Abstract
Arteries, capillaries, and veins form the vascular system that supplies oxygen and nutrients to all tissues and removes waste products. In the embryo the vascular system is the first system to emerge during vasculogenesis, and the factors that initiate the patterning of the endothelial network are, for the most part, involved in the adult angiogenesis. Dysfunctions of the vascular system cause numerous pathologies, including artherosclerosis, cancer, and ocular diseases. Understanding how endothelial cells differentiate and deciphering the cellular, molecular, and physical clues that drive blood vessel formation in the embryo may therefore provide means to develop therapies against vascular diseases in the adult. In this review, we present recent findings that identify new candidates controlling vascular system development.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adam MG, Berger C, Feldner A, Yang WJ, Wüstehube-Lausch J, Herberich SE, Pinder M, Gesierich S, Hammes HP, Augustin HG, Fischer A (2013) Synaptojanin-2 binding protein stabilizes the Notch ligands DLL1 and DLL4 and inhibits sprouting angiogenesis. Circ Res 113(11):1206–1218
Adamo L, Naveiras O, Wenzel PL, McKinney-Freeman S, Mack PJ, Gracia-Sancho J, Suchy-Dicey A, Yoshimoto M, Lensch MW, Yoder MC, García-Cardeña G, Daley GQ (2009) Biomechanical forces promote embryonic haematopoiesis. Nature 459(7250):1131–1135
Adams RH, Eichmann A (2010) Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2(5):a001875
Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, Klein R (1999) Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 13(3):295–306
Alitalo A, Detmar M (2012) Interaction of tumor cells and lymphatic vessels in cancer progression. Oncogene 31(42):4499–4508
Bates D, Taylor GI, Newgreen DF (2002) The pattern of neurovascular development in the forelimb of the quail embryo. Dev Biol 249(2):300–320
Bates D, Taylor GI, Minichiello J, Farlie P, Cichowitz A, Watson N, Klagsbrun M, Mamluk R, Newgreen DF (2003) Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev Biol 255(1):77–98
Bentley MT, Poole TJ (2009) Neurovascular anatomy of the embryonic quail hindlimb. Anat Rec 292(10):1559–1568
Buschmann I, Pries A, Styp-Rekowska B, Hillmeister P, Loufrani L, Henrion D, Shi Y, Duelsner A, Hoefer I, Gatzke N, Wang H, Lehmann K, Ulm L, Ritter Z, Hauff P, Hlushchuk R, Djonov V, van Veen T, le Noble F (2010) Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development 137(13):2187–2196
Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380(6573):435–439
Chapman WB (1918) The effect of the heart-beat upon the development of the vascular system in the chick. Am J Anat 23:175–203
Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457:887–891
Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125(4):725–732
Chung AS, Ferrara N (2011) Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 27:563–584
Corada M, Nyqvist D, Orsenigo F, Caprini A, Giampietro C, Taketo MM, Iruela-Arispe ML, Adams RH, Dejana E (2010) The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev Cell 18(6):938–949
Coultas L, Chawengsaksophak K, Rossant J (2005) Endothelial cells and VEGF in vascular development. Nature 438(7070):937–945
Cristofaro B, Shi Y, Faria M, Suchting S, Leroyer AS, Trindade A, Duarte A, Zovein AC, Iruela-Arispe ML, Nih LR, Kubis N, Henrion D, Loufrani L, Todiras M, Schleifenbaum J, Gollasch M, Zhuang ZW, Simons M, Eichmann A, le Noble F (2013) Dll4-Notch signaling determines the formation of native arterial collateral networks and arterial function in mouse ischemia models. Development 140(8):1720–1729
Cui C, Filla MB, Jones EA, Lansford R, Cheuvront T, Al-Roubaie S, Rongish BJ, Little CD (2013) Embryogenesis of the first circulating endothelial cells. PLoS One 8(5):e60841
Davis GE, Kim DJ, Meng CX, Norden PR, Speichinger KR, Davis MT, Smith AO, Bowers SL, Stratman AN (2013) Control of vascular tube morphogenesis and maturation in 3D extracellular matrices by endothelial cells and pericytes. Methods Mol Biol 1066:17–28
De Spiegelaere W, Casteleyn C, Van den Broeck W, Plendl J, Bahramsoltani M, Simoens P, Djonov V, Cornillie P (2012) Intussusceptive angiogenesis: a biologically relevant form of angiogenesis. J Vasc Res 49(5):390–404
del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivée B, Bréant C, Duarte A, Takakura N, Fukamizu A, Penninger J, Eichmann A (2010) Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116(19):4025–4033
De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP, Harris IS, Ehlers ML, Agarval P, Visel A, Xu SM, Pennacchio LA, Dubchak I, Krieg PA, Stainier DY, Black BL (2008) Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 135(6):1053–1064
D’Souza SL, Elefanty AG, Keller G (2005) SCL/Tal-1 is essential for hematopoietic commitment of the hemangioblast but not for its development. Blood 105(10):3862–3870
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(20):2474–2478
Eichmann A, Simons M (2012) VEGF signaling inside vascular endothelial cells and beyond. Curr Opin Cell Biol 24(2):188–193
Eichmann A, Thomas JL (2013) Molecular parallels between neural and vascular development. Cold Spring Harb Perspect Med 3(1):a006551
Eichmann A, Corbel C, Nataf V, Vaigot P, Bréant 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(10):5141–5146
Eilken HM, Nishikawa S-I, Schroeder T (2009) Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457:896–900
Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S, Peri F, Wilson SW, Ruhrberg C (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116(5):829–840
Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, Kouskoff V (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130(17):4217–4227
Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O’Shea KS, Powell-Braxton L, Hillan KJ, Moore MW (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380(6573):439–442
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(8):901–911
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(45):15949–15954
Gerety SS, Wang HU, Chen ZF, Anderson DJ (1999) Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 4(3):403–414
Gore AV, Swift MR, Cha YR, Lo B, McKinney MC, Li W, Castranova D, Davis A, Mukouyama YS, Weinstein BM (2011) Rspo1/Wnt signaling promotes angiogenesis via Vegfc/Vegfr3. Development 138(22):4875–4886
Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, Chimenti S, Landsman L, Abramovitch R, Keshet E (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124(1):175–189
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(1):45–57
Herzog Y, Kalcheim C, Kahane N, Reshef R, Neufeld G (2001) Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech Dev 109(1):115–119
Herzog Y, Guttmann-Raviv N, Neufeld G (2005) Segregation of arterial and venous markers in subpopulations of blood islands before vessel formation. Dev Dyn 232(4):1047–1055
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(7017):625–630
Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM (2003) Angiogenic network formation in the developing vertebrate trunk. Development 130(21):5281–5290
Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE, Weinstein BM (2006) Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442(7101):453–456
Klein R (2012) Eph/ephrin signalling during development. Development 139(22):4105–4109
Koch AW, Mathivet T, Larrivée B, Tong RK, Kowalski J, Pibouin-Fragner L, Bouvrée K, Stawicki S, Nicholes K, Rathore N, Scales SJ, Luis E, del Toro R, Freitas C, Bréantn C, Michaud A, Corvol P, Thomas JL, Wu Y, Peale F, Watts RJ, Tessier-Lavigne M, Bagri A, Eichmann A (2011) Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell 20(1):33–46
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(20):2469–2473
Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, Lacaud G (2009) The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457:892–895
Larrivée B, Prahst C, Gordon E, del Toro R, Mathivet T, Duarte A, Simons M, Eichmann A (2012) ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev Cell 22(3):489–500
Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM (2001) Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128(19):3675–3683
Le Douarin NM, Dieterlen-Lièvre F (2013) How studies on the avian embryo have opened new avenues in the understanding of development: a view about the neural and hematopoietic systems. Develop Growth Differ 55:1–14
le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V, Matthijsen R, Bréant C, Fleury V, Eichmann A (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131(2):361–375
Lenard A, Ellertsdottir E, Herwig L, Krudewig A, Sauteur L, Belting HG, Affolter M (2013) In vivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis. Dev Cell 25(5):492–506
Li W, Kohara H, Uchida Y, James JM, Soneji K, Cronshaw DG, Zou YR, Nagasawa T, Mukouyama YS (2013) Peripheral nerve-derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev Cell 24(4):359–371
Libby P, Ridker PM, Hansson GK (2011) Progress and challenges in translating the biology of atherosclerosis. Nature 473(7347):317–325
Lucitti JL, Jones EA, Huang C, Chen J, Fraser SE, Dickinson ME (2007) Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134(18):3317–3326
Magnon C, Hall SJ, Lin J, Xue X, Gerber L, Freedland SJ, Frenette PS (2013) Autonomic nerve development contributes to prostate cancer progression. Science 341(6142)
Manner J, Seidl W, Steding G (1995) Formation of the cervical flexure: an experimental study on chick embryos. Acta Anat 152:1–10
Marcelo KL, Goldie LC, Hirschi KK (2013a) Regulation of endothelial cell differentiation and specification. Circ Res 112(9):1272–1287
Marcelo KL, Sills TM, Coskun S, Vasavada H, Sanglikar S, Goldie LC, Hirschi KK (2013b) Hemogenic endothelial cell specification requires c-Kit, Notch signaling, and p27-mediated cell-cycle control. Dev Cell 27(5):504–515
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(6):693–705
Mukouyama YS, Gerber HP, Ferrara N, Gu C, Anderson DJ (2005) Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 132(5):941–952
Murray PDF (1932) The development “in vitro” of blood of the early chick embryo. Proc Roy Soc Lond B 111:497–521
Myers CT, Krieg PA (2013) BMP-mediated specification of the erythroid lineage suppresses endothelial development in blood island precursors. Blood, 7 Oct 2013 [Epub ahead of print]
Nishikawa S (2012) Hemangioblast: an in vitro phantom. Wiley Interdiscip Rev Dev Biol 1(4):603–608
Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 125(9):1747–1757
North TE, Goessling W, Peeters M, Li P, Ceol C, Lord AM, Weber GJ, Harris J, Cutting CC, Huang P, Dzierzak E, Zon LI (2009) Hematopoietic stem cell development is dependent on blood flow. Cell 137(4):736–748
Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling – in control of vascular function. Nat Rev Mol Cell Biol 7(5):359–371
Pardanaud L, Eichmann A (2006) Identification, emergence and mobilization of circulating endothelial cells or progenitors in the embryo. Development 133(13):2527–2537
Pardanaud L, Eichmann A (2011) Extraembryonic origin of circulating endothelial cells. PLoS One 6(10):e25889
Pardanaud L, Altmann C, Kitos P, Dieterlen-Lièvre F, Buck CA (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100(2):339–349
Pasquier E, Dias S (2010) Endothelial progenitor cells: hope beyond controversy. Curr Cancer Drug Targets 10(8):914–921
Pearson JD (2009) Endothelial progenitor cells – hype or hope? J Thromb Haemost 7(2):255–262
Planas-Paz L, Lammert E (2013) Mechanical forces in lymphatic vascular development and disease. Cell Mol Life Sci 70(22):4341–4354
Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146(6):873–887
Richard C, Drevon C, Canto PY, Villain G, Bollérot K, Lempereur A, Teillet MA, Vincent C, Rosselló Castillo C, Torres M, Piwarzyk E, Speck NA, Souyri M, Jaffredo T (2013) Endothelio-mesenchymal interaction controls runx1 expression and modulates the Notch pathway to initiate aortic hematopoiesis. Dev Cell 24(6):600–611
Risau W (1997) Mechanisms of angiogenesis. Nature 386(6626):671–674
Sabin FR (1920) Studies on the origin of blood-vessels and of red blood corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Carnegie Contrib Embryol 272:214–262
Schuh AC, Faloon P, Hu QL, Bhimani M, Choi K (1999) In vitro hematopoietic and endothelial potential of flk-1(−/−) embryonic stem cells and embryos. Proc Natl Acad Sci U S A 96(5):2159–2164
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(6535):62–66
Simons M, Eichmann A (2013) Lymphatics are in my veins. Science 341(6146):622–624
Song JW, Munn LL (2011) Fluid forces control endothelial sprouting. Proc Natl Acad Sci U S A 108(37):15342–15347
Strasser GA, Kaminker JS, Tessier-Lavigne M (2010) Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood 115(24):5102–5110
Swift MR, Weinstein BM (2009) Arterial-venous specification during development. Circ Res 104(5):576–588
Tammela T, Zarkada G, Nurmi H, Jakobsson L, Heinolainen K, Tvorogov D, Zheng W, Franco CA, Murtomäki A, Aranda E, Miura N, Ylä-Herttuala S, Fruttiger M, Mäkinen T, Eichmann A, Pollard JW, Gerhardt H, Alitalo K (2011) VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat Cell Biol 13(10):1202–1213
Thoma R (1893) Untersuchungen über due Histogenese und Histomechanik des Gefssytems. Ferdinand Enke, Stuttgart
Tirziu D, Jaba IM, Yu P, Larrivée B, Coon BG, Cristofaro B, Zhuang ZW, Lanahan AA, Schwartz MA, Eichmann A, Simons M (2012) Endothelial nuclear factor-κB-dependent regulation of arteriogenesis and branching. Circulation 126(22):2589–2600
Ueno H, Weissman IL (2006) Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. Dev Cell 11(4):519–533
Urbich C, Dimmeler S (2004) Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 14(8):318–322
Vermot J, Forouhar AS, Liebling M, Wu D, Plummer D, Gharib M, Fraser SE (2009) Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 7(11):e1000246
Vogeli KM, Jin SW, Martin GR, Stainier DY (2006) A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 443(7109):337–339
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(5):741–753
Weis SM, Cheresh DA (2011) Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 17(11):1359–1370
Wheater PR, Burkitt HG, Daniels VG (1978) Functional histology: a text and colour atlas. Churchill Livingstone, Edinburgh
Xu K, Cleaver O (2011) Tubulogenesis during blood vessel formation. Semin Cell Dev Biol 22(9):993–1004
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(6808):92–96
You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY (2005) Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435(7038):98–104
Yuan L, Moyon D, Pardanaud L, Bréant C, Karkkainen MJ, Alitalo K, Eichmann A (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129(20):4797–4806
Zape JP, Zovein AC (2011) Hemogenic endothelium: origins, regulation, and implications for vascular biology. Semin Cell Dev Biol 22(9):1036–1047
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(9):3546–3554
Zhong TP, Childs S, Leu JP, Fishman MC (2001) Gridlock signalling pathway fashions the first embryonic artery. Nature 414(6860):216–220
Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, Becker MS, Zanetta L, Dejana E, Gasson JC, Tallquist MD, Iruela-Arispe ML (2008) Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3:625–636
Zygmunt T, Gay CM, Blondelle J, Singh MK, Flaherty KM, Means PC, Herwig L, Krudewig A, Belting HG, Affolter M, Epstein JA, Torres-Vázquez J (2011) Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev Cell 21(2):301–314
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag France
About this chapter
Cite this chapter
Eichmann, A., Pardanaud, L. (2014). Emergence of Endothelial Cells During Vascular Development. In: Feige, JJ., Pagès, G., Soncin, F. (eds) Molecular Mechanisms of Angiogenesis. Springer, Paris. https://doi.org/10.1007/978-2-8178-0466-8_1
Download citation
DOI: https://doi.org/10.1007/978-2-8178-0466-8_1
Published:
Publisher Name: Springer, Paris
Print ISBN: 978-2-8178-0465-1
Online ISBN: 978-2-8178-0466-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)