Abstract
The cytoarchitecture of the walls of the bovine lateral ventricles was investigated by the use of immunocytochemistry. We defined three types of walls. Type 1 lined regions of white matter and had ciliated cuboidal ependyma, a few subependymal cells and a narrow subjacent glial layer. Type 2 lined the striatum and possessed ependymal cells with conspicuous basal processes that extended through a wide subependyma containing many subependymal cells and a wide subjacent glial network. Type 3 lined the rostral horn and displayed ependymal cells with the longest basal processes and wider subependymal and glial layers. Ependymal cells of type 2 and 3 walls were labelled with antibodies against S-100β protein, vimentin, GFAP, BLBP and nestin. Anti-βIII-tubulin stained small cells in the subependyma and inside the GFAP- and vimentin-positive subjacent glial network. Anti-PCNA-positive nuclei were abundant in the subependymal and glial layers of type 2 and 3 walls. DiI in vitro tracing studies revealed small bipolar cells in the glial layer at a distance from the site of the label deposit. These results suggest that neurogenesis takes place in adult bovine subependyma mostly in the walls of the striatum and the rostral horn, and that young neuroblasts may migrate in a rostro-ventral direction through the glial network.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alvarez-Buylla A, García-Verdugo JM, Mateo AS, Merchant-Larios H (1998) Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J Neurosci 18:1020–1037
Bernier PJ, Vinet J, Cossette M, Parent A (2000) Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2. Neurosci Res 37:67–78
Conover JC, Doetsch F, García-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3:1091–1097
Doetsch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 93:14895–14900
Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061
Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716
Götz M, Hartfuss E, Malatesta P (2002) Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 57:777–788
Hartfuss E, Galli R, Heins N, Götz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30
Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisén J (1999) Identification of a neural stem cell in the adult mammalian central nervous system Cell 96:25–34
Lendahl U, Zimmerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595
Leonhardt H (1980) Ependym und Circumventriculäre Organe. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen, IV/10. Neuroglia I. Springer, Berlin Heidelberg New York, pp 10–20
Lim DA, Tramontin AD, Trevejo JM, Herrera DG, García-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713–726
Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
Morshead CM, Kooy D van der (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249–256
Morshead CM, Reynolds BA, Craig CG, Mcburney MW, Staines WA, Morassutti D, Weiss S, Kooy D van der (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071–1082
Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22:3161–3173
Pérez-Martín M, Grondona JM, Cifuentes M, Pérez-Fígares JM, Jiménez JA, Fernández-Llebrez P (2000) Ependymal explants from the lateral ventricle of the adult bovine brain: a model system for morphological and functional studies of the ependyma. Cell Tissue Res 300:11–19
Pérez-Martín M, Cifuentes M, Grondona JM, Bermúdez-Silva FJ, Arrabal PM, Pérez-Fígares JM, Jiménez AJ, García-Segura LM, Fernández-Llebrez P (2003) Neurogenesis in explants from the walls of the lateral ventricle of adult bovine brain: role of endogenous IGF-1 as a survival factor. Eur J Neurosci17:205–211
RothJ, Lucocq JM, Charest PM (1984) Light and electron microscopic demonstration of sialic acid residues with the lectin from Limax flavus: a cytochemical affinity technique with the use of fetuin-gold complexes. J Histochem Cytochem 32:1167–1176
Rousselot P, Heintz N, Nottebohm F (1997) Expression of brain lipid binding protein in the brain of the adult canary and its implications for adult neurogenesis. J Comp Neurol 385:415–426
Thomas LB, Gates MA, Steindler DA (1996) Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 17:1-14
Tropepe V, Craig CG, Morshead CM, Kooy D van der (1997) Transforming growth factor-α null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17:7850–7859
Wei L-C, Shi M, Chen L-W, Cao R, Zhang P, Chan YS (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Dev Brain Res 139:9-17
Weickert CS, Webster MJ, Colvin SM, Herman MM, Hyde TM, Weinberger DR, Kleinman JE (2000) Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J Comp Neurol 423:359–372
Zimmer DB, Cronwall EH, Landar A, Song W (1995) The S100 protein family: history, function, and expression. Brain Res Bull 37:417–429
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by DGICYT (BFI2000-1360), FIS (01-0948, PI021517) and ISCIII (red CIEN, nodo Fundación Carlos Haya)
Rights and permissions
About this article
Cite this article
Rodríguez-Pérez, L.M., Pérez-Martín, M., Jiménez, A.J. et al. Immunocytochemical characterisation of the wall of the bovine lateral ventricle. Cell Tissue Res 314, 325–335 (2003). https://doi.org/10.1007/s00441-003-0794-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-003-0794-1