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Involvement of Marrow-Derived Endothelial Cells in Vascularization

  • B. Larrivée
  • A. KarsanEmail author
Chapter
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 180)

Abstract

Until recently, the adult neovasculature was thought to arise only through angiogenesis, the mechanism by which new blood vessels form from preexisting vessels through endothelial cell migration and proliferation. However, recent studies have provided evidence that postnatal neovasculature can also arise though vasculogenesis, a process by which endothelial progenitor cells are recruited and differentiate into mature endothelial cells to form new blood vessels. Evidence for the existence of endothelial progenitors has come from studies demonstrating the ability of bone marrow-derived cells to incorporate into adult vasculature. However, the exact nature of endothelial progenitor cells remains controversial. Because of the lack of definitive markers of endothelial progenitors, the in vivo contribution of progenitor cells to physiological and pathological neovascularization remains unclear. Early studies reported that endothelial progenitor cells actively integrate into the adult vasculature and are critical in the development of many types of vascular-dependent disorders such as neoplastic progression. Moreover, it has been suggested that endothelial progenitor cells can be used as a therapeutic strategy aimed at promoting vascular growth in a variety of ischemic diseases. However, increasing numbers of studies have reported no clear contribution of endothelial progenitors in physiological or pathological angiogenesis. In this chapter, we discuss the origin of the endothelial progenitor cell in the embryo and adult, and we discuss the cell’s link to the primitive hematopoietic stem cell. We also review the potential significance of endothelial progenitor cells in the formation of a postnatal vascular network and discuss the factors that may account for the current lack of consensus of the scientific community on this important issue.

Keywords

Endothelial progenitors Vasculogenesis Tumor blood vessels Endothelial progenitor cell Hematopoietic stem cell Hemangioblast Angiogenesis 

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References

  1. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968–973PubMedGoogle Scholar
  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 275:964–967PubMedGoogle Scholar
  3. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85:221–228PubMedGoogle Scholar
  4. Bailey AS, Jiang S, Afentoulis M, Baumann CI, Schroeder DA, Olson SB, Wong MH, Fleming WH (2004) Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 103:13–19PubMedGoogle Scholar
  5. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D (2003) Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest 111:1287–1295PubMedGoogle Scholar
  6. Bhatia M (2001) AC133 expression in human stem cells. Leukemia 15:1685–1688PubMedGoogle Scholar
  7. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932–936PubMedGoogle Scholar
  8. Chapel A, Bertho JM, Bensidhoum M, Fouillard L, Young RG, Frick J, Demarquay C, Cuvelier F, Mathieu E, Trompier F, et al (2003) Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med 5:1028–1038PubMedGoogle Scholar
  9. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125:725–732PubMedGoogle Scholar
  10. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, et al (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91:3527–3561PubMedGoogle Scholar
  11. Coulombel L (2004) Identification of hematopoietic stem/progenitor cells: strength and drawbacks of functional assays. Oncogene 23:7210–7222PubMedGoogle Scholar
  12. Crosby JR, Kaminski WE, Schatteman G, Martin PJ, Raines EW, Seifert RA, Bowen-Pope DF (2000) Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 87:728–730PubMedGoogle Scholar
  13. De Palma M, Venneri MA, Roca C, Naldini L (2003) Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 9:789–795PubMedGoogle Scholar
  14. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8:211–226PubMedGoogle Scholar
  15. Droetto S, Viale A, Primo L, Jordaney N, Bruno S, Pagano M, Piacibello W, Bussolino F, Aglietta M (2004) Vasculogenic potential of long term repopulating cord blood progenitors. FASEB J 18:1273–1275PubMedGoogle Scholar
  16. Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG (2005) Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension 46:7–18PubMedGoogle Scholar
  17. Dzierzak E, Medvinsky A, de Bruijn M (1998) Qualitative and quantitative aspects of haematopoietic cell development in the mammalian embryo. Immunol Today 19:228–236PubMedGoogle Scholar
  18. Eckfeldt CE, Mendenhall EM, Verfaillie CM (2005) Themolecular repertoire of the ‘almighty’ stem cell. Nat Rev Mol Cell Biol 6:726–737PubMedGoogle Scholar
  19. 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 U S A 94:5141–5146PubMedGoogle Scholar
  20. Ema M, Rossant J (2003) Cell fate decisions in early blood vessel formation. Trends Cardiovasc Med 13:254–259PubMedGoogle Scholar
  21. Ema M, Faloon P, Zhang WJ, Hirashima M, Reid T, Stanford WL, Orkin S, Choi K, Rossant J (2003) Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev 17:380–393PubMedGoogle Scholar
  22. 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 65:287–300PubMedGoogle Scholar
  23. Fernandez Pujol B, Lucibello FC, Zuzarte M, Lutjens P, Muller R, Havemann K, Fernandez Pujol B, Lucibello FC, Gehling UM, Lindemann K, et al (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 80:99–110PubMedGoogle Scholar
  24. Fina L, Molgaard HV, Robertson D, Bradley NJ, Monaghan P, Delia D, Sutherland DR, Baker MA, Greaves MF (1990) Expression of the CD34 gene in vascular endothelial cells. Blood 75:2417–2426PubMedGoogle Scholar
  25. Finch CA, Harker LA, Cook JD (1977) Kinetics of the formed elements of human blood. Blood 50:699–707PubMedGoogle Scholar
  26. Friedrich EB, Walenta K, Scharlau J, Nickenig G, Werner N (2006) CD34-/CD133+/VEGFR-2+ endothelial progenitor cell subpopulation with potent vasoregenerative capacities. Circ Res 98:e20–25PubMedGoogle Scholar
  27. Fuchs S, Baffour R, Zhou YF, Shou M, Pierre A, Tio FO, Weissman NJ, Leon MB, Epstein SE, Kornowski R (2001) Transendocardial delivery of autologous bone marrow enhances collateral perfusion and regional function in pigs with chronic experimental myocardial ischemia. J Am Coll Cardiol 37:1726–1732PubMedGoogle Scholar
  28. Galloway JL, Zon LI (2003) Ontogeny of hematopoiesis: examining the emergence of hematopoietic cells in the vertebrate embryo. Curr Top Dev Biol 53:139–158PubMedGoogle Scholar
  29. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R (2003) Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300:1155–1159PubMedGoogle Scholar
  30. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, et al (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95:3106–3112PubMedGoogle Scholar
  31. Gering M, Rodaway AR, Gottgens B, Patient RK, Green AR (1998) The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 17:4029–4045PubMedGoogle Scholar
  32. 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 88:167–174PubMedGoogle Scholar
  33. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797–1806PubMedGoogle Scholar
  34. Gothert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Gottgens B, Izon DJ, Begley CG (2004) Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 104:1769–1777PubMedGoogle Scholar
  35. 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 8:607–612PubMedGoogle Scholar
  36. Grompe M (2003) The role of bone marrow stem cells in liver regeneration. Semin Liver Dis 23:363–372PubMedGoogle Scholar
  37. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Yung S, Chimenti S, Landsman L, Abramovitch R, Keshet E (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124:175–189PubMedGoogle Scholar
  38. Haar JL, Ackerman GA (1971) A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat Rec 170:199–223PubMedGoogle Scholar
  39. Harraz M, Jiao C, Hanlon HD, Hartley RS, Schatteman GC (2001) CD34-blood-derived human endothelial cell progenitors. Stem Cells 19:304–312PubMedGoogle Scholar
  40. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, et al (2001) Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 193:1005–1014PubMedGoogle Scholar
  41. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S (2003) Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102:1340–1346PubMedGoogle Scholar
  42. Hilbe W, Dirnhofer S, Oberwasserlechner F, Schmid T, Gunsilius E, Hilbe G, Woll E, Kahler CM (2004) CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol 57:965–969PubMedGoogle Scholar
  43. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432:625–630PubMedGoogle Scholar
  44. 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 107:1395–1402PubMedGoogle Scholar
  45. Jiang S, Walker L, Afentoulis M, Anderson DA, Jauron-Mills L, Corless CL, Fleming WH (2004) Transplanted human bone marrow contributes to vascular endothelium. Proc Natl Acad Sci U S A 101:16891–16896PubMedGoogle Scholar
  46. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM (2002) Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896–904PubMedGoogle Scholar
  47. Kabrun N, Buhring HJ, Choi K, Ullrich A, Risau W, Keller G (1997) Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 124:2039–2048PubMedGoogle Scholar
  48. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T (2000) Transplantation of expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97:3422–3427PubMedGoogle Scholar
  49. Kallianpur AR, Jordan JE, Brandt SJ (1994) The SCL/TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83:1200–1208PubMedGoogle Scholar
  50. 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 expanded endothelial progenitor cells for myocardial ischemia. Circulation 103:634–637PubMedGoogle Scholar
  51. Kennedy M, Firpo M, Choi K, Wall C, Robertson S, Kabrun N, Keller G (1997) A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386:488–493PubMedGoogle Scholar
  52. Kinnaird T, Stabile E, Burnett MS, Epstein SE (2004) Bone-marrow-derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences. Circ Res 95:354–363PubMedGoogle Scholar
  53. 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 89:189–195PubMedGoogle Scholar
  54. 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 7:430–436PubMedGoogle Scholar
  55. Kopp HG, Ramos CA, Rafii S (2006) Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr Opin Hematol 13:175–181PubMedGoogle Scholar
  56. Kumaravelu P, Hook L, Morrison AM, Ure J, Zhao S, Zuyev S, Ansell J, Medvinsky A (2002) Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 129:4891–4899PubMedGoogle Scholar
  57. Kyba M, Perlingeiro RC, Daley GQ (2002) HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109:29–37PubMedGoogle Scholar
  58. Lajtha LG, Gilbert CW, Guzman E (1971) Kinetics of haemopoietic colony growth. Br J Haematol 20:343–354PubMedGoogle Scholar
  59. Larrivee B, Niessen K, Pollet I, Corbel SY, Long M, Rossi FM, Olive PL, Karsan A (2005) Minimal contribution of marrow-derived endothelial precursors to tumor vasculature. J Immunol 175:2890–2899PubMedGoogle Scholar
  60. Larrivee B, Olive PL, Karsan A (2006) Tissue distribution of endothelial cells in vivo following intravenous injection. Exp Hematol 12:1741–1745Google Scholar
  61. Lechner A, Habener JF (2003) Bone marrow stem cells find a path to the pancreas. Nat Biotechnol 21:755–756PubMedGoogle Scholar
  62. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71–77PubMedGoogle Scholar
  63. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, et al (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194–1201PubMedGoogle Scholar
  64. Machein MR, Renninger S, de Lima-Hahn E, Plate KH (2003) Minor contribution of bone marrow-derived endothelial progenitors to the vascularization of murine gliomas. Brain Pathol 13:582–597PubMedGoogle Scholar
  65. Mathews V, Hanson PT, Ford E, Fujita J, Polonsky KS, Graubert TA (2004) Recruitment of bone marrow-derived endothelial cells to sites of pancreatic beta-cell injury. Diabetes 53:91–98PubMedGoogle Scholar
  66. Matsuoka S, Tsuji K, Hisakawa H, Xu M, Ebihara Y, Ishii T, Sugiyama D, Manabe A, Tanaka R, Ikeda Y, et al (2001) Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood 98:6–12PubMedGoogle Scholar
  67. Matthews W, Jordan CT, Gavin M, Jenkins NA, Copeland NG, Lemischka IR (1991) Areceptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc Natl Acad Sci U S A 88:9026–9030PubMedGoogle Scholar
  68. Medvinsky A, Dzierzak E (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86:897–906PubMedGoogle Scholar
  69. Messner HA (1998) Human hematopoietic progenitor in bone marrow and peripheral blood. Stem Cells 16[Suppl 1]:93–96PubMedGoogle Scholar
  70. Moore MA, Metcalf D (1970) Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18:279–296PubMedGoogle Scholar
  71. Mukouyama Y, Hara T, Xu M, Tamura K, Donovan PJ, Kim H, Kogo H, Tsuji K, Nakahata T, Miyajima A (1998) In vitro expansion of murine multipotential hematopoietic progenitors from the embryonic aorta-gonad-mesonephros region. Immunity 8:105–114PubMedGoogle Scholar
  72. Muller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E (1994) Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1:291–301PubMedGoogle Scholar
  73. Murayama T, Tepper OM, Silver M, Ma H, Losordo DW, Isner JM, Asahara T, Kalka C (2002) Determination of bone marrow-derived endothelial progenitor cell significance in angiogenic growth factor-induced neovascularization in vivo. Exp Hematol 30:967–972PubMedGoogle Scholar
  74. Newman PJ (1997) The biology of PECAM-1. J Clin Invest 100:S25–S29PubMedGoogle Scholar
  75. Nieda M, Nicol A, Denning-Kendall P, Sweetenham J, Bradley B, Hows J (1997) Endothelial cell precursors are normal components of human umbilical cord blood. Br J Haematol 98:775–777PubMedGoogle Scholar
  76. Oberlin E, Tavian M, Blazsek I, Peault B (2002) Blood-forming potential of vascular endothelium in the human embryo. Development 129:4147–4157PubMedGoogle Scholar
  77. Palis J, Yoder MC (2001) Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 29:927–936PubMedGoogle Scholar
  78. Palis J, Robertson S, Kennedy M, Wall C, Keller G (1999) Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126:5073–5084PubMedGoogle Scholar
  79. Papetti M, Herman IM (2002) Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol 282:C947–970PubMedGoogle Scholar
  80. Pardanaud L, Eichmann A (2006) Identification, emergence and mobilization of circulating endothelial cells or progenitors in the embryo. Development 133:2527–2537PubMedGoogle Scholar
  81. Pardanaud L, Altmann C, Kitos P, Dieterlen-Lievre F, Buck CA (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349PubMedGoogle Scholar
  82. Park S, Tepper OM, Galiano RD, Capla JM, Baharestani S, Kleinman ME, Pelo CR, Levine JP, Gurtner GC (2004) Selective recruitment of endothelial progenitor cells to ischemic tissues with increased neovascularization. Plast Reconstr Surg 113:284–293PubMedGoogle Scholar
  83. Peault BM, Thiery JP, Le Douarin NM (1983) Surface marker for hemopoietic and endothelial cell lineages in quail that is defined by a monoclonal antibody. Proc Natl Acad Sci U S A 80:2976–2980PubMedGoogle Scholar
  84. 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 95:952–958PubMedGoogle Scholar
  85. Peters BA, Diaz LA, Polyak K, Meszler L, Romans K, Guinan EC, Antin JH, Myerson D, Hamilton SR, Vogelstein B, et al (2005) Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 11:261–262PubMedGoogle Scholar
  86. Pratt CI, Wu SQ, Bhattacharya M, Kao C, Gilchrist KW, Reznikoff CA (1992) Chromosome losses in tumorigenic revertants of EJ/ras-expressing somatic cell hybrids. Cancer Genet Cytogenet 59:180–190PubMedGoogle Scholar
  87. 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 115:186–194PubMedGoogle Scholar
  88. Rafii S, Heissig B, Hattori K (2002) Efficient mobilization and recruitment of marrow-derived endothelial and hematopoietic stem cells by adenoviral vectors expressing angiogenic factors. Gene Ther 9:631–641PubMedGoogle Scholar
  89. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P (2004) Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 104:2084–2086PubMedGoogle Scholar
  90. Reyes M, Verfaillie CM (2001) Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann N Y Acad Sci 938:231–233; discussion 233–235PubMedGoogle Scholar
  91. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM (2001) Purification and expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615–2625PubMedGoogle Scholar
  92. Robb L, Lyons I, Li R, Hartley L, Kontgen F, Harvey RP, Metcalf D, Begley CG (1995) Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci U S A 92:7075–7079PubMedGoogle Scholar
  93. Ruggeri ZM (2003) Von Willebrand factor. Curr Opin Hematol 10:142–149PubMedGoogle Scholar
  94. Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii S (2003) VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101:168–172PubMedGoogle Scholar
  95. Shaked Y, Bertolini F, Man S, Rogers MS, Cervi D, Foutz T, Rawn K, Voskas D, Dumont DJ, Ben-David Y, et al (2005) Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 7:101–111PubMedGoogle Scholar
  96. 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 376:62–66PubMedGoogle Scholar
  97. Shepard JL, Zon LI (2000) Developmental derivation of embryonic and adult macrophages. Curr Opin Hematol 7:3–8PubMedGoogle Scholar
  98. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, et al (1998) Evidence for circulating bone marrow-derived endothelial cells. Blood 92:362–367PubMedGoogle Scholar
  99. Shivdasani RA, Mayer EL, Orkin SH (1995) Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373:432–434PubMedGoogle Scholar
  100. Sikder H, Huso DL, Zhang H, Wang B, Ryu B, Hwang ST, Powell JD, Alani RM (2003) Disruption of Id1 reveals major differences in angiogenesis between transplanted and autochthonous tumors. Cancer Cell 4:291–299PubMedGoogle Scholar
  101. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G (2005) PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 7:870–879PubMedGoogle Scholar
  102. Stainier DY, Weinstein BM, Detrich HW, Zon LI, Fishman MC (1995) Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121:3141–3150PubMedGoogle Scholar
  103. Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schumichen C, Nienaber CA, Freund M, Steinhoff G (2003) Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361:45–46PubMedGoogle Scholar
  104. Takahashi K, Naito M (1993) Development, differentiation, and proliferation of macrophages in the rat yolk sac. Tissue Cell 25:351–362PubMedGoogle Scholar
  105. 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 5:434–438PubMedGoogle Scholar
  106. 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 102:199–209PubMedGoogle Scholar
  107. Tamura H, Okamoto S, Iwatsuki K, Futamata Y, Tanaka K, Nakayama Y, Miyajima A, Hara T (2002) In vivo differentiation of stem cells in the aorta-gonad-mesonephros region of mouse embryo and adult bone marrow. Exp Hematol 30:957–966PubMedGoogle Scholar
  108. Tavian M, Coulombel L, Luton D, Clemente HS, Dieterlen-Lievre F, Peault B (1996) Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87:67–72PubMedGoogle Scholar
  109. Tonini T, Rossi F, Claudio PP (2003) Molecular basis of angiogenesis and cancer. Oncogene 22:6549–6556PubMedGoogle Scholar
  110. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95:343–353PubMedGoogle Scholar
  111. Urbich C, Heeschen C, Aicher A, Dernbach E, Zeiher AM, Dimmeler S (2003) Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108:2511–2516PubMedGoogle Scholar
  112. Verfaillie CM, Schwartz R, Reyes M, Jiang Y (2003) Unexpected potential of adult stem cells. Ann N Y Acad Sci 996:231–234PubMedGoogle Scholar
  113. Voswinckel R, Ziegelhoeffer T, Heil M, Kostin S, Breier G, Mehling T, Haberberger R, Clauss M, Gaumann A, Schaper W, Seeger W (2003) Circulating vascular progenitor cells do not contribute to compensatory lung growth. Circ Res 93:372–379PubMedGoogle Scholar
  114. Wang X, Ge S, Gonzalez I, McNamara G, Rountree CB, Xi KK, Huang G, Bhushan A, Crooks GM (2006) Formation of pancreatic duct epithelium from bone marrow during neonatal development. Stem Cells 24:307–314PubMedGoogle Scholar
  115. Watt SM, Gschmeissner SE, Bates PA (1995) PECAM-1: its expression and function as a cell adhesion molecule on hemopoietic and endothelial cells. Leuk Lymphoma 17:229–244PubMedGoogle Scholar
  116. Wognum AW, Eaves AC, Thomas TE (2003) Identification and isolation of hematopoietic stem cells. Arch Med Res 34:461–475PubMedGoogle Scholar
  117. Wong PM, Chung SW, Chui DH, Eaves CJ (1986) Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac. Proc Natl Acad Sci U S A 83:3851–3854PubMedGoogle Scholar
  118. Xu MJ, Matsuoka S, Yang FC, Ebihara Y, Manabe A, Tanaka R, Eguchi M, Asano S, Nakahata T, Tsuji K (2001) Evidence for the presence of murine primitive megakaryocytopoiesis in the early yolk sac. Blood 97:2016–2022Google Scholar
  119. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, Bosch-Marce M, Masuda H, Losordo DW, Isner JM, Asahara T (2003) Stromal cell-derived factor-1 effects on expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322–1328PubMedGoogle Scholar
  120. Yoder MC, Hiatt K (1997) Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood 89:2176–2183PubMedGoogle Scholar
  121. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D (1997a) Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7:335–344PubMedGoogle Scholar
  122. Yoder MC, Hiatt K, Mukherjee P (1997b) In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A 94:6776–6780PubMedGoogle Scholar
  123. Yokomizo T, Ogawa M, Osato M, Kanno T, Yoshida H, Fujimoto T, Fraser S, Nishikawa S, Okada H, Satake M, et al (2001) Requirement of Runx1/AML1/PEBP2alphaB for the generation of haematopoietic cells from endothelial cells. Genes Cells 6:13–23PubMedGoogle Scholar
  124. Young PE, Baumhueter S, Lasky LA (1995) The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development. Blood 85:96–105PubMedGoogle Scholar
  125. Zammaretti P, Zisch AH (2005) Adult ‘endothelial progenitor cells’. Renewing vasculature. Int J Biochem Cell Biol 37:493–503PubMedGoogle Scholar
  126. Zentilin L, Tafuro S, Zacchigna S, Arsic N, Pattarini L, Sinigaglia M, Giacca M (2006) Bone marrow mononuclear cells are recruited to the sites of VEGF-induced neovascularization but are not incorporated into the newly formed vessels. Blood 107:3546–3554PubMedGoogle Scholar
  127. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W (2004) Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res 94:230–238PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  1. 1.Laboratoire de Médecine expérimentale, INSERM U36Collège de FranceParisFrance
  2. 2.Pathology and Laboratory Medicine and Medical BiophysicsBritish Columbia Cancer Agency Research CentreBritish ColumbiaCanada

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