Anatomy and Embryology

, Volume 184, Issue 6, pp 559–569 | Cite as

Glial cell differentiation in neuron-free and neuron-rich regions

II. Early appearance of S-100 protein positive astrocytes in human fetal hippocampus
  • Mette Stagaard Janas
  • Richard S. Nowakowski
  • Kjeld Møllgård
Article
Accepted:

Summary

The development of the human fetal hippocampus and dentate gyros has been studied immunocytochemically. The first glial cells to appear are vimentin-positive radial glial cells. A gradual transition from vimentin to glial fibrillary acidic protein (GFAP) reactivity in the radial glial cells occurs at week 8. The GFAP-positive radial glial cells transform into astrocytes from week 14. A population of small S-100-positive somata which morphologically and spatially are distinct from GFAP-positive radial glial cells and their transformed progeny, are found as early as week 9.5 in the hippocampus during the period of peak neurogenesis. The well-defined immunoreactivity of the morphologically homogenous cell subpopulation for S-100 protein, which has been used as an astrocytic marker in the adult hippocampus, indicates that astrocytes may differentiate at very early gestational ages in human fetuses. The S-100-positive astrocytes are thought to be derived from ventricular zone cells, which at the time of their appearance do not express any of the applied astrocytic markers (S-100, GFAP, vimentin). It is suggested that the S-100-positive astrocytic cell population interacts with the first incoming projection fibers, so modulating the pattern of connectivity.

Key words

Glial cell precursors Dentate gyrus Immunocytochemistry GFAP Vimentin 
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References

  1. Altman J, Bayer SA (1975) Postnatal development of the hippocampal dentate gyrus under normal and experimental conditions. In: Isaacson RL, Pribram KH (eds) The hippocampus I. Structure and development. Plenum Press, New York, pp 95–119Google Scholar
  2. 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 103:613–616PubMedGoogle Scholar
  3. Borit A, McIntosh GC (1981) Myelin basic protein and glial fibrillary acidic protein in human fetal brain. Neuropathol Appl Neurobiol 7:279–287PubMedGoogle Scholar
  4. Boyes BE, Kim SLY, Lee V, Sung SC (1986) Immunohistochemical co-localization of S-100b and the glial fibrillary acidic protein in rat brain. Neuroscience 17:857–865PubMedGoogle Scholar
  5. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475PubMedGoogle Scholar
  6. Choi BH (1988) Developmental events during the early stages of cerebral cortical neurogenesis in man. A correlative light, electron microscopic, immunohistochemical and Golgi study. Acta Neuropathol 75:441–447PubMedGoogle Scholar
  7. Choi BH, Kim RC, Lapham LW (1983) Do radial glia give rise to both astroglial and oligodendroglial cells? Dev Brain Res 8:119–130Google Scholar
  8. Cocchia D (1981) Immunocytochemical localization of S-100 protein in the brain of adult rat. Cell Tissue Res 214:529–540PubMedGoogle Scholar
  9. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL (1988) Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10:684–692Google Scholar
  10. Donato R, Prestagiovanni B, Zelano G (1986) Identity between cytoplasmic and membrane-bound S-100 proteins purified from bovine and rat brain. J Neurochem 46:1333–1337PubMedGoogle Scholar
  11. Duffy CJ, Rakic P (1983) Differentiation of granule cell dendrites in the dentate gyrus of the rhesus monkey: a quantitative Golgi study. J Comp Neurol 214:224–237PubMedGoogle Scholar
  12. Eckenhoff MF, Rakic P (1984) Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 223:1–21PubMedGoogle Scholar
  13. Elder GA, Major EO (1988) Early appearance of type II astrocytes in developing human fetal brain. Dev Brain Res 42:146–150Google Scholar
  14. Engel AK, Müller CM (1989) Postnatal development of vimentin-immunoreactive radial glial cells in the primary visual cortex of the cat. J Neurocytol 18:437–450PubMedGoogle Scholar
  15. ffrench-Constant C, Raff MC (1986) The oligodendrocyte type-2 astrocyte cell lineage is specialized for myelination. Nature 323:335–338PubMedGoogle Scholar
  16. Frederiksen K, McKay RDG (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144–1151PubMedGoogle Scholar
  17. Gasser UE, Hatten ME (1990) Neuron-glia interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation. J Neurosci 10:1276–1285PubMedGoogle Scholar
  18. Goldman JE, Geier SS, Hirano M (1986) Differentiation of astrocytes and oligodendrocytes from germinal matrix cells in primary culture. J Neurosci 6:52–60PubMedGoogle Scholar
  19. Gordon-Weeks PR (1989) GAP-43 - What does it do in the growth cone? Trends Neurosci 12:363–365PubMedGoogle Scholar
  20. 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 18:427–436PubMedGoogle Scholar
  21. Hatten ME (1990) Riding the glial mono-rail: a common mechanism for glial guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13:179–184PubMedGoogle Scholar
  22. Hines M (1922) Studies of the growth and differentiation of the telencephalon in man. The fissura hippocampi. J Comp Neurol 34:73–171Google Scholar
  23. Hirano M, Goldman JE (1988) Gliogenesis in rat spinal cord: evidence for origin of astrocytes and oligodendrocytes from radial precursors. J Neurosci Res 21:155–167PubMedGoogle Scholar
  24. Hockheld S, McKay RDG (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 12:3310–3328Google Scholar
  25. Humphrey T (1966a) Correlations between the development of the hippocampal formation and the differentiation of the olfactory bulbs. Ala J Med Sci 3:235–269PubMedGoogle Scholar
  26. Humphrey T (1966 b) The development of the human hippocampal formation correlated with some aspects of its phylogenetic history. In: Hassler R, Stephan H (eds) Evolution of the forebrain. Plenum Press, New York, pp 104–116Google Scholar
  27. Hutchins JB, Casagrande VA (1989) Vimentin: changes in distribution during brain development. Glia 2:55–66PubMedGoogle Scholar
  28. Hutchins KD, Dickson DW, Rashbaum WK, Lyman WD (1990) Localization of morphologically distinct microglial populations in the developing human fetal brain: implications for ontogeny. Dev Brain Res 55:95–102Google Scholar
  29. Ishikawa H, Nogami H, Shirasawa N (1983) Novel clonal strains from adult rat anterior pituitary producing S-100 protein. Nature 303:711–713PubMedGoogle Scholar
  30. Kostović I, Seress L, Mrzljak L, Judag M (1989) Early onset of synapse formation in the human hippocampus. a correlation with Nissl-Golgi architectonics in 15- and 16.5-weeks-old fetuses. Neuroscience 30:105–116PubMedGoogle Scholar
  31. Landry CF, Ivy GO, Dunn RJ, Marks A, Brown IR (1989) Expression of the gene encoding theβ-subunit of S-100 protein in the developing rat brain analyzed by in situ hybridization. Mol Brain Res 6:251–262PubMedGoogle Scholar
  32. Lauriola L, Coli D, 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 37:251–255Google Scholar
  33. LeVine SM, Goldman JE (1988) Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci 8: 3992–4006PubMedGoogle Scholar
  34. 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 193:815–840PubMedGoogle Scholar
  35. Levitt P, Cooper ML, Rakic P (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci 1: 27–39PubMedGoogle Scholar
  36. 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 96:472–484PubMedGoogle Scholar
  37. Ludwin SK, Kosek JC, Eng LF (1976) The topographical distribution of S-100 and GFA proteins in the adult rat brain: an immunohistochemical study using horseradish peroxidase-labelled antibodies. J Comp Neurol 165:197–208PubMedGoogle Scholar
  38. Matus A, Mughal S (1975) Immunohistochemical localisation of S-100 protein in brain. Nature 258:746–748PubMedGoogle Scholar
  39. Møllgård K, Balslev Y (1989) The subcellular distribution of transferrin in rat choroid plexus studied with immunogold labelling of ultracryosections. Histochem J 21:441–448Google Scholar
  40. Nowakowski RS, Rakic P (1981) The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J Comp Neurol 196:129–154PubMedGoogle Scholar
  41. Rakic P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471–476PubMedGoogle Scholar
  42. Rakic P (1984) Emergence of neuronal and glial cell lineages in primate brain. In: Black IB (ed) Cellular and molecular biology of neuronal development. Plenum Press, New York, pp 29–50Google Scholar
  43. Rakic P, Nowakowski RS (1981) The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99–128PubMedGoogle Scholar
  44. Reske-Nielsen E, Oster S, Reintoft I (1987) Astrocytes in the prenatal central nervous system. Acta Pathol Microbiol Immunol Scand, Sect A 95:339–346Google Scholar
  45. Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264:449–479PubMedGoogle Scholar
  46. Roessmann U, Gambetti P (1986) Astrocytes in the developing human brain. Acta Neuropathol 70:308–313PubMedGoogle Scholar
  47. Rogers J (1989) Calcium-binding proteins: the search for functions. Nature 339:661–662Google Scholar
  48. Rolland B, Le Prince G, Fages C, Nunez J, Tardy M (1990) GFAP turnover during astroglial proliferation and differentiation. Dev Brain Res 56:144–149Google Scholar
  49. Sasaki A, Hirato J, Nakazato Y, Ishda Y (1988) Immunohistochemical study of the early human fetal brain. Acta NeuroPathol 76:128–134PubMedGoogle Scholar
  50. Schmechel DE, Rakic P (1979a) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Science 277:303–305Google Scholar
  51. Schmechel DE, Rakic P (1979b) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115–152PubMedGoogle Scholar
  52. Schmechel DE, Marangos PJ, Brightman M (1978) Neurone-specific enolase is a molecular marker for peripheral and central neuroendocrine cells. Nature 276:834–836PubMedGoogle Scholar
  53. Schmidt-Kastner R, Szymas J (1990) Immunohistochemistry of glial fibrillary acidic protein, vimentin and S-100 protein for study of astrocytes in hippocampus of rat. J Chem Neuroanat 3:179–192PubMedGoogle Scholar
  54. Seto-Ohshima A, Yamazaki Y,Kawamura N, Kitajuma S, Sano M, Mizutani A (1987) The early expression of immunoreactivity for calmodulin in the nervous system of mouse embryos. Histochemistry 86:337–343PubMedGoogle Scholar
  55. Shinohara H, Semba R, Kato K, Kashiwamata S, Tanaka O (1986) Immunohistochemical localization of gamma-enolase in early human embryos. Brain Res 282:33–38Google Scholar
  56. Stagaard M, Møllgård K (1989) The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry. Anat Embryol 180:17–28PubMedGoogle Scholar
  57. Stagaard M, Nowakowski RS, Møllgård K (1990) S-100 immuno-reactivity is differentially localized during the development of neuron-free and neuron-rich areas (abstract). Eur J Neurosci [Suppl 3]:223Google Scholar
  58. Stagaard Janas M, Nowakowski RS, Terkelsen OBF, Møllgård K (1991) Glial cell differentiation in neuron-free and neuron-rich regions. I. Selective appearance of S-100 protein in radial glial cells of the hippocampal fimbria in human fetuses. Anat Embryol 184:549–558PubMedGoogle Scholar
  59. Takahashi T, Misson JP, Caviness VS (1990) Glial process elongation and branching in the developing murine neocortex — a qualitative and quantitative immunohistochemical analysis. J Comp Neurol 302:15–28PubMedGoogle Scholar
  60. Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rode J (1983) PGP 9.5 — A new marker for vertebrate neurones and neuroendocrine cells. Brain Res 278:224–228PubMedGoogle Scholar
  61. Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74–88Google Scholar
  62. Wilkinson M, Hume R, Strange R, Bell JE (1990) Glial and neuronal differentiation in the human fetal brain 9–23 weeks of gestation. Neuropathol Appl Neurobiol 16:493–204Google Scholar
  63. Winningham-Major F, Staecker JL, Barger SW, Coats S, van Eldik LJ (1989) Neurite extension and neuronal survival activities of recombinant S100β proteins that differ in the content and position of cysteine residues. J Cell Biol 109:3063–3071Google Scholar
  64. Yakolev PL, Lecours A-R (1967) The myelogenetic cycles of regional maturation of the brain. In: Minowski A (ed) Regional development of the brain in early foetal life. Blackwell, London, pp 3–70Google Scholar
  65. Zuckerman JE, Herschman JR, Levine L (1970) Appearance of a brain specific antigen (the S-100 protein) during human foetal development. J Neurochem 17:247–251PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Mette Stagaard Janas
    • 1
  • Richard S. Nowakowski
    • 2
  • Kjeld Møllgård
    • 1
  1. 1.Institute of Medical Anatomy A, and Neuroscience Center, Panum InstituteUniversity of CopenhagenCopenhagen NDenmark
  2. 2.Department of Neuroscience and Cell Biology, University of Medicine and Dentistry of New JerseyRobert Wood Johnson Medical SchoolPiscatawayUSA

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