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Development and Differentiation of Blood Vessels in the Central Nervous System

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Neuroendocrinology

  • 139 Accesses

Abstract

The central nervous system (CNS) develops from a pseudostratified ectodermal epithelium containing neuroblasts and glioblasts. Other constituents (microglia, blood vessels) are of mesodermal origin and successively invade the neuroectoderm. Using chick-quail chimeras it is possible to study the interaction between neuroectodermal and mesodermal cells. Vascular endothelial cells start invading the CNS of birds at about day 3.5 of development. They originate from the paraxial mesoderm of the head and the trunk. Thereafter, smooth muscle cells migrate along the endothelial routes. Neuroectodermal cells secrete vascular endothelial growth factor (VEGF), which is a highly specific angiogenic and chemoattractive factor. Angioblast and endothelial cells in the paraxial mesoderm are characterized by the expression of VEGF-receptor-2. Except for the choroid plexus, VEGF and VEGF receptors are not expressed in the adult brain. The organ-typical differentiation of endothelial cells in the CNS depends on interactions with local neuroectodermal cells. Development of blood-brain barrier characteristics are obviously due to inductive signals from astrocytes. In contrast, the epithelial cells of the choroid plexus induce development of highly permeable, fenestrated capillaries. Constitutive expression of VEGF and its receptors in the choroid plexus (and the kidney glomeruli) may serve as the basis for high permeability. VEGF has been shown to increase vascular permeability in a highly potent manner.

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References

  • Bouldin TW, Krigman MR (1975) Differential permeability of cerebral capillary and choroid plexus to lanthanum ion. Brain Res 99: 444–448

    Article  PubMed  CAS  Google Scholar 

  • Breier G, Albrecht U, Sterrer S, Risau W (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114: 521–532

    PubMed  CAS  Google Scholar 

  • Brightman MW (1967) Intracerebral movements of proteins injected into the blood and cerebrospinal fluid. Anat Ree 157: 219

    Google Scholar 

  • Castel M, Sahar A, Erlij D (1974) The movement of lanthanum across diffusion barriers in the choroid plexus of the cat. Brain Res 67: 178–184

    Article  PubMed  CAS  Google Scholar 

  • Couly G, Coltey P, Eichmann A, Le Douarin NM (1995) The angiogenic potentials of the cephalic mesoderm and the origin of brain and head blood vessels. Mech Dev 53: 97–112

    Article  PubMed  CAS  Google Scholar 

  • De Bault LE, Cancilla PA (1980) γ-glutamyl transpeptidase in isolated brain endothelial cells:induction by glial cells in vitro. Science 207: 653–655

    Article  Google Scholar 

  • Delorme P, Gayet J, Grignon G (1970) Ultrastructural study on trans-capillary exchange in the developing telencephalon of the chicken. Brain Res 22: 269–283

    Article  PubMed  CAS  Google Scholar 

  • Dermietzel R, Melier K, Tetzlaff W, Waeisch M (1977) In vivo and in vitro formation of the junctional complex in choroid epithelium. A freeze-etching study. Cell Tissue Res 181: 427–441

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich P (1885) Das Sauerstoff-Bedürfnis des Organismus. Eine farbenanalytische Studie. Habilitationsschrift. A. Hirschwald, Berlin

    Google Scholar 

  • Eichmann A, Marcelle C, Bréant C, Le Douarin NM (1993) Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev 42: 33–48

    Article  PubMed  CAS  Google Scholar 

  • Feder N, Reese TS, Brightman MW (1969) Microperoxidase, a new tracer of low molecular weight. A study of the interstitial compartements of the mouse brain. J Cell Biol 43: 35a-36a

    Google Scholar 

  • Feeney JF jr, Watterson RL (1946) The development of the vascular pattern within the walls of the central nervous system of the chick embryo. J Morphol 78: 231–304

    Article  PubMed  Google Scholar 

  • Flamme I, Breier G, Risau W (1995) Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 169: 699–712

    Article  PubMed  CAS  Google Scholar 

  • Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66–70

    Article  PubMed  CAS  Google Scholar 

  • Goldmann EE (1913) Vitalfarbung am Zentralnervensystem. Abh Preuss Akad. Wiss Phys-Math 1: 1–60

    Google Scholar 

  • Holash JA, Noden DM, Stewart PA (1993) Re-evaluating the role of astrocytes in blood-brain barrier induction. Dev Dynam 197: 14–25

    Article  CAS  Google Scholar 

  • Janzer RC, Raff MC (1987) Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325: 253–257

    Article  PubMed  CAS  Google Scholar 

  • 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: 290–298

    PubMed  CAS  Google Scholar 

  • Kurz H, Gärtner T, Eggli PS, Christ B (1996) First blood vessels in the avian neural tube are formed by a combination of dorsal angioblast immigration and ventral sprouting of endothelial cells. Dev Biol 173: 133–147

    Article  PubMed  CAS  Google Scholar 

  • Lewandowsky M (1900) Zur Lehre von der Cerebrospinalflüssigkeit. Z Klin Med 40: 480–494

    Google Scholar 

  • Melier K, Wechsler W (1965) Elektronenmikroskopische Untersuchungen der Entwicklung der telencephalen Plexus choroides des Huhnes. Z Zellforsch 65: 420–444

    Article  Google Scholar 

  • Meyer J, Rauti J, Galla HJ (1991) The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferate state. J Neurochem 57: 1971–1977

    Article  PubMed  CAS  Google Scholar 

  • Milhorat TH, Davis DA, Lloyd BT jr (1973) Two morphologically distinct blood-brain barriers preventing entry of cytochrome C into cerebrospinal fluid. Science 180: 76–78

    Article  CAS  Google Scholar 

  • Millauer B, Wizigmann-Voos S, Schnürch H, Martinez R, Moller NPH, Risau W, Ullrich A (1993) High affinity VEGF binding and developmental expression suggest flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72: 835–846

    Article  PubMed  CAS  Google Scholar 

  • Noden DM (1991) Origins and patterning of avian outflow tract endocardium. Development 111: 867–876

    PubMed  CAS  Google Scholar 

  • Oh S-J, Jeltsch MM, Birkenhäger R, McCarthy JEG, Weich HA, Christ B, Alitalo K, Wilting J (1997) VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol 188: 96–109

    Article  PubMed  CAS  Google Scholar 

  • Plate KH, Breier G, Weich HA, Risau W (1992) Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359: 845–848

    Article  PubMed  CAS  Google Scholar 

  • Reese TS, Karnowsky MJ (1967) Fine structural localisation of a blood brain barrier to exogenous peroxidase. J Cell Biol 34: 207–217

    Article  PubMed  CAS  Google Scholar 

  • Risau W (1994). Molecular biology of blood-brain-barrier ontogenesis and function. (Review). Acta Neurochirurgica (Suppl) 60: 109–112

    PubMed  CAS  Google Scholar 

  • Saunders NR (1992) Ontogenic development of brain barrier mechanisms. In: Bradbury MWB (ed)Handbook of experimental pharmacology. Springer, Berlin Heidelberg New York, pp 327–369

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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: 62–66

    Article  PubMed  CAS  Google Scholar 

  • Stewart PA, Wiley MJ (1981) Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells. Dev Biol 84: 183–192

    Article  PubMed  CAS  Google Scholar 

  • Strong LH (1961) The first appearance of vessels within the spinal cord of the mammal: their developing patterns as far as partial formation of the dorsal septum. Acta Anat 44: 80–108

    Article  Google Scholar 

  • Wakai S, Hirokawa N (1978) Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tissue Res 195: 195–203

    Article  PubMed  CAS  Google Scholar 

  • Wakai S, Hirokawa N (1981) Development of blood-cerebrospinal fluid barrier to horseradish peroxidase in the avian choroidal epithelium. Cell Tissue Res 214: 271–278

    Article  PubMed  CAS  Google Scholar 

  • Wilting J (1988) Ultrastrukturelle und funktionelle Untersuchungen der Entwicklung des Plexus choroideus bei Vogelchimären. Dissertationsarbeit, Ruhr-Universität Bochum

    Google Scholar 

  • Wilting J, Christ B (1989) An experimental and ultrastructural study on the development of the avian choroid plexus. Cell Tissue Res 255: 487–494

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Christ B (1996) Embryonic angiogenesis: a review. Naturwissenschaften 83: 153–164

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Christ B, Weich HA (1992) The effects of growth factors on the day 13 chorioallantoic membrane (CAM): a study of VEGF165 and PDGF-BB. Anat Embryol 186: 251–257

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Brand-Saberi B, Huang R, Zhi Q, Köntges G, Ordahl CP, Christ B (1995a) Angiogenic potential of the avian somite. Dev Dynam 202: 165–171

    Article  CAS  Google Scholar 

  • Wilting J, Ebensperger C, Müller TS, Koseki H, Wallin J, Christ B (1995b) Paxl in the development of the cervico-occipital transitional zone. Anat Embryol 192: 221–227

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Birkenhäger R, Eichmann A, Kurz H, Martiny-Baron G, Marme D, McCarthy JEG, Christ B, Weich HA (1996) VEGF121 induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of the chorioallantoic membrane. Dev Biol 176: 76–85

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Eichmann A, Christ B (1997) Expression of the avian VEGF receptor homologues Quekl and Quek2 in blood-vascular and lymphatic endothelial and non-endothelial cells during quail embryonic development. Cell Tissue Res 288: 207–223

    Article  PubMed  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Anatomisches Institut II, Albert-Ludwigs-Universität, Albertstraße 17, D-79104, Freiburg, Germany

    J. Wilting

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  1. J. Wilting
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Editors and Affiliations

  1. Dr. Senckenbergische Anatomie, Klinikum der J.W. Goethe-Universität, Theodor-Stern-Kai 7, D-60590, Frankfurt/Main, Germany

    Horst-Werner Korf

  2. Medizinische Klinik I, Klinikum der J.W. Goethe-Universität, Theodor-Stern-Kai 7, D-60590, Frankfurt/Main, Germany

    Klaus-Henning Usadel

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© 1997 Springer-Verlag Berlin Heidelberg

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Wilting, J. (1997). Development and Differentiation of Blood Vessels in the Central Nervous System. In: Korf, HW., Usadel, KH. (eds) Neuroendocrinology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60915-2_22

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  • DOI: https://doi.org/10.1007/978-3-642-60915-2_22

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64605-8

  • Online ISBN: 978-3-642-60915-2

  • eBook Packages: Springer Book Archive

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