Angiogenesis

, Volume 20, Issue 4, pp 463–478 | Cite as

History and conceptual developments in vascular biology and angiogenesis research: a personal view

Review Paper
First Online:
Received:
Accepted:

Abstract

Vascular biology is an important scientific domain that has gradually penetrated many medical and scientific fields. Scientists are most often focused on present problems in their daily scientific work and lack awareness regarding the evolution of their domain throughout history and of how philosophical issues are related to their research field. In this article, I provide a personal view with an attempt to conceptualize vascular development research that articulates lessons taken from history, philosophy, biology and medicine. I discuss selected aspects related to the history and the philosophy of sciences that can be extracted from the study of vascular development and how conceptual progress in this research field has been made. I will analyze paradigm shifts, cross-fertilization of different fields, technological advances and its impact on angiogenesis and discuss issues related to evolutionary biology, proximity of different molecular systems and scientific methodologies. Finally, I discuss briefly my views where the field is heading in the future.

Keywords

Angiogenesis Vascular biology History Conceptual developments 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Elements discussed in this article are based on the book « Une brève histoire du vaisseau sanguin et lymphatique » published by the author in 2016 (permission granted by EDP Science). An English version of the book will be edited by Springer Verlag and will be available in fall 2017. For a complete history of vascular biology from an angiogenesis perspective, the reader may refer to these books. This work was supported by the National Institute of Health and Medical Research (INSERM) and the Ligue Nationale du Cancer (Comités départementaux, Charente Maritime, etc.). The author would like to thank Clotilde Billottet, Klaus Petry and Lindsay Cooley (LAMC-INSERM U1029) for critical reading of the manuscript.

References

  1. 1.
    Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473(7347):298–307. doi: 10.1038/nature10144 PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Uchida S, Dimmeler S (2015) Long noncoding RNAs in cardiovascular diseases. Circ Res 116(4):737–750. doi: 10.1161/CIRCRESAHA.116.302521 PubMedCrossRefGoogle Scholar
  3. 3.
    Potente M, Carmeliet P (2016) The link between angiogenesis and endothelial metabolism. Annu Rev Physiol. doi: 10.1146/annurev-physiol-021115-105134 PubMedGoogle Scholar
  4. 4.
    Ferrara N, Mass RD, Campa C, Kim R (2007) Targeting VEGF-A to treat cancer and age-related macular degeneration. Annu Rev Med 58:491–504PubMedCrossRefGoogle Scholar
  5. 5.
    Welti J, Loges S, Dimmeler S, Carmeliet P (2013) Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Investig 123(8):3190–3200. doi: 10.1172/JCI70212 PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Ferrara N, Adamis AP (2016) Ten years of anti-vascular endothelial growth factor therapy. Nat Rev Drug Discov 15(6):385–403. doi: 10.1038/nrd.2015.17 PubMedCrossRefGoogle Scholar
  7. 7.
    Kuhn TS (1962) Historical structure of scientific discovery. Science 136(3518):760–764PubMedCrossRefGoogle Scholar
  8. 8.
    Schwann T (1847) Microscopical researches into the accordance in the structure and growth of animals and plants. Sydenham Society, LondonGoogle Scholar
  9. 9.
    His W (1865) Die Häute und Höhlen des Körpers. Schwighauser, BaselGoogle Scholar
  10. 10.
    Müller J, Baly W, Bell J (1843) Elements of physiology. Lea and Blanchard, PhiladelphiaGoogle Scholar
  11. 11.
    Earl JW (1835) On the nature of inflammation. Lond Med Gaz 16:6–12Google Scholar
  12. 12.
    Thiersch C (1869) Der Epithelialkrebs, namentlich der Haut mit Atlas: Eine Anatomisch-Klinische Untersuchung. Verlag von Wilhelm Engelmann, LeipzigGoogle Scholar
  13. 13.
    Goldmann E (1908) The Growth of Malignant Disease in Man and the Lower Animals, with special reference to the Vascular System. Proc R Soc Med 1(Surg Sect):1–13PubMedPubMedCentralGoogle Scholar
  14. 14.
    Gimbrone MA Jr, Leapman SB, Cotran RS, Folkman J (1972) Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 136(2):261–276PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Yao L, Sgadari C, Furuke K, Bloom ET, Teruya-Feldstein J, Tosato G (1999) Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood 93(5):1612–1621PubMedGoogle Scholar
  16. 16.
    Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, Rochaix P, Girard JP (2011) Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Can Res 71(17):5678–5687. doi: 10.1158/0008-5472.CAN-11-0431 CrossRefGoogle Scholar
  17. 17.
    Martinet L, Garrido I, Girard JP (2012) Tumor high endothelial venules (HEVs) predict lymphocyte infiltration and favorable prognosis in breast cancer. Oncoimmunology 1(5):789–790. doi: 10.4161/onci.19787 PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Allen E, Jabouille A, Rivera LB, Lodewijckx I, Missiaen R, Steri V, Feyen K, Tawney J, Hanahan D, Michael IP, Bergers G (2017) Combined antiangiogenic and anti-PD-L1 therapy stimulates tumor immunity through HEV formation. Sci Transl Med. doi: 10.1126/scitranslmed.aak9679 PubMedCentralGoogle Scholar
  19. 19.
    Jain RK (2001) Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 7(9):987–989. doi: 10.1038/nm0901-987 PubMedCrossRefGoogle Scholar
  20. 20.
    Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9(6):685–693. doi: 10.1038/nm0603-685 PubMedCrossRefGoogle Scholar
  21. 21.
    Algire GH, Chalkley HW, Earle WE, Legallais FY, Park HD, Shelton E, Schilling EL (1950) Vascular reactions of normal and malignant tissues in vivo. III. Vascular reactions’ of mice to fibroblasts treated in vitro with methylcholanthrene. J Natl Cancer Inst 11(3):555–580PubMedGoogle Scholar
  22. 22.
    Michaelson IC (1948) The mode of development of the vascular system of the retina, with some observations on its significance for certain retinal disease. Trans Ophthalmol Soc UK 68:137–180Google Scholar
  23. 23.
    Campbell FM (1951) The influence of a low atmospheric pressure on the development of the retinal vessels in the rat. Trans Ophthalmol Soc UK 71:287–300Google Scholar
  24. 24.
    Folkman J, Merler E, Abernathy C, Williams G (1971) Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133(2):275–288PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Ferrara N, Henzel WJ (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161(2):851–858PubMedCrossRefGoogle Scholar
  26. 26.
    Dvorak HF (2006) Discovery of vascular permeability factor (VPF). Exp Cell Res 312(5):522–526. doi: 10.1016/j.yexcr.2005.11.026 PubMedCrossRefGoogle Scholar
  27. 27.
    Senger DR, Perruzzi CA, Feder J, Dvorak HF (1986) A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Can Res 46(11):5629–5632Google Scholar
  28. 28.
    Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8(6):464–478. doi: 10.1038/nrm2183 PubMedCrossRefGoogle Scholar
  29. 29.
    Eichmann A, Makinen T, Alitalo K (2005) Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 19(9):1013–1021. doi: 10.1101/gad.1305405 PubMedCrossRefGoogle Scholar
  30. 30.
    Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246(4935):1306–1309PubMedCrossRefGoogle Scholar
  31. 31.
    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. doi: 10.1038/380435a0 PubMedCrossRefGoogle Scholar
  32. 32.
    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. doi: 10.1038/380439a0 PubMedCrossRefGoogle Scholar
  33. 33.
    Lange C, Storkebaum E, de Almodovar CR, Dewerchin M, Carmeliet P (2016) Vascular endothelial growth factor: a neurovascular target in neurological diseases. Nat Rev Neurol 12(8):439–454. doi: 10.1038/nrneurol.2016.88 PubMedCrossRefGoogle Scholar
  34. 34.
    Korpelainen EI, Karkkainen MJ, Tenhunen A, Lakso M, Rauvala H, Vierula M, Parvinen M, Alitalo K (1998) Overexpression of VEGF in testis and epididymis causes infertility in transgenic mice: evidence for nonendothelial targets for VEGF. J Cell Biol 143(6):1705–1712PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Risau W (1996) What, if anything, is an angiogenic factor? Cancer Metastasis Rev 15(2):149–151PubMedCrossRefGoogle Scholar
  36. 36.
    Cao Z, Ding BS, Guo P, Lee SB, Butler JM, Casey SC, Simons M, Tam W, Felsher DW, Shido K, Rafii A, Scandura JM, Rafii S (2014) Angiocrine factors deployed by tumor vascular niche induce B cell lymphoma invasiveness and chemoresistance. Cancer Cell 25(3):350–365. doi: 10.1016/j.ccr.2014.02.005 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Ayres P (2012) The life of Arthur Tansley. Wiley, OxfordCrossRefGoogle Scholar
  38. 38.
    Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92(6):735–745PubMedCrossRefGoogle Scholar
  39. 39.
    Brunet I, Gordon E, Han J, Cristofaro B, Broqueres-You D, Liu C, Bouvree K, Zhang J, del Toro R, Mathivet T, Larrivee B, Jagu J, Pibouin-Fragner L, Pardanaud L, Machado MJ, Kennedy TE, Zhuang Z, Simons M, Levy BI, Tessier-Lavigne M, Grenz A, Eltzschig H, Eichmann A (2014) Netrin-1 controls sympathetic arterial innervation. J Clin Investig 124(7):3230–3240. doi: 10.1172/JCI75181 PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Hinman VF, Davidson EH (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 104(49):19404–19409. doi: 10.1073/pnas.0709994104 PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Lazarus A, Del-Moral PM, Ilovich O, Mishani E, Warburton D, Keshet E (2011) A perfusion-independent role of blood vessels in determining branching stereotypy of lung airways. Development 138(11):2359–2368. doi: 10.1242/dev.060723 PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Magenheim J, Ilovich O, Lazarus A, Klochendler A, Ziv O, Werman R, Hija A, Cleaver O, Mishani E, Keshet E, Dor Y (2011) Blood vessels restrain pancreas branching, differentiation and growth. Development 138(21):4743–4752. doi: 10.1242/dev.066548 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Lammert E, Cleaver O, Melton D (2003) Role of endothelial cells in early pancreas and liver development. Mech Dev 120(1):59–64PubMedCrossRefGoogle Scholar
  44. 44.
    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 CB 13(12):1070–1074PubMedCrossRefGoogle Scholar
  45. 45.
    Rafii S, Butler JM, Ding BS (2016) Angiocrine functions of organ-specific endothelial cells. Nature 529(7586):316–325. doi: 10.1038/nature17040 PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kim J, Kang Y, Kojima Y, Lighthouse JK, Hu X, Aldred MA, McLean DL, Park H, Comhair SA, Greif DM, Erzurum SC, Chun HJ (2013) An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat Med 19(1):74–82. doi: 10.1038/nm.3040 PubMedCrossRefGoogle Scholar
  47. 47.
    Yang P, Read C, Kuc RE, Buonincontri G, Southwood M, Torella R, Upton PD, Crosby A, Sawiak SJ, Carpenter TA, Glen RC, Morrell NW, Maguire JJ, Davenport AP (2017) Elabela/toddler is an endogenous agonist of the apelin APJ receptor in the adult cardiovascular system, and exogenous administration of the peptide compensates for the downregulation of its expression in pulmonary arterial hypertension. Circulation 135(12):1160–1173. doi: 10.1161/CIRCULATIONAHA.116.023218 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    de Jesus Perez V, Yuan K, Alastalo TP, Spiekerkoetter E, Rabinovitch M (2014) Targeting the Wnt signaling pathways in pulmonary arterial hypertension. Drug Discov Today 19(8):1270–1276. doi: 10.1016/j.drudis.2014.06.014 CrossRefGoogle Scholar
  49. 49.
    Fan Y, Potdar AA, Gong Y, Eswarappa SM, Donnola S, Lathia JD, Hambardzumyan D, Rich JN, Fox PL (2014) Profilin-1 phosphorylation directs angiocrine expression and glioblastoma progression through HIF-1alpha accumulation. Nat Cell Biol 16(5):445–456. doi: 10.1038/ncb2954 PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Tamariz E, Varela-Echavarria A (2015) The discovery of the growth cone and its influence on the study of axon guidance. Front Neuroanat 9:51. doi: 10.3389/fnana.2015.00051 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    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(6):1163–1177. doi: 10.1083/jcb.200302047 PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Pelton JC, Wright CE, Leitges M, Bautch VL (2014) Multiple endothelial cells constitute the tip of developing blood vessels and polarize to promote lumen formation. Development 141(21):4121–4126. doi: 10.1242/dev.110296 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Thomas JL, Baker K, Han J, Calvo C, Nurmi H, Eichmann AC, Alitalo K (2013) Interactions between VEGFR and Notch signaling pathways in endothelial and neural cells. Cell Mol Life Sci CMLS 70(10):1779–1792. doi: 10.1007/s00018-013-1312-6 PubMedCrossRefGoogle Scholar
  54. 54.
    Ochsenbein AM, Karaman S, Proulx ST, Berchtold M, Jurisic G, Stoeckli ET, Detmar M (2016) Endothelial cell-derived semaphorin 3A inhibits filopodia formation by blood vascular tip cells. Development 143(4):589–594. doi: 10.1242/dev.127670 PubMedCrossRefGoogle Scholar
  55. 55.
    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(6947):391–397. doi: 10.1038/nature01784 PubMedCrossRefGoogle Scholar
  56. 56.
    Teuwen LA, Draoui N, Dubois C, Carmeliet P (2017) Endothelial cell metabolism: an update anno 2017. Curr Opin Hematol. doi: 10.1097/MOH.0000000000000335 PubMedGoogle Scholar
  57. 57.
    Kur E, Kim J, Tata A, Comin CH, Harrington KI, Costa Lda F, Bentley K, Gu C (2016) Temporal modulation of collective cell behavior controls vascular network topology. eLife 10:10. doi: 10.7554/eLife.13212 Google Scholar
  58. 58.
    Otteley D (1839) John Hunter F.R.S. Haswell, Barrington, and Haswell, PhiladelphiaGoogle Scholar
  59. 59.
    Shing Y, Folkman J, Sullivan R, Butterfield C, Murray J, Klagsbrun M (1984) Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor. Science 223(4642):1296–1299PubMedCrossRefGoogle Scholar
  60. 60.
    Jaffe EA, Nachman RL, Becker CG, Minick CR (1973) Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Investig 52(11):2745–2756. doi: 10.1172/JCI107470 PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Gimbrone MA Jr, Cotran RS, Folkman J (1973) Endothelial regeneration: studies with human endothelial cells in culture. Ser Haematol 6(4):453–455PubMedGoogle Scholar
  62. 62.
    Chamley-Campbell J, Campbell GR, Ross R (1979) The smooth muscle cell in culture. Physiol Rev 59(1):1–61PubMedGoogle Scholar
  63. 63.
    Campbell GR, Uehara Y, Mark G, Burnstock G (1971) Fine structure of smooth muscle cells grown in tissue culture. J Cell Biol 49(1):21–34PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Franco CA, Jones ML, Bernabeu MO, Geudens I, Mathivet T, Rosa A, Lopes FM, Lima AP, Ragab A, Collins RT, Phng LK, Coveney PV, Gerhardt H (2015) Dynamic endothelial cell rearrangements drive developmental vessel regression. PLoS Biol 13(4):e1002125. doi: 10.1371/journal.pbio.1002125 PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Tiozzo S, Voskoboynik A, Brown FD, De Tomaso AW (2008) A conserved role of the VEGF pathway in angiogenesis of an ectodermally-derived vasculature. Dev Biol 315(1):243–255. doi: 10.1016/j.ydbio.2007.12.035 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    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(6):865–876PubMedCrossRefGoogle Scholar
  67. 67.
    Munoz-Chapuli R (2011) Evolution of angiogenesis. Int J Dev Biol 55(4–5):345–351. doi: 10.1387/ijdb.103212rm PubMedCrossRefGoogle Scholar
  68. 68.
    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(3):739–752. doi: 10.1016/S0002-9440(10)65173-5 PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    McDonald DM, Munn L, Jain RK (2000) Vasculogenic mimicry: how convincing, how novel, and how significant? Am J Pathol 156(2):383–388. doi: 10.1016/S0002-9440(10)64740-2 PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Popper K (1935) Logik der Forschung. Julius Springer, WienCrossRefGoogle Scholar
  71. 71.
    Jain H, Jackson T (2017) Mathematical modeling of cellular cross-talk between endothelial and tumor cells highlights counterintuitive effects of VEGF-targeted therapies. Bull Math Biol. doi: 10.1007/s11538-017-0273-6 PubMedGoogle Scholar
  72. 72.
    Grogan JA, Connor AJ, Markelc B, Muschel RJ, Maini PK, Byrne HM, Pitt-Francis JM (2017) Microvessel chaste: an open library for spatial modeling of vascularized tissues. Biophys J 112(9):1767–1772. doi: 10.1016/j.bpj.2017.03.036 PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Akmal M, Zulkifle M, Ansari AH (2010) BN Nafis—a forgotten genius in the discovery of pulmonary blood circulation. Heart Views 11:26–30PubMedPubMedCentralGoogle Scholar
  74. 74.
    Columbo MR (1559) De re anatomica libri XV. Nicolò Bevilacqua, VeniceGoogle Scholar
  75. 75.
    Hofman CHM (2007, 2008) The restauration of Christianity: an English translation of Christianismi restitutio. The Edwin Mellen Press, LewinstonGoogle Scholar
  76. 76.
    Harvey W (1628) Exercitatio anatomica de motu cordis et sanguini in animalibus. Sumptibus Guiliemi Fitzeri, Frankfurt, GermanyGoogle Scholar
  77. 77.
    Schechter DC, Bergan JJ (1986) Popliteal aneurysm: a celebration of the bicentennial of John Hunter’s operation. Ann Vasc Surg 1(1):118–126. doi: 10.1016/S0890-5096(06)60712-7 PubMedCrossRefGoogle Scholar
  78. 78.
    Greenblatt M, Shubi P (1968) Tumor angiogenesis: transfilter diffusion studies in the hamster by the transparent chamber technique. J Natl Cancer Inst 41(1):111–124PubMedGoogle Scholar
  79. 79.
    Ehrmann RL, Knoth M (1968) Choriocarcinoma. Transfilter stimulation of vasoproliferation in the hamster cheek pouch. Studied by light and electron microscopy. J Natl Cancer Inst 41(6):1329–1341PubMedGoogle Scholar
  80. 80.
    Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285(21):1182–1186. doi: 10.1056/NEJM197111182852108 PubMedCrossRefGoogle Scholar
  81. 81.
    Shweiki D, Itin A, Neufeld G, Gitay-Goren H, Keshet E (1993) Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Investig 91(5):2235–2243. doi: 10.1172/JCI116450 PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Adams RH, Diella F, Hennig S, Helmbacher F, Deutsch U, Klein R (2001) The cytoplasmic domain of the ligand ephrinB2 is required for vascular morphogenesis but not cranial neural crest migration. Cell 104(1):57–69PubMedCrossRefGoogle Scholar
  83. 83.
    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(7014):179–186. doi: 10.1038/nature03080 PubMedCrossRefGoogle Scholar
  84. 84.
    Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86(3):353–364PubMedCrossRefGoogle Scholar
  85. 85.
    Murray PDF (1932) The development in vitro of the blood of the early chick embryo. Proc R Soc Biol Sci 3:497–519CrossRefGoogle Scholar
  86. 86.
    Dieterlen-Lievre F (1975) On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J Embryol Exp Morphol 33(3):607–619PubMedGoogle Scholar
  87. 87.
    Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15(7):1751PubMedPubMedCentralGoogle Scholar
  88. 88.
    Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126(14):3047–3055PubMedGoogle Scholar
  89. 89.
    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. doi: 10.1038/nature04923 PubMedCrossRefGoogle Scholar
  90. 90.
    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(2):312–322. doi: 10.1016/j.ydbio.2008.01.038 PubMedCrossRefGoogle Scholar
  91. 91.
    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(4):505–515. doi: 10.1016/j.devcel.2009.08.011 PubMedCrossRefGoogle Scholar
  92. 92.
    Storkebaum E, Lambrechts D, Carmeliet P (2004) VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays News Rev Mol Cell Dev Biol 26(9):943–954. doi: 10.1002/bies.20092 CrossRefGoogle Scholar
  93. 93.
    De Bock K, Georgiadou M, Schoors S, Kuchnio A, Wong BW, Cantelmo AR, Quaegebeur A, Ghesquiere B, Cauwenberghs S, Eelen G, Phng LK, Betz I, Tembuyser B, Brepoels K, Welti J, Geudens I, Segura I, Cruys B, Bifari F, Decimo I, Blanco R, Wyns S, Vangindertael J, Rocha S, Collins RT, Munck S, Daelemans D, Imamura H, Devlieger R, Rider M, Van Veldhoven PP, Schuit F, Bartrons R, Hofkens J, Fraisl P, Telang S, Deberardinis RJ, Schoonjans L, Vinckier S, Chesney J, Gerhardt H, Dewerchin M, Carmeliet P (2013) Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154(3):651–663. doi: 10.1016/j.cell.2013.06.037 PubMedCrossRefGoogle Scholar
  94. 94.
    Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294(5542):564–567. doi: 10.1126/science.1064344 PubMedCrossRefGoogle Scholar
  95. 95.
    Matsumoto K, Yoshitomi H, Rossant J, Zaret KS (2001) Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294(5542):559–563. doi: 10.1126/science.1063889 PubMedCrossRefGoogle Scholar
  96. 96.
    Ding BS, Nolan DJ, Guo P, Babazadeh AO, Cao Z, Rosenwaks Z, Crystal RG, Simons M, Sato TN, Worgall S, Shido K, Rabbany SY, Rafii S (2011) Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 147(3):539–553. doi: 10.1016/j.cell.2011.10.003 PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Buzney SM, Frank RN, Robison WG Jr (1975) Retinal capillaries: proliferation of mural cells in vitro. Science 190(4218):985–986PubMedCrossRefGoogle Scholar
  98. 98.
    de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT (1992) The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255(5047):989–991PubMedCrossRefGoogle Scholar
  99. 99.
    Jain RK, Ward-Hartley KA (1987) Dynamics of cancer cell interactions with microvasculature and interstitium. Biorheology 24(2):117–125PubMedCrossRefGoogle Scholar
  100. 100.
    Leunig M, Yuan F, Menger MD, Boucher Y, Goetz AE, Messmer K, Jain RK (1992) Angiogenesis, microvascular architecture, microhemodynamics, and interstitial fluid pressure during early growth of human adenocarcinoma LS174T in SCID mice. Can Res 52(23):6553–6560Google Scholar
  101. 101.
    Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A, Schulte-Merker S, Gerhardt H (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12(10):943–953. doi: 10.1038/ncb2103 PubMedCrossRefGoogle Scholar
  102. 102.
    Ogawa S, Lee TM (1990) Magnetic resonance imaging of blood vessels at high fields: in vivo and in vitro measurements and image simulation. Magn Reson Med 16(1):9–18PubMedCrossRefGoogle Scholar
  103. 103.
    Ido T, Wan CN, Casella V, Fowler JS, Wolf AP, Reivich M, Kuhl DE (1978) Labeled 2-deoxy-d-glucose analogs. 18F-labeled 2-deoxy-2-fluoro-d-glucose, 2-deoxy-2-fluoro-d-mannose and 14C-2-deoxy-2-fluoro-d-glucose. J Label Compd Radiopharm 14(2):175–183CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.INSERM U1029 (Angiogenesis and Tumor Microenvironment Laboratory)PessacFrance
  2. 2.Université Bordeaux (Angiogenesis and Tumor Microenvironment Laboratory)PessacFrance

Personalised recommendations