S., Keswani, S.G., Crombleholme, T.M., The role of stem cells in wound angiogenesis. Advances in Wound Care 3:10 (2014), 614–625.
14. Li, X., Chen, C., Wei, L., Li, Q., Niu, X., Xu, Y.,.. Zhao, J., Exosomes derived from endothelial progenitor cells attenuate vascular repair and accelerate reendothelialization by enhancing endothelial function. Cytotherapy 18:2 (2016), 253–262.
15. Li, N., Luo, H.C., Yang, C., Deng, J.J., Ren, M., Xie, X.Y.,.. Zhang, L.M., Cationic star-shaped polymer as a siRNA carrier for reducing MMP-9 expression in skin fibroblast cells and promoting wound healing in diabetic rats. International Journal of Nanomedicine 9 (2014), 3377–3387.
16. Liu, Y., Min, D., Bolton, T., Nube, V., Twigg, S.M., Yue, D.K., McLennan, S.V., Increased matrix metalloproteinase-9 predicts poor wound healing in diabetic foot ulcers. Diabetes Care 32:1 (2009), 117–119.
17. Madonna, R., De Caterina, R., Cellular and molecular mechanisms of vascular injury in diabetes – part II: Cellular mechanisms and therapeutic targets. Vascular Pharmacology 54:3-6 (2011), 75–79.
18. Mitchell, A., Fujisawa, T., Newby, D., Mills, N., Cruden, N.L., Vascular injury and repair: A potential target for cell therapies. Future Cardiology 11:1 (2015), 45–60.
19. Ranghino, A., Cantaluppi, V., Grange, C., Vitillo, L., Fop, F., Biancone, L.,.. Camussi, G., Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. International Journal of Immunopathology and Pharmacology 25:1 (2012), 75–85.
20. Raposo, G., Stoorvogel, W., Extracellular vesicles: Exosomes, microvesicles, and friends. The Journal of Cell Biology 200:4 (2013), 373–383.
21. Ribeiro, M.F., Zhu, H., Millard, R.W., Fan, G.C., Exosomes function in pro- and anti-angiogenesis. Current Angiogenesis 2:1 (2013), 54–59.
22. Sahoo, S., Klychko, E., Thorne, T., Misener, S., Schultz, K.M., Millay, M.,.. Losordo, D.W., Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circulation Research 109:7 (2011), 724–728.
23. Suh, W., Kim, K.L., Kim, J.M., Shin, I.S., Lee, Y.S., Lee, J.Y.,.. Kim, D.K., Transplantation of endothelial progenitor cells accelerates dermal wound healing with increased recruitment of monocytes/macrophages and neovascularization. Stem Cells 23:10 (2005), 1571–1578.
24. Tateishi-Yuyama, E., Matsubara, H., Murohara, T., Ikeda, U., Shintani, S., Masaki, H.,.. Therapeutic Angiogenesis using Cell Transplantation Study, I., Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 360:9331 (2002), 427–435.
25. Wong, V.W., Crawford, J.D., Vasculogenic cytokines in wound healing. BioMed Research International, 2013, 2013, 190486.
26. Yuan, H., Guan, J., Zhang, J., Zhang, R., Li, M., Exosomes secreted by human urine-derived stem cells accelerate skin wound healing by promoting angiogenesis in rat. Cell Biology International, 2016 [Epub ahead of print].
27. Zhang, J., Guan, J., Niu, X., Hu, G., Guo, S., Li, Q.,.. Wang, Y., Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. Journal of Translational Medicine, 13(1), 2015, 49.
28. Zhu, H., Fan, G.C., Extracellular/circulating microRNAs and their potential role in cardiovascular disease. American Journal of Cardiovascular Disease 1:2 (2011), 138–149.