Peripheralblood-derivedmesenchymalstromalcells promote angiogenesis via paracrine stimulation of vascular endothelial growth factor secretion in the equine model

Stem Cells Translational Medicine

Volumn 3, Issue 12, 2014, Pages 1514-1525

  Bussche, Leen ^a   Van De Walle, Gerlinde R ^a  

^a Cornell University ^*  (United States)

Author keywords

Mesenchymal stromal cells; Secretome; Vascular endothelial growth factor; Angiogenesis

Indexed keywords

ACTIVIN A; ANGIOPOIETIN 1; BETA1 INTEGRIN; ENDOGLIN; ENDOTHELIN 1; HERMES ANTIGEN; INTERLEUKIN 8; PLATELET DERIVED GROWTH FACTOR AA; SOMATOMEDIN BINDING PROTEIN 2; THY 1 ANTIGEN; UROKINASE; VASCULOTROPIN; VASCULOTROPIN A; CULTURE MEDIUM;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ANIMAL CELL; ARTICLE; BRDU ASSAY; CELL DIFFERENTIATION ASSAY; CELL FUNCTION; CELL PROLIFERATION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EQUIDAE; FLOW CYTOMETRY; GENE EXPRESSION; MESENCHYMAL STROMA CELL; NONHUMAN; PARACRINE SIGNALING; PERIPHERAL BLOOD DERIVED MESENCHYMAL STROMAL CELL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CULTURE MEDIUM; CYTOLOGY; HORSE; METABOLISM; PHARMACOLOGY; SECRETION (PROCESS);

EQUIDAE;

ANIMALS; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; HORSES; MESENCHYMAL STROMAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84913582222     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2014-0138     Document Type: Article

References (55)

1. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-660.
2. Yoo SY, Kwon SM. Angiogenesis and its therapeutic opportunities. Mediators Inflamm 2013;2013:e127170.
3. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011;146:873-887.
4. Sunkomat JNE, Gaballa MA. Stem cell therapy in ischemic heart disease. Cardiovasc Drug Rev 2003;21:327-342.
5. Li Y, Chen J, Chen XG et al. Human marrow stromal cell therapy for stroke in rat: Neurotro-phins and functional recovery. Neurology 2002; 59:514-523.
6. Li Y, Chen J, Zhang CL et al. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 2005;49: 407-417.
7. Tang YL, Tang Y, Zhang YC et al. Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol 2005; 46:1339-1350.
8. Togel F, Hu Z, Weiss K et al. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005;289:F31-F42.
9. Zhu X-Y, Lerman A, Lerman LO. Concise review: Mesenchymal stem cell treatment for ischemic kidney disease. Stem Cells 2013;31: 1731-1736.
10. Liew A, O’Brien T. Therapeutic potential for mesenchymal stem cell transplantation in critical limb ischemia. Stem Cell Res Ther 2012;3:28.
11. Altaner C, Altanerova V, Cihova M et al. Characterization of mesenchymal stem cells of “no-options” patients with critical limb ischemia treated by autologous bone marrow mononuclear cells. PLoS One 2013;8:e73722.
12. Bura A, Planat-Benard V, Bourin P et al. Phase I trial: The use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia. Cytotherapy 2014;16:245-257.
13. Das AK, Bin Abdullah BJ, Dhillon SS et al. Intra-arterial allogeneic mesenchymal stem cells for critical limb ischemia are safe and efficacious: Report of a phase I study. World J Surg 2013;37:915-922.
14. Kaneko E, Izumimoto N, Toyoshima K et al. Therapeutic angiogenesis for critical limb ischemia. Nippon Ronen Igakkai Zasshi 2013; 50:366-368.
15. Zhi K, Gao Z, Bai J et al. Application of adipose-derived stem cells in critical limb ischemia. Front Biosci (Landmark Ed) 2014;19: 768–776.
16. Lee EJ, Park H-W, Jeon H-J et al. Potentiated therapeutic angiogenesis by primed human mesenchymal stem cells in a mouse model of hindlimb ischemia. Regen Med 2013; 8:283–293.
17. Chen CP, Lee YJ, Chiu ST et al. The application of stem cells in the treatment of ischemic diseases. Histol Histopathol 2006;21: 1209–1216.
18. Ranganath SH, Levy O, Inamdar MS et al. Harnessing the mesenchymal stem cell secre-tome for the treatment of cardiovascular disease. Cell Stem Cell 2012;10:244–258.
19. De Schauwer C, Van de Walle GR, Van Soom A et al. Mesenchymal stem cell therapy in horses: Useful beyond orthopedic injuries? Vet Q 2013;33:234–241.
20. Gershwin LJ. Veterinary autoimmunity: Autoimmune diseases in domestic animals. Ann N Y Acad Sci 2007;1109:109–116.
21. Bähr A, Wolf E. Domestic animal models for biomedical research. Reprod Domest Anim 2012;47(suppl 4):59–71.
22. Fureix C, Jego P, Henry S et al. Towardsan ethological animal model of depression? A study on horses. PLoS One 2012;7:e39280.
23. Gregory MH, Capito N, Kuroki K et al. A review of translational animal models for knee osteoarthritis. Arthritis 2012;2012:e764621.
24. Spaas JH, Guest DJ, Van de Walle GR. Tendon regeneration in human and equine athletes: Ubi Sumus-Quo Vadimus (where are we and where are we going to)? Sports Med 2012;42:871–890.
25. Spaas JH, Schauwer C, De Cornillie P et al. Culture and characterisation of equine peripheral blood mesenchymal stromal cells. Vet J 2013;195:107–113.
26. De Schauwer C, van de Walle GR, Piepers S et al. Successful isolation of equine mesenchy-mal stromal cells from cryopreserved umbilical cord blood-derived mononuclear cell fractions. Equine Vet J 2013;45:518–522.
27. De Schauwer C, Goossens K, Piepers S et al. Characterization and profilingofimmuno-modulatory genesofequine mesenchymal stro-mal cells from non-invasive sources. Stem Cell Res Ther 2014;5:6.
28. Van de Walle GR, Peters ST, VanderVen BC et al. Equine herpesvirus 1 entry via endocy-tosis is facilitated by alphaV integrins and an RSD motif in glycoprotein D. J Virol 2008;82: 11859–11868.
29. Schnabel LV, Pezzanite LM, Antczak DF et al. Equine bone marrow-derived mesenchy-mal stromal cells are heterogeneous in MHC class II expression and capableofinciting anim-mune response in vitro. Stem Cell Res Ther 2014;5:13.
30. Bara JJ, McCarthy HE, Humphrey E et al. Bone marrow-derived mesenchymal stem cells become antiangiogenic when chondrogenically or osteogenically differentiated: Implications for bone and cartilage tissue engineering. Tissue Eng Part A 2014; 20:147–159.
31. Yew T-L, Hung Y-T, Li H-Y et al. Enhancement of wound healing by human multipotent stromal cell conditioned medium: The para-crine factors and p38 MAPK activation. Cell Transplant 2011;20:693–706.
32. Liu Y, Han ZP, Zhang SS et al. Effects of inflammatory factors on mesenchymal stem cells and their role in the promotion of tumor angio-genesis in colon cancer. J Biol Chem 2011;286: 25007–25015.
33. Smith AN, Muffley LA, Bell AN et al. Un-saturated fatty acids induce mesenchymal stem cells to increase secretion of angiogenic mediators. J Cell Physiol 2012;227:3225–3233.
34. Yu X, Lu C, Liu H et al. Hypoxic preconditioning with cobalt of bone marrow mesenchy-mal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. PLoS One 2013;8:e62703.
35. Hoeben A, Landuyt B, Highley MS et al. Vascular endothelial growth factor and angio-genesis. Pharmacol Rev 2004;56:549–580.
36. Spinella F, Rosanó L, Di Castro V et al. Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1a in ovarian carcinoma cells. J Biol Chem 2002; 277:27850–27855.
37. Shikada Y, Yonemitsu Y, Koga T et al. Platelet-derived growth factor-AA is an essential and autocrine regulator of vascular endo-thelial growth factor expression in non-small cell lung carcinomas. Cancer Res 2005;65: 7241–7248.
38. Martin D, Galisteo R, Gutkind JS. CXCL8/IL8 stimulates vascular endothelial growth factor (VEGF) expression and the auto-crine activation of VEGFR2 in endothelial cells by activating NFkappaB through the CBM (Carma3/Bcl10/Malt1) complex. J Biol Chem 2009;284:6038–6042.
39. Azar WJ, Azar SHX, Higgins S et al. IGFBP-2 enhances VEGF gene promoter activity and consequent promotion of angiogenesis by neuroblastoma cells. Endocrinology 2011;152: 3332–3342.
40. Das SK, Bhutia SK, Azab B et al. MDA-9/syntenin and IGFBP-2 promote angiogenesis in human melanoma. Cancer Res 2013;73: 844–854.
41. Katare R, Riu F, Rowlinson J et al. Perivas-cular delivery of encapsulated mesenchymal stem cells improves postischemic angiogenesis via paracrine activation of VEGF-A. Arterioscler Thromb Vasc Biol 2013;33:1872–1880.
42. Wang C-Y, Yang H-B, Hsu H-S et al. Mes-enchymal stem cell-conditioned medium facilitates angiogenesis and fracture healing in diabetic rats. J Tissue Eng Regen Med 2012;6: 559–569.
43. Bhang SH, Lee S, Shin J-Y et al. Efficacious and clinically relevant conditioned medium of human adipose-derived stem cells for therapeutic angiogenesis. Mol Ther 2014;22:862–872.
44. Boomsma RA, Geenen DL. Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS One 2012;7: e35685.
45. Kamal A, Iskandriati D, Dilogo I et al. Com-parisonof cultured mesenchymal stem cells derived from bone marrow or peripheral blood of rats. J Exp Integr Med 2014;4:17–22.
46. Chong P-P, Selvaratnam L, Abbas AA et al. Human peripheral blood derived mesenchymal stem cells demonstrate similar characteristics and chondrogenic differentiation potential to bone marrow derived mesenchymal stem cells. J Orthop Res 2012;30:634–642.
47. Watt SM, Gullo F, van der Garde M et al. The angiogenic properties of mesenchymal stem/stromal cells and their therapeutic potential. Br Med Bull 2013;108:25–53.
48. Windmolders S, De Boeck A, Koninckx R et al. Mesenchymal stem cell secreted platelet derived growth factor exerts a pro-migratory effect on resident cardiac atrial appendage stem Cells. J Mol Cell Cardiol 2014;66:177–188.
49. Salama M, Andrukhova O, Jaksch P et al. Endothelin-1 governs proliferation and migration of bronchoalveolar lavage-derived lung mesen-chymal stem cells in bronchiolitis obliterans syndrome. Transplantation 2011;92:155–162.
50. Salani D, Taraboletti G, Rosanò L et al. Endothelin-1 induces an angiogenic phenotype in cultured endothelialcells and stimulatesneo-vascularization in vivo. Am J Pathol 2000;157: 1703–1711.
51. Huang S-P, Wu M-S, Shun C-T et al. Interleukin-6 increases vascular endothelial growth factor and angiogenesis in gastric carcinoma. J Biomed Sci 2004;11:517–527.
52. Wu M-H, Huang C-Y, Lin J-A et al. Endothelin-1 promotes vascular endothelial growth factor-dependent angiogenesis in human chondro-sarcoma cells. Oncogene 2014;33:1725–1735.
53. Hou Y, Ryu CH, Jun JA et al. IL-8 enhances the angiogenic potential of human bone marrow mesenchymal stem cells by increasing vascular endothelial growth factor. Cell Biol Int 2014;38:1050–1059.
54. Müller K, Ellenberger C, Schoon H-A. His-tomorphological and immunohistochemical study of angiogenesis and angiogenic factors in the ovary of the mare. Res Vet Sci 2009;87: 421–431.
55. Müller K, Ellenberger C, Hoppen H-O et al. Immunohistochemical study of angiogen-esis and angiogenic factors in equine granulosa cell tumours. Res Vet Sci 2012;92:471–477.