Hemangioblasts, Angioblasts, and Adult Endothelial Cell Progenitors

Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology

Volumn 276, Issue 1, 2004, Pages 13-21

  Schatteman, Gina C ^a   Awad, Ola ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Bone marrow; Endothelial cell progenitor; Endothelium; Hemangioblast; Neovascularization; VEGF

Indexed keywords

ANGIOGENIC FACTOR; CD34 ANTIGEN; EPITOPE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; BLOOD FLOW; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; EMBRYO CELL; ENDOTHELIUM CELL; GENE THERAPY; GENE VECTOR; HEART FUNCTION; HEMANGIOBLAST; HUMAN; HUMAN CELL; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROGENY; REVIEW; STEM CELL; VASCULAR SURGERY; VASCULARIZATION;

HARNESS;

EID: 0347951327     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ar.a.10131     Document Type: Review

References (92)

1. Asahara T, Bauters C, Pastore C, Kearney M, Rossow S, Bunting S, Ferrara N, Symes JF, Isner JM. 1995. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 91:2793-2801.
2. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967.
3. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. 1999a. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85:221-228.
4. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. 1999b. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. Embo J 18:3964-3972.
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. 2002. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction. Circulation 106: 3009-3017.
6. Bautz F, Rafii S, Kanz L, Mohle R. 2000. Expression and secretion of vascular endothelial growth factor-A by cytokine-stimulated hematopoietic progenitor cells. Possible role in the hematopoietic microenvironment. Exp Hematol 28:700-706.
7. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL. 1999. Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534-537.
8. Campbell JH, Han CL, Campbell GR. 2001. Neointimal formation by circulating bone marrow cells. Ann NY Acad Sci 947:18-24.
9. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. 1998. A common precursor for hematopoietic and endothelial cells. Development 125:725-732.
10. Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H, Lendahl U, Frisen J. 2000. Generalized potential of adult neural stem cells. Science 288:1660-1663.
11. Crosby JR, Kaminski WE, Schatteman GC, Martin JC, Raines EW, Seifert RA, Bowen-Pope DF. 2000. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 87:728-730.
12. Davidoff AM, Ng CY, Brown P, Leary MA, Spurbeck WW, Zhou J, Horwitz E, Vanin EF, Nienhuis AW. 2001. 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 7:2870-2879.
13. Eichmann A, Marcelle C, Breant C, Le Douarin NM. 1993. Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev 42:33-48.
14. Eichmann A, Corbel C, Nataf V, Vaigot P, Breant C, Le Douarin NM. 1997. Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci USA 94:5141-5146.
15. Eiermann D, Johnson C, Haskill J. 1989. Human monocyte inflammatory mediator gene expression is selectively regulated by adherence substrates. Immunology 142:1970-1976.
16. Feigl W, Susani M, Ulrich W, Matejka M, Losert U, Sinzinger H. 1985. Organization of experimental thrombosis by blood cells. Virchows Arch A 406:133-148.
17. Fernandez Pujol B, Lucibello FC, Gehling UM, Lindemann K, Weidner N, Zuzarte ML, Adamkiewicz J, Elsasser HP, Muller R, Havemann K. 2000. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation 65:287-300.
18. Fernandez Pujol B, Lucibello FC, Zuzarte M, Lutjens P, Muller R, Havemann K. 2001. Dendritic cells derived from peripheral monocytes express endothelial markers and in the presence of angiogenic growth factors differentiate into endothelial-like cells. Eur J Cell Biol 80:99-110.
19. Flamme I, Breier G, Risau W. 1995. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 169:699-712.
20. Fritsch G, Stimpfl M, Kurz M, Leitner A, Printz D, Buchinger P, Hoecker P, Gadner H. 1995. Characterization of hematopoietic stem cells. Ann NY Acad Sci 770:42-52.
21. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schafer B, Hossfeld DK, Fiedler W. 2000. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95:3106-3112.
22. George F, Brisson C, Poncelet P, Laurent JC, Massot O, Arnoux D, Ambrosi P, Klein-Soyer C, Cazenave JP, Sampol J. 1992. Rapid isolation of human endothelial cells from whole blood using S-Endol monoclonal antibody coupled to immuno-magnetic beads: demonstration of endothelial injury after angioplasty. Thromb Haemost 67:147-153.
23. Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, Girardi L, Yurt R, Himel H, Rafii S. 2001. Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ Res 88:167-174.
24. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB, Scott EW. 2002. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 8:607-612.
25. Harraz M, Jiao C, Hanlon HD, Hartley RS, Schatteman GC. 2001. Cd34(-) blood-derived human endothelial cell progenitors. Stem Cells 19:304-312.
26. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MA, Rafii S. 2001. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 193:1005-1014.
27. Hausser G, Ludewig B, Gelderblom HR, Tsunetsugu-Yokota Y, Akagawa K, Meyerhans A. 1997. Monocyte-derived dendritic cells represent a transient stage of differentiation in the myeloid lineage. Immunobiology 197:534-542.
28. Hendrix MJ, Seftor EA, Meltzer PS, Gardner LM, Hess AR, Kirschmann DA, Schatteman GC, Seftor RE. 2001. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci USA 98: 8018-8023.
29. Hendrix MJ, Seftor RE, Seftor EA, Gruman LM, Lee LM, Nickoloff BJ, Miele L, Sheriff DD, Schatteman GC. 2002. Transendothelial function of human metastatic melanoma cells: role of the microenvironment in cell-fate determination. Cancer Res 62:665-668.
30. Hueper WC, Russell MA. 1932. Capillary-like formations in tissue culture of leukocytes. Arch Exp Zellforsch 12:407-424.
31. Ikenaga S, Hamano K, Nishida M, Kobayashi T, Li TS, Kobayashi S, Matsuzaki M, Zempo N, Esato K. 2001. Autologous bone marrow implantation induced angiogenesis and improved deteriorated exercise capacity in a rat ischemic hindlimb model. J Surg Res 96: 277-283.
32. Ikpeazu C, Davidson MK, Halteman D, Browning PJ, Brandt SJ. 2000. Donor origin of circulating endothelial progenitors after allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 6:301-308.
33. Issarachai S, Priestley GV, Nakamoto B, Papayannopoulou T. 2002. Cells with hemopoietic potential residing in muscle are itinerant bone marrow-derived cells. Exp Hematol 30:366-373.
34. Jackson KA, Mi T, Goodell MA. 1999. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482-14486.
35. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
36. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E, Pieczek A, Iwaguro H, Hayashi SI, Isner JM, Asahara T. 2000a. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 86:1198-1202.
37. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T. 2000b. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 97:3422-3427.
38. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, Symes JF. 2000c. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 70:829-834.
39. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Tsutsumi Y, Ozono R, Masaki H, Mori Y, Iba O, Tateishi E, Kosaki A, Shintani S, Murohara T, Imaizumi T, Iwasaka T. 2001. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation 104:1046-1052.
40. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. 2001. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103:634-637.
41. Kobayashi T, Hamano K, Li TS, Katoh T, Kobayashi S, Matsuzaki M, Esato K. 2000. Enhancement of angiogenesis by the implantation of self bone marrow cells in a rat ischemic heart model. J Surg Res 89:189-195.
42. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. 2001. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7:430-436.
43. Krause DS, Fackler MJ, Civin CI, May WS. 1996. CD34: structure, biology, and clinical utility. Blood 87:1-13.
44. Leu HJ, Feigl W, Susani M. 1987. Angiogenesis from mononuclear cells in thrombi. Virchows Arch A Pathol Anat Histopathol 411:5-14.
45. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. 2000. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71-77.
46. Mackenzie JR, Hackett M, Topuzlu C, Tibbs DJ. 1968. Origin of arterial prosthesis lining from circulating blood cells. Arch Surg 97:879-885.
47. Majka M, Janowska-Wieczorek A, Ratajczak J, Ehrenman K, Pietrzkowski Z, Kowalska MA, Gewirtz AM, Emerson SG, Ratajczak MZ. 2001. Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood 97:3075-3085.
48. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ. 1999. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739-752.
49. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA. 2002. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA 99:1341-1346.
50. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller NP, Risau W, Ullrich A. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72:835-846.
51. Minehata K, Mukouyama YS, Sekiguchi T, Hara T, Miyajima A. 2002. Macrophage colony stimulating factor modulates the development of hematopoiesis by stimulating the differentiation of endothelial cells in the AGM region. Blood 99:2360-2368.
52. Moldovan NI, Goldschmidt-Clermont PJ, Parker-Thornburg J, Shapiro SD, Kolattukudy PE. 2000. Contribution of monocytes/macrophages to compensatory neovascularization: the drilling of metalloelastase-positive tunnels in ischemic myocardium. Circ Res 87: 378-384.
53. Moore MA, Hattori K, Heissig B, Shieh JH, Dias S, Crystal RG, Rafii S. 2001. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann NY Acad Sci 938:36-45.
54. Murohara T, Ikeda H, Duan J, Shintani S, Sasaki K, Eguchi H, Onitsuka I, Matsui K, Imaizumi T. 2000. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 105:1527-1536.
55. Noishiki Y, Tomizawa Y, Yamane Y, Matsumoto A. 1996. Autocrine angiogenic vascular prosthesis with bone marrow transplantation. Nat Med 2:90-93.
56. 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. 2001. Bone marrow cells regenerate infarcted myocardium. Nature 410:701-705.
57. Parker RC. 1933. The development of organized vessels in cultures of blood cells. Science 77:544-546.
58. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA, Rafii S. 2000. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95:952-958.
59. Peters KG, De Vries C, Williams LT. 1993. Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 90:8915-8919.
60. Prathap K. 1972. Surface lining cells of healing thrombi in rat femoral veins, an electron-microscopic study. J Pathol 107:1-8.
61. Quirici N, Soligo D, Caneva L, Servida F, Bossolasco P, Deliliers GL. 2001. Differentiation and expansion of endothelial cells from human bone marrow CD133(+) cells. Br J Haematol 115:186-194.
62. Randolph GJ, Beaulieu S, Lebecque S, Steinman RM, Muller WA. 1998. Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282:480-483.
63. Risau W. 1995. Differentiation of endothelium. Faseb J 9:926-933.
64. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. 2002. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8:403-409.
65. Sbarbati R, de Boer M, Marzilli M, Scarlattini M, Rossi G, van Mourik JA. 1991. Immunologic detection of endothelial cells in human whole blood. Blood 77:764-769.
66. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA. 2000. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106:571-578.
67. Schmeisser A, Garlichs CD, Zhang H, Eskafi S, Graffy C, Ludwig J, Strasser RH, Daniel WG. 2001. Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc Res 49:671-680.
68. Schmeisser A, Strasser RH. 2002. Phenotypic overlap between hematopoietic cells with suggested angioblastic potential and vascular endothelial cells. J Hematother Stem Cell Res 11:69-79.
69. Schuh AC, Faloon P, Hu QL, Bhimani M, Choi K. 1999. In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc Natl Acad Sci USA 96:2159-2164.
70. Scott SM, Barth MG, Gaddy LR, Ahl Jr ET. 1994. The role of circulating cells in the healing of vascular prostheses. J Vasc Surg 19:585-593.
71. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66.
72. Shalaby F, Ho J, Stanford WL, Fischer KD, Schuh AC, Schwartz L, Bernstein A, Rossant J. 1997. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89:981-990.
73. Shi Q, Wu MH, Hayashida N, Wechezak AR, Clowes AW, Sauvage LR. 1994. Proof of fallout endothelialization of impervious Dacron grafts in the aorta and inferior vena cava of the dog. J Vasc Surg 20:546-556; discussion 556-547.
74. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. 1998. Evidence for circulating bone marrow-derived endothelial cells. Blood 92:362-367.
75. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T. 2001a. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103:2776-2779.
76. Shintani S, Murohara T, Ikeda H, Ueno T, Sasaki K, Duan J, Imaizumi T. 2001b. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103: 897-903.
77. Siena S, Bregni M, Brando B, Ravagnani F, Bonadonna G, Gianni AM. 1989. Circulation of CD34+ hematopoietic stem cells in the peripheral blood of high-dose cyclophosphamide-treated patients: enhancement by intravenous recombinant human granulocyte-macrophage colony-stimulating factor. Blood 74:1905-1914.
78. Sinzinger H, Fitscha P, Kritz H, Rogatti W, Grady JO. 1996. Prostaglandin E1 decreases circulating endothelial cells. Prostaglandins 51:61-68.
79. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P. 2002. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106:1913-1918.
80. Stump MM, Jordan JL, DeBakey ME, Halpert B. 1963. Endothelium grown from circulating blood on isolated intravascular Dacron hub. Am J Pathol 43:361-367.
81. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. 1999. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434-438.
82. Takakura N, Watanabe T, Suenobu S, Yamada Y, Noda T, Ito Y, Satake M, Suda T. 2000. A role for hematopoietic stem cells in promoting angiogenesis. Cell 102:199-209.
83. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. 2002. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106:2781-2786.
84. Tsapogas M, Streling G, Girolami M. 1967. Study on the organization of experimental thrombi. Angiology 18:825-832.
85. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. 2001. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89:E1-E7.
86. Waltenberger J, Lange J, Kranz A. 2000. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: a potential predictor for the individual capacity to develop collaterals. Circulation 102:185-190.
87. White GC, Parshley MS. 1950. Growth of in vitro blood vessels from bone marrow of adult chickens. Am J Anat 89:321-345.
88. Wisse E. 1974. Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastuc Res 46:393-426.
89. Wu MH, Shi Q, Wechezak AR, Clowes AW, Gordon IL, Sauvage LR. 1995. Definitive proof of endothelialization of a Dacron arterial prosthesis in a human being. J Vasc Surg 21:862-867.
90. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K. 2000. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408:92-96.
91. Young PE, Baumhueter S, Lasky LA. 1995. The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development. Blood 85:96-105.
92. Young PP, Hofling AA, Sands MS. 2002. VEGF increases engraftment of bone marrow-derived endothelial progenitor cells (EPCs) into vasculature of newborn murine recipients. Proc Natl Acad Sci USA 99:11951-11956.