Improvement of postnatal neovascularization by human embryonic stem cell-derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia

Circulation

Volumn 116, Issue 21, 2007, Pages 2409-2419

  Cho, Seung Woo ^a,b   Moon, Sung Hwan ^c   Lee, Soo Hong ^c   Kang, Sun Woong ^a   Kim, Jumi ^c   Lim, Jae Min ^a   Kim, Hyo Soo ^d   Kim, Byung Soo ^a   Chung, Hyung Min ^c  

^a Hanyang University   (South Korea)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c CHA University   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

Angiogenesis; Embryonic stem cells; Endothelial cells; Ischemia; Stem cell transplantation

Indexed keywords

MESSENGER RNA; VON WILLEBRAND FACTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SELECTION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; FEMALE; HINDLIMB ISCHEMIA; ISCHEMIA; ISOLATION PROCEDURE; LIMB SALVAGE; MOUSE; NONHUMAN; PERFUSION; PERINATAL PERIOD; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; CELL LINE; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; FEMALE; HINDLIMB; HUMANS; ISCHEMIA; MICE; MICE, NUDE; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION;

EID: 36348969952     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.106.687038     Document Type: Article

References (31)

1. Iba O, Matsubara H, Nozawa Y, Fujiyama S, Amano K, Mori Y, Kojima H, Iwasaka T. Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation. 2002;106:2019-2025.
2. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. 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.
3. Pesce M, Orlandi A, Iachininoto MG, Straino S, Torella AR, Rizzuti V, Pompilio G, Bonanno G, Scambia G, Capogrossi MC. Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res. 2003;93:e51-e62.
4. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004;109:1292-1298.
5. Madeddu P, Emanueli C, Pelosi E, Salis MB, Cerio AM, Bonanno G, Patti M, Stassi G, Condorelli G, Peschle C. Transplantation of low dose CD34+KDR+ cells promotes vascular and muscular regeneration in ischemic limbs. FASEB J. 2004;18:1737-1739.
6. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, Sung SM, Jung JS. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem. 2006;17:279-290.
7. Ma N, Stamm C, Kaminski A, Li W, Kleine HD, Muller-Hilke B, Zhang L, Ladilov Y, Egger D, Steinhoff G. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc Res. 2005;66:45-54.
8. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145-1147.
9. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2002;99:4391-4396.
10. Sone M, Itoh H, Yamashita J, Yurugi-Kobayashi T, Suzuki Y, Kondo Y, Nonoguchi A, Sawada N, Yamahara K, Miyashita K, Park K, Shibuya M, Nito S, Nishikawa S, Nakao K. Different differentiation kinetics of vascular progenitor cells in primate and mouse embryonic stem cells. Circulation. 2003;107:2085-2088.
11. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K, Nishikawa S. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 2000;408:92-96.
12. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Xu Q, Hu Y. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol. 2006;26:2244-2251.
13. Nakagami H, Nakagawa N, Takeya Y, Kashiwagi K, Ishida C, Hayashi S, Aoki M, Matsumoto K, Nakamura T, Ogihara T, Morishita R. Model of vasculogenesis from embryonic stem cells for vascular research and regenerative medicine. Hypertension. 2006;48:112-119.
14. McCloskey KE, Gilroy ME, Nerem RM. Use of embryonic stem cell-derived endothelial cells as a cell source to generate vessel structures in vitro. Tissue Eng. 2005;11:497-505.
15. Ahn SE, Kim S, Park KH, Moon SH, Lee HJ, Kim GJ, Lee YJ, Park KH, Cha KY, Chung HM. Primary bone-derived cells induce osteogenic differentiation without exogenous factors in human embryonic stem cells. Biochem Biophys Res Commun. 2006;340:403-408.
16. Park JH, Kim SJ, Oh EJ, Moon SY, Roh SI, Kim CG, Yoon HS. Establishment and maintenance of human embryonic stem cells on STO, a permanently growing cell line. Biol Reprod. 2003;69:2007-2014.
17. Couffinhal T, Silver M, Zheng LP, Kearney M, Witzenbichler B, Isner JM. Mouse model of angiogenesis. Am J Pathol. 1998;152:1667-1679.
18. Choi JH, Hur J, Yoon CH, Kim JH, Lee CS, Youn SW, Oh IY, Skurk C, Murohara T, Park YB, Walsh K, Kim HS. Augmentation of therapeutic angiogenesis using genetically modified human endothelial progenitor cells with altered glycogen synthase kinase-3beta activity. J Biol Chem. 2004;279:49430-49438.
19. Nakagami H, Maeda K, Morishita R, Iguchi S, Nishikawa T, Takami Y, Kikuchi Y, Saito Y, Tamai K, Ogihara T, Kaneda Y. 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.
20. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, Itskovitz-Eldor J, Thomson JA. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol. 2000;227:271-278.
21. O'Shea KS. Embryonic stem cell models of development. Anat Rec. 1999;257:32-41.
22. Drukker M, Katchman H, Katz G, Even-Tov Friedman S, Shezen E, Hornstein E, Mandelboim O, Reisner Y, Benvenisty N. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells. 2006;24:221-229.
23. Min JY, Yang Y, Converso KL, Liu L, Huang Q, Morgan JP, Xiao YF. Transplantation of embryonic stem cells improves cardiac function in postinfarcted rats. J Appl Physiol. 2002;92:288-296.
24. Menard C, Hagege AA, Agbulut O, Barro M, Morichetti MC, Brasselet C, Bel A, Messas E, Bissery A, Bruneval P, Desnos M, Puceat M, Menasche P. Transplantation of cardiac-committed mouse embryonic stem cells to infarcted sheep myocardium: a preclinical study. Lancet. 2005;366:1005-1012.
25. Nussbaum J, Minami E, Laflamme MA, Virag JA, Ware CB, Masino A, Muskheli V, Pabon L, Reinecke H, Murry CE. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J. 2007;21:1345-1357.
26. Kupatt C, Horstkotte J, Vlastos GA, Pfosser A, Lebherz C, Semisch M, Thalgott M, Buttner K, Browarzyk C, Mages J, Hoffmann R, Deten A, Lamparter M, Muller F, Beck H, Buning H, Boekstegers P, Hatzopoulos AK. Embryonic endothelial progenitor cells expressing a broad range of proangiogenic and remodeling factors enhance vascularization and tissue recovery in acute and chronic ischemia. FASEB J. 2005;19:1576-1578.
27. Kobayashi K, Kondo T, Inoue N, Aoki M, Mizuno M, Komori K, Yoshida J, Murohara T. 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.
28. Iwase T, Nagaya N, Fujii T, Itoh T, Ishibashi-Ueda H, Yamagishi M, Miyatake K, Matsumoto T, Kitamura S, Kangawa K. Adrenomedullin enhances angiogenic potency of bone marrow transplantation in a rat model of hindlimb ischemia. Circulation. 2005;111:356-362.
29. Kofidis T, de Bruin JL, Yamane T, Tanaka M, Lebl DR, Swijnenburg RJ, Weissman IL, Robbins RC. Stimulation of paracrine pathways with growth factors enhances embryonic stem cell engraftment and host-specific differentiation in the heart after ischemic myocardial injury. Circulation. 2005;111:2486-2493.
30. Gimond C, Marchetti S, Pages G. Differentiation of mouse embryonic stem cells into endothelial cells: genetic selection and potential use in vivo. Methods Mol Biol. 2006;330:303-329.
31. Kofidis T, Lebl DR, Martinez EC, Hoyt G, Tanaka M, Robbins RC. Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation. 2005;112(suppl):I-173-I-177.