Endothelial progenitor cells as therapeutic vectors in cardiovascular disorders: From experimental models to human trials

Pharmacology and Therapeutics

Volumn 115, Issue 1, 2007, Pages 25-36

  Ben Shoshan, Jeremy ^a,b   George, Jacob ^a,b  

^a TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Bone marrow; Cardiovascular diseases; Cell based therapy; Endothelial progenitor cells; Mobilization; Peripheral blood

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR;

ACUTE HEART INFARCTION; ANGIOGENESIS; AUTOLOGOUS STEM CELL TRANSPLANTATION; BLOOD FLOW; BLOOD VESSEL; CARDIOVASCULAR DISEASE; CELL CULTURE; CELL THERAPY; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; ENDOTHELIUM CELL; EVIDENCE BASED MEDICINE; HEART FAILURE; HEMATOPOIETIC STEM CELL; HUMAN; ISCHEMIC HEART DISEASE; MEDICAL DOCUMENTATION; MOBILIZATION; NONHUMAN; PERIPHERAL VASCULAR DISEASE; PHENOTYPE; PILOT STUDY; POSTNATAL GROWTH; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REVIEW;

ANIMALS; CELLS, CULTURED; CLINICAL TRIALS; ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 34250856777     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2007.03.012     Document Type: Review

References (117)

1. Aicher A., Heeschen C., Mildner-Rihm C., Urbich C., Ihling C., Technau-Ihling K., et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9 11 (2003) 1370-1376
2. Aoki J., Serruys P.W., van Beusekom H., Ong A.T., McFadden E.P., Sianos G., et al. Endothelial progenitor cell capture by stents coated with antibody against CD34: the HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) Registry. J Am Coll Cardiol 45 10 (2005) 1574-1579
3. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 5302 (1997) 964-967
4. Asahara T., Takahashi T., Masuda H., Kalka C., Chen D., Iwaguro H., et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18 14 (1999) 3964-3972
5. Atluri P., Liao G.P., Panlilio C.M., Hsu V.M., Leskowitz M.J., Morine K.J., et al. Neovasculogenic therapy to augment perfusion and preserve viability in ischemic cardiomyopathy. Ann Thorac Surg 81 5 (2006) 1728-1736
6. Bahlmann F.H., Degroot K., Duckert T., Niemczyk E., Bahlmann E., Boehm S.M., et al. Endothelial progenitor cell proliferation and differentiation is regulated by erythropoietin. Kidney Int 64 5 (2003) 1648-1652
7. Bartunek J., Vanderheyden M., Vandekerckhove B., Mansour S., De Bruyne B., De Bondt P., et al. Intracoronary injection of CD133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: feasibility and safety. Circulation 112 9 Suppl (2005) I178-I183
8. Bruno S., Bussolati B., Scacciatella P., Marra S., Sanavio F., Tarella C., et al. Combined administration of G-CSF and GM-CSF stimulates monocyte-derived pro-angiogenic cells in patients with acute myocardial infarction. Cytokine 34 1-2 (2006) 56-65
9. Capillo M., Mancuso P., Gobbi A., Monestiroli S., Pruneri G., Dell'Agnola C., et al. Continuous infusion of endostatin inhibits differentiation, mobilization, and clonogenic potential of endothelial cell progenitors. Clin Cancer Res 9 1 (2003) 377-382
10. Caplice N.M., Bunch T.J., Stalboerger P.G., Wang S., Simper D., Miller D.V., et al. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci U S A 100 8 (2003) 4754-4759
11. Ceradini D.J., Kulkarni A.R., Callaghan M.J., Tepper O.M., Bastidas N., Kleinman M.E., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10 8 (2004) 858-864
12. Chavakis E., Aicher A., Heeschen C., Sasaki K., Kaiser R., El Makhfi N., et al. Role of β2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med 201 1 (2005) 63-72
13. Choi J.H., Kim K.L., Huh W., Kim B., Byun J., Suh W., et al. Decreased number and impaired angiogenic function of endothelial progenitor cells in patients with chronic renal failure. Arterioscler Thromb Vasc Biol 24 7 (2004) 1246-1252
14. Davidoff A.M., Ng C.Y., Brown P., Leary M.A., Spurbeck W.W., Zhou J., et al. Bone marrow-derived cells contribute to tumor neovasculature and, when modified to express an angiogenesis inhibitor, can restrict tumor growth in mice. Clin Cancer Res 7 9 (2001) 2870-2879
15. Erbs S., Linke A., Adams V., Lenk K., Thiele H., Diederich K.W., et al. Transplantation of blood-derived progenitor cells after recanalization of chronic coronary artery occlusion: first randomized and placebo-controlled study. Circ Res 97 8 (2005) 756-762
16. Fadini P., Miorin M., Facco M., Bonamico S., Baesso I., Grego F., et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol 45 9 (2005) 1449-1457
17. Fernandez-Aviles F., San Roman J.A., Garcia-Frade J., Fernandez M., Penarrubia M.J., de la Fuente L., et al. Experimental and clinical regenerative capability of human bone marrow cells after myocardial infarction. Circ Res 95 7 (2004) 742-748
18. Fuchs S., Baffour R., Zhou Y.F., Shou M., Pierre A., Tio F.O., et al. Transendocardial delivery of autologous bone marrow enhances collateral perfusion and regional function in pigs with chronic experimental myocardial ischemia. J Am Coll Cardiol 37 6 (2001) 1726-1732
19. Fuchs S., Satler L.F., Kornowski R., Okubagzi P., Weisz G., Baffour R., et al. Catheter-based autologous bone marrow myocardial injection in no-option patients with advanced coronary artery disease: a feasibility study. J Am Coll Cardiol 41 10 (2003) 1721-1724
20. George J., Herz I., Goldstein E., Abashidze S., Deutch V., Finkelstein A., et al. Number and adhesive properties of circulating endothelial progenitor cells in patients with in-stent restenosis. Arterioscler Thromb Vasc Biol 23 12 (2003) e57-e60
21. George J., Goldstein E., Abashidze S., Deutsch V., Shmilovich H., Finkelstein A., et al. Circulating endothelial progenitor cells in patients with unstable angina: association with systemic inflammation. Eur Heart J 25 12 (2004) 1003-1008
22. George J., Afek A., Abashidze A., Shmilovich H., Deutsch V., Kopolovich J., et al. Transfer of endothelial progenitor and bone-marrow cells influences atherosclerotic plaque size and composition in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 25 12 (2005) 2636-2641
23. George J., Goldstein E., Abashidze S., Wexler D., Hamed S., Shmilovich H., et al. Erythropoietin promotes endothelial progenitor cell proliferative and adhesive properties in a PI 3-kinase-dependent manner. Cardiovasc Res 68 2 (2005) 299-306
24. George J., Shmilovich H., Deutsch V., Miller H., Keren G., and Roth A. Comparative analysis of methods for assessment of circulating endothelial progenitor cells. Tissue Eng 12 2 (2006) 331-335
25. Gill M., Dias S., Hattori K., Rivera M.L., Hicklin D., Witte L., et al. Vascular trauma induces rapid but transient mobilization of VEGFR2 + AC133+ endothelial precursor cells. Circ Res 88 2 (2001) 167-174
26. Griese D.P., Achatz S., Batzlsperger C.A., Strauch U.G., Grumbeck B., Weil, et al. Vascular gene delivery of anticoagulants by transplantation of retrovirally-transduced endothelial progenitor cells. Cardiovasc Res 58 52 (2003) 469-477
27. Hamano K., Nishida M., Hirata K., Mikamo A., Li T.S., Harada M., et al. Local implantation of autologous bone marrow cells for therapeutic angiogenesis in patients with ischemic heart disease: clinical trial and preliminary results. Jpn Circ J 65 9 (2001) 845-847
28. Hamed S., Barshack I., Luboshits G., Wexler D., Deutsch V., Keren G., et al. Erythropoietin improves myocardial performance in doxorubicin-induced cardiomyopathy: a potential role for endothelial progenitor cells. Eur Heart J 27 (2006) 1876-1883
29. Harraz M., Jiao C., Hanlon H.D., Hartley R.S., and Schatteman G.C. CD34-blood-derived human endothelial cell progenitors. Stem Cells 19 4 (2001) 304-312
30. Heeschen C., Aicher A., Lehmann R., Fichtlscherer S., Vasa M., Urbich C., et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102 4 (2004) 1340-1346
31. Heissig B., Hattori K., Dias S., Friedrich M., Ferris B., Hackett N.R., et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109 5 (2002) 625-637
32. Hill J.M., Zalos G., Halcox J.P., Schenke W.H., Waclawiw M.A., Quyyumi A.A., et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348 7 (2003) 593-600
33. Hillebrands J.L., Klatter F.A., van DijK W.D., and Rozing J. Bone marrow does not contribute substantially to endothelial-cell replacement in transplant arteriosclerosis. Nat Med 8 3 (2003) 194-195
34. Hofmann M., Wollert K.C., Meyer G.P., Menke A., Arseniev L., Hertenstein B., et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111 17 (2005) 2198-2202
35. Hu Y., Davison F., Zhang Z., and Xu Q. Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation 108 25 (2003) 3122-3127
36. Hur J., Yoon C.H., Kim H.S., Choi J.H., Kang H.J., Hwang K.K., et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24 2 (2004) 288-293
37. Iba O., Matsubara H., Nozawa Y., Fujiyama S., Amano K., Mori, et al. Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation 106 15 (2002) 2019-2025
38. Ii M., Takenaka H., Asai J., Ibusuki K., Mizukami Y., Maruyama K., et al. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res 98 5 (2006) 697-704
39. Ikenaga S., Hamano K., Nishida M., Kobayashi T., Li T.S., Kobayashi S., et al. Autologous bone marrow implantation induced angiogenesis and improved deteriorated exercise capacity in a rat ischemic hindlimb model. J Surg Res 96 2 (2001) 277-283
40. Imanishi T., Hano T., and Nishio I. Estrogen reduces endothelial progenitor cell senescence through augmentation of telomerase activity. J Hypertens 23 9 (2005) 1699-1706
41. Imanishi T., Moriwaki C., Hano T., and Nishio I. Endothelial progenitor cell senescence is accelerated in both experimental hypertensive rats and patients with essential hypertension. J Hypertens 23 10 (2005) 1831-1837
42. Ince H., Petzsch M., Kleine H.D., Eckard H., Rehders T., Burska D., et al. Prevention of left ventricular remodeling with granulocyte colony-stimulating factor after acute myocardial infarction: final 1-year results of the front-integrated revascularization and stem cell liberation in evolving acute myocardial infarction by granulocyte colony-stimulating factor (FIRSTLINE-AMI) trial. Circulation 112 9 Suppl (2005) I73-I80
43. Ito H., Rovira I.I., Bloom M.L., Takeda K., Ferrans V.J., Quyyumi A.A., et al. Endothelial progenitor cells as putative targets for angiostatin. Cancer Res 59 23 (1999) 5875-5877
44. Iwaguro H., Yamaguchi J., Kalka C., Murasawa S., Masuda H., Hayashi S., et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105 6 (2002) 732-738
45. Iwakura A., Luedemann C., Shastry S., Hanley A., Kearney M., Aikawa R., et al. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 108 25 (2003) 3115-3121
46. Jeon O., Hwang K.C., Yoo K.J., and Kim B.S. Combined sustained delivery of basic fibroblast growth factor and administration of granulocyte colony-stimulating factor: synergistic effect on angiogenesis in mouse ischemic limbs. J Endovasc Ther 13 2 (2006) 175-181
47. Kalka C., Tehrani H., Laudenberg B., Vale P.R., Isner J.M., Asahara T., et al. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 70 3 (2000) 829-834
48. Kalka C., Masuda H., Takahashi T., Kalka-Moll W.M., Silver M., Kearney M., et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97 7 (2000) 3422-3427
49. Kamihata H., Matsubara H., Nishiue T., Fujiyama S., Amano K., Iba O., et al. Improvement of collateral perfusion and regional function by implantation of peripheral blood mononuclear cells into ischemic hibernating myocardium. Arterioscler Thromb Vasc Biol 22 11 (2002) 1804-1810
50. Kang H.J., Kim H.S., Zhang S.Y., Park K.W., Cho H.J., Koo B.K., et al. Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial. Lancet 363 9411 (2004) 751-756
51. Kawamoto A., Gwon H.C., Iwaguro H., Yamaguchi J.I., Uchida S., Masuda H., et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103 5 (2001) 634-637
52. Kawamoto A., Tkebuchava T., Yamaguchi J., Nishimura H., Yoon Y.S., Milliken C., et al. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107 3 (2003) 461-468
53. Kobayashi T., Hamano K., Li T.S., Katoh T., Kobayashi S., Matsuzaki M., et al. Enhancement of angiogenesis by the implantation of self bone marrow cells in a rat ischemic heart model. J Surg Res 89 2 (2000) 189-195
54. Kocher A.A., Schuster M.D., Szabolcs M.J., Takuma S., Burkhoff D., Wang J., et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7 4 (2001) 430-436
55. Kong D., Melo L.G., Mangi A.A., Zhang L., Lopez-Ilasaca M., Perrella M.A., et al. Enhanced inhibition of neointimal hyperplasia by genetically engineered endothelial progenitor cells. Circulation 109 14 (2004) 1769-1775
56. Koyanagi M., Urbich C., Chavakis E., Hoffmann J., Rupp S., Badorff C., et al. Differentiation of circulating endothelial progenitor cells to a cardiomyogenic phenotype depends on E-cadherin. FEBS Lett 579 27 (2005) 6060-6066
57. Kuethe F., Richartz B.M., Sayer H.G., Kasper C., Werner G.S., Hoffken K., et al. Lack of regeneration of myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans with large anterior myocardial infarctions. Int J Cardiol 97 1 (2004) 123-127
58. Kuethe F., Figulla H.R., Voth M., Richartz B.M., Opfermann T., Sayer H.G., et al. Mobilization of stem cells by granulocyte colony stimulating factor for the regeneration of myocardial tissue after myocardial infarction. Dtsch Med Wochenschr 129 9 (2004) 424-428
59. Kuethe F., Richartz B.M., Kasper C., Sayer H.G., Hoeffken K., Werner G.S., et al. Autologous intracoronary mononuclear bone marrow cell transplantation in chronic ischemic cardiomyopathy in humans. Int J Cardiol 100 3 (2005) 485-491
60. Kuethe F., Figulla H.R., Herzau M., Voth M., Fritzenwanger M., Opfermann T., et al. Treatment with granulocyte colony-stimulating factor for mobilization of bone marrow cells in patients with acute myocardial infarction. Am Heart J 150 1 (2005) 115
61. Laufs U., Werner N., and Link A. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109 2 (2004) 220-226
62. Li B., Sharpe E.E., Maupin A.B., Teleron A.A., Pyle A.L., Carmeliet P., et al. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 20 (2006) 1495-1497
63. Llevadot J., Murasawa S., Kureishi Y., Uchida S., Masuda H., Kawamoto A., et al. HMG-CoA reductase inhibitor mobilizes bone marrow derived endothelial progenitor cells. J Clin Invest 108 3 (2001) 399-405
64. Loomans C.J., de Koning E.J., Staal F.J., Rookmaaker M.B., Verseyden C., de Boer H.C., et al. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53 1 (2004) 195-199
65. Lunde K., Solheim S., Aakhus S., Arnesen H., Abdelnoor M., and Forfang K. Autologous stem cell transplantation in acute myocardial infarction: The ASTAMI randomized controlled trial. Intracoronary transplantation of autologous mononuclear bone marrow cells, study design and safety aspects. Scand Cardiovasc J 39 3 (2005) 150-158
66. Lusis A.J. Atherosclerosis. Nature 407 6801 (2000) 233-241
67. Matsumura G., Miyagawa-Tomita S., Shin'oka T., Ikada Y., and Kurosawa H. First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation 108 14 (2003) 1729-1734
68. Minatoguchi S., Takemura G., Chen X.H., Wang N., Uno Y., Koda M., et al. Acceleration of the healing process and myocardial regeneration may be important as a mechanism of improvement of cardiac function and remodeling by postinfarction granulocyte colony-stimulating factor treatment. Circulation 109 21 (2004) 2572-2580
69. Naruse K., Hamada Y., Nakashima E., Kato K., Mizubayashi R., Kamiya H., et al. Therapeutic neovascularization using cord blood-derived endothelial progenitor cells for diabetic neuropathy. Diabetes 54 6 (2005) 1823-1828
70. Natori T., Sata M., Washida M., Hirata Y., Nagai R., and Makuuchi M. G-CSF stimulates angiogenesis and promotes tumor growth: potential contribution of bone marrow-derived endothelial progenitor cells. Biochem Biophys Res Commun 297 4 (2002) 1058-1061
71. Ohki Y., Heissig B., Sato Y., Akiyama H., Zhu Z., Hicklin D.J., et al. Granulocyte colony-stimulating factor promotes neovascularization by releasing vascular endothelial growth factor from neutrophils. FASEB J 19 14 (2005) 2005-2007
72. Orlic D., Kajstura J., Chimenti S., Jakoniuk I., Anderson S.M., Li B., et al. Bone marrow cells regenerate infarcted myocardium. Nature 410 6829 (2001) 701-705
73. Ozbaran M., Omay S.B., Nalbantgil S., Kultursay H., Kumanlioglu K., Nart D., et al. Autologous peripheral stem cell transplantation in patients with congestive heart failure due to ischemic heart disease. Eur J Cardiothorac Surg 25 3 (2004) 342-350
74. Packard J.C. Influence of pravastatin and plasma lipids on clinical events in the West of Scotland Coronary Prevention Study (WOSCOPS). Circulation 97 15 (1998) 1440-1445
75. Peichev M., Naiyer A.J., Pereira D., Zhu Z., Lane W.J., Williams M., et al. Expression of VEGFR-2 and AC133 by circulating human CD34+ cells identifies a population of functional endothelial precursors. Blood 95 3 (2000) 952-958
76. Pelosi E., Valtieri M., Coppola S., Botta R., Gabbianelli M., Lulli V., et al. Identification of the hemangioblast in postnatal life. Blood 100 9 (2002) 3203-3208
77. Perin E. Transendocardial injection of autologous mononuclear bone marrow cells in end-stage ischemic heart failure patients: one-year follow-up. Int J Cardiol 95 Suppl 1 (2004) S45-S46
78. Perin E.C., Dohmann H.F., Borojevic R., Silva S.A., Sousa A.L., Mesquita C.T., et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107 18 (2003) 2294-2302
79. Pistrosch F., Herbrig K., Oelschlaegel U., Richter S., Passauer J., Fischer S., et al. PPARγ-agonist rosiglitazone increases number and migratory activity of cultured endothelial progenitor cells. Atherosclerosis 183 1 (2005) 163-167
80. Rauscher F.M., Goldschmidt-Clermont P.J., Davis B.H., Wang T., Gregg D., Ramaswami P., et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 108 4 (2003) 457-463
81. Ripa R.S., Jorgensen E., Wang Y., Thune J.J., Nilsson J.C., Sondergaard L., et al. Stem cell mobilization induced by subcutaneous granulocyte-colony stimulating factor to improve cardiac regeneration after acute st-elevation myocardial infarction: result of the double-blind, randomized, placebo-controlled stem cells in myocardial infarction (STEMMI) trial. Circulation 113 16 (2006) 1983-1992
82. Risau W. Mechanisms of angiogenesis. Nature 386 6626 (1997) 671-674
83. Rivard A., Fabre J.E., Silver M., Chen D., Murohara T., Kearney M., et al. Age dependent impairment of angiogenesis. Circulation 99 1 (1999) 111-120
84. Ruan W., Pan C.Z., Huang G.Q., Li Y.L., Ge J.B., and Shu X.H. 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 14 (2005) 1175-1181
85. Schachinger V., Assmus B., Britten M.B., Honold J., Lehmann R., Teupe C., et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI trial. J Am Coll Cardiol 44 8 (2004) 1690-1699
86. Schachinger V., Erbs S., Elsasser A., Haberbosch W., Hambrecht R., Holschermann H., et al. Intracoronary infusion of bone marrow-derived progenitor cells in acute myocardial infarction: a randomized, double-blind, placebo-controlled multicenter trial (REPAIR-AMI). Circulation 112 (2005) 3362
87. Schwartzenberg S., Ben-Shoshan J., Keren G., and George J. Erythropoietin - a cardioprotective agent and a potential surrogate marker. Expert Rev Cardiovasc Ther 4 1 (2006) 41-50
88. Segal M.S., Shah R., Afzal A., Perrault C.M., Chang K., Schuler A., et al. Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes. Diabetes 55 1 (2006) 102-109
89. Semenza G.L. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med 54 (2003) 17-28
90. Shi Q., Raffi S., Wu M.H., Wijelath E.S., Yu C., Ishida A., et al. Evidence of circulating bone-marrow derived endothelial cells. Blood 92 2 (1998) 362-367
91. Shintani S., Murohara T., Ikeda H., Ueno T., Honma T., Katoh A., et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103 23 (2001) 2776-2779
92. Shirota T., Yasui H., Shimokawa H., and Matsuda T. Fabrication of endothelial progenitor cell (EPC)-seeded intravascular stent devices and in vitro endothelialization on hybrid vascular tissue. Biomaterials 24 13 (2003) 2295-2302
93. Shmilovich H., Deutsch V., Roth A., Miller H., Keren G., and George J. Circulating endothelial progenitor cells in patients with cardiac syndrome X. Heart. (2006) (hrt.2005.077909)
94. Silva G.V., Perin E.C., Dohmann H.F., Borojevic R., Silva S.A., Sousa A.L., et al. Catheter-based transendocardial delivery of autologous bone-marrow-derived mononuclear cells in patients listed for heart transplantation. Tex Heart Inst J 31 3 (2004) 214-219
95. Simper D., Wang S., Deb A., Holmes D., McGregor C., Frantz R., et al. Endothelial progenitor cells are decreased in blood of cardiac allograft patients with vasculopathy and endothelial cells of noncardiac origin are enriched in transplant atherosclerosis. Circulation 108 2 (2003) 143-149
96. Stamm C., Westphal B., Kleine H.D., Petzsch M., Kittner C., Klinge H., et al. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361 9351 (2003) 45-46
97. Steiner S., Niessner A., Ziegler S., Richter B., Seidinger D., Pleiner J., et al. Endurance training increases the number of endothelial progenitor cells in patients with cardiovascular risk and coronary artery disease. Atherosclerosis 18 2 (2005) 305-310
98. Strauer B.E., Brehm M., Zeus T., Kostering M., Hernandez A., Sorg R.V., et al. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106 15 (2002) 1913-1918
99. Strehlow K., Werner N., Berweiler J., Link A., Dirnagl U., Priller J., et al. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation 107 24 (2003) 3059-3065
100. Takahashi T., Kalka C., Masuda H., Chen D., Silver M., Kearney M., et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5 4 (1999) 434-438
101. Tateishi-Yuyama E., Matsubara H., Murohara T., Ikeda U., Shintani S., Masaki H., et al. Therapeutic angiogenesis for patients with limb ischemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360 9331 (2002) 427-435
102. Tepper O.M., Galiano R.D., Capla J.M., Kalka C., Gagne P.J., Jacobowitz G.R., et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106 22 (2002) 2781-2786
103. Tse H.F., Kwong Y.L., Chan J.K., Lo G., Ho C.L., and Lau C.P. Angiogenesis in ischemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation. Lancet 361 9351 (2003) 47-49
104. Urbich C., Aicher A., Heeschen C., Dernbach E., Hofmann W.K., Zeiher A.M., et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 39 5 (2005) 733-742
105. Valgimigli M., Rigolin G.M., Fucili A., Porta M.D., Soukhomovskaia O., Malagutti P., et al. CD34+ and endothelial progenitor cells in patients with various degrees of congestive heart failure. Circulation 110 10 (2004) 1209-1212
106. Valgimigli G.M., Rigolin C., Cittanti P., Malagutti S., Curello G., Percoco, et al. Use of granulocyte-colony stimulating factor during acute myocardial infarction to enhance bone marrow stem cell mobilization in humans: clinical and angiographic safety profile. Eur Heart J 26 18 (2005) 1838-1845
107. Vasa M., Fichtlscherer S., Adler K., Aicher A., Martin H., Zeiher A.M., et al. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 103 24 (2001) 2885-2890
108. Wang Y., Tagil K., Ripa R.S., Nilsson J.C., Carstensen S., Jorgensen E., et al. Effect of mobilization of bone marrow stem cells by granulocyte colony stimulating factor on clinical symptoms, left ventricular perfusion and function in patients with severe chronic ischemic heart disease. Int J Cardiol 100 3 (2005) 477-483
109. Wang C.H., Verma S., Hsieh I.C., Chen Y.J., Kuo L.T., Yang N.I., et al. Enalapril increases ischemia-induced endothelial progenitor cell mobilization through manipulation of the CD26 system. J Mol Cell Card 41 (2006) 34-43
110. Werner L., Deutsch V., Barshack I., Miller H., Keren G., and George J. Transfer of endothelial progenitor cells improves myocardial performance in rats with dilated cardiomyopathy induced following experimental myocarditis. J Mol Cell Cardiol 39 4 (2005) 691-697
111. Werner N., Kosiol S., Schiegl T., Ahlers P., Walenta K., Link A., et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353 10 (2005) 999-1007
112. Wollert K.C., Meyer G.P., Lotz J., Ringes-Lichtenberg S., Lippolt P., Breidenbach C., et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364 9429 (2004) 141-148
113. Xu Q., Zhang Z., Davison F., and Hu Y. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ Res 93 8 (2003) e76-e86
114. Yoon Y.S., Park J.S., Tkebuchava T., Luedeman C., and Losordo D.W. Unexpected severe calcification after transplantation of bone marrow cells in acute myocardial infarction. Circulation 109 25 (2004) 3154-3157
115. Yoon C.H., Hur J., Oh I.Y., Park K.W., Kim T.Y., Shin J.H., et al. Intercellular adhesion molecule-1 is upregulated in ischemic muscle, which mediates trafficking of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 26 5 (2006) 1066-1072
116. Zhang Z.G., Zhang L., Jiang Q., and Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 90 3 (2002) 284-288
117. Zohlnhofer D., Ott I., Mehilli J., Schomig K., Michalk F., Ibrahim T., et al. Stem cell mobilization by granulocyte colony-stimulating factor in patients with acute myocardial infarction a randomized controlled trial. JAMA 295 9 (2006) 1003-1010