Stem cell-based therapies to promote angiogenesis in ischemic cardiovascular disease

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 4, 2016, Pages H455-H465

  Hou, Luqia ^a,b   Kim, Joseph J ^a,b   Woo, Y Joseph ^b   Huang, Ngan F ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Angiogenesis; Hindlimb ischemia; Myocardial infarction; Peripheral arterial disease; Pluripotent stem cell; Stem cell therapy

Indexed keywords

ADULT STEM CELL; ANGIOGENESIS; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELLS BY BODY ANATOMY; ENDOTHELIAL PROGENITOR CELL; HEART INFARCTION; HUMAN; MESENCHYMAL STEM CELL; MONONUCLEAR CELL; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION; TREATMENT INDICATION; ANIMAL; ISCHEMIA; MYOCARDIAL ISCHEMIA; PROCEDURES;

ANIMALS; HUMANS; ISCHEMIA; MYOCARDIAL ISCHEMIA; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION;

EID: 84958568576     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00726.2015     Document Type: Review

References (119)

1. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8: 376-388, 2011.
2. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997.
3. Asahara T, Kawamoto A. Endothelial progenitor cells for postnatal vasculogenesis. Am J Physiol Cell Physiol 287: C572-C579, 2004.
4. Asahara T, Kawamoto A, Masuda H. Concise review: Circulating endothelial progenitor cells for vascular medicine. Stem Cells 29: 1650-1655, 2011.
5. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106: 3009-3017, 2002.
6. Baranski JD, Chaturvedi RR, Stevens KR, Eyckmans J, Carvalho B, Solorzano RD, Yang MT, Miller JS, Bhatia SN, Chen CS. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc Natl Acad Sci USA 110: 7586-7591, 2013.
7. Bernacki SH, Wall ME, Loboa EG. Isolation of human mesenchymal stem cells from bone and adipose tissue. Methods Cell Biol 86: 257-278, 2008.
8. Boilson BA, Kiernan TJ, Harbuzariu A, Nelson RE, Lerman A, Simari RD. Circulating CD34_cell subsets in patients with coronary endothelial dysfunction. Nat Clin Pract Cardiovasc Med 5: 489-496, 2008.
9. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 98: 2396-2402, 2001.
10. Caplan AI. Mesenchymal stem cells. J Orthop Res 9: 641-650, 1991.
11. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864, 2004.
12. Chen X, Aledia AS, Popson SA, Him L, Hughes CC, George SC. Rapid anastomosis of endothelial progenitor cell-derived vessels with host vasculature is promoted by a high density of cotransplanted fibroblasts. Tissue Eng Part A 16: 585-594, 2010.
13. Cho SW, Moon SH, Lee SH, Kang SW, Kim J, Lim JM, Kim HS, Kim BS, Chung HM. Improvement of postnatal neovascularization by human embryonic stem cell derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation 116: 2409-2419, 2007.
14. Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ, Mahoney WM, Van Biber B, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem HP, Laflamme MA, Murry CE. Human embryonic-stem-cellderived cardiomyocytes regenerate non-human primate hearts. Nature 510: 273-277, 2014.
15. Cooke JP, Losordo DW. Modulating the vascular response to limb ischemia: angiogenic and cell therapies. Circ Res 116: 1561-1578, 2015.
16. Costa AR, Panda NC, Yong S, Mayorga ME, Pawlowski GP, Fan K, Penn MS, Laurita KR. Optical mapping of cryoinjured rat myocardium grafted with mesenchymal stem cells. Am J Physiol Heart Circ Physiol 302: H270-H277, 2012.
17. De Haro J, Acin F, Lopez-Quintana A, Florez A, Martinez-Aguilar E, Varela C. Meta-analysis of randomized, controlled clinical trials in angiogenesis: gene and cell therapy in peripheral arterial disease. Heart Vessels 24: 321-328, 2009.
18. Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28: 875-884, 2000.
19. Dormandy JA, Rutherford RB. Management of peripheral arterial disease (PAD). TASC Working Group TransAtlantic Inter-Society Consensus (TASC). J Vasc Surg 31: S1-S296, 2000.
20. Gallo P, Peschle C, Condorelli G. Sources of cardiomyocytes for stem cell therapy: an update. Pediatr Res 59: 79R-83R, 2006.
21. Gersh BJ, Simari RD, Behfar A, Terzic CM, Terzic A. Cardiac cell repair therapy: a clinical perspective. Mayo Clin Proc 84: 876-892, 2009.
22. Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 20: 661-669, 2006.
23. Goumans MJ, Maring JA, Smits AM. A straightforward guide to the basic science behind cardiovascular cell-based therapies. Heart 100: 1153-1157, 2014.
24. Gu M, Nguyen PK, Lee AS, Xu D, Hu S, Plews JR, Han L, Huber BC, Lee WH, Gong Y, de Almeida PE, Lyons J, Ikeno F, Pacharinsak C, Connolly AJ, Gambhir SS, Robbins RC, Longaker MT, Wu JC. Microfluidic single-cell analysis shows that porcine induced pluripotent stem cell-derived endothelial cells improve myocardial function by paracrine activation. Circ Res 111: 882-893, 2012.
25. Han KH, Kim AK, Kim MH, Kim DH, Go HN, Kim DI. Enhancement of angiogenic effects by hypoxia-preconditioned human umbilical cordderived mesenchymal stem cells in a mouse model of hindlimb ischemia. Cell Biol Int. 2015 Jul 29. doi: 10. 1002/cbin. 10519. [Epub ahead of print].
26. Hare JM, Fishman JE, Gerstenblith G, DiFede Velazquez DL, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, Breton E, Davis-Sproul J, Schulman IH, Byrnes J, Mendizabal AM, Lowery MH, Rouy D, Altman P, Wong Po Foo C, Ruiz P, Amador A, Da Silva J, McNiece IK, Heldman AW, George R, Lardo A. Comparison of allogeneic vs autologous bone marrowderived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 308: 2369-2379, 2012.
27. Heldman AW, DiFede DL, Fishman JE, Zambrano JP, Trachtenberg BH, Karantalis V, Mushtaq M, Williams AR, Suncion VY, McNiece IK, Ghersin E, Soto V, Lopera G, Miki R, Willens H, Hendel R, Mitrani R, Pattany P, Feigenbaum G, Oskouei B, Byrnes J, Lowery MH, Sierra J, Pujol MV, Delgado C, Gonzalez PJ, Rodriguez JE, Bagno LL, Rouy D, Altman P, Foo CW, da Silva J, Anderson E, Schwarz R, Mendizabal A, Hare JM. Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial. JAMA 311: 62-73, 2014.
28. Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, Moore H, Andrews PW. Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 20: 329-337, 2002.
29. Hendrikx M, Hensen K, Clijsters C, Jongen H, Koninckx R, Bijnens E, Ingels M, Jacobs A, Geukens R, Dendale P, Vijgen J, Dilling D, Steels P, Mees U, Rummens JL. Recovery of regional but not global contractile function by the direct intramyocardial autologous bone marrow transplantation: results from a randomized controlled clinical trial. Circulation 114: I101-I107, 2006.
30. Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, Krook SH, Hunninghake DB, Comerota AJ, Walsh ME, McDermott MM, Hiatt WR. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA 286: 1317-1324, 2001.
31. Hirsch AT, Haskal ZJ, Hertzer NR, Bakal CW, Creager MA, Halperin JL, Hiratzka LF, Murphy WR, Olin JW, Puschett JB, Rosenfield KA, Sacks D, Stanley JC, Taylor LM Jr, White CJ, White J, White RA, Antman EM, Smith SC Jr, Adams CD, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Hunt SA, Jacobs AK, Nishimura R, Ornato JP, Page RL, Riegel B; American Association for Vascular Surgery; Society for Vascular Surgery; Society for Cardiovascular Angiography and Interventions; Society for Vascular Medicine and Biology; Society of Interventional Radiology; ACC/AHA Task Force on Practice Guidelines Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease; American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; Vascular Disease Foundation. ACC/AHA 2005 Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation 113: e463-e654, 2006.
32. Hodgson DM, Behfar A, Zingman LV, Kane GC, Perez-Terzic C, Alekseev AE, Puceat M, Terzic A. Stable benefit of embryonic stem cell therapy in myocardial infarction. Am J Physiol Heart Circ Physiol 287: H471-H479, 2004.
33. Hoover-Plow J, Gong Y. Challenges for heart disease stem cell therapy. Vasc Health Risk Manag 8: 99-113, 2012.
34. Hristov M, Erl W, Weber PC. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23: 1185-1189, 2003.
35. Huang NF, Niiyama H, De A, Gambhir SS, Cooke JP. Embryonic stem cell-derived endothelial cells for treatment of hindlimb ischemia. J Vis Exp 23: pii: 1034, 2009.
36. Huang NF, Chu J, Lee RJ, Li S. Biophysical and chemical effects of fibrin on mesenchymal stromal cell gene expression. Acta Biomater 6: 3947-3956, 2010.
37. Huang NF, Niiyama H, Peter C, De A, Natkunam Y, Fleissner F, Li Z, Rollins MD, Wu JC, Gambhir SS, Cooke JP. Embryonic stem cell-derived endothelial cells engraft into the ischemic hindlimb and restore perfusion. Arterioscler Thromb Vasc Biol 30: 984-991, 2010.
38. Huang P, Li S, Han M, Xiao Z, Yang R, Han ZC. Autologous transplantation of granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care 28: 2155-2160, 2005.
39. Iafrati MD, Hallett JW, Geils G, Pearl G, Lumsden A, Peden E, Bandyk D, Vijayaraghava KS, Radhakrishnan R, Ascher E, Hingorani A, Roddy S. Early results and lessons learned from a multicenter, randomized, double-blind trial of bone marrow aspirate concentrate in critical limb ischemia. J Vasc Surg 54: 1650-1658, 2011.
40. Iwase T, Nagaya N, Fujii T, Itoh T, Murakami S, Matsumoto T, Kangawa K, Kitamura S. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia. Cardiovasc Res 66: 543-551, 2005.
41. Jeon O, Song SJ, Bhang SH, Choi CY, Kim MJ, Kim BS. Additive effect of endothelial progenitor cell mobilization and bone marrow mononuclear cell transplantation on angiogenesis in mouse ischemic limbs. J Biomed Sci 14: 323-330, 2007.
42. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49, 2002.
43. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Amano K, Iba O, Imada T, Iwasaka T. Improvement of collateral perfusion and regional function by implantation of peripheral blood mononuclear cells into ischemic hibernating myocardium. Arterioscler Thromb Vasc Biol 22: 1804-1810, 2002.
44. Kikuchi K, Poss KD. Cardiac regenerative capacity and mechanisms. Annu Rev Cell Dev Biol 28: 719-741, 2012.
45. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94: 678-685, 2004.
46. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109: 1543-1549, 2004.
47. 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 26: 1465-1472, 2006.
48. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, O'Sullivan C, Collins L, Chen Y, Minami E, Gill EA, Ueno S, Yuan C, Gold J, Murry CE. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024, 2007.
49. Li H, Zuo S, He Z, Yang Y, Pasha Z, Wang Y, Xu M. Paracrine factors released by GATA-4 overexpressed mesenchymal stem cells increase angiogenesis and cell survival. Am J Physiol Heart Circ Physiol 299: H1772-H1781, 2010.
50. Li Z, Wu JC, Sheikh AY, Kraft D, Cao F, Xie X, Patel M, Gambhir SS, Robbins RC, Cooke JP, Wu JC. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116: I46-I54, 2007.
51. Lian X, Bao X, Al-Ahmad A, Liu J, Wu Y, Dong W, Dunn KK, Shusta EV, Palecek SP. Efficient differentiation of human pluripotent stem cells to endothelial progenitors via small-molecule activation of WNT signaling. Stem Cell Reports 3: 804-816, 2014.
52. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, Antosiewicz-Bourget J, O'Malley R, Castanon R, Klugman S, Downes M, Yu R, Stewart R, Ren B, Thomson JA, Evans RM, Ecker JR. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471: 68-73, 2011.
53. Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, Amrani D, Ewenstein BM, Riedel N, Story K, Barker K, Povsic TJ, Harrington RA, Schatz RA, Investigators AC. Intramyocardial, autologous CD34_cell therapy for refractory angina. Circ Res 109: 428-436, 2011.
54. Lu D, Chen B, Liang Z, Deng W, Jiang Y, Li S, Xu J, Wu Q, Zhang Z, Xie B, Chen S. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: a double-blind, randomized, controlled trial. Diabetes Res Clin Pract 92: 26-36, 2011.
55. Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marban E. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379: 895-904, 2012.
56. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, Dzau VJ. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 9: 1195-1201, 2003.
57. 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 366: 1005-1012, 2005.
58. Menasche P, Hagege AA, Vilquin JT, Desnos M, Abergel E, Pouzet B, Bel A, Sarateanu S, Scorsin M, Schwartz K, Bruneval P, Benbunan M, Marolleau JP, Duboc D. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 41: 1078-1083, 2003.
59. Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin JT, Marolleau JP, Seymour B, Larghero J, Lake S, Chatellier G, Solomon S, Desnos M, Hagege AA. The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117: 1189-1200, 2008.
60. Michael LH, Entman ML, Hartley CJ, Youker KA, Zhu J, Hall SR, Hawkins HK, Berens K, Ballantyne CM. Myocardial ischemia and reperfusion: a murine model. Am J Physiol Heart Circ Physiol 269: H2147-H2154, 1995.
61. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12: 459-465, 2006.
62. Mohammadzadeh L, Samedanifard SH, Keshavarzi A, Alimoghaddam K, Larijani B, Ghavamzadeh A, Ahmadi AS, Shojaeifard A, Ostadali MR, Sharifi AM, Amini MR, Mahmoudian A, Fakhraei H, Aalaa M, Mohajeri-Tehrani MR. Therapeutic outcomes of transplanting autologous granulocyte colony-stimulating factor-mobilised peripheral mononuclear cells in diabetic patients with critical limb ischaemia. Exp Clin Endocrinol Diabetes 121: 48-53, 2013.
63. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, de Ferranti S, Despres J, Fullerton HJ, Howard VJ, Huffman MD, Judd SE, Kissela BM, Lackland DT, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Matchar DB, McGuire DK, Mohler ER, 3rd Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Willey JZ, Woo D, Yeh RW, Turner MB. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation 131: e29-e322, 2015.
64. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, de Ferranti S, Després JP, Fullerton HJ, Howard VJ, Huffman MD, Judd SE, Kissela BM, Lackland DT, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Willey JZ, Woo D, Yeh RW, Turner MB; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation 131: e29-e322, 2015.
65. Muller-Ehmsen J, Whittaker P, Kloner RA, Dow JS, Sakoda T, Long TI, Laird PW, Kedes L. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 34: 107-116, 2002.
66. Mureli S, Gans CP, Bare DJ, Geenen DL, Kumar NM, Banach K. Mesenchymal stem cells improve cardiac conduction by upregulation of connexin 43 through paracrine signaling. Am J Physiol Heart Circ Physiol 304: H600-H609, 2013.
67. Niiyama H, Huang NF, Rollins MD, Cooke JP. Murine model of hindlimb ischemia. J Vis Exp 23: pii: 1035, 2009.
68. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature 410: 701-705, 2001.
69. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, Werner C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22: 377-384, 2004.
70. Ouriel K. Peripheral arterial disease. Lancet 358: 1257-1264, 2001.
71. Ozturk A, Kucukardali Y, Tangi F, Erikci A, Uzun G, Bashekim C, Sen H, Terekeci H, Narin Y, Ozyurt M, Ozkan S, Sayan O, Rodop O, Nalbant S, Sildiroglu O, Yalniz FF, Senkal IV, Sabuncu H, Oktenli C. Therapeutical potential of autologous peripheral blood mononuclear cell transplantation in patients with type 2 diabetic critical limb ischemia. J Diabetes Complications 26: 29-33, 2012.
72. Perin EC, Willerson JT, Pepine CJ, Henry TD, Ellis SG, Zhao DX, Silva GV, Lai D, Thomas JD, Kronenberg MW, Martin AD, Anderson RD, Traverse JH, Penn MS, Anwaruddin S, Hatzopoulos AK, Gee AP, Taylor DA, Cogle CR, Smith D, Westbrook L, Chen J, Handberg E, Olson RE, Geither C, Bowman S, Francescon J, Baraniuk S, Piller LB, Simpson LM, Loghin C, Aguilar D, Richman S, Zierold C, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD; Cardiovascular Cell Therapy Research Network (CCTRN). Effect of transendocardial delivery of autologous bone marrow mononuclear cells on functional capacity, left ventricular function, and perfusion in chronic heart failure: the FOCUS-CCTRN trial. JAMA 307: 1717-1726, 2012.
73. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147, 1999.
74. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 95: 9-20, 2004.
75. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74, 1997.
76. Raval Z, Losordo DW. Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ Res 112: 1288-1302, 2013.
77. Reinecke H, Zhang M, Bartosek T, Murry CE. Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 100: 193-202, 1999.
78. Resch T, Pircher A, Kahler CM, Pratschke J, Hilbe W. Endothelial progenitor cells: current issues on characterization and challenging clinical applications. Stem Cell Rev 8: 926-939, 2012.
79. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18: 399-404, 2000.
80. Rhee YH, Ko JY, Chang MY, Yi SH, Kim D, Kim CH, Shim JW, Jo AY, Kim BW, Lee H, Lee SH, Suh W, Park CH, Koh HC, Lee YS, Lanza R, Kim KS, Lee SH. Protein-based human iPS cells efficiently generate functional dopamine neurons and can treat a rat model of Parkinson disease. J Clin Invest 121: 2326-2335, 2011.
81. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Soliman EZ, Sorlie PD, Sotoodehnia N, Turan TN, Virani SS, Wong ND, Woo D, Turner MB; American Heart Association Statistics Committee Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125: 188-197, 2012.
82. Ruan W, Pan CZ, Huang GQ, Li YL, Ge JB, Shu XH. Assessment of left ventricular segmental function after autologous bone marrow stem cells transplantation in patients with acute myocardial infarction by tissue tracking and strain imaging. Chin Med J (Engl) 118: 1175-1181, 2005.
83. Rufaihah AJ, Huang NF, Jame S, Lee JC, Nguyen HN, Byers B, De A, Okogbaa J, Rollins M, Reijo-Pera R, Gambhir SS, Cooke JP. Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease. Arterioscler Thromb Vasc Biol 31: e72-e79, 2011.
84. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Assmus B, Tonn T, Dimmeler S, Zeiher AM, Investigators RA. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355: 1210-1221, 2006.
85. Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S. Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 28: 766-772, 2007.
86. Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature 451: 937-942, 2008.
87. Shake JG, Gruber PJ, Baumgartner WA, Senechal G, Meyers J, Redmond JM, Pittenger MF, Martin BJ. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg 73: 1919-1925, 2002.
88. Shintani S, Murohara T, Ikeda H, Ueno T, Sasaki K, Duan J, Imaizumi T. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103: 897-903, 2001.
89. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78: 55-62, 1991.
90. Suuronen EJ, Veinot JP, Wong S, Kapila V, Price J, Griffith M, Mesana TG, Ruel M. Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD133_progenitors expanded from the peripheral blood. Circulation 114: I138-I144, 2006.
91. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676, 2006.
92. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872, 2007.
93. Takeshita S, Zheng LP, Brogi E, Kearney M, Pu LQ, Bunting S, Ferrara N, Symes JF, Isner JM. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 93: 662-670, 1994.
94. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, Shimada K, Iwasaka T, Imaizumi T; Therapeutic Angiogenesis using Cell Transplantation (TACT) Study Investigators. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360: 427-435, 2002.
95. Telukuntla KS, Suncion VY, Schulman IH, Hare JM. The advancing field of cell-based therapy: insights and lessons from clinical trials. J Am Heart Assoc 2: e000338, 2013.
96. Templin C, Zweigerdt R, Schwanke K, Olmer R, Ghadri JR, Emmert MY, Muller E, Kuest SM, Cohrs S, Schibli R, Kronen P, Hilbe M, Reinisch A, Strunk D, Haverich A, Hoerstrup S, Luscher TF, Kaufmann PA, Landmesser U, Martin U. Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression. Circulation 126: 430-439, 2012.
97. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147, 1998.
98. Thum T, Tsikas D, Stein S, Schultheiss M, Eigenthaler M, Anker SD, Poole-Wilson PA, Ertl G, Bauersachs J. Suppression of endothelial progenitor cells in human coronary artery disease by the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine. J Am Coll Cardiol 46: 1693-1701, 2005.
99. Traverse JH, Henry TD, Ellis SG, Pepine CJ, Willerson JT, Zhao DX, Forder JR, Byrne BJ, Hatzopoulos AK, Penn MS, Perin EC, Baran KW, Chambers J, Lambert C, Raveendran G, Simon DI, Vaughan DE, Simpson LM, Gee AP, Taylor DA, Cogle CR, Thomas JD, Silva GV, Jorgenson BC, Olson RE, Bowman S, Francescon J, Geither C, Handberg E, Smith DX, Baraniuk S, Piller LB, Loghin C, Aguilar D, Richman S, Zierold C, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD; Cardiovascular Cell Therapy ResearchNetwork. Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the Late TIME randomized trial. JAMA 306: 2110-2119, 2011.
100. Traverse JH, Henry TD, Pepine CJ, Willerson JT, Zhao DX, Ellis SG, Forder JR, Anderson RD, Hatzopoulos AK, Penn MS, Perin EC, Chambers J, Baran KW, Raveendran G, Lambert C, Lerman A, Simon DI, Vaughan DE, Lai D, Gee AP, Taylor DA, Cogle CR, Thomas JD, Olson RE, Bowman S, Francescon J, Geither C, Handberg E, Kappenman C, Westbrook L, Piller LB, Simpson LM, Baraniuk S, Loghin C, Aguilar D, Richman S, Zierold C, Spoon DB, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD; Cardiovascular Cell Therapy Research Network (CCTRN). Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: the TIME randomized trial. JAMA 308: 2380-2389, 2012.
101. Van Laake LW, Van Hoof D, Mummery CL. Cardiomyocytes derived from stem cells. Ann Med 37: 499-512, 2005.
102. van Laake LW, Hassink R, Doevendans PA, Mummery C. Heart repair and stem cells. J Physiol 577: 467-478, 2006.
103. Van Tongeren RB, Hamming JF, Fibbe WE, Van Weel V, Frerichs SJ, Stiggelbout AM, Van Bockel JH, Lindeman JH. Intramuscular or combined intramuscular/intra-arterial administration of bone marrow mononuclear cells: a clinical trial in patients with advanced limb ischemia. J Cardiovasc Surg (Torino) 49: 51-58, 2008.
104. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7, 2001.
105. Walter DH, Krankenberg H, Balzer JO, Kalka C, Baumgartner I, Schluter M, Tonn T, Seeger F, Dimmeler S, Lindhoff-Last E, Zeiher AM, Investigators P. Intraarterial administration of bone marrow mononuclear cells in patients with critical limb ischemia: a randomized-start, placebo-controlled pilot trial (PROVASA). Circ Cardiovasc Interv 4: 26-37, 2011.
106. Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25: 1817-1823, 2005.
107. Wang X, Li Q, Hu Q, Suntharalingam P, From AH, Zhang J. Intra-myocardial injection of both growth factors and heart derived Sca-1_/CD31-cells attenuates post-MI LV remodeling more than does cell transplantation alone: neither intervention enhances functionally significant cardiomyocyte regeneration. PLoS One 9: e95247, 2014.
108. White MP, Rufaihah AJ, Liu L, Ghebremariam YT, Ivey KN, Cooke JP, Srivastava D. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem Cells 31: 92-103, 2013.
109. Wingate K, Bonani W, Tan Y, Bryant SJ, Tan W. Compressive elasticity of three-dimensional nanofiber matrix directs mesenchymal stem cell differentiation to vascular cells with endothelial or smooth muscle cell markers. Acta Biomater 8: 1440-1449, 2012.
110. Wingate K, Floren M, Tan Y, Tseng PO, Tan W. Synergism of matrix stiffness and vascular endothelial growth factor on mesenchymal stem cells for vascular endothelial regeneration. Tissue Eng Part A 20: 2503-2512, 2014.
111. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 85: 635-678, 2005.
112. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364: 141-148, 2004.
113. Xiong Q, Hill KL, Li Q, Suntharalingam P, Mansoor A, Wang X, Jameel MN, Zhang P, Swingen C, Kaufman DS, Zhang J. A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventricular remodeling. Stem Cells 29: 367-375, 2011.
114. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19: 971-974, 2001.
115. Xu Y, Meng H, Li C, Hao M, Wang Y, Yu Z, Li Q, Han J, Zhai Q, Qiu L. Umbilical cord-derived mesenchymal stem cells isolated by a novel explantation technique can differentiate into functional endothelial cells and promote revascularization. Stem Cells Dev 19: 1511-1522, 2010.
116. Yamada S, Nelson TJ, Crespo-Diaz RJ, Perez-Terzic C, Liu XK, Miki T, Seino S, Behfar A, Terzic A. Embryonic stem cell therapy of heart failure in genetic cardiomyopathy. Stem Cells 26: 2644-2653, 2008.
117. Yamahara K, Sone M, Itoh H, Yamashita JK, Yurugi-Kobayashi T, Homma K, Chao TH, Miyashita K, Park K, Oyamada N, Sawada N, Taura D, Fukunaga Y, Tamura N, Nakao K. Augmentation of neovascularization [corrected] in hindlimb ischemia by combined transplantation of human embryonic stem cells-derived endothelial and mural cells. PLoS One 3: e1666, 2008.
118. 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 408: 92-96, 2000.
119. Zhang H, Zhang N, Li M, Feng H, Jin W, Zhao H, Chen X, Tian L. Therapeutic angiogenesis of bone marrow mononuclear cells (MNCs) and peripheral blood MNCs: transplantation for ischemic hindlimb. Ann Vasc Surg 22: 238-247, 2008.