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Embryonic Vasculogenesis and Hematopoietic Specification

  • Lauren C. Goldie
  • Melissa K. Nix
  • Karen K. Hirschi
Part of the Molecular Biology Intelligence Unit book series (MBIU)

Abstract

Vasculogenesis is the process by which blood vessels are formed de novo. In mammals, vasculogenesis occurs in parallel with hematopoiesis, the formation of blood cells. Thus, it is debated whether vascular endothelial cells and blood cells are derived from a common progenitor. Whether or not this is the case, there certainly is commonality among regulatory factors that control the differentiation and differentiated function of both cell lineages. VEGF is a major regulator of both cell types and plays a critical role, in coordination with other signaling pathways and transcriptional regulators, in controlling the differentiation and behavior of endothelial and blood cells during early embryonic development, as further discussed herein.

Keywords

Vascular Endothelial Growth Factor Endothelial Cell Proliferation Fluid Shear Stress Side Population Cell Primitive Streak 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Tarn PPL, Behringer RR. Mouse gastrulation: the formation of a mammalian body plan. Mech Dev 1997; 68:3–25.CrossRefGoogle Scholar
  2. 2.
    Winnier G, Blessing M, Labosky PA, Hogan BL. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995; 9:2105–2116.PubMedCrossRefGoogle Scholar
  3. 3.
    Saxton TM, Pawson T. Morphogenetic movements at gastrulation require the SH2 tyrosine phosphatase Shp2. Proc Natl Acad Sci U S A 1999; 96:3790–3795.PubMedCrossRefGoogle Scholar
  4. 4.
    Dyer MA, Farrington SM, Mohn D et al. Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 2001; 128:1717–1730.PubMedGoogle Scholar
  5. 5.
    Poole TJ, Finkelstein EB, Cox CM. The role of FGF and VEGF in angioblast induction and migration during vascular development. Dev Dyn 2001; 220:1–17.PubMedCrossRefGoogle Scholar
  6. 6.
    Flamme I, Risau W. Induction of vasculogenesis and hematopoiesis in vitro. Development 1992; 116:435–439.PubMedGoogle Scholar
  7. 7.
    Motoike T, Loughna S, Perens E et al. Universal GFP reporter for the study of vascular development. Genesis 2000; 28:75–81.PubMedCrossRefGoogle Scholar
  8. 8.
    Damert A, Miquerol L, Gertsenstein M et al. Insufficient VEGF-A activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 2002; 129:1881–1892.PubMedGoogle Scholar
  9. 9.
    Carmeliet P, Ferreira V, Breier G et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380:435–440.PubMedCrossRefGoogle Scholar
  10. 10.
    Shalaby F, Rossant J, Yamaguchi TP et al. Failure of blood-island formation and vasculogenesis in Flk1-deficient mice. Nature 1995; 376:62–67.PubMedCrossRefGoogle Scholar
  11. 11.
    Drake CJ, LaRue A, Ferrara N, Little CD. VEGF regulates cell behavior during vasculogenesis. Dev Biol 2000; 224:178–188.PubMedCrossRefGoogle Scholar
  12. 12.
    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.PubMedGoogle Scholar
  13. 13.
    Cleaver O, Tonissen KF, Saha MS, Krieg PA. Neovascularization of the Xenopus embryo. Dev Dyn 1997; 210:66–77.PubMedCrossRefGoogle Scholar
  14. 14.
    Soker S, Takashima S, Miao HQ et al. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998; 92:735–745.PubMedCrossRefGoogle Scholar
  15. 15.
    Chen H, Chedotal A, He Z et al. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and SemaIV but not Sema III. Neuron 1997; 19:547–559.PubMedCrossRefGoogle Scholar
  16. 16.
    Kolodkin AL, Levengood DV, Rowe EG et al. Neuropilin is a semaphorin III receptor. Cell 1997; 90:753–762.PubMedCrossRefGoogle Scholar
  17. 17.
    Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J Biol Chem 2000; 275:18040–18045.PubMedCrossRefGoogle Scholar
  18. 18.
    Kawasaki T, Kitsukawa T, Bekku Y et al. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999; 126:4895–4902.PubMedGoogle Scholar
  19. 19.
    Chen H, Bagri A, Zupicich JA et al. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 2000; 25:43–56.PubMedCrossRefGoogle Scholar
  20. 20.
    Takashima S, Kitakaze M, Asakura M et al. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Nat Acad Sci U S A 2002; 99:3657–3662.CrossRefGoogle Scholar
  21. 21.
    Wong C, Jin ZG. Protein kinase Calpha-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by VEGF. J Biol Chem 2005; Epub ahead of print.Google Scholar
  22. 22.
    Leung DW, Cachianes G, Kuang WJ et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246:1306–1309.PubMedCrossRefGoogle Scholar
  23. 23.
    Guo D, Jia Q, Song HY et al. Vascular endothelial growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains. Association with endothelial cell proliferation. J Biol Chem 1995; 270:6729–6733.PubMedCrossRefGoogle Scholar
  24. 24.
    Yoshida A, Anand-Apte B, Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 1996; 13:57–64.PubMedCrossRefGoogle Scholar
  25. 25.
    Miquerol L, Gertsenstein M, Harpal K et al. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev Biol 1999; 212:307–322.PubMedCrossRefGoogle Scholar
  26. 26.
    Cleaver O, Krieg PA. VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 1998; 125:3905–3914.PubMedGoogle Scholar
  27. 27.
    Lindner V, Majack RA, Reidy MA. Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest 1990; 85:2004–2008.PubMedCrossRefGoogle Scholar
  28. 28.
    Seghezzi G, Patel S, Ren CJ et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Biol Chem 1998; 141:1659–1673.Google Scholar
  29. 29.
    Goto F, Goto K, Weindel K, Folkman J. Synergistic effects of vascular endothelial growth factor and basic fibroblast growth factor on the proliferation and cord formation of bovine capillary endothelial cells within collagen gels. Lab Invest 1993; 69:508–517.PubMedGoogle Scholar
  30. 30.
    Cai J, Jiang WG, Ahmed A, Boulton M. Vascular endothelial growth factor-induced endothelial cell proliferation is regulated by interaction between VEGFR-2, SH-PTP1 and eNOS. Microvasc Res 2005; 71:20–31.PubMedCrossRefGoogle Scholar
  31. 31.
    Zeng H, Dvorak HF, Mukhopadhyay D. Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) receptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylnositol 3-kinase-dependent pathways. J Biol Chem 2001; 276(29):26969–26979.PubMedCrossRefGoogle Scholar
  32. 32.
    Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376:66–71.PubMedCrossRefGoogle Scholar
  33. 33.
    Fong GH, Zhang L, Bryce DM, Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 1999; 126:3015–3025.PubMedGoogle Scholar
  34. 34.
    Lai L, Bohnsack BL, Niederreither K, Hirschi KK. Retinoic acid regulates endothelial cell proliferation during vasculogenesis. Development 2003; 130:6465–6474.PubMedCrossRefGoogle Scholar
  35. 35.
    Bohnsack BL, Lai L, Dolle P, Hirschi KK. Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev 2004; 18:1345–1358.PubMedCrossRefGoogle Scholar
  36. 36.
    Wasserman SM, Mehraban F, Komuves LG et al. Gene expression profile of human endothelial cells exposed to sustained fluid shear stress. Physiol Genomics 2002; 12:13–23.PubMedGoogle Scholar
  37. 37.
    Brooks AR, Lelkes PI, Rubanyi GM. Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol Genomics 2002; 9:27–41.PubMedGoogle Scholar
  38. 38.
    Chen BPC, Li Y-S, Zhao Y et al. DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol Genomics 2001; 7:55–63.PubMedCrossRefGoogle Scholar
  39. 39.
    McCormick SM, Eskin SG, McIntire LV et al. DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc Natl Acad Sci U S A 2001; 98:8955–8960.PubMedCrossRefGoogle Scholar
  40. 40.
    Garcia-Cardena G, Comander J, Anderson KR et al. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci U S A 2001; 98:4478–4485.PubMedCrossRefGoogle Scholar
  41. 41.
    Urbich C, Stein M, Reisinger K et al. Fluid shear stress-induced transcriptional activation of the vascular endothelial growth factor receptor-2 gene requires Sp1-dependent DNA binding. FEBS Lett 2003; 535:87–93.PubMedCrossRefGoogle Scholar
  42. 42.
    Chen KD, Li YS, Kim M et al. Mechanotransduction in response to shear stress. J Biol Chem 1999; 274:18393–18400.PubMedCrossRefGoogle Scholar
  43. 43.
    Jalali S, Li YS, Sotoudeh M et al. Shear stress activates p60-src-Ras-MAPK signaling pathways in vascular endothelial cells. Arterioscler Thromb Vasc Biol 1998; 18:227–234.PubMedGoogle Scholar
  44. 44.
    Lee HJ, Koh GY. Shear stress activates Tie2 receptor tyrosine kinase in human endothelial cells. Biochem Biophys Res Comm 2003; 304:399–404.PubMedCrossRefGoogle Scholar
  45. 45.
    Jin ZG, Ueba H, Tanimoto T et al. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res 2003; 93:354–363.PubMedCrossRefGoogle Scholar
  46. 46.
    Dimmeler S, Fleming I, Fisslthaler B et al. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999; 399:601–606.PubMedCrossRefGoogle Scholar
  47. 47.
    Dimmeler S, Assmus B, Hermann C et al. Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells. Circ Res 1998; 83:334–341.PubMedGoogle Scholar
  48. 48.
    Mattiussi S, Turrini P, Testolin L et al. p21Wafl/Cip1/Sdi1 mediates shear stress-dependent antiapoptotic function. Cardiovasc Res 2004; 61:693–704.PubMedCrossRefGoogle Scholar
  49. 49.
    Akimoto S, Mitsumata M, Sasaguri T, Yoshida Y. Laminar shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21Sdi1/Cip1/Waf1. Circ Res 2000; 86:185–190.PubMedGoogle Scholar
  50. 50.
    Silver L, Palis J. Initiation of murine embryonic erythropoiesis: a spatial analysis. Blood 1997; 89:1154–1164.PubMedGoogle Scholar
  51. 51.
    Palis J, Yoder MC. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 2001; 29:927–936.PubMedCrossRefGoogle Scholar
  52. 52.
    Dzierzak E, Medvinsky A, de Bruijn M. Qualitative and quantitative aspects of hematopoietic cell development in the mammalian embryo. Immunol Today 1998; 19:228–236.PubMedCrossRefGoogle Scholar
  53. 53.
    Godin I, Cumano A. The hare and the tortoise: an embryonic haematopoietic race. Nature Rev 2002; 2:593–604.Google Scholar
  54. 54.
    Garcia-Porrero JA, Godin IE, Dieterlen-Lievre F. Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat Embryol 1995; 192:425–435.PubMedCrossRefGoogle Scholar
  55. 55.
    Nishikawa S-I, Nishikawa S, Kawamoto H. In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 1998; 8:761–769.PubMedCrossRefGoogle Scholar
  56. 56.
    Hirai H, Ogawa M, Suzuki N et al. Hemogenic and nonhemogenic endothelium can be distinguished by the activity of fetal liver kinase (Flk)-1 promoter/enhancer during mouse embryogenesis. Blood 2003; 101:886–893.PubMedCrossRefGoogle Scholar
  57. 57.
    Choi K, Kennedy M, Kazarov A et al. A common precursor for hematopoietic and endothelial cells. Development 1998; 125:725–732.PubMedGoogle Scholar
  58. 58.
    Faloon P, Arentson E, Kazarov A et al. Basic fibroblast growth factor positively regulates hematopoietic development. Development 2000; 127:1931–1941.PubMedGoogle Scholar
  59. 59.
    Chung YS, Zhang WJ, Arentson E et al. Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development 2002; 129:5511–5520.PubMedCrossRefGoogle Scholar
  60. 60.
    Yamaguchi TP, Dumont DJ, Conlon RA et al. Flk-1, a Fit-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 1993; 118:489–498.PubMedGoogle Scholar
  61. 61.
    Millauer B, Wizigmann-Voos S, Schnurch H et al. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 1993; 72:835–846.PubMedCrossRefGoogle Scholar
  62. 62.
    Kabrun N, Buhring HJ, Choi K et al. Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 1997; 124:2039–2048.PubMedGoogle Scholar
  63. 63.
    Kallianpur AR, Jordan JE, Brandt SJ. The SCL/Tal-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 1994; 83:1200–1208.PubMedGoogle Scholar
  64. 64.
    Breier G, Breviario F, Caveda L et al. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of the cardiovascular system. Blood 1996; 87:630–641.PubMedGoogle Scholar
  65. 65.
    Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood 1992; 80:575–581.PubMedGoogle Scholar
  66. 66.
    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.PubMedCrossRefGoogle Scholar
  67. 67.
    Nadin BM, Goodell MA, Hirschi KK. Phenotype and hematopoietic potential of side population cells throughout embryonic development. Blood 2003; 102(7):2436–2443.PubMedCrossRefGoogle Scholar
  68. 68.
    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.PubMedCrossRefGoogle Scholar
  69. 69.
    Dumont DJ, Fong GH, Puri MC et al. Vascularization of the mouse embryo: a study of Flk-1, Tek, Tie and vascular endothelial growth factor expression during development. Tek, Tie and vascular endothelial growth factor expression during development. Dev Dyn 1995; 203:80–92.PubMedGoogle Scholar
  70. 70.
    Shalaby F, Ho J, Stanford WL et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997; 89:981–990.PubMedCrossRefGoogle Scholar
  71. 71.
    Martin R, Lahlil R, Damert A et al. SCL interacts with VEGF to suppress apoptosis at the onset of hematopoiesis. Development 2003; 131:693–702.CrossRefGoogle Scholar
  72. 72.
    Schuh AC, Faloon P, Hu Q-L et al. In vitro hematopoietic and endothelial potential of flk-1-/-embryonic stem cells and embryos. Proc Natl Acad Sci U S A 1999; 96:2159–2164.PubMedCrossRefGoogle Scholar
  73. 73.
    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.PubMedGoogle Scholar
  74. 74.
    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.PubMedGoogle Scholar
  75. 75.
    Visvader JE, Fujiwara Y, Orkin SH. Unsuspected role for the T-cell leukemia protein SCL/Tal-1 in vascular development. Genes Dev 1998; 12 (473–479).PubMedCrossRefGoogle Scholar
  76. 76.
    Shivdasani RA, Mayer EL, Orkin SH. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein Tal-1/SCL. Nature 1995; 373:432–434.PubMedCrossRefGoogle Scholar
  77. 77.
    Robb L, Begley CG. The helix-loop-helix gene SCL: implicated in T-cell acute lymphoblastic leukaemia and in normal haematopoietic development. Int J Biochem Cell Biol 1996; 28:609–618.PubMedCrossRefGoogle Scholar
  78. 78.
    Ema M, Faloon P, Zhang WJ et al. Combinatorial effects of Flk1 and Tall on vascular and hematopoietic development in the mouse. Genes Dev 2003; 17:380–393.PubMedCrossRefGoogle Scholar
  79. 79.
    Fujiwara Y, Browne CP, Cunniff K et al. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A 1996; 93:12355–12358.PubMedCrossRefGoogle Scholar
  80. 80.
    Tsai FY, Keller G, Kuo FC et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994; 371:221–226.PubMedCrossRefGoogle Scholar
  81. 81.
    Yamada Y, Pannell R, Forster A, Rabbitts TH. The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice. Proc Natl Acad Sci U S A 2000; 97(1):320–324.PubMedCrossRefGoogle Scholar
  82. 82.
    Warren AJ, Colledge WH, Carlton MB et al. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell 1994; 78:45–57.PubMedCrossRefGoogle Scholar
  83. 83.
    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.PubMedCrossRefGoogle Scholar
  84. 84.
    North TE, de Bruijn MF, Stacy T et al. Runxl expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002; 16(5):661–672.PubMedCrossRefGoogle Scholar
  85. 85.
    North T, Gu TL, Stacy T et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 1999; 126:2563–2575.PubMedGoogle Scholar
  86. 86.
    Lacaud G, Gore L, Kennedy M et al. Runxl is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood 2002; 100:458–466.PubMedCrossRefGoogle Scholar
  87. 87.
    Ema M, Rossant J. Cell fate decisions in early blood vessel formation. Trends Cardiovasc Med 2003; 13(6):254–259.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  • Lauren C. Goldie
    • 1
  • Melissa K. Nix
    • 2
  • Karen K. Hirschi
    • 2
    • 3
  1. 1.Department of Pediatrics, Children’ Nutrition Research Center and Center for Cell and Gene TherapyBaylor College of MedicineHoustonUSA
  2. 2.Department of Molecular and Cellular Biology Center for Cell and Gene TherapyBaylor College of MedicineHoustonUSA
  3. 3.Department of PediatricsChildren’s Nutrition Research CenterHoustonUSA

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