Trends in Cardiovascular Medicine
Volume 16, Issue 4 , Pages 128-139 , May 2006

Are Intra-Aortic Hemopoietic Cells Derived from Endothelial Cells During Ontogeny?

  • Françoise Dieterlen-Lièvre

      Affiliations

    • UMR 7128 Laboratoire d'Embryologie Cellulaire et Moléculaire, 94130 Nogent-sur-Marne, France
    • Corresponding Author InformationAddress correspondence to: Françoise Dieterlen-Lièvre and Thierry Jaffredo, UMR 7622 Laboratoire de Biologie du Développement, 75252 Paris Cedex 05, France.
    • Present address: IAF, UPR2197, 91198 Gif sur Yvette, France.
  • ,
  • Claire Pouget

      Affiliations

    • UPMC, CNRS UMR7622, Laboratoire de Biologie du Développement, 75252 Paris Cedex 05, France
  • ,
  • Karine Bollérot

      Affiliations

    • UPMC, CNRS UMR7622, Laboratoire de Biologie du Développement, 75252 Paris Cedex 05, France
  • ,
  • Thierry Jaffredo

      Affiliations

    • UMR 7128 Laboratoire d'Embryologie Cellulaire et Moléculaire, 94130 Nogent-sur-Marne, France
    • UPMC, CNRS UMR7622, Laboratoire de Biologie du Développement, 75252 Paris Cedex 05, France
    • Corresponding Author InformationAddress correspondence to: Françoise Dieterlen-Lièvre and Thierry Jaffredo, UMR 7622 Laboratoire de Biologie du Développement, 75252 Paris Cedex 05, France.

References 

  1. Ambler CA, Nowicki JL, Burke AC, Bautch VL. Assembly of trunk and limb blood vessels involves extensive migration and vasculogenesis of somite-derived angioblasts. Dev Biol. 2001;234:352–364
  2. Bertrand JY, Giroux S, Golub R, et al. Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc Natl Acad Sci U S A. 2005;102:134–139
  3. Bollerot K, Romero S, Dunon D, Jaffredo T. Core binding factor in the early avian embryo: cloning of Cbfbeta and combinatorial expression patterns with Runx1. Gene Expr Patterns. 2005;6:29–39
  4. Cai Z, De Bruijn M, Ma X, et al. Haploinsufficiency of AML1 affects the temporal and spatial generation of hematopoietic stem cells in the mouse embryo. Immunity. 2000;13:423–431
  5. Choi K, Kennedy M, Kazarov A, et al. A common precursor for hematopoietic and endothelial cells. Development. 1998;125:725–732
  6. Corbel C. Expression of αVβ3 integrin in the chick embryo aortic endothelium. Int J Dev Biol. 2002;46:827–830
  7. Corbel C, Salaun J. AlphaIIb integrin expression during development of the murine hemopoietic system. Dev Biol. 2002;243:301–311
  8. Dantschakoff V. Uber das erste Auftreten der Blutelemente beim Hühnerembryo. Folia Haematol. 1907;4
  9. De Bruijn M, Ma X, Robin C, et al. Hematopoietic stem cells localise to the endothelial cell layer in the midgestation mouse aorta. Immunity. 2002;16:673–683
  10. Dieterlen-Lièvre F, Pardanaud L, Caprioli A, Joffredo T. Non-yolk sac hematopoietic stem cells: the avian paradigm. In:  Li Z editors. Hematopoiesis, a developmental approach. New York: Oxford University Press; 2001;
  11. Eichmann A, Marcelle C, Breant C, Le Douarin NM. Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev. 1993;42:33–48
  12. Eichmann A, Corbel C, Nataf V, et al. 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. 1997;94:5141–5146
  13. Elefanty AG, Begley CG, Hartley L, et al. SCL expression in the mouse embryo detected with a targeted lacZ reporter gene demonstrates its localization to hematopoietic, vascular, and neural tissues. Blood. 1999;94:3754–3763
  14. Ema M, Faloon P, Zhang WJ, et al. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 2003;17:380–393
  15. Ema M, Takahashi S, Rossant J. Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood. 2006;107:111–117
  16. Emambokus NR, Frampton J. The glycoprotein IIb molecule is expressed on early murine hematopoietic progenitors and regulates their numbers in sites of hematopoiesis. Immunity. 2003;19:33–45
  17. Fehling HJ, Lacaud G, Kubo A, et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development. 2003;130:4217–4227
  18. Flamme I, Breier G, Risau W. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol. 1995;169:699–712
  19. Garcia-Porrero JA, Godin IE, Dieterlen-Lievre F. Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat Embryol (Berl). 1995;192:425–435
  20. Godin I, Cumano A. The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol. 2002;2:593–604
  21. Huang H, Auerbach R. Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo. Proc Natl Acad Sci U S A. 1993;90:10110–10114
  22. Huber TL, Kouskoff V, Fehling HJ, et al. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432:625–630
  23. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development. 1998;125:4575–4583
  24. Jaffredo T, Gautier R, Brajeul V, Dieterlen-Lievre F. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol. 2000;224:204–214
  25. Jaffredo T, Bollerot K, Sugiyama D, et al. Tracing the hemangioblast during embryogenesis: developmental relationships between endothelial and hematopoietic cells. Int J Dev Biol. 2005;49:269–277
  26. Jeurissen SH, Janse EM. The use of chicken-specific antibodies in veterinary research involving three other avian species. Vet Q. 1998;20:140–143
  27. Jordan HE. Evidence of hemogenic capacity of endothelium. Anat Rec. 1916;10:417–420
  28. Jordan HE. Aortic cell clusters in vertebrate embryos. Proc Natl Acad Sci U S A. 1917;3:149–156
  29. Kennedy M, Firpo M, Choi K, et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature. 1997;386:488–493
  30. Kinder SJ, Tsang TE, Quinlan GA, et al. The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development. 1999;126:4691–4701
  31. Kundu M, Chen A, Anderson S, et al. Role of Cbfb in hematopoiesis and perturbations resulting from expression of the leukemic fusion gene, CBFB-MYH11. Blood. 2002;100:2449–2456
  32. Lacaud G, Gore L, Kennedy M, et al. Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood. 2002;100:458–466
  33. Lecuyer E, Hoang T. SCL: from the origin of hematopoiesis to stem cells and leukemia. Exp Hematol. 2004;32:11–24
  34. Manaia A, Lemarchandel V, Klaine M, et al. Lmo2 and GATA-3 associated expression in intraembryonic hemogenic sites. Development. 2000;127:643–653
  35. Marshall CJ, Thrasher AJ. The embryonic origins of human hematopoiesis. Br J Haematol. 2001;112:838–850
  36. Marshall CJ, Moore RL, Thorogood P, et al. Detailed characterization of the human aorta–gonad–mesonephros region reveals morphological polarity resembling a hematopoietic stromal layer. Dev Dyn. 1999;215:139–147
  37. Marshall CJ, Kinnon C, Thrasher AJ. Polarized expression of bone morphogenetic protein-4 in the human aorta–gonad–mesonephros region. Blood. 2000;96:1591–1593
  38. Mikkola HK, Fujiwara Y, Schlaeger TM, et al. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood. 2003;101:508–516
  39. Minko K, Bollerot K, Drevon C, et al. From mesoderm to blood islands: patterns of key molecules during yolk sac erythropoiesis. Gene Expr Patterns. 2003;3:261–272
  40. Murray PDF. The development “in vitro” of blood of the early chick embryo. Strangeways Res Lab. 1932;497–521
  41. Naik UP, Parise LV. Structure and function of platelet alpha IIb beta 3. Curr Opin Hematol. 1997;4:317–322
  42. Niki M, Okada H, Takano H, et al. Hematopoiesis in the fetal liver is impaired by targeted mutagenesis of a gene encoding a non-DNA binding subunit of the transcription factor, polyomavirus enhancer binding protein 2/core binding factor. Proc Natl Acad Sci U S A. 1997;94:5697–5702
  43. Nimmagadda S, Geetha Loganathan P, Huang R, et al. BMP4 and noggin control embryonic blood vessel formation by antagonistic regulation of VEGFR-2 (Quek1) expression. Dev Biol. 2005;280:100–110
  44. Nishikawa S-I, Nishikawa S, Hirashima M, et al. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hematopoietic lineages. Development. 1998;125:1747–1757
  45. Noden DM. Embryonic origins and assembly of blood vessels. Am Rev Respir Dis. 1989;140:1097–1103
  46. North T, Gu TL, Stacy T, et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 1999;126:2563–2575
  47. North TE, De Bruijn MF, Stacy T, et al. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity. 2002;16:661–672
  48. North TE, Stacy T, Matheny CJ, et al. Runx1 is expressed in adult mouse hematopoietic stem cells and differentiating myeloid and lymphoid cells, but not in maturing erythroid cells. Stem Cells. 2004;22:158–168
  49. Ody C, Vaigot P, Quere P, et al. Glycoprotein IIb–IIIa is expressed on avian multilineage hematopoietic progenitor cells. Blood. 1999;93:2898–2906
  50. Okuda T, van Deursen J, Hiebert SW, et al. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84:321–330
  51. Ottersbach K, Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell. 2005;8:377–387
  52. Palis J, Yoder MC. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol. 2001;29:927–936
  53. Palis J, Robertson S, Kennedy M, et al. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development. 1999;126:5073–5084
  54. Pardanaud L, Dieterlen-Lievre F. Expression of C-ETS1 in early chick embryo mesoderm: Relationship to the hemangioblastic lineage. Cell Adhes Commun. 1993;1:151–160
  55. Pardanaud L, Dieterlen-Lievre F. Manipulation of the angiopoietic/hemangiopoietic commitment in the avian embryo. Development. 1999;126:617–627
  56. Pardanaud L, Altmann C, Kitos P, et al. Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development. 1987;100:339–349
  57. Pardanaud L, Yassine F, Dieterlen-Lievre F. Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development. 1989;105:473–485
  58. Pardanaud L, Luton D, Prigent M, et al. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development. 1996;122:1363–1371
  59. Petrenko O, Beavis A, Klaine M, et al. The molecular characterization of the fetal stem cell marker AA4. Immunity. 1999;10:691–700
  60. Pouget C, Gautier R, Teillet MA, Jaffredo T. Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development. 2006;133:1013–1022
  61. Pudliszewski M, Pardanaud L. Vasculogenesis and angiogenesis in the mouse embryo studied using quail/mouse chimeras. Int J Dev Biol. 2005;49:355–361
  62. Risau W, Lemmon V. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol. 1988;125:441–450
  63. Robertson SM, Kennedy M, Shannon JM, Keller G. A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development. 2000;127:2447–2459
  64. Sabin F. Origin and development of the primitive vessels of the chick and of the pig. Contrib Embryol Carnegie Inst. 1917;226:61–124
  65. Sasaki K, Yagi H, Bronson RT, et al. Absence of fetal liver hematopoiesis in mice deficient in transcriptional coactivator core binding factor beta. Proc Natl Acad Sci U S A. 1996;93:12359–12363
  66. Schlaeger TM, Mikkola HK, Gekas C, et al. Tie2Cre-mediated gene ablation defines the stem-cell leukemia gene (SCL/tal1)-dependent window during hematopoietic stem-cell development. Blood. 2005;105:3871–3874
  67. Spangrude GJ, Brooks DM. Mouse strain variability in the expression of the hematopoietic stem cell antigen Ly-6A/E by bone marrow cells. Blood. 1993;82:3327–3332
  68. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science. 1988;241:58–62
  69. Sugiyama D, Ogawa M, Hirose I, et al. Erythropoiesis from acetyl LDL incorporating endothelial cells at the preliver stage. Blood. 2003;101:4733–4738
  70. Taoudi S, Morrison AM, Inoue H, et al. Progressive divergence of definitive haematopoietic stem cells from the endothelial compartment does not depend on contact with the foetal liver. Development. 2005;132:4179–4191
  71. Tavian M, Peault B. Embryonic development of the human hematopoietic system. Int J Dev Biol. 2005;49:243–250
  72. Tavian M, Coulombel L, Luton D, et al. Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood. 1996;87:67–72
  73. Tavian M, Cortes F, Charbord P, et al. Emergence of the haematopoietic system in the human embryo and foetus. Haematologica. 1999;84:1–3
  74. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105:617–626
  75. Walmsley M, Ciau-Uitz A, Patient R. Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus. Development. 2002;129:5683–5695
  76. Wang Q, Stacy T, Binder M, et al. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996;93:3444–3449
  77. Wang Q, Stacy T, Miller JD, et al. The CBFbeta subunit is essential for CBFalpha2 (AML1) function in vivo. Cell. 1996;87:697–708
  78. Wang L, Li L, Shojaei F, et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity. 2004;21:31–41
  79. Wang L, Menendez P, Shojaei F, et al. Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med. 2005;201:1603–1614
  80. Wilting J, Kurz H, Brand-Saberi B, et al. Kinetics and differentiation of somite cells forming the vertebral column: studies on human and chick embryos. Anat Embryol (Berl). 1994;190:573–581
  81. Wood HB, May G, Healy L, et al. CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood. 1997;90:2300–2311
  82. Yokomizo T, Ogawa M, Osato M, et al. Requirement of Runx1/AML1/PEBP2aB for the generation of haematopoietic cells from endothelial cells. Genes Cells. 2001;6:13–23
  83. Ziegler BL, Valtieri M, Porada GA, et al. KDR receptor: a key marker defining hematopoietic stem cells. Science. 1999;285:1553–1558

PII: S1050-1738(06)00042-9

doi: 10.1016/j.tcm.2006.02.005

Trends in Cardiovascular Medicine
Volume 16, Issue 4 , Pages 128-139 , May 2006