Locally delivered growth factor enhances the angiogenic efficacy of adipose-derived stromal cells transplanted to ischemic limbs

Stem Cells

Volumn 27, Issue 8, 2009, Pages 1976-1986

  Bhang, Suk Ho ^a   Cho, Seung Woo ^b   Lim, Jae Min ^a   Kang, Jin Muk ^a   Lee, Tae Jin ^a   Yang, Hee Seok ^a   Song, Young Soo ^a   Park, Moon Hyang ^a   Kim, Hyo Soo ^d   Yoo, Kyung Jong ^e   Jang, Yangsoo ^e   Langer, Robert ^b,c   Anderson, Daniel G ^c   Kim, Byung Soo ^a  

^a Hanyang University   (South Korea)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Seoul National University College of Medicine   (South Korea)

^e Yonsei University College of Medicine   (South Korea)

Author keywords

Fibroblast growth factor 2; Hind limb ischemia; Human adipose derived stromal cell; Local delivery; Paracrine effect; Therapeutic angiogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GROWTH FACTOR; HEPARIN; OXYGEN; SCATTER FACTOR; VASCULOTROPIN;

ADIPOSE TISSUE DERIVED STROMAL CELL; ANGIOGENESIS; ARTICLE; CELL TRANSPLANTATION; CELLULAR DISTRIBUTION; DRUG EFFICACY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMB ISCHEMIA; PARACRINE SIGNALING; STEM CELL TRANSPLANTATION; STROMA CELL;

ADIPOSE TISSUE; ADIPOSITY; ANGIOGENESIS INDUCING AGENTS; ANGIOGENIC PROTEINS; ANIMALS; APOPTOSIS; CELL HYPOXIA; DISEASE MODELS, ANIMAL; FIBROBLAST GROWTH FACTOR 2; FLUORESCENT ANTIBODY TECHNIQUE; HINDLIMB; HUMANS; ISCHEMIA; LIMB SALVAGE; MICE; MICE, NUDE; STROMAL CELLS;

EID: 69249149297     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.115     Document Type: Article

References (51)

1. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001;7:211-228.
2. Zuk PA, Zhu M, Ashjian P, De Ugarte DA et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-4295.
3. Tholpady SS, Katz AJ, Ogle RC. Mesenchymal stem cells from rat visceral fat exhibit multipotential differentiation in vitro. Anat Rec A Discov Mol Cell Evol Biol 2003;272:398-402.
4. Miranville A, Heeschen C, Sengenès C et al. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 2004;110:349-355.
5. Planat-Benard V, Silvestre JS, Cousin B et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004;109:656-663.
6. Rehman J, Traktuev D, Li J et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004;109:1292-1298.
7. Cai L, Johnstone BH, Cook TG et al. Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells 2007;25:3234-3243.
8. Nakagami H, Maeda K, Morishita R et al. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 2005;25:2542-2547.
9. Miyahara Y, Nagaya N, Kataoka M et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006;12:459-465.
10. Valina C, Pinkernell K, Song YH et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 2007;28:2667-2677.
11. Entenmann G, Hauner H. Relationship between replication and differentiation in cultured human adipocyte precursor cells. Am J Physiol 1996;270:C1011--C1016.
12. 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.
13. Zhu W, Chen J, Cong X et al. Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006;24:416-425.
14. Toma C, Pittenger MF, Cahill KS et al. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002;105:93-98.
15. Zhang M, Methot D, Poppa V et al. Cardiomyocyte grafting for cardiac repair: graft cell death and antideath strategies. J Mol Cell Cardiol 2001;33:907-921.
16. Hill E, Boontheekul T, Mooney DJ. Regulating activation of transplanted cells controls tissue regeneration. Proc Natl Acad Sci U S A 2006;103:2494-2499.
17. Jeon O, Kang SW, Lim HW et al. Long-term and zero-order release of basic fibroblast growth factor from heparin-conjugated poly(L-lactide-co-glycolide) nanospheres and fibrin gel. Biomaterials 2006;27:1598-1607.
18. Cho SW, Song KW, Rhie JW et al. Engineered adipose tissue formation enhanced by basic fibroblast growth factor and a mechanically stable environment. Cell Transplant 2007;16:421-434.
19. Cho SW, Moon SH, Lee SH et al. Improvement of postnatal neovascularization by human embryonic stem cell derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation 2007;116:2409-2419.
20. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Institutes of Health; 1996. NIH publication no. 85-23.
21. Bhang SH, Lee YE, Cho SW et al. Basic fibroblast growth factor promotes bone marrow stromal cell transplantation-mediated neural regeneration in traumatic brain injury. Biochem Biophys Res Commun 2007;359:40-45.
22. Iba O, Matsubara H, Nozawa Y et al. Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation 2002;106:2019-2025.
23. Kamihata H, Matsubara H, Nishiue T et al. Improvement of collateral perfusion and regional function by implantation of peripheral blood mononuclear cells into ischemic hibernating myocardium. Arterioscler Thromb Vasc Biol 2002;22:1804-1810.
24. Kocher AA, Schuster MD, Szabolcs MJ et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001;7:430-436.
25. Shintani S, Murohara T, Ikeda H et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 2001;103:897-903.
26. Kalka C, Masuda H, Takahashi T et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 2000;97:3422-3427.
27. Tateishi-Yuyama E, Matsubara H, Murohara T et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 2002;360:427-435.
28. Yamashiro H, Inamoto T, Yagi M et al. Efficient proliferation and adipose differentiation of human adipose tissue-derived vascular stromal cells transfected with basic fibroblast growth factor gene. Tissue Eng 2003;9:881-892.
29. Song H, Kwon K, Lim S et al. Transfection of mesenchymal stem cells with the FGF-2 gene improves their survival under hypoxic conditions. Mol Cells 2005;19:402-407.
30. Tokuda H, Kozawa O, Uematsu T. Basic fibroblast growth factor stimulates vascular endothelial growth factor release in osteoblasts: divergent regulation by p42/p44 mitogen-activated protein kinase and p38 mitogen-activated protein kinase. J Bone Miner Res 2000;15:2371-2379.
31. Nugent MA, Iozzo RV. Fibroblast growth factor-2. Int J Biochem Cell Biol 2000;32:15-20.
32. Shi YH, Bingle L, Gong LH et al. Basic FGF augments hypoxia induced HIF-1-alpha expression and VEGF release in T47D breast cancer cells. Pathology 2007;39:396-400.
33. Calvani M, Rapisarda A, Uranchimeg B et al. Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. Blood 2006;107:2705-2712.
34. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003;9:677-684.
35. Li QF, Wang XR, Yang YW et al. Hypoxia upregulates hypoxia inducible factor (HIF)-3alpha expression in lung epithelial cells: characterization and comparison with HIF-1alpha. Cell Res 2006;16:548-558.
36. Yoon CH, Hur J, Oh IY et al. Intercellular adhesion molecule-1 is upregulated in ischemic muscle, which mediates trafficking of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2006;26:1066-1072.
37. Traktuev DO, Merfeld-Clauss S, Li J et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008;102:77-85.
38. Zannettino AC, Paton S, Arthur A et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008;214:413-421.
39. Sasaki K, Murohara T, Ikeda H et al. Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis. J Clin Invest 2002;109:603-611.
40. Ziebart T, Yoon CH, Trepels T et al. Sustained persistence of transplanted proangiogenic cells contributes to neovascularization and cardiac function after ischemia. Circ Res 2008;103:1327-1334.
41. Ryu JH, Kim IK, Cho SW et al. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 2005;26:319-326.
42. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-676.
43. Kim SE, Jeon O, Lee JB et al. Enhancement of ectopic bone formation by bone morphogenetic protein-2 delivery using heparin-conjugated PLGA nanoparticles with transplantation of bone marrow-derived mesenchymal stem cells. J Biomed Sci 2008;15:771-777.
44. Gnecchi M, He H, Liang OD et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368.
45. Gnecchi M, He H, Noiseux N et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006;20:661-669.
46. Li W, Ma N, Ong LL et al. Bcl-2 engineered MSCs inhibited apoptosis and improved heart function. Stem Cells 2007;25:2118-2127.
47. Kobayashi K, Kondo T, Inoue N et al. Combination of in vivo angiopoietin-1 gene transfer and autologous bone marrow cell implantation for functional therapeutic angiogenesis. Arterioscler Thromb Vasc Biol 2006;26:1465-1472.
48. Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003;4:346-358.
49. Merdan T, Kopecek J, Kissel T. Prospects for cationic polymers in gene and oligonucleotide therapy against cancer. Adv Drug Deliv Rev 2002;54:715-758.
50. Ashikari-Hada S, Habuchi H, Kariya Y et al. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem 2004;279:12346-12354.
51. Richardson TP, Peters MC, Ennett AB et al. Polymeric system for dual growth factor delivery. Nat Biotechnol 2001;19:1029-1034.