Abstract
Intraventricular transplants of neural tissues were performed in ovo from embryo to embryo. Fragments of the nervous wall of the optic lobe (tectum) from 14-day chick or 12-day quail embryos (donor) were inserted into the ventricle of the right optic lobe of 6-day chick or 5-day quail embryos (host). Chick-to-chick, chick-to-quail and quail-to-chick grafts were carried out. The vascularization changes occurring in the host tectum and in the grafted neural tissues were analysed under light, transmission, and scanning electron microscopes and by morphometric methods. In the host embryo tectum, the neural graft stimulates a statistically significant increment in vessel density and a vessel sprouting into the ventricle of the optic lobe. The vascular sprouts reach the transplanted tissue and establish connections with its native microvasculature. The chick-to-quail and quail-to chick grafts, submitted to immunoreaction with a quailspecific antibody which recognizes an antigen (MB1) present on endothelial cells, indicate that re-establishment of the circulation in the graft depends upon anastomoses between host and donor vasculatures and the rapid new growth of host-derived and donor-native vessels. The presence of macrophage-like cells escorting the new-growing vessels suggests that these cells are involved in the host and donor tissue angiogenesis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahlskog JE, Tyce GM, Kelly PJ, Heerden JA van, Stoddard SL, Carmichael SW (1989) Cerebrospinal fluid indices of blood-brain barrier permeability following adrenal-brain transplantation in patients with Parkinson's disease. Exp Neurol 105:152–161
Anagnostopoulos J, Knoth R, Duffner T, Klein PJ, Volk B (1987) Vascularization of fetal cerebellar tissue transplanted into the striatum of adult rats. In: Cervós-Navarro JE, Ferszt R (eds) Stroke and microcirculation. Raven Press, New York, pp 171–177
Ausprunk DH, Knighton DR, Folkman J (1975) Vascularization of normal and neoplastic tissues grafted to the chick chorioallantois. Am J Pathol 79:597–618
Bär T (1980) The vascular system of the cerebral cortex. Adv Anat Embryol Cell Biol 59:1–62
Bertossi M, Riva A, Virgintino D, Roncali L (1992) A correlative SEM/TEM examination of the endothelium surface in neural capillaries. J Submicrosc Cytol Pathol 24:215–224
Björklund A, Stenevi U (1979) Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplant. Brain Res 177:555–560
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
Brightman MW (1992) Ultrastructure of brain endothelium. In: Bradbury MWB (ed) Handbook of experimental pharmacology. Physiology and pharmacology of the blood-brain barrier, vol 103. Springer, Berlin Heidelberg New York, pp 1–22
Broadwell RD (1988) Absence of a blood-brain barrier within transplanted brain tissue? Science 241:473
Broadwell RD, Charlton HM, Ganong WF, Salcman M, Sofroniew M (1989) Allografts of CNS tissue possess a blood-brain barrier. I. Grafts of medial preoptic area in hypogonadal mice. Exp Neurol 105:135–151
Cuadros MA, Coltey P, Nieto MC, Martin C (1992) Demonstration of a phagocytic cell system belonging to the hemopoietic lineage and originating from the yolk sac in the early avian embryo. Development 115:157–168
Cuadros MA, Martin C, Coltey P, Almendros A, Navascués J (1993) First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J Comp Neurol 330:113–129
D'Amore PA, Klagsbrun M (1989) Angiogenesis. Factors and mechanisms. In: Sirica AE (ed) The pathobiology of neoplasia. Plenum Press, New York, pp 513–531
Elias H, Hyde DM (1983) Stereological measurements of isotropic structures. In: Elias H, Hyde DM (eds) A guide to practical stereology. Karger, Basel, pp 25–44
Hallas BH, Das GD, Das KG (1980) Transplantation of brain tissue in the rat brain. II. Growth characteristics of neocortical transplants in hosts of different ages. Am J Anat 158:147–159
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Hansen JT, Gash DM (1991) Functional aspects of mammalian neural transplantation. Neurobiology 6:79–98
Klausen BS, Swenson RS, Zimmer J, Castro AJ (1992) Fetal neocortical transplants in rats: blood-brain barrier development and partial permeability to IgG in long-surviving grafts. Restor Neurol Neurosci 4:393–400
Knighton DR, Hunt TK, Schevenstuhl H, Halliday BJ, Werb Z, Banda MJ (1983) Oxygen tension regulates the expression of angiogenesis factor by macrophages. Science 221:1283–1285
Krum JM, Rosenstein JM (1985) Temporal sequence of angiogenesis in neural transplant models. Soc Neurosci Abs 15:1149
Krum JM, Rosenstein JM (1987) Patterns of angiogenesis in neural transplant models. I. Autonomic tissue transplants. J Comp Neurol 258:420–434
Krum JM, Rosenstein JM (1988) Patterns of angiogenesis in neural transplant models. II. Fetal neocortical transplants. J Comp Neurol 271:331–345
Krum JM, Rosenstein JM (1989) The fine structure of vascular-astroglial relations in transplanted fetal neocortex. Exp Neurol 103:203–212
LaVail JH, Cowan WM (1971) The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res 28:391–419
Leigh K, Elisevich K, Rogers KA (1994) Vascularization and microvascular permeability in solid versus cell-suspension embryonic neural grafts. J Neurosurg 81:272–283
Mancini L, Bertossi M, Ribatti D, Bartoli F, Nico B, Lozupone E, Roncali L (1991) The effects of long-term hypoxia on epicardium and myocardium in developing chick embryo hearts. Int J Microcirc Clin Exp 10:359–371
Martin-Partido C, Cuadros MA, Martin C, Coltey P, Navascues J (1991) Macrophage-like cells invading the suboptic necrotic centres of the avian embryo diencephalon originate from haemopoietic precursors. J Neurocytol 20:962–968
Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Møller 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
Naradzay JFX, Rosenstein JM (1989) Vascular morphology and permeability in fetal CNS grafts to the renal capsule. Exp Neurol 104:284–291
Pannese E (1994) The neuroglial cells of the central nervous system. In: Neurocytology. Fine structure of neurons, nerve processes, and neuroglial cells. Thieme, Stuttgart, pp 156–189
Peault BM, Thiery JP, Le Douarin N (1983) Surface marker for hemopoietic and endothelial cell lineages in quail that is defined by a monoclonal antibody. Proc Natl Acad Sci USA 80:2976–2980
Perlow MF, Freed WF, Hoffer BJ, Seiger A, Olson L, Wyatt RJ (1979) Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science 204:643–647
Poltorak M, Freed WJ (1988) Cerebellar allografts in brain of Quaking mice. Exp Brain Res 71:163–170
Poltorak M, Freed WJ, Sternberger LA, Sternberger NH (1988) A comparison of intraventricular and intraparenchymal cerebellar allografts in rat brain: evidence for normal phosphorylation of neurofilaments. J Neuroimmunol 20:63–72
Ribatti D, Mancini L, Roncali L, Nico B, Bertossi M (1989) Morphometric analysis on the effects of the hypoxia during the central nervous system vasculogenesis. Int J Microcirc Clin Exp 8:135–142
Risau W (1986) Developing brain produces an angiogenesis factor. Proc Natl Acad Sci USA 83:3855–3859
Risau W, Gautschi-Sova P, Bohlen P (1988) Endothelial cell growth factors in the embryonic and adult chick brain are related to human acidic fibroblast growth factor. EMBO J 7:959–962
Roncali L, Ribatti D, Ambrosi G (1985a) Vasculogenesis in the chick embryo optic tectum. Acta Anat 122:299–234
Roncali L, Ribatti D, Ambrosi G (1985b) Ultrastructural basis of the vessel wall differentiation in the chick optic tectum. J Submicrosc Cytol 17:83–88
Roncali L, Nico B, Ribatti D, Bertossi M, Mancini L (1986) Microscopical and ultrastructural investigations on the development of the blood-brain barrier in the chick embryo optic tectum. Acta Neuropathol (Berl) 70:193–201
Rosenstein JM (1987a) Neocortical transplants in the mammalian brain lack a bood-brain barrier to macromolecules. Science 235:772–774
Rosenstein JM (1987b) Adrenal medulla grafts produce blood brain barrier dysfunction. Brain Res 414:192–196
Rosenstein JM (1988) Absence of a blood-brain barrier within transplanted brain tissue. A response. Science 241:473–474
Rosenstein JM (1991) Permeability to a blood-borne protein and HGABA in CNS tissue grafts. I. Intraventricular grafts. J Comp Neurol 305:676–690
Rosenstein JM, Brightman MW (1978) Intact cerebral ventricle as a site for tissue transplantation. Nature 275:83–85
Rosenstein JM, Brightman MW (1986) Alterations of the blood brain barrier after transplantation of autonomic ganglia into the mammalian central nervous system. J Comp Neurol 250:339–352
Rosenstein JM, Phillips TM (1988) Blood-brain and blood-cere-brospinal fluid alterations following neural transplantation. Prog Brain Res 78:297–302
Stewart PA, Wiley MJ (1981) Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev Biol 84:183–192
Stewart PA, Clements LG, Wiley MJ (1984) Revascularization of skin transplanted into the brain: source of the graft endothelium. Microvasc Res 28:113–124
Sunderkotter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C (1994) Macrophages and angiogenesis. J Leukoc Biol 55:410–422
Swenson RS, Shaw P, Alones V, Kozlowski G, Zimmer J, Castro AJ (1989) Neocortical transplants grafted into the newborn rat brain demonstrate a blood-brain barrier to macromolecules. Neurosci Lett 100:35–39
Thomas WE (1992) Brain macrophages: evaluation of microglia and their functions. Brain Res Rev 17:61–74
Thompson WG (1890) Successful brain grafting. N Y Med J 51:701–702
Triahou LD, Cerro M del, Herndon RM (1985) Ultrastructural evidence for phagocytosis by oligodendroglia. Neurosci Lett 53:185–189
Vinores SA, Herman MM (1993) Phagocytosis of myelin by astrocytes in expiants of adult rabbit cerebral white matter maintained on Gelfoam matrix. J Neuroimmunol 43:169–176
Virgintino D, Ribatti D, Nico B, Bertossi M, Roncali L (1992) Vascular supply in embryonic neural transplants. In: Steiner R, Weisz PB, Langer R (eds) Angiogenesis. Birkhäuser Verlag, Basel, pp 69–73
Woerly S, Marchand R (1990) 100 ans de neurotransplantation chez les mammifères. J Neurochirurgie 36:71–95
Wu W, Scott DE, Miller E (1990) Transplantation of the pineal gland in the mammalian third cerebral ventricle. Exp Neurol 108:23–32
Zacchei AM (1961) The embryonic development of the Japanese quail, Coturnix coturnix japonica (in Italian). Arch Ital Anat Embriol 66:36–62
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Roncali, L., Virgintino, D., Coltey, P. et al. Morphological aspects of the vascularization in intraventricular neural transplants from embryo to embryo. Anat Embryol 193, 191–203 (1996). https://doi.org/10.1007/BF00198323
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00198323