Membrane vesicles mediate pro-angiogenic activity of equine adipose-derived mesenchymal stromal cells

Veterinary Journal

Volumn 202, Issue 2, 2014, Pages 361-366

  Pascucci, Luisa ^a   Alessandri, Giulio ^b   Dall'Aglio, Cecilia ^a   Mercati, Francesca ^a   Coliolo, Paola ^a   Bazzucchi, Cinzia ^a   Dante, Sara ^a   Petrini, Stefano ^a   Curina, Giovanni ^a   Ceccarelli, Piero ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Angiogenesis; Horse; Membrane vesicles; Mesenchymal stromal cells; Microvesicles

Indexed keywords

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL ISOLATION; CELL MIGRATION; CELL SURFACE; CELL VACUOLE; EXOSOME; LONG TERM EXPOSURE; MEMBRANE VESICLE; MESENCHYMAL STROMA CELL; NONHUMAN; SCANNING ELECTRON MICROSCOPY; ULTRACENTRIFUGATION; ADIPOSE TISSUE; ANIMAL; HORSE; MEMBRANE STRUCTURE; MESENCHYMAL STEM CELL TRANSPLANTATION; PHYSIOLOGY; VETERINARY;

EQUIDAE; RATTUS;

ANGIOGENIC FACTOR;

ADIPOSE TISSUE; ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL MEMBRANE STRUCTURES; HORSES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84919393345     PISSN: 10900233     EISSN: 15322971     Source Type: Journal    
DOI: 10.1016/j.tvjl.2014.08.021     Document Type: Article

References (41)

1. Aplin A.C., Fogel E., Zorzi P., Nicosia R.F. The aortic ring model of angiogenesis. Methods in Enzymology 2008, 443:119-136.
2. Aplin A.C., Fogel E., Nicosia R.F. MCP-1 promotes mural cell recruitment during angiogenesis in the aortic ring model. Angiogenesis 2010, 13:219-226.
3. Baglio S.R., Pegtel D.M., Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Frontiers in Physiology 2012, 3:1-11.
4. Barile L., Gherghiceanu M., Popescu L.M., Moccetti T., Vassalli G. Ultrastructural evidence of exosome secretion by progenitor cells in adult mouse myocardium and adult human cardiospheres. Journal of Biomedicine and Biotechnology 2012, 2012:1-10.
5. Boomsma R.A., Geenen D.L. Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS ONE 2012, 7:1-8.
6. Bruno S., Collini F., Deregibus M.C., Grange C., Tetta C., Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells and Development 2013, 22:758-771.
7. Camussi G., Deregibus M.C., Bruno S., Cantalupi V., Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney International 2010, 78:838-848.
8. Caplan A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. Journal of Cellular Physiology 2007, 213:341-347.
9. Caplan A.I., Bruder S.P. Mesenchymal stem cells: Building blocks for molecular medicine in the 21st century. Trends in Molecular Medicine 2001, 7:259-264.
10. Caplan A.I., Dennis J.E. Mesenchymal stem cells as trophic mediators. Journal of Cellular Biochemistry 2006, 98:1076-1084.
11. Collino F., Deregibus M.C., Bruno S., Sterpone L., Aghemo G., Viltono L., Tetta C., Camussi G. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE 2010, 5:1-15.
12. Deregibus M.C., Cantaluppi V., Calogero R., Lo Iacono M., Tetta C., Biancone L., Bruno S., Bussolati B., Camussi G. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110:2440-2448.
13. Fortier L.A., Travis A.J. Stem cells in veterinary medicine. Stem Cell Research and Therapeutics 2011, 2:9-14.
14. Gatti S., Bruno S., Deregibus M.C., Sordi A., Cantaluppi V., Tetta C., Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrology, Dialysis, Transplantation 2011, 26:1474-1483.
15. Gnecchi M., Zhang Z., Ni A., Dzau V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circulation Research 2008, 103:1204-1219.
16. Godwin E.E., Young N.J., Dudhia J., Beamish I.C., Smith R.K. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon. Equine Veterinary Journal 2012, 44:25-32.
17. Gyorgy B., Szabo T.G., Pasztoi M., Pal Z., Misjak P., Aradi B., Laszlo V., Pallinger E., Pap E., Kittel A., et al. Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cellular and Molecular Life Sciences 2011, 68:2667-2688.
18. Horwitz E.M., Prather W.R. Cytokines as the major mechanism of MSC clinical activity: Expanding the spectrum of cell therapy. Israel Medical Association World Federation Conference 2009, 1:132-133.
19. Iso Y., Spees J.L., Serrano C., Bakondi B., Pochampally R., Song Y.H., Sobel B.E., Delafontaine P., Prockop D.J. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochemical and Biophysical Research Communications 2007, 354:700-706.
20. Jaffe E.A., Nachman R.L., Becker C.G., Minick R. Culture of human endothelial cells derived from umbilical veins: Identification by morphological and immune criteria. Journal of Clinical Investigation 1973, 52:2745-2756.
21. Kim H.O., Choi S.M., Kim H.S. Mesenchymal stem cell-derived secretome and microvesicles as a cell-free therapeutics for neurodegenerative disorders. Tissue Engineering and Regenerative Medicine 2013, 10:93-101.
22. Kim H.S., Choi D.Y., Yun S.J., Choi S.M., Kang J.W., Jung J.W., Hwang D., Kim K.P., Kim D.W. Proteomic analysis of microvesicles derived from human mesenchymal stem cells. Journal of Proteome Research 2012, 11:839-849.
23. Kleinman H.K., Martin G.R. Matrigel basement membrane extracellular matrix with biological activity. Seminars in Cancer Biology 2005, 15:378-386.
24. Kopen G.C., Prockop D.J., Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proceedings of the National Academy of Sciences 1999, 96:10711-10716.
25. Lamalice L., Le Bouef F., Huot J. Endothelial cell migration during angiogenesis. Circulation Research 2007, 100:782-794.
26. Li J., Zhang Y., Liu Y., Dai X., Li W., Cai X., Yin Y., Wang Q., Xue Y., Wang C., et al. Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. The Journal of Biological Chemistry 2013, 288:23586-23596.
27. Martinez M.C., Andriantsitohaina R. Microparticles in angiogenesis: Therapeutic potential. Circulation Research 2011, 109:110-119.
28. Mezey E., Chandross K.J., Harta G., Maki R.A., McKercher S.R. Turning blood into brain: Cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000, 290:1779-1782.
29. Nicosia R.F., Ottinetti A. Growth of microvessels in serum-free matrix culture of rat aorta: A quantitative assay of angiogenesis in vitro. Laboratory Investigation 1990, 63:115-122.
30. Pascucci L., Curina G., Mercati F., Marini C., Dall'Aglio C., Paternesi B., Ceccarelli P. Flow cytometric characterization of culture expanded multipotent mesenchymal stromal cells (MSCs) from horse adipose tissue: Towards the definition of minimal stemness criteria. Veterinary Immunology and Immunopathology 2011, 144:499-506.
31. Ponce M.L. Tube formation: An in vitro matrigel angiogenesis assay. Methods in Molecular Biology 2009, 467:183-188.
32. Prockop D.J. Repair of tissues by adult stem/progenitor cells (MSCs): Controversies, myths, and changing paradigms. Molecular Therapy: The Journal of the American Society of Gene Therapy 2009, 17:939-946.
33. Raposo G., Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. Journal of Cell Biology 2013, 200:373-383. The Rockefeller University Press.
34. Sahoo S., Klychko E., Thorne T., Misener S., Schultz K.M., Millay M., Ito A., Liu T., Kamide C., Agrawal H., et al. Exosomes from human CD34+ stem cells mediate their proangiogenic paracrine activity. Circulation Research 2011, 109:724-728.
35. Shai E., Varon D. Development, cell differentiation, angiogenesis-Microparticles and their roles in angiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology 2011, 31:10-14.
36. Sykova E., Forostyak S. Stem cells in regenerative medicine. Laser Therapy 2013, 22:87-92.
37. Tetta C., Bruno S., Fonsato V., Deregibus M.C., Camussi G. The role of microvesicles in tissue repair. Organogenesis 2011, 7:105-115.
38. van der Pol E., Boing A.N., Harrison P., Sturk A., Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacological Reviews 2012, 64:676-705.
39. Vrijsen K.R., Sluijter J.P., Schuchardt M.W., van Balkom B.W., Noort W.A., Chamuleau S.A., Doevendans P.A. Cardiomyocyte progenitor cell-derived exosomes stimulate migration of endothelial cells. Journal of Cellular and Molecular Medicine 2010, 14:1064-1070.
40. Zhu W., Huang L., Li Y., Zhang X., Gu J., Yan Y., Xu X., Wang M., Qian H., Xu W. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Letters 2012, 315:28-37.
41. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A. Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell 2002, 13:4279-4295.