Summary
The neuroepithelial cells, which constitute the primordium of the CNS, are potentially capable of generating neuronal and glial cell lineages concomitantly. The appearance and morphological development of vimentin-positive neuroepithelial cells in human embryonic and fetal brain (4–16 weeks) were studied with immunocytochemistry. In embryos aged 4–6 weeks, vimentin-reactivity was seen in all neuroepithelial cells, including those which exhibited mitotic figures. The distribution of reactivity changed according to a general developmental pattern, which commenced and proceeded temporally different in various regions of the CNS. All regions exhibited vimentin-positive neuroepithelial cells, the distribution and morphology of which gradually changed, resulting in lamination of the neural wall into two and subsequently three layers. The neocortex and midline raphe were the only regions to differ significantly from the general pattern. When reactivity to glial fibrillary acidic protein developed at 7–8 weeks, the distribution was very much like that of vimentin at the same stage. Reactivity to glial, neuronal and other cellular markers (S-100, neurofilament, neuron specific enolase, desmin, and cytokeratin) revealed different distributions. Although cells retaining vimentin beyond the ventricular zone stage are radial glial cells and presumptive fibrous astrocytes, it seems unlikely that vimentin is a marker for a distinct cell lineage during early CNS development. It is suggested that all neuroepithelial cells in vivo differentiate to a stage where they express vimentin, and that vimentin may have a functional role in cellular movements and during the interkinetic nuclear migration.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alvarez-Buylla A, Buskirk DR, Nottebohm F (1987) Monoclonal antibody reveals radial glia in adult avian brain. J Comp Neurol 264:159–170
Antanitus DS, Choi BH, Lapham LW (1976) The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence. Brain Res 103:613–616
Bennett GS, Lullo S (1985) Transient expression of a neurofilament protein by replicating neuroepithelial cells of the embryonic chick brain. Dev Biol 107:107–127
Bignami A, Raju T, Dahl D (1982) Localization of vimentin, the nonspecific intermediate filament protein in embryonal glia and in early differentiating neurons. Dev Biol 91:286–295
Bovolenta P, Liem RKH, Mason CA (1984) Development of cerebellar astroglia: Transition in form and cytoskeletal content. Dev Biol 102:248–259
Boulder Comittee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–261
Buse E (1987) Ventricular cells from the mouse neural plate, Stage Theiler 12, transform into different neuronal cell classes in vitro. Anat Embryol 176:295–302
Choi BH (1981) Radial glia of developing human fetal spinal cord: Golgi, immunohistochemical and electron microscopic study. Dev Brain Res 1:249–267
Choi BH, Lapham LW (1978) Radial glia in the human fetal cerebrum: A combined Golgi, immunofluorescent and electron microscopic study. Brain Res 148:295–311
Choi BH, Lapham LW (1980) Evolution of Bergmann glia in developing human fetal cerebellum: A Golgi, electron microscopic and immunofluorescent study. Brain Res 190:369–383
Cochard P, Paulin D (1984) Initial expression of neurofilaments and vimentin in the central and peripheral nervous system of the mouse embryo in vivo. J Neurosci 4:2080–2094
Dahl D (1981) The vimentin-GFA transition in rat neuroglia cytoskeleton occuurs at the time of myelination. J Neurosci Res 6:741–748
Dahl D, Ruegger DC, Bignami A, Weber K, Osborn M (1981) Vimentin, the 57000 dalton protein of fibroblast filament, is the major cytoskeletal component in immature glia. Eur J Cell Biol 24:191–196
Dahl D, Zapatka S, Bignami A (1986) Heterogeneity of desmin, the muscle-type intermediate filament protein, in blood vessels and astrocytes. Histochem 84:145–150
Erickson CA, Tucker RP, Edwards BF (1987) Changes in the distribution of intermediate filament types in Japanese quail embryos during morphogenesis. Differentiation 34:88–97
Franke WW, Schmid E, Osborn M, Weber K (1978) Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci USA 75(10):5034–5038
Hansen SH, Stagaard M, Møllgård K (1989) Neurofilament-like pattern of reactivity in human foetal PNS and spinal cord following immunostaining with polyclonal anti-glial fibrillary acidic protein antibodies J Neurocytol 18: (In press)
Hatten ME, Liem RKH, Mason CA (1984) Two forms of cerebellar glial cells interact differently with neurons in vitro. J Cell Biol 98:193–204
Hinds JW, Ruffet TL (1971) Cell proliferation in the neural tube: an electron microscopic and Golgi analysis in the mouse cerebral vesicle. Z Zellforsch 115:226–264
His W (1889) Die Neuroblasten und deren Entstehung im embryonal Marke. Abh Math Phys Cl Kgl Sach Ges Wiss 15:313–372
Hockfield S, McKay RDG (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310–3328
Houle J, Fedoroff S (1983) Temporal relationship between the appearance of vimentin and neural tube development. Dev Brain Res 9:189–195
Hudspeth AJ, Yee AG (1973) The intercellular junctional complexes of retinal pigment epithelia. Invest Ophthalmol 12:354–365
Kasper M, Goertchen R, Stosiek P, Perry G, Karsten U (1986) Coexistence of cytokeratin, vimentin and neurofilament protein in human choroid plexus. An immunohistochemical study of intermediate filaments in neuroepithelial tissues. Virchows Arch [A] 410:173–177
Kasper M, Moll R, Stosiek P, Karsten U (1988) Patterns of cytokeratin and vimentin expression in the human eye. Histochem 89:369–377
Lauriola L, Coli A, Cocchia D, Tallini G, Michetti F (1987) Comparative study by S-100 and GFAP immunohistochemistry of glial cell populations in the early stages of human spinal cord development. Dev Brain Res 37:251–255
Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing Rhesus monkey brain. J Comp Neurol 193:815–840
Levitt P, Cooper ML, Rakic P (1983) Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone. Dev Biol 96:472–484
Lidov HGW, Molliver ME (1982) An immunohistochemical study of seretonin neuron development in the rat: Ascending pathways and terminal fields. Brain Res Bull 8:389–430
Marin-Padilla M (1983) Structural organization of the human cerebral cortex prior to appearance of the cortical plate. Anat Embryol 168:21–40
Møllgård K, Jacobsen M (1984) Immunohistochemical identification of some plasma proteins in human embryonic and fetal forebrain with particular reference to the development of the neocortex. Dev Brain Res 13:49–63
Møllgård K, Balslev Y, Lauritzen B, Saunders NR (1987) Cell junctions and membrane specializations in the ventricular zone (germinal matrix) of the developing sheep brain: a CSF-brain barrier. J Neurocytol 16:433–444
Osborn M, Debus E, Weber K (1984) Monoclonal antibodies specific for vimentin. Eur J Cell Biol 34:137–143
Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303:390–396
Rakic P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471–476
Rakic P (1981a) Developmental events leading to laminar and areal organization of the neocortex. In: Schmitt FO (ed) The organization of the cerebral neocortex. MIT Press, Cambridge Massachusetts London, pp 6–16
Rakic P (1981b) Neuronal-glial interaction during brain development. Tr Neurosci 7:184–187
Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264:449–479
Reske-Nielsen E, Oster S, Reintoft I (1987) Astrocytes in the prenatal central nervous system. Acta Pathol Microbiol Immunol Scand Sect A 95:339–346
Roessmann U, Gambetti P (1986) Astrocytes in the developing human brain. An immunohistochemical study. Acta Neuropathol 70:308–313
Sasaki A, Hirato J, Nakazato Y, Ishda Y (1988) Immunohistochemical study of the early human fetal brain. Acta Neuropathol 72:128–134
Sauer FC (1936) The interkinetic migration of embryonic epithelial nuclei. J Morphol 60:1–11
Schnitzer J, Franke WW, Schachner M (1981) Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J Cell Biol 90:435–447
Shinohara H, Semba R, Kato K, Kashiwamata S, Tanaka O (1986) Immunohistochemical localization of gamma-enolase in early human embryos. Brain Res 282:33–38
Szaro BG, Gainer H (1988) Immunocytochemical identification of non-neuronal intermediate filament proteins in the developing Xenopus laevis nervous system. Dev Brain Res 43:207–224
Tapscott SJ, Bennett GS, Toyama Y, Kleinbart F, Holtzer H (1981) Intermediate filament proteins in the developing chick spinal cord. Dev Biol 86:40–54
van Hartesveldt C, Moore B, Hartman BK (1986) Transient midline raphe glial structure in developing rat. J Comp Neurol 153:175–184
Varon SS, Somjen GG (1979) Neuron-glia interactions. Neurosciences Res Prog Bull, vol 17, No 1
Viebahn C, Lane EB, Ramaekers FCS (1988) Keratin and vimentin expression in early organogenesis of the rabbit embryo. Cell Tissue Res 253:553–562
Windle WF (1970) Development of neural elements in human embryos of four to seven weeks gestation. Exp Neurol [Suppl] 5:44–70
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Stagaard, M., Møllgård, K. The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry. Anat Embryol 180, 17–28 (1989). https://doi.org/10.1007/BF00321896
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00321896