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How Is the Branching of Animal Blood Vessels Implemented?

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Branching Morphogenesis

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

For centuries, the cardiovascular system of animals has been described as a branching tree with the heart in its very centre. Although this description dates back to Galen (c. 130–200 A.D.), and structural similarities with trees are obvious, it has to be empha-sized that, unlike a tree, the animal blood circulation does not contain blind ending branches. The discoveries of Harvey (1578–1657) and Malpighi (1628–1694) demonstrated that the blood circulation, especially when studied at light microscopic dimensions, forms a “closed system” of circuits in which every single blood vessel is continuous with another one. Arterial vessels leave the heart, branch, and connect through a capillary network to corresponding veins that drain the blood back to the heart. It is therefore more appropriate to understand the circulatory system as a network of conductive units of varying sizes.

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References

  1. Galen, De foetuum formatione. Harris CRS. The heart and the vascular system in ancient Greek medicine. Oxford: Clarendon Press, 1973.

    Google Scholar 

  2. Fülleborn F. Beiträge zur Entwicklung der Allantois der Vögel. Inaug Diss. Berlin: Francke 1895.

    Google Scholar 

  3. Danchakoff V. The position of the respiratory vascular net in the allantois of the chick. Am J Anat 1917; 21:407–420.

    Article  Google Scholar 

  4. Clark ER. Studies on the growth of blood vessels, by observation of living tadpoles and by experiments on chicken embryos. Anat Rec 1915; 9:17–68.

    Google Scholar 

  5. Clark ER. Studies on the growth of blood-vessels in the tail of the frog larva — by observation and experiment on the living animal. Am J Anat 1918; 23:37–88.

    Article  Google Scholar 

  6. Clark ER, Clark EL. Microscopic observations on the growth of blood capillaries in the living mammal. Am J Anat 1939; 64:251–299.

    Article  Google Scholar 

  7. Ausprunk D, Folkman J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 1977; 14 53–65.

    Article  PubMed  CAS  Google Scholar 

  8. Sabin FR. Origin and development of the primitive vessels of the chick and of the pig. Contrib Embryol Carnegie Inst Publ Wash 1917; 6:61–124.

    Google Scholar 

  9. Sabin FR. 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 Carnegie Inst Publ Wash 1920; 36:213–259.

    Google Scholar 

  10. Pardanaud L, Altmann C, Kitos P et al. Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 1987; 100:339–349.

    PubMed  CAS  Google Scholar 

  11. Pardanaud L, Yassine F, Dieterlen-Lièvre F. Relationship between vasculogenesis, angiogenesis and hematopoiesis during avian ontogeny. Development 1989; 105:473–485.

    PubMed  CAS  Google Scholar 

  12. Noden DM. The formation of avian embryonic blood vessels. Am Rev Respir Dis 1989; 140:1097–1103.

    PubMed  CAS  Google Scholar 

  13. Poole TJ, Coffin JD. Vasculogenesis and angiogenesis: Two distinct morphogenetic mechanisms establish the embryonic vascular pattern. J Exp Zool 1989; 251:224–231.

    Article  PubMed  CAS  Google Scholar 

  14. Risau W. Vasculogenesis, angiogenesis and endothelial cell differentiation during embryonic development. In: Feinberg RN, Sherer GK, Auerbach R, eds. The development of the vascular system. Issues Biomed 14. Basel: Karger 1991:58–68.

    Google Scholar 

  15. Poole TJ, Coffin D. Morphogenetic mechanisms in avian vascular development. In: Feinberg RN, Sherer GK, Auerbach R, eds. The development of the vascular system. Issues Biomed 14, Basel: Karger 1991:25–36.

    Google Scholar 

  16. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11:73–91.

    Article  PubMed  CAS  Google Scholar 

  17. Risau W. Mechanisms of angiogenesis. Nature 1997; 386:671–674.

    Article  PubMed  CAS  Google Scholar 

  18. Patan S, Haenni B, Burri PH. Evidence for intussusceptive capillary growth in the chicken chorio-allantoic membrane (CAM). Anat Embryol 1993; 187:121–130.

    Article  PubMed  CAS  Google Scholar 

  19. Patan S, Heanni B, Burri PH. Implementation of intussusceptive microvascular growth in the chicken chorio-allantoic membrane (CAM): 1. Pillar formation by folding of the capillary wall. Microvasc Res 1996; 51:80–98.

    Article  PubMed  CAS  Google Scholar 

  20. Patan S, Haenni B, Burri PH. Implementation of intussusceptive microvascular growth in the chicken chorio-allantoic membrane (CAM): 2. Pillar formation by capillary fusion. Microvasc Res 1997; 53:33–52.

    Article  PubMed  CAS  Google Scholar 

  21. Patan, S. Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neuro-Oncol 2000; 50:1–15.

    Article  CAS  Google Scholar 

  22. Patan S. Vasculogenesis and angiogenesis. In: Black P, Kirsch M, eds. Angiogenesis in brain tumors. Cancer Treatment and Research, Boston: Kluwer Academic Publishers, 2004:3–32.

    Google Scholar 

  23. Patan S. TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth. Microvasc Res 1998; 56:1–21.

    Article  PubMed  CAS  Google Scholar 

  24. Gilbert SG. Pictorial human embryology. Seattle and London: University of Washington Press, 1989.

    Google Scholar 

  25. Short RHD. Alveolar epithelium in relation to growth of the lung. Philos Trans R Soc London Ser B 1950; 235:35–87.

    Google Scholar 

  26. Caduff JH, Fischer LC, Burri PH. Scanning electron microscope study of the developing microvas-culature in the postnatal rat lung. Anat Rec 1986; 216:154–164.

    Article  PubMed  CAS  Google Scholar 

  27. Burri PH, Tarek MR. A novel mechanism of capillary growth in the rat pulmonary microcirculation. Anat Rec 1990; 228:35–45.

    Article  PubMed  CAS  Google Scholar 

  28. Van Groningen JP, Wenink ACG, Testers LHM. Myocardial capillaries: Increase in number by splitting of existing vessels. Anat Embryol 1991; 184:65–70.

    Article  PubMed  Google Scholar 

  29. Patan S, Alvarez MJ, Schittny JC et al. Intussusceptive microvascular growth: Common alternative to endothelial sprouting. Arch Histol Cytol 1992; 55(Suppl):65–75.

    PubMed  Google Scholar 

  30. Patan S, Munn LL, Jain RK. Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft: A novel mechanism of tumor angiogenesis. Microvasc Res 1996; 51:260–272.

    Article  PubMed  CAS  Google Scholar 

  31. Patan S, Tanda S, Roberge S et al. Vascular morphogenesis and remodeling in a human tumor xenograft. Blood vessel formation and growth after ovariectomy and tumor implantation. Circ Res 2001; 89:732–739.

    PubMed  CAS  Google Scholar 

  32. Patan S, Munn LL, Tanda S et al. Vascular morphogenesis and remodeling in a model of tissue repair. Blood vessel formation and growth in the ovarian pedicle after ovariectomy. Circ Res 2001; 89:723–731.

    PubMed  CAS  Google Scholar 

  33. Suri C, Jones PF, Patan S et al. Requisite role of Angiopoietin-1, a ligand for the TIE2 receptor during embryonic angiogenesis. Cell 1996; 87:1171–1180.

    Article  PubMed  CAS  Google Scholar 

  34. Nagy JA, Morgan ES, Herzberg KT et al. Pathogenesis of ascites tumor growth: Angiogenesis, vascular remodeling, and stroma formation in the peritoneal lining. Cancer Res 1995; 55:376–85.

    PubMed  CAS  Google Scholar 

  35. Dvorak HF. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986; 315:1650–1659.

    Article  PubMed  CAS  Google Scholar 

  36. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1995; 1:27–31.

    Article  PubMed  CAS  Google Scholar 

  37. St. Croix B, Rago C, Velculescu V et al. Genes expressed in human tumor endothelium. Science 2000; 289:1197–1202.

    Article  PubMed  CAS  Google Scholar 

  38. Warren BA, Shubik P. The growth of the blood supply to melanoma transplants in the hamster cheek pouch chamber. Lab Invest 1966; 15:464–478.

    PubMed  CAS  Google Scholar 

  39. Hammersen F, Osterkamp-Baust U, Endrich B. Ein Beitrag zum Feinbau terminaler Strombahnen und ihrer Entstehung in bösartigen Tumoren. Mikrozirk Forsch Klin 1983; 2:15–51.

    Google Scholar 

  40. Hammersen F, Endrich B, Messmer K. The fine structure of tumor blood vessels. I. Participation of nonendothelial cells in tumor angiogenesis. Int J Microcirc Clin Exp 1985; 4:31–43.

    PubMed  CAS  Google Scholar 

  41. Ware JA, Simons M. Angiogenesis in ischemic heart disease. Nature Med 1997; 3:158–164.

    Article  PubMed  CAS  Google Scholar 

  42. Fernandez B, Buehler A, Wolfram S et al. Transgenic myocardial overexpression of fibroblast growth factor-1 increases coronary artery density and branching. Circ Res 2000; 87:176–178.

    Google Scholar 

  43. Xin X, Yang S, Ingle G et al. Hepatocyte growth factor enhances vascular endothelial growth factor induced angiogenesis in vitro and in vivo. Am J Pathol 2001; 158:1111–1120.

    PubMed  CAS  Google Scholar 

  44. Hellstrom M, Gerhardt H, Kalen M et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 2001; 153:543–553.

    Article  PubMed  CAS  Google Scholar 

  45. Sato TN, Quin Y, Kozak CA et al. tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc Natl Acad Sci USA 1993; 90:9355–9358.

    Article  PubMed  CAS  Google Scholar 

  46. Dumont DJ, Gradwohl G, Fong GH et al. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 1994; 8:1897–1909.

    PubMed  CAS  Google Scholar 

  47. Davis S, Aldrich TH, Jones PF et al. Isolation of angiopoietin-1, a ligand for the angiogenic TIE2 receptor, by secretion-trap expression cloning. Cell 1996; 87:1161–1169.

    Article  PubMed  CAS  Google Scholar 

  48. Wang HU, Chen CF, Anderson DJ. Molecular distinction and angiogenic interaction of embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998; 93:741–753.

    Article  PubMed  CAS  Google Scholar 

  49. Adams RH, Wilkinson GA, Weiss C et al. Roles of ephrin-B ligands and EphB receptors in cardiovascular development: Demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 1999; 3:295–306.

    Google Scholar 

  50. Marron MB, Hughes DP, Edge MD et al. Evidence for heterotypic interaction between the receptor tyrosine kinases Tie-1 and Tie-2. J Biol Chem 2000; 275:39741–39746.

    Article  PubMed  CAS  Google Scholar 

  51. Ruhrberg C, Gerhardt H, Golding M et al. Spatially restricted patterning cues provided by haparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 2002; 16:2684–2698.

    Article  PubMed  CAS  Google Scholar 

  52. Tardy Y, Resnick N, Nagel T et al. Shear stress gradients remodel endothelial monolayers in vitro via a cell proliferation-migration-loss cycle. Arterioscler Thromb Vasc Biol 1997; 17:3102–3106.

    PubMed  CAS  Google Scholar 

  53. Sumpio BE, Du W, Galagher G et al. Regulation of PDGF-B in endothelial cells exposed to cyclic strain. Arterioscler Thromb Vasc Biol 1998; 18:349–355.

    PubMed  CAS  Google Scholar 

  54. Nagel T, Resnick N, Dewey Jr CF et al. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler Thromb Vasc Biol 1999; 19:1825–1834.

    PubMed  CAS  Google Scholar 

  55. Jin Z-G, Ueba H, Tanimoto T et al. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res 2003; 93:354–363.

    Article  PubMed  CAS  Google Scholar 

  56. Boo YC, Jo H. Flow-dependent regulation of endothgelial nitric oxide synthase: Role of protein kinases. Am J Physiol Cell Physiol 2003; 285:C4999–C508.

    Google Scholar 

  57. Rizzo V, Morton C, DePola N et al. Recruitment of endothelial caveolae into mechanotransduction pathways by flow-conditioning in vitro. Am J Physiol Heart Circ Physiol 2003; 285:H1720–H1729.

    PubMed  CAS  Google Scholar 

  58. Kawasaki K, Smith Jr RS, Hsieh CM et al. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 2003; 23:5726–5737.

    Article  PubMed  CAS  Google Scholar 

  59. Schwentker A, Billiar TR. Nitric oxide and wound repair. Surg Clin North Am 2003:83:521–530.

    Article  PubMed  Google Scholar 

  60. Lin Z, Chen S, Ye C et al. Nitric oxide synthase expression in human bladder cancer and its relation to angiogenesis. Urol Res 2003; 31:232–235.

    Article  PubMed  CAS  Google Scholar 

  61. Sundberg C, Kowanetz M, Brown LF et al. Stable expression of angiopoietin-1 and other markers by cultured pericytes: Phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab Invest 2002; 82:387–401.

    PubMed  CAS  Google Scholar 

  62. Gerety SS, Anderson DJ. Cardiovascular ephrin B2 function is essential for embryonic angiogenesis. Development 2002; 129:1397–1410.

    PubMed  CAS  Google Scholar 

  63. Davis S, Gale NW, Aldrich TH et al. Ligands for EPH-related receptor tyrosine kinases that require. membrane attachment or clustering for activity. Science 1994; 266:816–819.

    Article  PubMed  CAS  Google Scholar 

  64. Franco del Amo F, Smith DE, Swiatek PJ et al. Expression of Motch, a mouse homologue of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 1992; 115:737–745.

    CAS  Google Scholar 

  65. Krebs LT, Xue Y, Norton CR et al. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 2000; 14:1343–1352.

    PubMed  CAS  Google Scholar 

  66. Krüger O, Plum A, Kim J-S et al. Defective vascular development in connexin 45 deficient mice. Development 2000; 127:4179–4193.

    PubMed  Google Scholar 

  67. Chang C, Werb Z. The many faces of metalloproteases: Cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 2001; 11:S37–S43.

    PubMed  CAS  Google Scholar 

  68. Oh J, Takahashi R, Kondo S et al. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 2001; 107:789–800.

    Article  PubMed  CAS  Google Scholar 

  69. Connolly JO, Simpson N, Hewlett L et al. Rac regulates endothelial morphogenesis and capillary assembly. Mol Biol Cell 2002; 13:2474–2485.

    Article  PubMed  CAS  Google Scholar 

  70. Yamazaki D, Suetsugu S, Miki H et al. WAVE2 is required for directed cell migration and cardiovascular development. Nature 2003; 424:452–456.

    Article  PubMed  CAS  Google Scholar 

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Patan, S. (2005). How Is the Branching of Animal Blood Vessels Implemented?. In: Branching Morphogenesis. Molecular Biology Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/0-387-30873-3_6

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