Biologic Properties of Endothelial Progenitor Cells and Their Potential for Cell Therapy

Progress in Cardiovascular Diseases

Volumn 49, Issue 6, 2007, Pages 421-429

  Young, Pampee P ^a,b   Vaughan, Douglas E ^a,b   Hatzopoulos, Antonis K ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ARTICLE; BLOOD; BONE MARROW; CELL THERAPY; CELL TYPE; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; HEART SURGERY; HUMAN; ISCHEMIA; MONONUCLEAR CELL; NONHUMAN; REGENERATION; REGENERATIVE ABILITY; STEM CELL; TISSUE ENGINEERING; TISSUE EXPANSION; TISSUE REPAIR; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE THERAPY; GENES, TRANSGENIC, SUICIDE; HEART DISEASES; HUMANS; ISCHEMIA; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE ENGINEERING;

EID: 34247857552     PISSN: 00330620     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pcad.2007.02.004     Document Type: Article

References (98)

1. Asahara T., Murohara T., Sullivan A., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997) 964-967
2. Risau W., and Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 11 (1995) 73-91
3. Crosby J.R., Kaminski W.E., Schatteman G., et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 87 (2000) 728-735
4. Kaushal S., Amiel G.E., Guleserian K.J., et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med 7 (2001) 1035-1040
5. Raffi S., and Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9 (2003) 702-712
6. Young P.P., Hofling A.A., and Sands M.S. VEGF increases engraftment of bone marrow-derived endothelial progenitor cells (EPCs) into vasculature of newborn murine recipients. Proc Natl Acad Sci U S A 99 (2002) 11951-11956
7. Hristov M., and Weber C. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 8 (2004) 498-508
8. Dimmeler S., Zeiher A.M., and Schneider M.D. Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest 115 (2005) 572-583
9. Bahlmann F.H., Groot K., Spandau J., et al. Erythropoietin regulates endothelial progenitor cells. Blood 103 (2004) 921-926
10. Haeshen C., Aicher A., Lehmann R., et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102 (2003) 1340-1346
11. Hill J.M., Zalos G., Halcox J.P.J., et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 248 (2003) 593-600
12. Isner J.M. Tissue responses to ischemia: local and remote responses for preserving perfusion of ischemic muscle. J Clin Invest 106 (2000) 615-620
13. Jin D.K., Shido K., Kopp H.G., et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemagiocytes. Nat Med 12 (2006) 557-567
14. Dimmeler S., Aicher A., Vasa M., et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest 108 (2001) 391-397
15. Shintani S., Murohara T., Ikeda H., et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103 (2001) 2776-2779
16. Hirashima M., Kataoka H., Nishikawa S., et al. Maturation of embyronic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 4 (1999) 1253-1263
17. Peichev M., Naiyer A.J., Pereira D., et al. Expression of VEGFR-2 and AC 133 by circulating human CD34+ cells identifies a population of functional endothelial precursors. Blood 95 (2000) 952-958
18. Kalka C., Masuda H., Tomono T., et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97 (1999) 3422-3427
19. Schatteman G., Hanlon H.D., Jiao C., et al. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106 (2000) 571-578
20. Lin Y., Chang L., Solovey A., et al. Use of blood outgrowth endothelial cells for gene therapy for hemophilia A. Blood 99 (2002) 457-462
21. Tepper O.M., Galiano R.D., Capla J.M., et al. Human endothelial progenitor cells from type II diabetes exhibit impaired proliferation, adhesion and incorporation into vascular structures. Circulation 106 (2002) 2781-2786
22. Boyer M., Townsend L.E., Vogel M., et al. Isolation of endothelial cells and their progenitor cells from human peripheral blood. J Vasc Surg 31 (2000) 181-189
23. Assmus B., Schachinger V., Teupe C., et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106 (2002) 3009-3017
24. Asakage M., Tsuno N.H., Kitayama J., et al. Early-outgrowth of endothelial progenitor cells can function as antigen-presenting cells. Cancer Immunol Immunother 55 (2006) 708-716
25. Romagnani P., Annunziato F., Liotta F., et al. CD14+CD34low cells with stem cell phenotype and functional features are the major source of circulating endothelial progenitors. Circ Res 97 (2005) 314-322
26. Sharpe E.E., Teleron A.A., Li B., et al. The origin and in vivo significance of murine and human culture expanded endothelial progenitor cells (CE-EPCs). Am J Pathol 168 (2006) 1710-1720
27. Gulati R., Jevremovic D., Peterson T.E., et al. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 93 (2003) 1023-1025
28. Harraz M.C., Jiao C., Hanlon H.D., et al. CD34- blood-derived human endothelial cell progenitors. Stem Cells 19 (2001) 304-312
29. Rehman J., Jingling L., Orschell C.M., et al. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107 (2003) 1164-1169
30. Schmeisser A., Garlichs C.D., Zhang H., et al. Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc Res 49 (2001) 671-680
31. Loomans C.J., Wan H., de Crom R., et al. Angiogenic murine endothelial progenitor cells are derived from a myeloid bone marrow fraction and can be identified by endothelial NO synthase expression. Arterioscler Thromb Vasc Biol 26 (2006) 1760-1767
32. Kim S.Y., Park S.Y., Kim J.M., et al. Differentiation of endothelial cells from human umbilical cord AC 133-CD14+ cells. Ann Hematol 84 (2005) 417-422
33. Rhode E., Malischnik C., Thaler D., et al. Blood monocytes mimic endothelial progenitor cells. Stem Cells 24 (2006) 357-367
34. Pujol B.F., Lucibello F.C., Gehling U.M., et al. Endothelial-like cells derived from human CD 14 positive monocytes. Differentiation 65 (2000) 287-300
35. Elsheikh E., Uzunel M., He Z., et al. Only a specific subset of human peripheral-blood monocytes has endothelial-like functional capacity. Blood 106 (2005) 2347-2355
36. Li B., Sharpe E.E., Teleron A.A., et al. VEGF and P1GF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at site of tumor neovascularization. FASEB J 20 (2006) 1495-1497
37. Tepper O.M., Capla J.M., Galiano R.D., et al. Adult vasculogenesis occurs through in situ recruitment, proliferation and tubilization of circulating bone marrow-derived cells. Blood 105 (2005) 1068-1077
38. Ingram D.A., Mead L.E., Tanaka H., et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104 (2004) 2752-2760
39. Kalka C., Masuda H., Takahashi T., et al. Vascular endothelial growth factor 165 gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 86 (2000) 1198-1202
40. Seeger F.H., Haendeler J., Walter D.H., et al. p38 mitogen-activated protein kinase downregulates endothelial progenitor cells. Circulation 111 (2005) 1184-1191
41. Yamaguchi J., Kusano K.F., Masuo O., et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107 (2003) 1322-1328
42. Hur J., Yoon C.H., Kim H.S., et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Hypertension 24 (2004) 1-6
43. Lin Y., Weisdorf D.J., Solovey A., et al. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105 (2000) 71-77
44. Grant M.B., May W.S., Cabellero S., et al. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 2002 (2002) 607-612
45. Reyes M., Dudek A., Jahagirdar B., et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109 (2002) 337-346
46. Kawamoto A., Gwon H.C.I., Yamguchi J.L., et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103 (2001) 634-637
47. Murohara T., Ikeda H., Duan J., et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 105 (2000) 1527-1536
48. Urbich C., and Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95 (2004) 343-353
49. Gehling U.M., Ergun S., Schumacher U., et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95 (2000) 3106-3112
50. Lee N., Thorne T., Losordo D.W., et al. Repair of ischemic heart disease with novel bone marrow-derived multipotent stem cells. Cell Cycle 4 (2005) 861-864
51. Moore X.L., Lu J., Sun L., et al. Endothelial progenitor cells' "homing" specificity to brain tumors. Gene Ther (2004) 1-8 10.1038/sj.gt.3302151
52. Zimmet J.M., and Hare J.M. Emerging role for bone marrow derived mesenchymal stem cells in myocardial regenerative therapy. Basic Res Cardiol 100 (2005) 471-481
53. Bengel F.M., Schachinger V., and Dimmeler S. Cell-based therapies and imaging in cardiology. Eur J Nucl Med Mol Imaging 32 (2005) S404-S416
54. Galiano R.D., Tepper O.M., Pelo C.R., et al. Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 164 (2004) 1935-1946
55. Dobaczewski M., Bujak M., Zymek P., et al. Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res 324 (20061) 475-488
56. Takamiya M., Okigaki M.J.D., Takai S., et al. Granulocyte colony-stimulating factor-mobilized circulating c-Kit+/Flk-l+ progenitor cells regenerate endothelium and inhibit neointimal hyperplasia after vascular injury. Aterioscler Thromb Vasc Biol 26 (2006) 751-757
57. Ricousse-Roussanne S., Barateau V., Contreres J., et al. Ex vivo differentiated endothelial and smooth muscle cells from human cord blood progenitors home to the angiogenic tumor vasculature. Cardiovasc Res 62 (2004) 176-184
58. Wei J., Blum S., Unger M., et al. Embryonic endothelial progenitor cells armed with a suicide gene target hypoxic lung metastasis after intravenous delivery. Cancer Cell 5 (2004) 477-488
59. Kupatt C., Hinkel R., Lamparter M., et al. Retro fusion of embryonic endothelial progenitor cells attenuates ischemia-reperfusion injury in pigs: role of phosphatidylinositol 3-kinase/AKT kinase. Circulation 112 (2005) I117-I122
60. Murayama T., Tepper O.M., Silver M., et al. Determination of bone marrow-derived endothelial progenitor cell significance in angiogenic growth factor-induced neovascularization in vivo. Exp Hematol 30 (2002) 967-972
61. Amado L.C., Saliaris A.P., Schuleri K.H., et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci U S A 102 (2005) 11474-11479
62. Laflamme M.A., and Murry C.E. Regenerating the heart. Nat Biotechnol 7 (2005) 845-856
63. Janssens S., Dubois C., Bogaert J., et al. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind randomised controlled trial. Lancet 367 (2006) 113-121
64. Lunde K., Solheim S., Aakhus S., et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 355 (2006) 1199-1209
65. Schachinger V., Erbs S., Elsasser A., et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355 (2006) 1210-1221
66. Assmus B., Honold J., Schachinger V., et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 355 (2006) 1222-1232
67. Englemann I., Madisch I., Pommer H., et al. Autologous bone marrow stem cell mobilization induced by granulocyte colony-stimulating factor after subacute ST-segment elevation myocardial infarction undergoing late revascularization: final results from the G-CSF-STEMI (Granulocyte Colony-Stimulating Factor ST-Segment Elevation Myocardial Infarction trial. J Am Coll Cardiol 48 (2006) 1712-1721
68. Ripa R.S., Jorgensen E., Wang Y., et al. Stem cell mobilization induced by subcutaneous granuloctye-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 (2006) 1983-1992
69. Zohlnhofer D., Ott I., Mehilli J., et al. Stem cell mobilization by granulocyte colony-stimulating factor in patients with acute myocardial infarction: a randomized controlled trial. JAMA 295 (2006) 1003-1010
70. Meyer G.P., Wollert K.C., Lotz J., et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation 113 (2006) 1287-1294
71. Carmeliet P., and Jain R.K. Angiogenesis in cancer and other diseases. Nature 407 (2000) 249-257
72. Vajkoczy P., Blum S., Lamparter M., et al. Multistep nature of microvascular recruitment of ex vivo expanded embryonic endothelial progenitor cells during tumor angiogenesis. J Exp Med 197 (2003) 1755-1765
73. Annabi B., Naud E., Lee Y., et al. Vascular progenitors derived from murine bone marrow stromal cells are regulated by fibroblast growth factor and are avidly recruited by vascularizing tumors. J Cell Biochem 91 (2004) 1146-1158
74. Peters B.A., Diaz L.A., Polyak K., et al. Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 11 (2005) 261-262
75. Conejo-Garcia J.R., Benencia F., Courreges M., et al. Tumor-infiltrating dendritic cell precursors recruited by a b-defensin contribute to vasculogenesis under the influence of VEGF-A. Nat Med 10 (2004) 950-958
76. Duda D.G., Cohen K.S., Koszin S.V., et al. Evidence for incorporation of bone marrow-derived endothelial cells into perfused blood vessels in tumors. Blood 107 (2006) 2774-2776
77. Asahara T., Masuda H., Takahashi T., et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85 (1999) 221-228
78. Lyden D., Hattori K., Dias S., et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7 (2001) 1194-1201
79. Jiang Y., Jahagirdar B.N., Reinhardt R.L., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
80. Yurugi-Kobayashi T., Itoh H., Yamashita J., et al. Effective contribution of transplanted vascular progenitor cells derived from embryonic stem cells to adult neovascularization in proper differentiation stage. Blood 101 (2003) 2675-2678
81. Larrivee B., Niessen K., Pollet I., et al. Minimal contribution of marrow-derived endothelial precursors to tumor vasculature. J Immunol 175 (2005) 2890-2899
82. Conejo-Garcia J.R., Buckanovich R.J., Benencia F., et al. Vascular leukocytes contribute to tumor vascularization. Blood 105 (2005) 679-681
83. Gothert J.R., Gustin S.E., van Eekelen J.A., et al. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 104 (2004) 1769-1777
84. Weissleder R. Bone marrow-derived lin(-)c-kit(+)sca-1+ stem cells do not contribute to vasculogenesis in Lewis lung carcinoma. Neoplasia 7 (2005) 234-240
85. Ii M., Nishimura H., Iwakura A., et al. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation 111 (2005) 1114-1120
86. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIP-1 induction of SDF-1. Nat Med 10 (2004) 858-864
87. de Palma M., Vanneri M.A., Roca C., et al. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 9 (2003) 789-795
88. Yang L., De Busk L.M., Fukuda K., et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor bearing host directly promotes tumor angiogenesis. Cancer Cell 6 (2004) 409-421
89. De Palma M., Venneri M.A., Galli R., et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8 (2005) 211-226
90. Kerjaschki D., Hurttary N., Raab I., et al. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12 (2006) 230-234
91. Chard R.B., Johnson D.C., Nunn G.R., et al. Aorta-coronary bypass grafting with polytetrafluoroethylene conduits. Early and late outcome in eight patients. J Thorac Cardiovasc Surg 94 (1987) 132-134
92. Weinberg C.B., and Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science 231 (1986) 397-400
93. Lheureux N., Paquet S., Labbe R., et al. A completely biological tissue-engineered human blood vessel. FASEB J 12 (1998) 47-56
94. Deutsch M., Meinhart J., Fischlein T., et al. Clinical autologous in vitro endothelialization of infrainguinal ePTFE grafts in 100 patients: a 9-year experience. Surgery 126 (1999) 847-855
95. Inoue M., Ono I., Tateshita T., et al. Effect of a collagen matrix containing epidermal growth factor on wound repair. Wound Repair Regen 6 (1998) 213-222
96. Bhattacharya V., McSweeney P.A., Shi Q., et al. Enhanced endothelialization and microvessel formation in polyester grafts seeded with CD34+ bone marrow cells. Blood 95 (2000) 581-585
97. Shi Q., Bhattacharya V., Hong- De W.M., et al. Utilizing granulocyte colony-stimulating factor to enhance vascular graft endothelialization from circulating blood cells. Ann Vasc Surg 16 (2002) 314-320
98. Ziegelhoeffer T., Fernandez B., Kostin S., et al. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res 94 (2003) 230-238