Endothelial progenitors

Blood Cells, Molecules, and Diseases

Volumn 52, Issue 4, 2014, Pages 186-194

  Pelosi, Elvira ^a   Castelli, Germana ^a   Testa, Ugo ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Endothelial cells; Hematopoiesis; Regenerative medicine

Indexed keywords

ANGIOGENESIS; BLOOD VESSEL WALL; CELL ACTIVITY; CELL ASSAY; CELL FUNCTION; CELL POPULATION; CELL THERAPY; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; EARLY ENDOTHELIAL PROGENITOR CELL; ENDOTHELIAL COLONY FORMING CELL; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; HEMANGIOBLAST; HEMATOPOIETIC CELL; HUMAN; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PARACRINE SIGNALING; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VON WILLEBRAND DISEASE;

ENDOTHELIAL CELLS; HEMATOPOIESIS; REGENERATIVE MEDICINE;

ANIMALS; ANTIGENS, SURFACE; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOPHENOTYPING; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84895548526     PISSN: 10799796     EISSN: 10960961     Source Type: Journal    
DOI: 10.1016/j.bcmd.2013.11.004     Document Type: Review

References (114)

1. Asahara T., Murohara T., Sullivan A., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1977, 275:964-967.
2. Shi Q., Rafii S., Wu H.M., et al. Evidence for bone marrow-derived endothelial cells. Blood 1998, 92:362-367.
3. Asahara T., Masuda H., Takahashi T., et al. Bone marrow origin of endothelial progenitor cells for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85:221-228.
4. Migliaccio G., Migliaccio A.R., Petti S., et al. Human embryonic hematopoiesis. Kinetics of progenitors and precursors underlying the yolk sac-liver transition. J. Clin. Invest. 1986, 78:51-60.
5. Palis J., Chan R.J., Koniski A., et al. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(98):4528-4533.
6. McGrath K.E., Frame J.M., From G.J., et al. A transient definitive erythroid lineage with unique regulation of the beta-globin locus in the mammalian embryo. Blood 2011, 117:4600-4608.
7. Zi L., Lan Y., He W., et al. Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell Dev. 2012, 11:663-675.
8. Sabin F. Origin and development of the primitive vessels of the chick and of the pig. Canegie Inst Pub Contribs Embryol 1917, 6:61-124.
9. Muller A.M., Medvinsky A., Strouboulis J., et al. Development of the hematopoietic stem cell activity in the mouse embryo. Immunity 1994, 1:291-301.
10. Medvinsky A., Dzierzak E. Definitive hematopoiesis is autonomously initiated in the AGM region. Cell 1996, 86:897-906.
11. de Bruijn M.F., Ma X., Robin C., et al. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002, 16:673-683.
12. Cumano A., Dieterlen-Lievre F., Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intramebryonic splanchnopleura. Cell 1996, 86:907-916.
13. Zovein A.C., Hofmann J.J., Lynch M., et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008, 3:626-636.
14. Boisset J.C., van Cappellen W., Andrieu-Soler C., et al. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010, 464:116-120.
15. Kissa K., Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 2010, 464:112-115.
16. Bertrand J.Y., Chi N.C., Santoso B., et al. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 2010, 464:108-111.
17. Yokomizo T., Dzierzak E. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 2010, 137:3651-3661.
18. Gekas C., Dieterlen-Lièvre F., Orkin S.H., et al. The placenta is a niche for hematopoietic stem cells. Dev. Cell 2005, 8:365-375.
19. Li W., Ferkowicz M.J., Johnson S.A., et al. Endothelial cells in the early murine yolk sac give rise to CD41-expressing hematopoietic cells. Stem Cells Dev. 2005, 14:44-54.
20. Nakano H., Liu X., Arshi A., et al. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat. Commun. 2013, 4:1564.
21. Hirschi K. Hemogenic endothelium during development and beyond. Blood 2012, 119:4823-4827.
22. + cells produce hemogenic endothelium. PLoS ONE 2012, 7:e51109.
23. + cells: efficient production in the co-culture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 2005, 105:617-626.
24. Choi K.D., Yu J., Omuga-Otto K., et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 2009, 27:559-567.
25. Vodyanik M.A., Wu J., Zhang X., et al. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell stem Cell 2010, 7:718-729.
26. Choi K.D., Vodyanik M.A., Togarrati P.P., et al. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell. Reprogram. 2012, 2:553-567.
27. Kennedy M., D'Souza S.L., Lynch-Kattman M., et al. Development of the hemangioblasts defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 2007, 109:2679-2687.
28. Rafii S., Kloss C., Butler J., et al. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood 2013, 121:770-780.
29. Chen M.J., Yokomizo T., Ziegler B.M., et al. Runx1 is required for the endothelial to hematopoietic cell transition but not thereafter. Nature 2009, 467:887-891.
30. Lichinger M., Ingram R., Hannah R., et al. RUNX1 reshapes the epigenetic landscape at the onset of hematopoiesis. EMBO J. 2012, 31:4318-4333.
31. Van Handel B., Rantel-Agen A., Sasidharan R., et al. Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 2012, 150:590-605.
32. Iacovino M., Chang D., Szatmari I., et al. HOXA3 is an apical regulator of haemogenic endothelium. Nat. Cell Biol. 2011, 13:72-78.
33. Nakajima-Takagi Y., Osawa M., Oshima M., et al. Role of SOX17 in hematopoietic development from human embryonic stem cells. Blood 2013, 121:447-458.
34. Pereira C.F., Chang B., Qiu J., et al. Induction of hemogenic program in mouse fibroblasts. Cell Stem Cell 2013, 13:1-14.
35. Zhu M.X., Zhao J.Y., Chen G.A. Mesoderm is committed to hemato-endothelial and cardiac lineages in human embryoid bodies by sequential exposure to cytokines. Exp. Cell Res. 2013, 319:21-34.
36. Yue R., Li H., Liu H., et al. Thrombin receptor regulates hematopoiesis and endothelial to hematopoietic transition. Dev. Cell 2012, 22:1092-1100.
37. Ito H., Rovira I., Bloom M., et al. Endothelial progenitor cells as putative targets for angiostatin. Cancer Res. 1999, 59:5875-5877.
38. Hill J.M., Zalos G., Halcox J. Circulating endothelial progenitor cells, vascular function and cardiovascular risk. N. Engl. J. Med. 2003, 348:593-600.
39. Medina R., O'Niell C., Sweeney M., et al. Molecular analysis of endothelial progenitor cell (EPC) subtypes reveals two distinct cell populations with different identities. BMC Med. Genomics 2012, 3:18.
40. 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.
41. Masuda H., Alev C., Akimaru H., et al. Methodological development of a clonogenic assay to determine endothelial progenitor cell potential. Circ. Res. 2011, 109:20-37.
42. Pelchev M., Naiyer A.J., Perreira I.D., et al. Expression of VEGF-R2 and CD133 by circulation human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000, 95:952-958.
43. + cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp. Hematol. 2007, 35:1109-1118.
44. Yoder M.C. Human endothelial progenitor cells. Cold Spring Harb. Perspect. Med. 2012, 2:a006692.
45. Lin Y., Weisdorf D., Solovey A., et al. Origins of circulating endothelial cells and endothelial outgrowth from blood. J. Clin. Invest. 2000, 105:71-77.
46. Ingram D.A., Mewad L.E., Tasnaka H., et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004, 104:2752-2760.
47. Ingram D.A., Caplice N.M., Yoder M.C. Unresolved questions, and novel paradigms for defining endothelial progenitor cells. Blood 2007, 106:1525-1531.
48. Yoder M.C., Mead L.E., Prater D., et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007, 109:1801-1809.
49. Reinisch A., Hoffmann N., Obenauf A., et al. Humanized large-scale expanded endothelial colony-forming cells function in vitro and in vivo. Blood 2009, 113:6716-6725.
50. Oshima-Sudo N., Li Q., Hoshino Y., et al. Optimized method for culturing outgrowth endothelial progenitor cells. Inflamm. Regen. 2011, 31:219-227.
51. + hematopoietic precursors. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1572-1579.
52. Mund J., Estes M., Yoder M., et al. Flow cytometric identification and functional characterization of immature and mature circulating endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2012, 32:1045-1053.
53. Tura O., Skinner E., Barclay R., Samuel K., Gallagher R., et al. Late outgrowth endothelial cells resemble mature endothelial cells and are not derived from bone marrow. Stem Cells 2013, 31:338-348.
54. Nagano M., Yamashita T., Hamada H., et al. Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood. Blood 2007, 110:151-160.
55. He T., Petersom T., Katusic Z. Paracrine mitogenic effect of human endothelial progenitor cells: role of interleukin-8. Am. J. Physiol. Heart 2005, 289:H968-H972.
56. Kimura T., Kohno H., Matsuoka Y., et al. CXCL8 enhances the angiogenic activity of umbilical cord blood-derived outgrowth endothelial cells in vitro. Cell Biol. Int. 2011, 35:201-208.
57. Hemansen S.E., Lund T., Kalstad T., et al. Adrenomedullin augments the angiogenic potential of late outgrowth endothelial progenitor cells. Am. J. Physiol. Cell Physiol. 2011, 300:C783-C791.
58. Ingram D.A., Mead L.E., Moore D.B., et al. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 2005, 105:2783-2786.
59. Yoder M.C. Progenitor cells in the pulmonary circulation. Proc. Am. Thorac. Soc. 2011, 8:466-470.
60. Alvarez D.F., Huang L., King J.A., et al. Lung microvascular endothelium is enriched with progenitor cells that exhibit vasculogenic capacity. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L419-L430.
61. Schniedermann J., Rennecke M., Buttler K., et al. Mouse lung contains endothelial progenitors with high capacity to form blood and lymphatic vessels. BMC Cell Biol. 2010, 11:50.
62. Huang L., Harkenrider M., Thompson M., et al. A hierarchy of endothelial colony-forming cell activity displayed by bovine corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 2010, 51:3943-3949.
63. + adult vascular endothelial stem cells. PLoS Biol. 2012, 10:e1001407.
64. Lin R.Z., Moreno-Luma R., Munoz-Hernandez R., et al. Human white adipose tissue vasculature contains endothelial-colony forming cells with robust in vivo vasculogenic potential 2013, 16:735-744.
65. Bertolini F., Sheked Y., Mancuso P., et al. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat. Rev. Cancer 2006, 6:835-845.
66. Kerbel R.S. Tumor angiogenesis. N. Engl. J. Med. 2008, 358:2039-2049.
67. Hagensen M.K., Vanhoutte P.M., Bentzon J.F. Arterial endothelial cells: still the craftsmen of regenerated endothelium. Cardiovasc. Res. 2012, 95:281-289.
68. Hagensen M.K., Shim J., Thim T., et al. Circulating endothelial progenitor cells do not contribute to plaque endothelium in murine atherosclerosis. Circulation 2010, 121:898-905.
69. Hagensem M.K., Shim J., Falk E., et al. Flanking recipient vasculature, not circulating progenitor cells, contributes to endothelium and smooth muscle in murine allograft vasculopathy. Arterioscler. Thromb. Vasc. Biol. 2011, 31:808-813.
70. Rinchevich Y., Lindau P., Ueno H., et al. Germ-layer lineage-restricted stem/progenitors regenerate the digit tip. Nature 2011, 476:409-413.
71. Purhonen S., Palm J., Rossi D., et al. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6620-6625.
72. Okuno Y., Nakamura-Ishizu A., Kishi K., et al. Bone marrow-derived cells serve as proangiogenic macrophages but not endothelial cells serve as proangiogenic macrophages but not endothelial cells in wound healing. Blood 2011, 117:5264-5272.
73. Hagensen M.K., Raarup M., Mortensen M., et al. Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovasc. Res. 2012, 93:223-231.
74. Liu J., Huang J., Yao W.Y., et al. The origin of vascularization in tumors. Front. Biosci. 2012, 17:2559-2565.
75. 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 2005, 8:211-216.
76. Bieback K., Vinci M., Elvers-Hornung S., et al. Recruitment of cord blood-derived endothelial colony-forming cells to sites of tumor angiogenesis. Cytotherapy 2013, 15:726-739.
77. Starke R.D., Ferraro F., Paschalaki K.E., et al. Endothelial von Willebrand factor regulates angiogenesis. Blood 2010, 117:1071-1080.
78. Starke R.D., Paschalaki K.E., Dyer C., et al. Cellular and molecular basis of von Willebrand disease: studies on blood outgrowth endothelial cells. Blood 2013, 121:2773-2784.
79. Wang J.W., Bouwens E., Pintao M.C., et al. Analysis of the storage and secretion of von Willebrand in blood outgrowth endothelial cells derived from patients with von Willebrand disease. Blood 2013, 121:2762-2772.
80. Piaggio G., Rosti V., Corselli M., et al. Endothelial colony-forming cells from patients with chronic myeloproliferative disorders lack the disease-specific molecular clonality maker. Blood 2009, 114:3127-3130.
81. Teofili L., Martini M., Iachininoto Mg.G. Endothelial progenitor cells are clonal and exhibit the JAK2V617F mutation in a subset of thrombotic patients with Ph-negative myeloproliferative neoplasms. Blood 2011, 117:2700-2707.
82. Fernandez A., Sanz-Rodriguez F., Zarrabeitia R., et al. Blood outgrowth endothelial cells from hereditary haemorrhagic telangiectasia patients reveal abnormalities compatible with vascular lesions. Cardiovasc. Res. 2005, 68:235-248.
83. Toshner M., Voswinckel R., Southwood M., et al. Evidence of dysfunction of endothelial progenitors in pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 2009, 180:780-787.
84. Orlic D., Kajstura J., Chimenti S., et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001, 410:701-705.
85. Kawamura A., Horie T., Tsuda I., et al. Prevention of limb amputation in patients ulcers by autologous peripheral blood mononuclear cell implantation. Ther. Apher. Dial. 2005, 9:59-63.
86. Rafii S., Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 2003, 9:702-712.
87. Schachinger V., Assmus B., Britten M.B., et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year result of the TOPCARE-AMI trial. J. Am. Coll. Cardiol. 2004, 44:1690-1699.
88. Alaiti M.A., Ishikawa M., Costa M. Bone marrow and circulating stem/progenitor cells for regenerative cardiovascular therapy. Transl. Res. 2010, 156:112-129.
89. Templin C., Luscher T.F., Landmesser U. Cell-based cardiovascular repair and regeneration in acute myocardial infarction and chronic ischemic cardiomyopathy current status and future developments. Int. J. Dev. Biol. 2011, 55:407-417.
90. Fadini G.P., Agostini C., Avogaro A. Autologous stem cell therapy for peripheral arterial disease meta-analysis and systematic review of the literature. Atherosclerosis 2010, 209:10-17.
91. Lawall H., Bramlage P., Amann B. Stem cell and progenitor cell therapy in peripheral artery disease. A critical appraisal. Thromb. Hemost. 2010, 103:696-709.
92. + bone marrow mononuclear cells. Stem Cells Int. 2013, e658480.
93. + cell administration in patients with refractory angina: design of the RENEW study. Am. J. Heart 2013, 165:854-861.
94. Maval Z., Losordo D.W. Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ. Res. 2013, 112:1288-1302.
95. Au P., Daheron L.M., Duda D.G., et al. Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 2008, 111:1302-1306.
96. Melero-Martin J.M., De Obaldia M.E., Kang S.Y., et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ. Res. 2008, 103:194-202.
97. He T., Smith L.A., Herrington S., et al. Transplantation of circulating endothelial progenitor cells restores endothelial function of denuded rabbit carotid arteries. Stroke 2004, 35:2378-2384.
98. Hur J., Yoon C.H., Kim H.S., et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculoangiogenesis. Arterioscler. Thromb. Vasc. Biol. 2004, 24:288-293.
99. Dubois C., Liu X., Claus P., et al. Differential effects of progenitor cell populations on left ventricular remodeling and myocardial neovascularization after myocardial infarction. J. Am. Coll. Cardiol. 2010, 55:2232-2243.
100. Medina R., O'Neill C.L., Humphreis M.W., et al. Outgrowth endothelial cells: characterization and their potential for reversing ischemic retinopathy. Invest. Ophthalmol. Vis. Sci. 2010, 51:5906-5913.
101. Moubarik C., Guillet B., Youssef B., et al. Transplanted late outgrowth endothelial progenitor cells as cell therapy product for stroke. Stem Cell Rev. 2011, 7:208-220.
102. Wang W., Lang J.K., Suzuki G., et al. Statins enhance clonal growth of late outgrowth endothelial progenitors and increase myocardial capillary density in the chronically ischemic heart. PLoS ONE 2011, 6:e24864.
103. Liu S.Q., Li Z.L., Cao Y.X., et al. Transfusion of autologous late-outgrowth endothelial cells reduces arterial neointimal formation after injury. Cardiovasc. Res. 2011, 90:171-181.
104. Sipos P.I., Rens W., Schlecht H., et al. Uterine vasculature remodelling in human pregnancy involves functional macro-chimerism by endothelial colony forming cells of fetal origin. Stem Cells 2013, 31:1363-1370.
105. Shelley W.C., Leapley A.C., Huang L., et al. Changes in the frequency and in vivo vessel-forming ability of rhesus monkeys circulating endothelial colony-forming cells across the lifespan (birth to aged). Pediatr. Res. 2012, 71:156-161.
106. Barclay G.R., Tura O., Samuel K., et al. Systematic assessment in an animal model of the angiogenic potential of different human cell sources for therapeutic revascularization. Stem Cell Res. Ther. 2012, 9:23.
107. Yoon C.H., Hur J., Park K.W., et al. Synergistic neo-vascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 2005, 112:1618-1627.
108. Basile D.P., Yoder M.C. Circulating and tissue resident endothelial progenitor cells. J. Cell. Physiol. 2014, 229:10-16.
109. Schwarz T.M., Leicht S.F., Radic T., et al. Vascular incorporation of endothelial-colony forming cells is essential for functional recovery of murine ischemic tissue following cell therapy. Arterioscler. Thromb. Vasc. Biol. 2012, 32:e13-e21.
110. Hoch A.I., Binder B.Y., Genetos D.C., et al. Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells. PLoS ONE 2012, 7:e35579.
111. Liu Y., Tech S.H., Chong M., et al. Vasculogenic and osteogenesis enhancing potential of human umbilical cord blood endothelial colony-forming cells. Stem Cells 2012, 30:1911-1924.
112. Hofmann N.A., Ortner A., Jacamo R., et al. Oxygen sensing mesenchymal progenitors promote neo-vasculogenesis in a humanized model in vivo. PLoS ONE 2012, 7:e44468.
113. Campioni D., Zauli G., Gambatti S., et al. In vitro characterization of circulating endothelial progenitor cells isolated from patients with acute coronary syndrome. PLoS ONE 2013, 8:e56377.
114. Colombo E., Calcaterra F., Coppelletti M., et al. Comparison of fibronectin and collagen in supporting the isolation and the expansion of endothelial progenitor cells from human adult peripheral blood. PLoS ONE 2013, 18:e66734.