Skip to main content
Springer Nature Link
Log in

Development of the Endothelium

  • Chapter
The Vascular Endothelium I

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 176/I))

  • 1730 Accesses

  • 10 Citations

Abstract

Our understanding of the regulation of vascular development has exploded over the past decade. Prior to this time, our knowledge of vascular development was primarily based on classic descriptive studies. The identification of stem cells, lineage markers, specific growth factors and their receptors, and signalling pathways has facilitated a rapid expansion in information regarding details of the mechanisms that govern development of the vascular system.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Allende ML, Yamashita T, Proia RL (2003) G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102:3665–3667

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Silva M, Belo-Diabangouaya P, Salaun J, Dieterlen-Lievre F (2003) Mouse placenta is a major hematopoietic organ. Development 130:5437–5444

    Article  PubMed  CAS  Google Scholar 

  • Antonelli-Orlidge A, Smith SR, D’Amore PA (1989) Influence of pericytes on capillary endothelial cell growth. Am Rev Respir Dis 140:1129–1131

    PubMed  CAS  Google Scholar 

  • Argraves KM, Wilkerson BA, Argraves WS, Fleming PA, Obeid LM, Drake CJ (2004) Sphingosine-1-phosphate signaling promotes critical migratory events in vasculogenesis. J Biol Chem 279:50580–50590

    Article  PubMed  CAS  Google Scholar 

  • Barandon L, Couffinhal T, Ezan J, Dufourcq P, Costet P, Alzieu P, Leroux L, Moreau C, Dare D, Duplaa C (2003) Reduction of infarct size and prevention of cardiac rupture in transgenic mice overexpressing FrzA. Circulation 108:2282–2289

    Article  PubMed  CAS  Google Scholar 

  • Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84:869–901

    Article  PubMed  CAS  Google Scholar 

  • Beck L Jr, D’Amore PA (1997) Vascular development: cellular and molecular regulation. FASEB J 11:365–373

    PubMed  CAS  Google Scholar 

  • Bohnsack BL, Lai L, Dolle P, Hirschi KK (2004) Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev 18:1345–1358

    Article  PubMed  CAS  Google Scholar 

  • Byrd N, Becker S, Maye P, Narasimhaiah R, St-Jacques B, Zhang X, McMahon J, McMahon A, Grabel L (2002) Hedgehog is required for murine yolk sac angiogenesis. Development 129:361–372

    PubMed  CAS  Google Scholar 

  • Chen CZ, Li M, de Graaf D, Monti S, Gottgens B, Sanchez MJ, Lander ES, Golub TR, Green AR, Lodish HF (2002) Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci U S A 99:15468–15473

    Article  PubMed  CAS  Google Scholar 

  • Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K (2002) Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development 129:5511–5520

    Article  PubMed  CAS  Google Scholar 

  • Cortes F, Debacker C, Peault B, Labastie MC (1999) Differential expression of KDR/VEGFR-2 and CD34 during mesoderm development of the early human embryo. Mech Dev 83:161–164

    Article  PubMed  CAS  Google Scholar 

  • Daly C, Wong V, Burova E, Wei Y, Zabski S, Griffiths J, Lai KM, Lin HC, Ioffe E, Yancopoulos GD, Rudge JS (2004) Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev 18:1060–1071

    Article  PubMed  CAS  Google Scholar 

  • Damert A, Miquerol L, Gertsenstein M, Risau W, Nagy A (2002) Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 129:1881–1892

    PubMed  CAS  Google Scholar 

  • Darland DC, D’Amore PA (2001a) Cell-cell interactions in vascular development. Curr Top Dev Biol 52:107–149

    PubMed  CAS  Google Scholar 

  • Darland DC, D’Amore PA (2001b) TGF beta is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/2 and endothelial cells. Angiogenesis 4:11–20

    Article  PubMed  CAS  Google Scholar 

  • Darland DC, Massingham LJ, Smith SR, Piek E, Saint-Geniez M, D’Amore PA (2003) Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264:275–288

    Article  PubMed  CAS  Google Scholar 

  • Ding R, Darland DC, Parmacek MS, D’Amore PA (2004) Endothelial-mesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/pericyte differentiation. Stem Cells Dev 13:509–520

    PubMed  CAS  Google Scholar 

  • Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, Klonjkowski B, Berrou E, Mericskay M, Li Z, Tournier-Lasserve E, Gridley T, Joutel A (2004) Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 18:2730–2735

    Article  PubMed  CAS  Google Scholar 

  • Drake CJ, Fleming PA (2000) Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95:1671–1679

    PubMed  CAS  Google Scholar 

  • Duan LJ, Nagy A, Fong GH (2003) Gastrulation and angiogenesis, not endothelial specification, is sensitive to partial deficiency in vascular endothelial growth factor-A in Mice. Biol Reprod 69:1852–1858

    Article  PubMed  CAS  Google Scholar 

  • Duarte A, Hirashima M, Benedito R, Trindade A, Diniz P, Bekman E, Costa L, Henrique D, Rossant J (2004) Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 18:2474–2478

    Article  PubMed  CAS  Google Scholar 

  • Dyer MA, Farrington SM, Mohn D, Munday JR, Baron MH (2001) Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 128:1717–1730

    PubMed  CAS  Google Scholar 

  • Elvert G, Kappel A, Heidenreich R, Englmeier U, Lanz S, Acker T, Rauter M, Plate K, Sieweke M, Breier G, Flamme I (2003) Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J Biol Chem 278:7520–7530

    Article  PubMed  CAS  Google Scholar 

  • 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 17:380–393

    Article  PubMed  CAS  Google Scholar 

  • Ezan J, Leroux L, Barandon L, Dufourcq P, Jaspard B, Moreau C, Allieres C, Daret D, Couffinhal T, Duplaa C (2004) FrzA/sFRP-1, a secreted antagonist of the Wnt-Frizzled pathway, controls vascular cell proliferation in vitro and in vivo. Cardiovasc Res 63:731–738

    Article  PubMed  CAS  Google Scholar 

  • Faloon P, Arentson E, Kazarov A, Deng CX, Porcher C, Orkin S, Choi K (2000) Basic fibroblast growth factor positively regulates hematopoietic development. Development 127:1931–1941

    PubMed  CAS  Google Scholar 

  • Feraud O, Prandini MH, Vittet D (2003) Vasculogenesis and angiogenesis from in vitro differentiation of mouse embryonic stem cells. Methods Enzymol 365:214–228

    PubMed  CAS  Google Scholar 

  • Ferkowicz MJ, Starr M, Xie X, Li W, Johnson SA, Shelley WC, Morrison PR, Yoder MC (2003) CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130:4393–4403

    Article  PubMed  CAS  Google Scholar 

  • Fiedler U, Scharpfenecker M, Koidl S, Hegen A, Grunow V, Schmidt JM, Kriz W, Thurston G, Augustin HG (2004) The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 103:4150–4156

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein EB, Poole TJ (2003) Vascular endothelial growth factor: a regulator of vascular morphogenesis in the Japanese quail embryo. Anat Rec 272A:403–414

    Article  CAS  Google Scholar 

  • Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M (2004) The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev 18:901–911

    Article  PubMed  CAS  Google Scholar 

  • Fraser ST, Ogawa M, Yokomizo T, Ito Y, Nishikawa S, Nishikawa S (2003) Putative intermediate precursor between hematogenic endothelial cells and blood cells in the developing embryo. Dev Growth Differ 45:63–75

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto T, Ogawa M, Minegishi N, Yoshida H, Yokomizo T, Yamamoto M, Nishikawa S (2001) Step-wise divergence of primitive and definitive haematopoietic and endothelial cell lineages during embryonic stem cell differentiation. Genes Cells 6:1113–1127

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara Y, Chang AN, Williams AM, Orkin SH (2004) Functional overlap of GATA-1 and GATA-2 in primitive hematopoietic development. Blood 103:583–585

    Article  PubMed  CAS  Google Scholar 

  • Fuller T, Korff T, Kilian A, Dandekar G, Augustin HG (2003) Forward EphB4 signaling in endothelial cells controls cellular repulsion and segregation from ephrinB2 positive cells. J Cell Sci 116:2461–2470

    Article  PubMed  CAS  Google Scholar 

  • Gale NW, Thurston G, Hackett SF, Renard R, Wang Q, McClain J, Martin C, Witte C, Witte MH, Jackson D, Suri C, Campochiaro PA, Wiegand SJ, Yancopoulos GD (2002) Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by angiopoietin-1. Dev Cell 3:411–423

    Article  PubMed  CAS  Google Scholar 

  • Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD (2004) Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci U S A 101:15949–15954

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt H, Ruhrberg C, Abramsson A, Fujisawa H, Shima D, Betsholtz C (2004) Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn 231:503–509

    Article  PubMed  CAS  Google Scholar 

  • Gitler AD, Lu MM, Epstein JA (2004) PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 7:107–116

    Article  PubMed  CAS  Google Scholar 

  • Godin I, Cumano A (2002) The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2:593–604

    PubMed  CAS  Google Scholar 

  • Goodwin AM, D’Amore PA (2002) Wnt signaling in the vasculature. Angiogenesis 5:1–9

    Article  PubMed  CAS  Google Scholar 

  • Gottgens B, Nastos A, Kinston S, Piltz S, Delabesse EC, Stanley M, Sanchez MJ, Ciau-Uitz A, Patient R, Green AR (2002) Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J 21:3039–3050

    Article  PubMed  CAS  Google Scholar 

  • Graef IA, Chen F, Chen L, Kuo A, Crabtree GR (2001) Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105:863–875

    Article  PubMed  CAS  Google Scholar 

  • Gridley T (2003) Notch signaling and inherited disease syndromes. Hum Mol Genet 12 Spec No 1:R9–R13

    Article  PubMed  CAS  Google Scholar 

  • Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5:45–57

    Article  PubMed  CAS  Google Scholar 

  • Gu C, Yoshida Y, Livet J, Reimert DV, Mann F, Merte J, Henderson CE, Jessell TM, Kolodkin AL, Ginty DD (2005) Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307:265–268

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Chan R, Ramsey H, Li W, Xie X, Shelley WC, Martinez-Barbera JP, Bort B, Zaret K, Yoder M, Hromas R (2003) The homeoprotein Hex is required for hemangioblast differentiation. Blood 102:2428–2435

    Article  PubMed  CAS  Google Scholar 

  • Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, Luo Z, Mei L, Chien KR, Sussman DJ, Wynshaw-Boris A (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129:5827–5838

    Article  PubMed  CAS  Google Scholar 

  • Hammes HP, Lin J, Renner O, Shani M, Lundqvist A, Betsholtz C, Brownlee M, Deutsch U (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107–3112

    PubMed  CAS  Google Scholar 

  • Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553

    Article  PubMed  CAS  Google Scholar 

  • Hiratsuka S, Kataoka Y, Nakao K, Nakamura K, Morikawa S, Tanaka S, Katsuki M, Maru Y, Shibuya M (2005) Vascular endothelial growth factor A (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol Cell Biol 25:355–363

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KK, Rohovsky SA, D’Amore PA (1998) PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141:805–814

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KK, Rohovsky SA, Beck LH, Smith SR, D’Amore PA (1999) Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ Res 84:298–305

    PubMed  CAS  Google Scholar 

  • Hirschi KK, Burt JM, Hirschi KD, Dai C (2003) Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation. Circ Res 93:429–437

    Article  PubMed  CAS  Google Scholar 

  • Hobson JP, Rosenfeldt HM, Barak LS, Olivera A, Poulton S, Caron MG, Milstien S, Spiegel S (2001) Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 291:1800–1803

    Article  PubMed  CAS  Google Scholar 

  • Hoch RV, Soriano P (2003) Roles of PDGF in animal development. Development 130:4769–4784

    Article  PubMed  CAS  Google Scholar 

  • Hogan KA, Ambler CA, Chapman DL, Bautch VL (2004) The neural tube patterns vessels developmentally using the VEGF signaling pathway. Development 131:1503–1513

    Article  PubMed  CAS  Google Scholar 

  • Hosaka T, Biggs WH 3rd, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC (2004) Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci U S A 101:2975–2980

    Article  PubMed  CAS  Google Scholar 

  • Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432:625–630

    Article  PubMed  CAS  Google Scholar 

  • Huelsken J, Behrens J (2002) The Wnt signalling pathway. J Cell Sci 115:3977–3978

    Article  PubMed  CAS  Google Scholar 

  • Hughes S, Chan-Ling T (2004) Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest Ophthalmol Vis Sci 45:2795–2806

    Article  PubMed  Google Scholar 

  • Iozzo RV, San Antonio JD (2001) Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J Clin Invest 108:349–355

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa T, Tamai Y, Zorn AM, Yoshida H, Seldin MF, Nishikawa S, Taketo MM (2001) Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128:25–33

    PubMed  CAS  Google Scholar 

  • Iso T, Hamamori Y, Kedes L (2003) Notch signaling in vascular development. Arterioscler Thromb Vasc Biol 23:543–553

    Article  PubMed  CAS  Google Scholar 

  • Jones N, Voskas D, Master Z, Sarao R, Jones J, Dumont DJ (2001) Rescue of the early vascular defects in Tek/Tie2 null mice reveals an essential survival function. EMBO Rep 2:438–445

    PubMed  CAS  Google Scholar 

  • Jonker L, Arthur HM (2002) Endoglin expression in early development is associated with vasculogenesis and angiogenesis. Mech Dev 110:193–196

    Article  PubMed  CAS  Google Scholar 

  • Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP, Gallahan D, Closson V, Kitajewski J, Callahan R, Smith GH, Stark KL, Gridley T (2000) Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14:1343–1352

    PubMed  CAS  Google Scholar 

  • Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL, Gridley T (2004) Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 18:2469–2473

    Article  PubMed  CAS  Google Scholar 

  • Lawson ND, Weinstein BM (2002) Arteries and veins: making a difference with Zebrafish. Nat Rev Genet 3:674–682

    Article  PubMed  CAS  Google Scholar 

  • Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P (2004) Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 23:4018–4028

    Article  PubMed  CAS  Google Scholar 

  • Leong KG, Hu X, Li L, Noseda M, Larrivee B, Hull C, Hood L, Wong F, Karsan A (2002) Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation. Mol Cell Biol 22:2830–2841

    Article  PubMed  CAS  Google Scholar 

  • Li L, Miano JM, Cserjesi P, Olson EN (1996) SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res 78:188–195

    PubMed  CAS  Google Scholar 

  • Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C (2003) Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17:1835–1840

    Article  PubMed  CAS  Google Scholar 

  • Ling KW, Ottersbach K, van Hamburg JP, Oziemlak A, Tsai FY, Orkin SH, Ploemacher R, Hendriks RW, Dzierzak E (2004) GATA-2 plays two functionally distinct roles during the ontogeny of hematopoietic stem cells. J Exp Med 200:871–882

    Article  PubMed  CAS  Google Scholar 

  • Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, Dotto GP, Fairman RM, Velazquez OC, Herlyn M (2003) Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol 23:14–25

    Article  PubMed  CAS  Google Scholar 

  • Lobov IB, Brooks PC, Lang RA (2002) Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci U S A 99:11205–11210

    Article  PubMed  CAS  Google Scholar 

  • Lockman K, Hinson JS, Medlin MD, Morris D, Taylor JM, Mack CP (2004) Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J Biol Chem 279:42422–42430

    Article  PubMed  CAS  Google Scholar 

  • Loureiro RM, Maharaj AS, Dankort D, Muller WJ, D’Amore PA (2005) ErbB2 overexpression in mammary cells upregulates VEGF through the core promoter. Biochem Biophys Res Commun 326:455–465

    Article  PubMed  CAS  Google Scholar 

  • Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Breant C, Claes F, De Smet F, Thomas JL, Autiero M, Carmeliet P, Tessier-Lavigne M, Eichmann A (2004) The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432:179–186

    Article  PubMed  CAS  Google Scholar 

  • Manabe I, Owens GK (2001) CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J Clin Invest 107:823–834

    Article  PubMed  CAS  Google Scholar 

  • Mann KM, Ray JL, Moon ES, Sass KM, Benson MR (2004) Calcineurin initiates smooth muscle differentiation in neural crest stem cells. J Cell Biol 165:483–491

    Article  PubMed  CAS  Google Scholar 

  • Martin R, Lahlil R, Damert A, Miquerol L, Nagy A, Keller G, Hoang T (2004) SCL interacts with VEGF to suppress apoptosis at the onset of hematopoiesis. Development 131:693–702

    Article  PubMed  CAS  Google Scholar 

  • McGrath KE, Koniski AD, Malik J, Palis J (2003) Circulation is established in a stepwise pattern in the mammalian embryo. Blood 101:1669–1675

    Article  PubMed  CAS  Google Scholar 

  • Mehlen P, Mazelin L (2003) The dependence receptors DCC and UNC5H as a link between neuronal guidance and survival. Biol Cell 95:425–436

    Article  PubMed  CAS  Google Scholar 

  • Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773–2783

    PubMed  CAS  Google Scholar 

  • Morris PN, Dunmore BJ, Tadros A, Marchuk DA, Darland DC, D’Amore PA, Brindle NP (2005) Functional analysis of a mutant form of the receptor tyrosine kinase Tie2 causing venous malformations. J Mol Med 83:58–63

    Article  PubMed  CAS  Google Scholar 

  • Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, Bode C, Bautch VL, Conlon FL, Patterson C (2003) BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol 23:5664–5679

    Article  PubMed  CAS  Google Scholar 

  • Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ (2002) Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109:693–705

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa T, Li JH, Garcia G, Mu W, Piek E, Bottinger EP, Chen Y, Zhu HJ, Kang DH, Schreiner GF, Lan HY, Johnson RJ (2004) TGF-beta induces proangiogenic and antiangiogenic factors via parallel but distinct Smad pathways. Kidney Int 66:605–613

    Article  PubMed  CAS  Google Scholar 

  • Ng YS, Rohan R, Sunday ME, Demello DE, D’Amore PA (2001) Differential expression of VEGF isoforms in mouse during development and in the adult. Dev Dyn 220:112–121

    Article  PubMed  CAS  Google Scholar 

  • Ng YS, Ramsauer M, Loureiro RM, D’Amore PA (2004) Identification of genes involved in VEGF-mediated vascular morphogenesis using embryonic stem cell-derived cystic embryoid bodies. Lab Invest 84:1209–1218

    Article  PubMed  CAS  Google Scholar 

  • Nishishita T, Lin PC (2004) Angiopoietin 1, PDGF-B, and TGF-beta gene regulation in endothelial cell and smooth muscle cell interaction. J Cell Biochem 91:584–593

    Article  PubMed  CAS  Google Scholar 

  • Noseda M, Chang L, McLean G, Grim JE, Clurman BE, Smith LL, Karsan A (2004) Notch activation induces endothelial cell cycle arrest and participates in contact inhibition: role of p21Cip1 repression. Mol Cell Biol 24:8813–8822

    Article  PubMed  CAS  Google Scholar 

  • Oberlin E, Tavian M, Blazsek I, Peault B (2002) Blood-forming potential of vascular endothelium in the human embryo. Development 129:4147–4157

    PubMed  CAS  Google Scholar 

  • Orlidge A, D’Amore PA (1987) Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455–1462

    Article  PubMed  CAS  Google Scholar 

  • Oshima M, Oshima H, Taketo MM (1996) TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 179:297–302

    Article  PubMed  CAS  Google Scholar 

  • Papetti M, Shujath J, Riley KN, Herman IM (2003) FGF-2 antagonizes the TGF-beta1-mediated induction of pericyte alpha-smooth muscle actin expression: a role for myf-5 and Smad-mediated signaling pathways. Invest Ophthalmol Vis Sci 44:4994–5005

    Article  PubMed  Google Scholar 

  • Park C, Afrikanova I, Chung YS, Zhang WJ, Arentson E, Fong Gh, Rosendahl A, Choi K (2004) A hierarchical order of factors in the generation of FLK1-and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131:2749–2762

    Article  PubMed  CAS  Google Scholar 

  • Perlegas D, Xie H, Sinha S, Somlyo AV, Owens GK (2005) ANG II type 2 receptor regulates smooth muscle growth and force generation in late fetal mouse development. Am J Physiol Heart Circ Physiol 288:H96–H102

    Article  PubMed  CAS  Google Scholar 

  • Pola R, Ling LE, Aprahamian TR, Barban E, Bosch-Marce M, Curry C, Corbley M, Kearney M, Isner JM, Losordo DW (2003) Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation 108:479–485

    Article  PubMed  Google Scholar 

  • Puri MC, Bernstein A (2003) Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis. Proc Natl Acad Sci U S A 100:12753–12758

    Article  PubMed  CAS  Google Scholar 

  • Ramirez-Bergeron DL, Runge A, Dahl KDC, Fehling HJ, Keller G, Simon MC(2004) Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131:4623–4634

    Article  PubMed  CAS  Google Scholar 

  • Reese DE, Hall CE, Mikawa T (2004) Negative regulation of midline vascular development by the notochord. Dev Cell 6:699–708

    Article  PubMed  CAS  Google Scholar 

  • Rensen SS, Thijssen VL, De Vries CJ, Doevendans PA, Detera-Wadleigh SD, Van Eys GJ (2002) Expression of the smoothelin gene is mediated by alternative promoters. Cardiovasc Res 55:850–863

    Article  PubMed  CAS  Google Scholar 

  • Roberts DM, Kearney JB, Johnson JH, Rosenberg MP, Kumar R, Bautch VL (2004) The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol 164:1531–1535

    PubMed  CAS  Google Scholar 

  • Saint-Geniez M, Argence CB, Knibiehler B, Audigier Y (2003) The msr/apj gene encoding the apelin receptor is an early and specific marker of the venous phenotype in the retinal vasculature. Gene Expr Patterns 3:467–472

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Rifkin DB (1989) Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 109:309–315

    Article  PubMed  CAS  Google Scholar 

  • Seki T, Yun J, Oh SP (2003) Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ Res 93:682–689

    Article  PubMed  CAS  Google Scholar 

  • Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, Tessier-Lavigne M, Taniguchi M, Puschel AW, Bussolino F (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391–397

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T, Stavrakis G, Isner J, Folkman J, Gimbrone MA Jr, Anderson DJ (2001) Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev Biol 230:139–150

    Article  PubMed  CAS  Google Scholar 

  • Sorensen LK, Brooke BS, Li DY, Urness LD (2003) Loss of distinct arterial and venous boundaries in mice lacking endoglin, a vascular-specific TGFbeta coreceptor. Dev Biol 261:235–250

    Article  PubMed  CAS  Google Scholar 

  • Stalmans I, Ng YS, Rohan R, Fruttiger M, Bouche A, Yuce A, Fujisawa H, Hermans B, Shani M, Jansen S, Hicklin D, Anderson DJ, Gardiner T, Hammes HP, Moons L, Dewerchin M, Collen D, Carmeliet P, D’Amore PA (2002) Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest 109:327–336

    Article  PubMed  CAS  Google Scholar 

  • Takashima S, Kitakaze M, Asakura M, Asanuma H, Sanada S, Tashiro F, Niwa H, Miyazaki Ji J, Hirota S, Kitamura Y, Kitsukawa T, Fujisawa H, Klagsbrun M, Hori M (2002) Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci U S A 99:3657–3662

    Article  PubMed  CAS  Google Scholar 

  • 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 87:67–72

    PubMed  CAS  Google Scholar 

  • Thurston G (2003) Role of Angiopoietins and Tie receptor tyrosine kinases in angiogenesis and lymphangiogenesis. Cell Tissue Res 314:61–68

    Article  PubMed  CAS  Google Scholar 

  • Tremblay KD, Dunn NR, Robertson EJ (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128:3609–3621

    PubMed  CAS  Google Scholar 

  • Uemura A, Ogawa M, Hirashima M, Fujiwara T, Koyama S, Takagi H, Honda Y, Wiegand SJ, Yancopoulos GD, Nishikawa S (2002) Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest 110:1619–1628

    Article  PubMed  CAS  Google Scholar 

  • Usui S, Sugimoto N, Takuwa N, Sakagami S, Takata S, Kaneko S, Takuwa Y (2004) Blood lipid mediator sphingosine 1-phosphate potently stimulates platelet-derived growth factor-A and-B chain expression through S1P1-Gi-Ras-MAPK-dependent induction of Kruppel-like factor 5. J Biol Chem 279:12300–12311

    Article  PubMed  CAS  Google Scholar 

  • Uyttendaele H, Ho J, Rossant J, Kitajewski J (2001) Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc Natl Acad Sci U S A 98:5643–5648

    Article  PubMed  CAS  Google Scholar 

  • Villa N, Walker L, Lindsell CE, Gasson J, Iruela-Arispe ML, Weinmaster G (2001) Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech Dev 108:161–164

    Article  PubMed  CAS  Google Scholar 

  • Wang DZ, Olson EN (2004) Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev 14:558–566

    Article  PubMed  CAS  Google Scholar 

  • Wang HU, Chen ZF, Anderson DJ (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93:741–753

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Li L, Shojaei F, Levac K, Cerdan C, Menendez P, Martin T, Rouleau A, Bhatia M (2004a) Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21:31–41

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Cohen K, Shao Y, Mole P, Dombkowski D, Scadden DT (2004b) Ephrin receptor, EphB4, regulates ES cell differentiation of primitive mammalian hemangioblasts, blood, cardiomyocytes, and blood vessels. Blood 103:100–109

    Article  PubMed  CAS  Google Scholar 

  • Waters CM, Connell MC, Pyne S, Pyne NJ (2005) c-Src is involved in regulating signal transmission from PDGFbeta receptor-GPCR(s) complexes in mammalian cells. Cell Signal 17:263–277

    Article  PubMed  CAS  Google Scholar 

  • Wechezak AR, Coan DE (2003) Subcellular distribution of Wnt-1 at adherens junctions and actin-rich densities in endothelial cells. Exp Cell Res 288:335–343

    Article  PubMed  CAS  Google Scholar 

  • Wechezak AR, Coan DE (2005) Dvl2 silencing in postdevelopmental cells results in aberrant cell membrane activity and actin disorganization. J Cell Physiol 202:867–873

    Article  PubMed  CAS  Google Scholar 

  • Whitehead KJ, Plummer NW, Adams JA, Marchuk DA, Li DY (2004) Ccm1 is required for arterial morphogenesis: implications for the etiology of human cavernous malformations. Development 131:1437–1448

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yao YG, Duh EJ (2004) VEGF selectively induces Down syndrome critical region 1 gene expression in endothelial cells: a mechanism for feedback regulation of angiogenesis? Biochem Biophys Res Commun 321:648–656

    Article  PubMed  CAS  Google Scholar 

  • Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K, Eichmann A (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129:4797–4806

    PubMed  CAS  Google Scholar 

  • Zachary I (2003) VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem Soc Trans 31:1171–1177

    Article  PubMed  CAS  Google Scholar 

  • Zhang XQ, Takakura N, Oike Y, Inada T, Gale NW, Yancopoulos GD, Suda T (2001) Stromal cells expressing ephrin-B2 promote the growth and sprouting of ephrin-B2(+) endothelial cells. Blood 98:1028–1037

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Facultad de Ciencias Biomédicas, Universidad Austral, B1629AHJ, Buenos Aires, Argentina

    A. M. Suburo

  2. Schepens Eye Research Institute and Harvard Medical School, Boston, MA, 02114, USA

    P. A. D’Amore

Authors
  1. A. M. Suburo
    View author publications

    Search author on:PubMed Google Scholar

  2. P. A. D’Amore
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to P. A. D’Amore .

Editor information

Editors and Affiliations

  1. The Wolfson Institute for Biomedical Research, University College London, Gower Street, London, WC1E 6BT, UK

    Salvador Moncada FRCP FRS  & Annie Higgs  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Suburo, A.M., D’Amore, P.A. (2006). Development of the Endothelium. In: Moncada, S., Higgs, A. (eds) The Vascular Endothelium I. Handbook of Experimental Pharmacology, vol 176/I. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-32967-6_3

Download citation

Publish with us

Policies and ethics