Skip to main content

Advertisement

SpringerLink
Log in

Formation of cardiovascular tubes in invertebrates and vertebrates

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The cardiovascular system developed early in evolution and is pivotal for the transport of oxygen, nutrients, and waste products within the organism. It is composed of hollow tubular structures and has a high level of complexity in vertebrates. This complexity is, at least in part, due to the endothelial cell lining of vertebrate blood vessels. However, vascular lumen formation by endothelial cells is still controversially discussed. For example, it has been suggested that the lumen mainly forms via coalescence of large intracellular vacuoles generated by pinocytosis. Alternatively, it was proposed that the vascular lumen initiates extracellularly between adjacent apical endothelial cell surfaces. Here we discuss invertebrate and vertebrate cardiovascular lumen formation and highlight the possible modes of blood vessel formation. Finally, we point to the importance of a better understanding of vascular lumen formation for treating human pathologies, including cancer and coronary heart disease.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Fisher SA, Burggren WW (2007) Role of hypoxia in the evolution and development of the cardiovascular system. Antioxid Redox Signal 9:1339–1352

    Article  CAS  PubMed  Google Scholar 

  2. Yarnitzky T, Volk T (1995) Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev Biol 169:609–618

    Article  CAS  PubMed  Google Scholar 

  3. Burighel P, Cloney RA (1997) Urochordata: Ascidiacea. In: Harrison FW (ed) Microscopic anatomy of invertebrates. Hemichordata Chaetognatha and Invertebrate Chordates. Wiley-Liss, Wilmington, pp 221–347

    Google Scholar 

  4. Barber VC, Graziadei P (1965) Fine structure of cephalopod blood vessels. I. Some smaller peripheral vessels. Z Zellforsch Und Mikrosk Anat 66:765–781

    Article  CAS  Google Scholar 

  5. Herreid CF, Larussa VF, Defesi CR (1976) Blood vascular system of sea-cucumber, Stichopus moebii. J Morphol 150:423–451

    Article  Google Scholar 

  6. Smith P (1986) Development of the blood vascular system in Sabellaria cementarium (Annelida, Polychaeta). An ultrastructural investigation. Zoomorphology 106:67–74

    Article  Google Scholar 

  7. Ruppert E (1997) Cephalochordata (Acrania). In: Harrison FW (ed) Microscopic anatomy of invertebrates. Wiley-Liss, Wilmington, pp 394–509

    Google Scholar 

  8. Ruppert E, Carle K (1983) Morphology of metazoan circulatory systems. Zoomorphology 103:193–208

    Article  Google Scholar 

  9. Hartenstein V, Mandal L (2006) The blood/vascular system in a phylogenetic perspective. Bioessays 28:1203–1210

    Article  PubMed  Google Scholar 

  10. Hartenstein V (2006) Blood cells and blood cell development in the animal kingdom. Annu Rev Cell Dev Biol 22:677–712

    Article  CAS  PubMed  Google Scholar 

  11. Yano K, Gale D, Massberg S, Cheruvu PK, Monahan-Earley R, Morgan ES, Haig D, von Andrian UH, Dvorak AM, Aird WC (2007) Phenotypic heterogeneity is an evolutionarily conserved feature of the endothelium. Blood 109:613–615

    Article  CAS  PubMed  Google Scholar 

  12. Strilic B, Kucera T, Eglinger J, Hughes MR, McNagny KM, Tsukita S, Dejana E, Ferrara N, Lammert E (2009) The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17:505–515

    Article  CAS  PubMed  Google Scholar 

  13. Eichmann A, Yuan L, Moyon D, Lenoble F, Pardanaud L, Breant C (2005) Vascular development: from precursor cells to branched arterial and venous networks. Int J Dev Biol 49:259–267

    Article  CAS  PubMed  Google Scholar 

  14. Stenzel D, Nye E, Nisancioglu M, Adams RH, Yamaguchi Y, Gerhardt H (2009) Peripheral mural cell recruitment requires cell-autonomous heparan sulfate. Blood 114:915–924

    Article  CAS  PubMed  Google Scholar 

  15. Betsholtz C, Lindblom P, Gerhardt H (2005) Role of pericytes in vascular morphogenesis. EXS 115-125

  16. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH (2006) Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 124:161–173

    Article  CAS  PubMed  Google Scholar 

  17. Stach T (1998) Coelomic cavities may function as a vascular system in amphioxus larvae. Biol Bull 195:260–263

    Article  Google Scholar 

  18. Kucera T, Strilic B, Regener K, Schubert M, Laudet V, Lammert E (2009) Ancestral vascular lumen formation via basal cell surfaces. PLoS ONE 4:e4132

    Article  PubMed  CAS  Google Scholar 

  19. Adachi T, Tomita M, Yoshizato K (2005) Synthesis of prolyl 4-hydroxylase alpha subunit and type IV collagen in hemocytic granular cells of silkworm, Bombyx mori: involvement of type IV collagen in self-defense reaction and metamorphosis. Matrix Biol 24:136–154

    Article  CAS  PubMed  Google Scholar 

  20. Fessler JH, Fessler LI (1989) Drosophila extracellular matrix. Annu Rev Cell Biol 5:309–339

    Article  CAS  PubMed  Google Scholar 

  21. Rhodes CP, Ratcliffe NA, Rowley AF (1982) Presence of coelomocytes in the primitive chordate amphioxus (Branchiostoma lanceolatum). Science 217:263–265

    Article  CAS  PubMed  Google Scholar 

  22. Moller PC, Philpott CW (1973) The circulatory system of Amphioxus (Branchiostoma floridae). I. Morphology of the major vessels of the pharyngeal area. J Morphol 139:389–406

    Article  CAS  PubMed  Google Scholar 

  23. Bagnat M, Cheung ID, Mostov KE, Stainier DY (2007) Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol 9:954–960

    Article  CAS  PubMed  Google Scholar 

  24. Barcroft LC, Moseley AE, Lingrel JB, Watson AJ (2004) Deletion of the Na/K-ATPase alpha1-subunit gene (Atp1a1) does not prevent cavitation of the preimplantation mouse embryo. Mech Dev 121:417–426

    CAS  PubMed  Google Scholar 

  25. Rugendorff A, Younossi-Hartenstein A, Hartenstein V (1994) Embryonic origin and differentiation of the Drosophila heart. Rouxs Arch Dev Biol 203:266–280

    Article  Google Scholar 

  26. Santiago-Martinez E, Soplop NH, Kramer SG (2006) Lateral positioning at the dorsal midline: Slit and Roundabout receptors guide Drosophila heart cell migration. Proc Natl Acad Sci USA 103:12441–12446

    Article  CAS  PubMed  Google Scholar 

  27. MacMullin A, Jacobs JR (2006) Slit coordinates cardiac morphogenesis in Drosophila. Dev Biol 293:154–164

    Article  CAS  PubMed  Google Scholar 

  28. Qian L, Liu J, Bodmer R (2005) Slit and Robo control cardiac cell polarity and morphogenesis. Curr Biol 15:2271–2278

    Article  CAS  PubMed  Google Scholar 

  29. Haag TA, Haag NP, Lekven AC, Hartenstein V (1999) The role of cell adhesion molecules in Drosophila heart morphogenesis: faint sausage, shotgun/DE-cadherin, and laminin A are required for discrete stages in heart development. Dev Biol 208:56–69

    Article  CAS  PubMed  Google Scholar 

  30. Medioni C, Astier M, Zmojdzian M, Jagla K, Semeriva M (2008) Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation. J Cell Biol 182:249–261

    Article  CAS  PubMed  Google Scholar 

  31. Santiago-Martinez E, Soplop NH, Patel R, Kramer SG (2008) Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J Cell Biol 182:241–248

    Article  CAS  PubMed  Google Scholar 

  32. Aurrand-Lions M, Johnson-Leger C, Imhof BA (2002) The last molecular fortress in leukocyte trans-endothelial migration. Nat Immunol 3:116–118

    Article  CAS  PubMed  Google Scholar 

  33. Springer TA (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301–314

    Article  CAS  PubMed  Google Scholar 

  34. Butcher EC (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67:1033–1036

    Article  CAS  PubMed  Google Scholar 

  35. Langer HF, Chavakis T (2009) Leukocyte-endothelial interactions in inflammation. J Cell Mol Med 13:1211–1220

    Article  CAS  PubMed  Google Scholar 

  36. Vestweber D (2007) Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol Rev 218:178–196

    Article  CAS  PubMed  Google Scholar 

  37. Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294:564–567

    Article  CAS  PubMed  Google Scholar 

  38. Crivellato E, Nico B, Ribatti D (2007) Contribution of endothelial cells to organogenesis: a modern reappraisal of an old Aristotelian concept. J Anat 211:415–427

    CAS  PubMed  Google Scholar 

  39. Nikolova G, Lammert E (2003) Interdependent development of blood vessels and organs. Cell Tissue Res 314:33–42

    Article  PubMed  Google Scholar 

  40. Sakaguchi TF, Sadler KC, Crosnier C, Stainier DY (2008) Endothelial signals modulate hepatocyte apicobasal polarization in zebrafish. Curr Biol 18:1565–1571

    Article  CAS  PubMed  Google Scholar 

  41. Burton GJ, Charnock-Jones DS, Jauniaux E (2009) Regulation of vascular growth and function in the human placenta. Reproduction 138:895–902

    Article  CAS  PubMed  Google Scholar 

  42. Regina A, Morchoisne S, Borson ND, McCall AL, Drewes LR, Roux F (2001) Factor(s) released by glucose-deprived astrocytes enhance glucose transporter expression and activity in rat brain endothelial cells. Biochim Biophys Acta 1540:233–242

    Article  CAS  PubMed  Google Scholar 

  43. Lee SW, Kim WJ, Choi YK, Song HS, Son MJ, Gelman IH, Kim YJ, Kim KW (2003) SSeCKS regulates angiogenesis and tight junction formation in blood–brain barrier. Nat Med 9:900–906

    Article  CAS  PubMed  Google Scholar 

  44. Liebner S, Corada M, Bangsow T, Babbage J, Taddei A, Czupalla CJ, Reis M, Felici A, Wolburg H, Fruttiger M, Taketo MM, von Melchner H, Plate KH, Gerhardt H, Dejana E (2008) Wnt/beta-catenin signaling controls development of the blood–brain barrier. J Cell Biol 183:409–417

    Article  CAS  PubMed  Google Scholar 

  45. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983–985

    Article  CAS  PubMed  Google Scholar 

  46. Lammert E, Gu G, McLaughlin M, Brown D, Brekken R, Murtaugh LC, Gerber HP, Ferrara N, Melton DA (2003) Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 13:1070–1074

    Article  CAS  PubMed  Google Scholar 

  47. Salmon AH, Neal CR, Bates DO, Harper SJ (2006) Vascular endothelial growth factor increases the ultrafiltration coefficient in isolated intact Wistar rat glomeruli. J Physiol 570:141–156

    Article  CAS  PubMed  Google Scholar 

  48. Maharaj AS, Saint-Geniez M, Maldonado AE, D’Amore PA (2006) Vascular endothelial growth factor localization in the adult. Am J Pathol 168:639–648

    Article  CAS  PubMed  Google Scholar 

  49. Rahr H (1981) The ultrastructure of the blood-vessels of Branchiostoma lanceolatum (Pallas) (Cephalochordata).1. Relations between blood-vessels, epithelia, basal laminae, and connective-tissue. Zoomorphology 97:53–74

    Article  Google Scholar 

  50. Hama K (1960) The fine structure of some blood vessels of the earthworm, Eisenia foetida. J Biophys Biochem Cytol 7:717–724

    Article  CAS  PubMed  Google Scholar 

  51. Pardos F, Benedito R (1988) Blood vessels and related structures in the gill bars of Glossobalanus minutus (Enteropneusta). Acta Zoologica 69:87–94

    Article  Google Scholar 

  52. Curtis SK, Cowden RR (1979) Histochemical and ultrastructural features of the aorta of the slug (Limax maximus). J Morphol 161:1–21

    Article  Google Scholar 

  53. Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, Perrimon N (2004) The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev Cell 7:73–84

    Article  PubMed  Google Scholar 

  54. Heino TI, Karpanen T, Wahlstrom G, Pulkkinen M, Eriksson U, Alitalo K, Roos C (2001) The Drosophila VEGF receptor homolog is expressed in hemocytes. Mech Dev 109:69–77

    Article  CAS  PubMed  Google Scholar 

  55. Cho NK, Keyes L, Johnson E, Heller J, Ryner L, Karim F, Krasnow MA (2002) Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108:865–876

    Article  CAS  PubMed  Google Scholar 

  56. Goldie LC, Nix MK, Hirschi KK (2008) Embryonic vasculogenesis and hematopoietic specification. Organogenesis 4:257–263

    Article  PubMed  Google Scholar 

  57. Newman PJ, Berndt MC, Gorski J, White GC 2nd, Lyman S, Paddock C, Muller WA (1990) PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247:1219–1222

    Article  CAS  PubMed  Google Scholar 

  58. Van den Bossche J, Bogaert P, van Hengel J, Guerin CJ, Berx G, Movahedi K, Van den Bergh R, Pereira-Fernandes A, Geuns JM, Pircher H, Dorny P, Grooten J, De Baetselier P, Van Ginderachter JA (2009) Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 114:4664–4674

    Article  PubMed  CAS  Google Scholar 

  59. Buttler K, Kreysing A, von Kaisenberg CS, Schweigerer L, Gale N, Papoutsi M, Wilting J (2006) Mesenchymal cells with leukocyte and lymphendothelial characteristics in murine embryos. Dev Dyn 235:1554–1562

    Article  CAS  PubMed  Google Scholar 

  60. Buttler K, Ezaki T, Wilting J (2008) Proliferating mesodermal cells in murine embryos exhibiting macrophage and lymphendothelial characteristics. BMC Dev Biol 8:43

    Article  PubMed  CAS  Google Scholar 

  61. Vogeli KM, Jin SW, Martin GR, Stainier DY (2006) A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 443:337–339

    Article  CAS  PubMed  Google Scholar 

  62. Weng W, Sukowati EW, Sheng G (2007) On hemangioblasts in chicken. PLoS ONE 2:e1228

    Article  PubMed  CAS  Google Scholar 

  63. 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  CAS  PubMed  Google Scholar 

  64. Kennedy M, D’Souza SL, Lynch-Kattman M, Schwantz S, Keller G (2007) Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109:2679–2687

    CAS  PubMed  Google Scholar 

  65. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125:725–732

    CAS  PubMed  Google Scholar 

  66. Eilken HM, Nishikawa S, Schroeder T (2009) Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457:896–900

    Article  CAS  PubMed  Google Scholar 

  67. 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

    Article  CAS  PubMed  Google Scholar 

  68. Nishikawa SI, Nishikawa S, Kawamoto H, Yoshida H, Kizumoto M, Kataoka H, Katsura Y (1998) In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 8:761–769

    Article  CAS  PubMed  Google Scholar 

  69. Young PE, Baumhueter S, Lasky LA (1995) The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development. Blood 85:96–105

    CAS  PubMed  Google Scholar 

  70. Doyonnas R, Nielsen JS, Chelliah S, Drew E, Hara T, Miyajima A, McNagny KM (2005) Podocalyxin is a CD34-related marker of murine hematopoietic stem cells and embryonic erythroid cells. Blood 105:4170–4178

    Article  CAS  PubMed  Google Scholar 

  71. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L Jr (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24:909–969

    CAS  PubMed  Google Scholar 

  72. Simoes-Costa MS, Vasconcelos M, Sampaio AC, Cravo RM, Linhares VL, Hochgreb T, Yan CY, Davidson B, Xavier-Neto J (2005) The evolutionary origin of cardiac chambers. Dev Biol 277:1–15

    Article  CAS  PubMed  Google Scholar 

  73. Vrancken Peeters MP, Gittenberger-de Groot AC, Mentink MM, Poelmann RE (1999) Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol (Berl) 199:367–378

    Article  CAS  Google Scholar 

  74. Perez-Pomares JM, Macias-Lopez D, Garcia-Garrido L, Munoz-Chapuli R (1999) Immunohistochemical evidence for a mesothelial contribution to the ventral wall of the avian aorta. Histochem J 31:771–779

    Article  CAS  PubMed  Google Scholar 

  75. Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM (2005) The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132:5317–5328

    Article  CAS  PubMed  Google Scholar 

  76. Que J, Wilm B, Hasegawa H, Wang F, Bader D, Hogan BL (2008) Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc Natl Acad Sci USA 105:16626–16630

    Article  CAS  PubMed  Google Scholar 

  77. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8:464–478

    Article  CAS  PubMed  Google Scholar 

  78. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling—in control of vascular function. Nat Rev Mol Cell Biol 7:359–371

    Article  CAS  PubMed  Google Scholar 

  79. Risau W, Flamme I (1995) Vasculogenesis. Annu Rev Cell Dev Biol 11:73–91

    Article  CAS  PubMed  Google Scholar 

  80. Walls JR, Coultas L, Rossant J, Henkelman RM (2008) Three-dimensional analysis of vascular development in the mouse embryo. PLoS One 3:e2853

    Article  PubMed  Google Scholar 

  81. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318

    Article  CAS  PubMed  Google Scholar 

  82. Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT, Wang RA, Shokat KM, Stainier DY (2009) Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 326:294–298

    Article  CAS  PubMed  Google Scholar 

  83. Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE, Weinstein BM (2006) Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442:453–456

    Article  CAS  PubMed  Google Scholar 

  84. Blum Y, Belting HG, Ellertsdottir E, Herwig L, Luders F, Affolter M (2008) Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev Biol 316:312–322

    Article  CAS  PubMed  Google Scholar 

  85. Billroth T (1856) Untersuchungen über die Entwicklung der Blutgefässe, nebst Beobachtungen aus der königlichen chirurgischen Universitäts-Klinik zu Berlin (in German). Georg Reimer, Berlin

  86. 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. Contrib Embryol 9:215

    Google Scholar 

  87. Davis GE, Camarillo CW (1996) An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224:39–51

    Article  CAS  PubMed  Google Scholar 

  88. Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288:551–556

    Article  CAS  PubMed  Google Scholar 

  89. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132:5199–5209

    Article  CAS  PubMed  Google Scholar 

  90. Parker LH, Schmidt M, Jin SW, Gray AM, Beis D, Pham T, Frantz G, Palmieri S, Hillan K, Stainier DY, De Sauvage FJ, Ye W (2004) The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation. Nature 428:754–758

    Article  CAS  PubMed  Google Scholar 

  91. Ribeiro C, Neumann M, Affolter M (2004) Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr Biol 14:2197–2207

    Article  CAS  PubMed  Google Scholar 

  92. De Maziere A, Parker L, Van Dijk S, Ye W, Klumperman J (2008) Egfl7 knockdown causes defects in the extension and junctional arrangements of endothelial cells during zebrafish vasculogenesis. Dev Dyn 237:580–591

    Article  PubMed  Google Scholar 

  93. Carman CV, Springer TA (2008) Trans-cellular migration: cell-cell contacts get intimate. Curr Opin Cell Biol 20:533–540

    Article  CAS  PubMed  Google Scholar 

  94. Bar T, Guldner FH, Wolff JR (1984) “Seamless” endothelial cells of blood capillaries. Cell Tissue Res 235:99–106

    Article  CAS  PubMed  Google Scholar 

  95. Wolff JR, Bar T (1972) ‘Seamless’ endothelia in brain capillaries during development of the rat’s cerebral cortex. Brain Res 41:17–24

    Article  CAS  PubMed  Google Scholar 

  96. Gervais L, Casanova J (2010) In vivo coupling of cell elongation and lumen formation in a single cell. Curr Biol 20:359–366

    Article  CAS  PubMed  Google Scholar 

  97. Rasmussen JP, English K, Tenlen JR, Priess JR (2008) Notch signaling and morphogenesis of single-cell tubes in the C. elegans digestive tract. Dev Cell 14:559–569

    Article  CAS  PubMed  Google Scholar 

  98. Zovein AC, Luque A, Turlo KA, Hofmann JJ, Yee KM, Becker MS, Fassler R, Mellman I, Lane TF, Iruela-Arispe ML (2010) Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell 18:39–51

    Article  CAS  PubMed  Google Scholar 

  99. Lampugnani MG, Orsenigo F, Rudini N, Maddaluno L, Boulday G, Chapon F, Dejana E (2010) CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J Cell Sci 123:1073–1080

    Article  CAS  PubMed  Google Scholar 

  100. Ferrari A, Veligodskiy A, Berge U, Lucas MS, Kroschewski R (2008) ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J Cell Sci 121:3649–3663

    Article  CAS  PubMed  Google Scholar 

  101. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, Mostov K (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128:383–397

    Article  CAS  PubMed  Google Scholar 

  102. 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  CAS  PubMed  Google Scholar 

  103. Resnick N, Einav S, Chen-Konak L, Zilberman M, Yahav H, Shay-Salit A (2003) Hemodynamic forces as a stimulus for arteriogenesis. Endothelium 10:197–206

    Article  PubMed  Google Scholar 

  104. Wiegreffe C, Christ B, Huang R, Scaal M (2009) Remodeling of aortic smooth muscle during avian embryonic development. Dev Dyn 238:624–631

    Article  PubMed  Google Scholar 

  105. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT (2002) Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 16:2684–2698

    Article  CAS  PubMed  Google Scholar 

  106. Stenman JM, Rajagopal J, Carroll TJ, Ishibashi M, McMahon J, McMahon AP (2008) Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322:1247–1250

    Article  CAS  PubMed  Google Scholar 

  107. Thomas M, Augustin HG (2009) The role of the Angiopoietins in vascular morphogenesis. Angiogenesis 12:125–137

    Article  CAS  PubMed  Google Scholar 

  108. Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10:165–177

    Article  CAS  PubMed  Google Scholar 

  109. 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 USA 99:11205–11210

    Article  CAS  PubMed  Google Scholar 

  110. Kidoya H, Ueno M, Yamada Y, Mochizuki N, Nakata M, Yano T, Fujii R, Takakura N (2008) Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J 27:522–534

    Article  CAS  PubMed  Google Scholar 

  111. Kim KE, Cho CH, Kim HZ, Baluk P, McDonald DM, Koh GY (2007) In vivo actions of angiopoietins on quiescent and remodeling blood and lymphatic vessels in mouse airways and skin. Arterioscler Thromb Vasc Biol 27:564–570

    Article  CAS  PubMed  Google Scholar 

  112. Thurston G, Wang Q, Baffert F, Rudge J, Papadopoulos N, Jean-Guillaume D, Wiegand S, Yancopoulos GD, McDonald DM (2005) Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period. Development 132:3317–3326

    Article  CAS  PubMed  Google Scholar 

  113. 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 USA 98:5643–5648

    Article  CAS  PubMed  Google Scholar 

  114. Kim YH, Hu H, Guevara-Gallardo S, Lam MT, Fong SY, Wang RA (2008) Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis. Development 135:3755–3764

    Article  CAS  PubMed  Google Scholar 

  115. 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

    CAS  PubMed  Google Scholar 

  116. Kucera T, Lammert E (2009) Ancestral vascular tube formation and its adoption by tumors. Biol Chem 390:985–994

    Article  CAS  PubMed  Google Scholar 

  117. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739–752

    CAS  PubMed  Google Scholar 

  118. McDonald DM, Munn L, Jain RK (2000) Vasculogenic mimicry: how convincing, how novel, and how significant? Am J Pathol 156:383–388

    CAS  PubMed  Google Scholar 

  119. Maniotis AJ, Chen X, Garcia C, DeChristopher PJ, Wu D, Pe’er J, Folberg R (2002) Control of melanoma morphogenesis, endothelial survival, and perfusion by extracellular matrix. Lab Invest 82:1031–1043

    PubMed  Google Scholar 

  120. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444:1032–1037

    Article  CAS  PubMed  Google Scholar 

  121. 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 USA 101:15949–15954

    Article  CAS  PubMed  Google Scholar 

  122. Benedito R, Trindade A, Hirashima M, Henrique D, da Costa LL, Rossant J, Gill PS, Duarte A (2008) Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev Biol 8:117

    Article  PubMed  CAS  Google Scholar 

  123. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444:1083–1087

    Article  CAS  PubMed  Google Scholar 

  124. Yan M, Callahan CA, Beyer JC, Allamneni KP, Zhang G, Ridgway JB, Niessen K, Plowman GD (2010) Chronic DLL4 blockade induces vascular neoplasms. Nature 463:E6–E7

    Article  CAS  PubMed  Google Scholar 

  125. Schaper W, Ito WD (1996) Molecular mechanisms of coronary collateral vessel growth. Circ Res 79:911–919

    CAS  PubMed  Google Scholar 

  126. Nanka O, Valasek P, Dvorakova M, Grim M (2006) Experimental hypoxia and embryonic angiogenesis. Dev Dyn 235:723–733

    Article  CAS  PubMed  Google Scholar 

  127. Gray C, Packham IM, Wurmser F, Eastley NC, Hellewell PG, Ingham PW, Crossman DC, Chico TJ (2007) Ischemia is not required for arteriogenesis in zebrafish embryos. Arterioscler Thromb Vasc Biol 27:2135–2141

    Article  CAS  PubMed  Google Scholar 

  128. Deindl E, Buschmann I, Hoefer IE, Podzuweit T, Boengler K, Vogel S, van Royen N, Fernandez B, Schaper W (2001) Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit. Circ Res 89:779–786

    Article  CAS  PubMed  Google Scholar 

  129. Schierling W, Troidl K, Troidl C, Schmitz-Rixen T, Schaper W, Eitenmuller IK (2009) The role of angiogenic growth factors in arteriogenesis. J Vasc Res 46:365–374

    Article  CAS  PubMed  Google Scholar 

  130. Lee CW, Stabile E, Kinnaird T, Shou M, Devaney JM, Epstein SE, Burnett MS (2004) Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J Am Coll Cardiol 43:474–482

    Article  CAS  PubMed  Google Scholar 

  131. Menshikov M, Elizarova E, Plakida K, Timofeeva A, Khaspekov G, Beabealashvilli R, Bobik A, Tkachuk V (2002) Urokinase upregulates matrix metalloproteinase-9 expression in THP-1 monocytes via gene transcription and protein synthesis. Biochem J 367:833–839

    Article  CAS  PubMed  Google Scholar 

  132. Sahni A, Francis CW (2004) Stimulation of endothelial cell proliferation by FGF-2 in the presence of fibrinogen requires alphavbeta3. Blood 104:3635–3641

    Article  CAS  PubMed  Google Scholar 

  133. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W (1998) Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 101:40–50

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We apologize to colleagues whose original research was not cited due to space constraints. We thank our friends and colleagues for helpful discussions. This work was supported by the DFG LA1216/2-3 and the Research Project MSM 0021620807 from the Ministry of Education, Youth and Sports of Czech Republic.

Author information

Authors and Affiliations

  1. Institute of Metabolic Physiology, Heinrich-Heine-University Düsseldorf, 40225, Düsseldorf, Germany

    Boris Strilić & Eckhard Lammert

  2. Department of Pharmacology, Max Planck Institute for Heart and Lung Research, W.G. Kerckhoff-Institute, 61231, Bad Nauheim, Germany

    Boris Strilić

  3. First Faculty of Medicine, Charles University in Prague, Institute of Histology and Embryology, Prague, 12800, Czech Republic

    Tomáš Kučera

Authors
  1. Boris Strilić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomáš Kučera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eckhard Lammert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eckhard Lammert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Strilić, B., Kučera, T. & Lammert, E. Formation of cardiovascular tubes in invertebrates and vertebrates. Cell. Mol. Life Sci. 67, 3209–3218 (2010). https://doi.org/10.1007/s00018-010-0400-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-010-0400-0

Keywords

Search

Navigation