Harnessing the Angiogenic Potential of Stem Cell-Derived Exosomes for Vascular Regeneration

Stem Cells International

Volumn 2016, Issue , 2016, Pages

  Alcayaga Miranda, F ^a,b   Varas Godoy, M ^a   Khoury, M ^a,b,c  

^a UNIVERSIDAD DE LOS ANDES   (Chile)

^b Chilean Consortium for Regenerative Medicine   (Chile)

^c Chilean Consortium for Regenerative Medicine ^*  (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA;

ANGIOGENESIS; BIOGENESIS; BRAIN INJURY; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CEREBROVASCULAR ACCIDENT; EXOSOME; HUMAN; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOLECULAR INTERACTION; NEOPLASM; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW; STRESS; WOUND HEALING;

EID: 84966320792     PISSN: None     EISSN: 16879678     Source Type: Journal    
DOI: 10.1155/2016/3409169     Document Type: Review

References (83)

1. F. Alcayaga-Miranda, J. Cuenca, P. Luz-Crawford et al., "Characterization of menstrual stem cells: angiogenic effect, migration and hematopoietic stem cell support in comparison with bone marrow mesenchymal stem cells, " Stem Cell Research and Therapy, vol. 6, article 32, 2015.
2. P. L. González, C. Carvajal, J. Cuenca et al., "Chorion mesenchymal stem cells show superior differentiation, immunosuppressive, and angiogenic potentials in comparison with haploidentical maternal placental cells, " StemCells Translational Medicine, vol. 4, no. 10, pp. 1109-1121, 2015.
3. R. C. Lai, R. W. Y. Yeo, and S. K. Lim, "Mesenchymal stemcell exosomes, " Seminars in Cell & Developmental Biology, vol. 40, pp. 82-88, 2015.
4. M. Mendicino, A. M. Bailey, K. Wonnacott, R. K. Puri, and S. R. Bauer, "MSC-based product characterization for clinical trials: an FDA perspective, " Cell Stem Cell, vol. 14, no. 2, pp. 141-145, 2014.
5. Y. Iso, J. L. Spees, C. Serrano et al., "Multipotent human stromal cells improve cardiac function after myocardial infarction in micewithout long-termengraftment, " Biochemical and Biophysical Research Communications, vol. 354, no. 3, pp. 700-706, 2007.
6. P. Luz-Crawford, M. J. Torres, D. Noël et al., "The immunosuppressive signature of menstrual blood mesenchymal stem cells entails opposite effects on experimental arthritis and graft versus host diseases, " STEM CELLS, vol. 34, no. 2, pp. 456-469, 2016.
7. J. L. Spees, S. D. Olson, J. Ylostalo et al., "Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epitheliumby human adult stemcells from bonemarrow stroma, " Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2397-2402, 2003.
8. R. C. Lai, F. Arslan, M. M. Lee et al., "Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury, " Stem Cell Research, vol. 4, no. 3, pp. 214-222, 2010.
9. S. Rani, A. E. Ryan, M. D. Griffin, and T. Ritter, "Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications, " Molecular Therapy, vol. 23, no. 5, pp. 812-823, 2015.
10. S. R. Baglio, K. Rooijers, D. Koppers-Lalic et al., "Human bone marrow-and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species, " Stem Cell Research andTherapy, vol. 6, no. 1, article 127, 2015.
11. B. Costa-Silva, N. M. Aiello, A. J. Ocean et al., "Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver, " Nature Cell Biology, vol. 17, no. 6, pp. 816-826, 2015.
12. L. A. Mulcahy, R. C. Pink, and D. R. F. Carter, "Routes and mechanisms of extracellular vesicle uptake, " Journal of Extracellular Vesicles, vol. 3, article 24641, 2014.
13. C. Urbich, A. Kuehbacher, and S. Dimmeler, "Role of microRNAs in vascular diseases, inflammation, and angiogenesis, " Cardiovascular Research, vol. 79, no. 4, pp. 581-588, 2008.
14. A. Shabbir, A. Cox, L. Rodriguez-Menocal, M. Salgado, and B. E. Van, "Mesenchymal stem cell exosomes induce proliferation and migration of normal and chronic wound fibroblasts, and enhance angiogenesis in vitro, " Stem Cells andDevelopment, vol. 24, no. 14, pp. 1635-1647, 2015.
15. J.-K. Lee, S.-R. Park, B.-K. Jung et al., "Exosomes derived from mesenchymal stem cells suppress angiogenesis by downregulating VEGF expression in breast cancer cells, " PLoS ONE, vol. 8, no. 12, Article ID e84256, 2013.
16. M. F. Ribeiro, H. Zhu, R. W. Millard, and G. C. Fan, "Exosomes function in pro-and anti-angiogenesis, " Current Angiogenesis, vol. 2, no. 1, pp. 54-59, 2013.
17. W. Zhu, L. Huang, Y. Li et al., "Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo, " Cancer Letters, vol. 315, no. 1, pp. 28-37, 2012.
18. K. Kang, R. Ma, W. Cai et al., "Exosomes secreted from CXCR4 overexpressing mesenchymal stem cells promote cardioprotection viaAkt signaling pathway followingmyocardial infarction, " Stem Cells International, vol. 2015, Article ID 659890, 14 pages, 2015.
19. J. D. Anderson, H. J. Johansson, C. S. Graham et al., "Comprehensive proteomic analysis of mesenchymal stemcell exosomes revealsmodulationof angiogenesis vianuclear factor-Bsignaling, " STEM CELLS, vol. 34, no. 3, pp. 601-613, 2016.
20. T. Benameur, R. Soleti, C. Porro, R. Andriantsitohaina, and M. C. Martínez, "Microparticles carrying sonic hedgehog favor neovascularization through the activation of nitric oxide pathway in mice, " PLoSONE, vol. 5, no. 9, Article IDe12688, pp. 1-10, 2010.
21. H.-S. Kim, D.-Y. Choi, S. J. Yun et al., "Proteomic analysis of microvesicles derived from human mesenchymal stem cells, " Journal of Proteome Research, vol. 11, no. 2, pp. 839-849, 2012.
22. T. S. Chen, R. C. Lai, M. M. Lee, A. B. H. Choo, C. N. Lee, and S. K. Lim, "Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs, "NucleicAcids Research, vol. 38, no. 1, pp. 215-224, 2009.
23. H.-C. Zhang, X.-B. Liu, S. Huang et al., "Microvesicles derived fromhuman umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo, " Stem Cells and Development, vol. 21, no. 18, pp. 3289-3297, 2012.
24. B.-T. Pan and R. M. Johnstone, "Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor, " Cell, vol. 33, no. 3, pp. 967-978, 1983.
25. T. Katsuda, N. Kosaka, F. Takeshita, and T. Ochiya, "The therapeutic potential ofmesenchymal stem cell-derived extracellular vesicles, " Proteomics, vol. 13, no. 10-11, pp. 1637-1653, 2013.
26. A. V. Vlassov, S. Magdaleno, R. Setterquist, and R. Conrad, "Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials, " Biochimica et Biophysica Acta-General Subjects, vol. 1820, no. 7, pp. 940-948, 2012.
27. R. J. Simpson, S. S. Jensen, and J. W. E. Lim, "Proteomic profiling of exosomes: current perspectives, " Proteomics, vol. 8, no. 19, pp. 4083-4099, 2008.
28. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall, "Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, " Nature Cell Biology, vol. 9, no. 6, pp. 654-659, 2007.
29. B. Yu, X. Zhang, and X. Li, "Exosomes derived from mesenchymal stem cells, " International Journal of Molecular Sciences, vol. 15, no. 3, pp. 4142-4157, 2014.
30. L. Biancone, S. Bruno, M. C. Deregibus, C. Tetta, and G. Camussi, "Therapeutic potential of mesenchymal stem cellderived microvesicles, " Nephrology Dialysis Transplantation, vol. 27, no. 8, pp. 3037-3042, 2012.
31. S. Munich, A. Sobo-Vujanovic, W. J. Buchser, D. Beer-Stolz, and N. L. Vujanovic, "Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands, " OncoImmunology, vol. 1, no. 7, pp. 1074-1083, 2012.
32. S. C. Saunderson, P. C. Schuberth, A. C. Dunn et al., "Induction of exosome release in primary B cells stimulated via CD40 and the IL-4 receptor, " Journal of Immunology, vol. 180, no. 12, pp. 8146-8152, 2008.
33. C. Théry, M. Ostrowski, and E. Segura, "Membrane vesicles as conveyors of immune responses, " Nature Reviews Immunology, vol. 9, no. 8, pp. 581-593, 2009.
34. S. Keller, A.-K. König, F. Marmé et al., "Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes, " Cancer Letters, vol. 278, no. 1, pp. 73-81, 2009.
35. E. Cocucci, G. Racchetti, and J. Meldolesi, "Shedding microvesicles: artefacts no more, " Trends in Cell Biology, vol. 19, no. 2, pp. 43-51, 2009.
36. C. Escrevente, S. Keller, P. Altevogt, and J. Costa, "Interaction and uptake of exosomes by ovarian cancer cells, " BMC Cancer, vol. 11, no. 1, article 108, 2011.
37. R. J. Simpson, H. Kalra, and S. Mathivanan, "ExoCarta as a resource for exosomal research, " Journal of Extracellular Vesicles, vol. 1, Article ID18374, pp. 1-6, 2012.
38. J. Zhang, S. Li, L. Li et al., "Exosome and exosomal microRNA: trafficking, sorting, and function, " Genomics, Proteomics and Bioinformatics, vol. 13, no. 1, pp. 17-24, 2015.
39. J. Guduric-Fuchs, A. O'Connor, B. Camp, C. L. O'Neill, R. J. Medina, and D. A. Simpson, "Selective extracellular vesiclemediated export of an overlapping set of microRNAs from multiple cell types, " BMC Genomics, vol. 13, no. 1, article 357, 2012.
40. K. Ohshima, K. Inoue, A. Fujiwara et al., "Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line, " PLoS ONE, vol. 5, no. 10, Article ID e13247, 2010.
41. J. Skog, T. Würdinger, S. van Rijn et al., "Glioblastoma microvesicles transport RNAand proteins that promote tumour growth and provide diagnostic biomarkers, " Nature Cell Biology, vol. 10, no. 12, pp. 1470-1476, 2008.
42. J. Silva, V. García, Á Zaballos et al., "Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival, " European Respiratory Journal, vol. 37, no. 3, pp. 617-623, 2011.
43. C. Salomon, J. Ryan, L. Sobrevia et al., "Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis, " PLoS ONE, vol. 8, no. 7, pp. 1-24, 2013.
44. L. Kilpinen, U. Impola, L. Sankkila et al., "Extracellular membrane vesicles from umbilical cord blood-derived MSC protect against ischemic acute kidney injury, a feature that is lost after inflammatory conditioning, " Journal of Extracellular Vesicles, vol. 2, pp. 1-15, 2013.
45. A. Del Fattore, R. Luciano, R. Saracino et al., "Differential effects of extracellular vesicles secreted by mesenchymal stem cells fromdifferent sources on glioblastoma cells, " ExpertOpinion on BiologicalTherapy, vol. 15, no. 4, pp. 495-504, 2015.
46. D. Ti, H. Hao, C. Tong et al., "LPS-preconditionedmesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b, " Journal of Translational Medicine, vol. 13, no. 1, article 308, 2015.
47. H. Xin, Y. Li, Y. Cui, J. J. Yang, Z. G. Zhang, and M. Chopp, "Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats, " Journal of Cerebral Blood Flow and Metabolism, vol. 33, no. 11, pp. 1711-1715, 2013.
48. Y. Zhang, M. Chopp, Y. Meng et al., "Effect of exosomes derived frommultipluripotentmesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury, " Journal of Neurosurgery, vol. 122, no. 4, pp. 856-867, 2015.
49. S. Bian, L. Zhang, L. Duan, X. Wang, Y. Min, and H. Yu, "Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model, " Journal of Molecular Medicine, vol. 92, no. 4, pp. 387-397, 2014.
50. X. Teng, L. Chen, W. Chen, J. Yang, Z. Yang, and Z. Shen, "Mesenchymal stem cell-derived exosomes improve the microenvironment of infarctedmyocardium contributing to angiogenesis and anti-inflammation, " Cellular Physiology and Biochemistry, vol. 37, no. 6, pp. 2415-2424, 2015.
51. Y. Zhao, X. Sun, W. Cao et al., "Exosomes derived from human umbilical cordmesenchymal stem cells relieve acutemyocardial ischemic injury, " Stem Cells International, vol. 2015, Article ID 761643, 12 pages, 2015.
52. S. M. Watt, F. Gullo, M. Van Der Garde et al., "The angiogenic properties of mesenchymal stem/stromal cells and their therapeutic potential, " British Medical Bulletin, vol. 108, no. 1, pp. 25-53, 2013.
53. S. Pacini and I. Petrini, "Are MSCs angiogenic cells New insights on human nestin-positive bone marrow-derived multipotent cells, " Frontiers in Cell and Developmental Biology, vol. 2, article 20, 2014.
54. M. Khoury, F. Alcayaga-Miranda, S. E. Illanes, and F. E. Figueroa, "The promising potential of menstrual stem cells for antenatal diagnosis and cell therapy, " Frontiers in Immunology, vol. 5, p. 205, 2014.
55. H. Wegmeyer, A.-M. Bröske, M. Leddin et al., "Mesenchymal stromal cell characteristics vary depending on their origin, " Stem Cells and Development, vol. 22, no. 19, pp. 2606-2618, 2013.
56. T. Lopatina, S. Bruno, C. Tetta, N. Kalinina, M. Porta, and G. Camussi, "Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential, " Cell Communication and Signaling, vol. 12, no. 1, article 26, 2014.
57. J. Matsui, T. Wakabayashi, M. Asada, K. Yoshimatsu, and M. Okada, "Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells, "The Journal of Biological Chemistry, vol. 279, no. 18, pp. 18600-18607, 2004.
58. A. M. Abu El-Asrar, S. Struyf, G. Opdenakker, J. van Damme, and K. Geboes, "Expression of stem cell factor/c-kit signaling pathway components in diabetic fibrovascular epiretinal membranes, " Molecular Vision, vol. 16, pp. 1098-1107, 2010.
59. X. Wang, H. Gu, D. Qin et al., "Exosomal miR-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis, " Scientific Reports, vol. 5, Article ID 13721, 2015.
60. X. Li, C. Chen, L. Wei et al., "Exosomesderived fromendothelial progenitor cells attenuate vascular repair and accelerate reendothelialization by enhancing endothelial function, " Cytotherapy, vol. 18, no. 2, pp. 253-262, 2016.
61. F. T. Borges, S. A. Melo, B. C. Özdemir et al., "TGF-1-Containing exosomes from injured epithelial cells activate fibroblasts to initiate tissue regenerative responses and fibrosis, " Journal of theAmerican Society of Nephrology, vol. 24, no. 3, pp. 385-392, 2013.
62. P. Kucharzewska, H. C. Christianson, J. E. Welch et al., "Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development, " Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 18, pp. 7312-7317, 2013.
63. L. Kordelas, V. Rebmann, A.-K. Ludwig et al., "MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versushost disease, " Leukemia, vol. 28, no. 4, pp. 970-973, 2014.
64. S. Xu, J. Wang, N. Ding et al., "Exosome-mediated microRNA transfer plays a role in radiation-induced bystander effect, " RNA Biology, vol. 12, no. 12, pp. 1355-1363, 2015.
65. K. B. Johnsen, J. M. Gudbergsson, M. N. Skov, L. Pilgaard, T. Moos, and M. Duroux, "A comprehensive overview of exosomes as drug delivery vehicles-endogenous nanocarriers for targeted cancer therapy, " Biochimica et Biophysica Acta-Reviews on Cancer, vol. 1846, no. 1, pp. 75-87, 2014.
66. G. Fuhrmann, A. Serio, M. Mazo, R. Nair, and M. M. Stevens, "Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins, " Journal of Controlled Release, vol. 205, pp. 35-44, 2015.
67. A. S. Go, D. Mozaffarian, V. L. Roger et al., "Heart disease and stroke statistics-2014 update: a report from the American Heart Association, " Circulation, vol. 125, no. 1, pp. e28-e292, 2013.
68. A. J. Boyle, S. P. Schulman, and J. M. Hare, "Stem cell therapy for cardiac repair: ready for the next step, " Circulation, vol. 114, no. 4, pp. 339-352, 2006.
69. S. H. Ranganath, O. Levy, M. S. Inamdar, and J. M. Karp, "Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease, " Cell Stem Cell, vol. 10, no. 3, pp. 244-258, 2012.
70. M. Takahashi, T.-S. Li, R. Suzuki et al., "Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes fromischemic injury, " American Journal of Physiology-Heart and Circulatory Physiology, vol. 291, no. 2, pp. H886-H893, 2006.
71. M. Korf-Klingebiel, T. Kempf, T. Sauer et al., "Bone marrowcells are a rich source of growth factors and cytokines: implications for cell therapy trials after myocardial infarction, " European Heart Journal, vol. 29, no. 23, pp. 2851-2858, 2008.
72. L. Timmers, S. K. Lim, F. Arslan et al., "Reduction ofmyocardial infarct size by human mesenchymal stem cell conditioned medium, " Stem Cell Research, vol. 1, no. 2, pp. 129-137, 2008.
73. T. Zhang, Y. Lee, Y. Rui, T. Cheng, X. Jiang, and G. Li, "Bone marrow-derived mesenchymal stem cells promote growth and angiogenesis of breast and prostate tumors, " Stem Cell Research &Therapy, vol. 4, no. 3, article 70, 2013.
74. B. M. Beckermann, G. Kallifatidis, A. Groth et al., "VEGF expression by mesenchymal stemcells contributes to angiogenesis in pancreatic carcinoma, " British Journal of Cancer, vol. 99, no. 4, pp. 622-631, 2008.
75. S. Orecchioni, G. Gregato, I. Martin-Padura et al., "Complementary populations of human adipose CD34+ progenitor cells promote growth, angiogenesis, and metastasis of breast cancer, " Cancer Research, vol. 73, no. 19, pp. 5880-5891, 2013.
76. M. Kéramidas, F. de Fraipont, A. Karageorgis et al., "The dual effect of mscs on tumour growth and tumour angiogenesis, " Stem Cell Research &Therapy, vol. 4, no. 2, article 41, 2013.
77. K. Otsu, S. Das, S. D. Houser, S. K. Quadri, S. Bhattacharya, and J. Bhattacharya, "Concentration-dependent inhibition of angiogenesis by mesenchymal stemcells, " Blood, vol. 113, no. 18, pp. 4197-4205, 2009.
78. I. A. W. Ho, H. C. Toh, W. H. Ng et al., "Human bone marrow-derived mesenchymal stem cells suppress human glioma growth through inhibition of angiogenesis, " Stem Cells, vol. 31, no. 1, pp. 146-155, 2013.
79. M. G. Tonnesen, X. Feng, and R. A. F. Clark, "Angiogenesis in wound healing, " Journal of Investigative Dermatology Symposium Proceedings, vol. 5, no. 1, pp. 40-46, 2000.
80. E. K. Jun, Q. Zhang, B. S. Yoon et al., "Hypoxic conditioned medium from human amniotic fluid-derived mesenchymal stem cells accelerates skin wound healing through TGF-/SMAD2 and PI3K/AKT pathways, " International Journal of Molecular Sciences, vol. 15, no. 1, pp. 605-628, 2014.
81. M. N. M. Walter, K. T. Wright, H. R. Fuller, S. MacNeil, and W. E. B. Johnson, "Mesenchymal stem cell-conditioned medium accelerates skin wound healing: an in vitro study of fibroblast and keratinocyte scratch assays, " Experimental Cell Research, vol. 316, no. 7, pp. 1271-1281, 2010.
82. S. Sano, K. S. Chan, and J. DiGiovanni, "Impact of Stat3 activation upon skin biology: a dichotomy of its role between homeostasis and diseases, " Journal of Dermatological Science, vol. 50, no. 1, pp. 1-14, 2008.
83. J. Zhang, J. Guan, X. Niu et al., "Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis, " Journal of Translational Medicine, vol. 13, no. 1, article 49, 2015.