Advertisement

Anatomy and Embryology

, Volume 184, Issue 6, pp 549–558 | Cite as

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
  • Mette Stagaard Janas
  • Richard S. Nowakowski
  • Ole B. F. Terkelsen
  • Kjeld Møllgård
Article

Summary

The proliferative cells of the developing hippocampal fiber tract fimbria have only the potential for gliogenesis; thus the developing fimbria provides an ideal model for the study of the development and differentiation of its constituent glial cells. In the first stage of development, the fimbrial primordium can be distinguished morphologically, and during the second stage, the fimbria becomes a well-defined fiber tract. In the third stage, a divergent immunocytochemical staining pattern clearly demarcates the neuron-free fimbria from the hippocampus, where a mixed neuro- and gliogenesis occurs. The distinct expression of S-100 protein in radial glial cells is restricted to the fimbria. During the final stage of development, the ventricular lining of the fimbria will mature into an ependyma. It is suggested that the S-100-positive radial glial cells of the fimbria, which probably retain their proliferative capacity, represent a homogeneous population of precursor cells that will give rise to the glial cells of the adult fimbria. The appearance of S-100 in the fimbria' radial glial cells seems to occur coincidentally with the establishment of hippocampal commissural connections. The S-100-positive radial glial cells of the fimbria may guide and segregate populations of growing axons by providing physical and chemical cues. Thus, S-100 protein per se seems to be intimately involved in modulation and regulation of axonal growth and patterning.

Key words

Glial cell precursors Astrocytes Hippocampus Axon guidance Glioepithelium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

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. Altman J, Bayer SA (1990 a) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325–342PubMedGoogle Scholar
  3. Altman J, Bayer SA (1990b) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum-pyramidale. J Comp Neurol 301:343–364PubMedGoogle Scholar
  4. Altman J, Bayer SA (1990c) Vertical compartmentation and cellular transformation in the germinal matrices of the embryonic rat cerebral cortex. Exp Neurol 107:23–35PubMedGoogle Scholar
  5. Arroyo-Guijarro J, Prats-Galino A, Costa-Llobet C, Ruano-Gil D (1987) Aspects of the glia in the fimbria of the fighting bull's hippocampus. Arch Ital Anat Embryol 92:103–114Google Scholar
  6. Bayer SA, Altman J (1974) Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 158:55–80PubMedGoogle Scholar
  7. Bayer SA, Altman J (1975) Radiation-induced interference with postnatal hippocampal cytogenesis in rats and its long-term effects on the acquisition of neurons and glia. J Comp Neurol 163:1–20PubMedGoogle Scholar
  8. Bignami A, Dahl D (1982) Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J Comp Neurol 153:27–38Google Scholar
  9. de Blas AL (1984) Monoclonal antibodies to specific astroglial and neuronal antigens reveal the cytoarchitecture of the Bergmann glia fibers in the cerebellum. J Neurosci 4:265–273PubMedGoogle Scholar
  10. Boulder Committee (1970) Embryonic vertebrate central nervous system. Revised terminology. Anat Rec 166:257–261Google Scholar
  11. Bovolenta P, Liem RKH, Mason CA (1984) Development of cerebellar astroglia: transitions in form and cytoskeletal content. Dev Biol 102:248–259PubMedGoogle Scholar
  12. Buchhalter JR, Fieles A, Dichter MA (1990) Hippocampal commissural connections in the neonatal rat. Dev Brain Res 56:211–216Google Scholar
  13. Choi BH, Kim RC, Lapham LW (1983) Do radial glia give rise to both atroglial and oligodendroglial cells? Dev Brain Res 8:119–130Google Scholar
  14. Cocchia D (1981) Immunocytochemical localization of S-100 protein in the brain of adult rat. Cell Tissue Res 214:529–540PubMedGoogle Scholar
  15. 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
  16. Dahl D (1981) The vimentin-GFA transition in rat neuroglia cytoskeleton occurs at the time of myelination. J Neurosci Res 6:741–748PubMedGoogle Scholar
  17. Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Møllgård K, Belin MF (1986) Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, non-specialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245:343–351PubMedGoogle Scholar
  18. Dupouey P, Benjelloun S, Gomes D (1985) Immunohistochemical demonstration of an organized cytoarchitecture of the radial glia in the CNS of the embryonic mouse. Dev Neurosci 7:81–93PubMedGoogle Scholar
  19. 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
  20. Eckenhoff MF, Rakic P (1988) Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729–2747PubMedGoogle Scholar
  21. Elder GA, Major EO (1988) Early appearance of type II astrocytes in developing human fetal brain. Dev Brain Res 42:146–150Google Scholar
  22. ffrench-Constant C, Raff MC (1986) Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 319:449–502PubMedGoogle Scholar
  23. Galileo DS, Gray GE, Owens GC, Majors J, Sanes JR (1990) Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci USA 87:458–462PubMedGoogle Scholar
  24. 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
  25. 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
  26. Gomez LA, Brusco A, Saavedra JP (1990) Immunocytochemical study of S-100 positive glial cells in the brainstem and spinal cord of the rat embryo. Int J Dev Neurosci 8:55–64PubMedGoogle Scholar
  27. Gooday DJ (1990) Retinal axons inXenopus laevis recognize differences between tectal and diencephalic glial cells in vitro. Cell Tissue Res 259:595–598PubMedGoogle Scholar
  28. Gould SJ, Howard S, Papadaki L (1990) The development of ependyma in the human fetal brain: an immunohistological and electron microscopic study. Dev Brain Res 55:255–267Google Scholar
  29. 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
  30. van Hartesveldt C, Moore B, Hartman BK (1986) Transient midline raphe glial structure in the developing rat. J Comp Neurol 253:175–184Google Scholar
  31. 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
  32. Henrikson CK, Vaughn JE (1974) Fine structural relationships between neurites and radial glial processes in developing mouse spinal cord. J Neurocytol 3:659–675PubMedGoogle Scholar
  33. Hines M (1922) Studies of the growth and differentiation of the telencephalon in man. The fissura hippocampi. J Comp Neurol 34:73–171Google Scholar
  34. 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
  35. 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
  36. 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
  37. Hutchins JB, Casagrande VA (1989) Vimentin: changes in distribution during brain development. Glia 2:56–66Google Scholar
  38. Ishikawa H, Nogami H, Shirasawa N (1983) Novel clonal strains for adult rat anterior pituitary producing S-100 protein. Nature 303:711–713PubMedGoogle Scholar
  39. Kostović I, Seress L, Mrzljak L, Judas 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 30:105–116Google Scholar
  40. LaMantia A-S, Rakic P (1990) Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J Comp Neurol 291:520–537PubMedGoogle Scholar
  41. 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
  42. Landry CF, Ivy GO, Brown IR (1990) Developmental expression of glial fibrillary acidic protein mRNA in the rat brain analysed by in situ hybridization. J Neurosci Res 25:194–203PubMedGoogle Scholar
  43. 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
  44. 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 193:815–840Google Scholar
  45. Miller RH, ffrench-Constant C, Raff MC (1989) The macroglial cells of the rat optic nerve. Ann Rev Neurosci 12:517–534PubMedGoogle Scholar
  46. Milller F, O'Rahilly R (1990) The human brain at stages 21–23, with particular reference to the cerebral cortical plate and to the development of the cerebellum. Anat Embryol 182:375–400PubMedGoogle Scholar
  47. Møllgård K, Balslev Y (1989) The subcellular distribution of transferrin in rat choroid plexus studied with immunogold labelling of ultracryosections. Histochem J 21:441–448PubMedGoogle Scholar
  48. Nowakowski RS, Rakic P (1979) The mode of migration of neurons to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 8:697–718PubMedGoogle Scholar
  49. Nowakowski RS, Rakic P (1981) The site of origin and route and rate of migration of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:129–154Google Scholar
  50. Raff MC (1990) Subclasses of astrocytes in culture: What should we call them? In: Levi G (ed) Differentiation and functions of glial cells. Liss, New York, pp 17–23Google Scholar
  51. Raff MC, Abney EA, Cohen J, Lindsay R, Noble M (1983) Two types of astrocytes in culture of developing rat white matter: difference in morphology, surface gangliosides and growth characteristics. J Neurosci 3: 1289–1300PubMedGoogle Scholar
  52. Rakic P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471–476Google Scholar
  53. Rakic P (1988 a) Specification of cerebral cortical areas. Science 241:170–176PubMedGoogle Scholar
  54. Rakic P (1988 b) Intrinsic end extrinsic determinants of neocortical parcellation: a radial unit model. In: Rakic P, Singer W (eds) Neurobiology of neocortex. Wiley, New York, pp 5–27Google Scholar
  55. Rakic P, Yakolev PL (1968) Development of the corpus callosum and cavum septi in man. J Comp Neurol 132:45–72PubMedGoogle Scholar
  56. Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264:449–479Google Scholar
  57. Rogers J (1989) Calcium-binding proteins: the search for functions. Nature 339:661–662PubMedGoogle Scholar
  58. Rousselet A, Autillo-Touati A, Araud D, Prochiantz A (1990) In vitro regulation of neuronal morphogenesis and polarity by astrocyte-derived factors. Dev Biol 137:33–45PubMedGoogle Scholar
  59. Schmechel DE, Rakic P (1979 a) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115–152PubMedGoogle Scholar
  60. Schmechel DE, Rakic P (1979 b) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Science 277:303–305Google Scholar
  61. 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
  62. Schwab ME, Caroni P (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fbroblast spreading in vitro. J Neurosci 8:2381–2393PubMedGoogle Scholar
  63. Silver J, Lorenz SE, Wahlsten D, Coughlin J (1982) Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol 210:10–29PubMedGoogle Scholar
  64. Singer M, Nordlander RH, Egar M (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blueprint hypothesis of neuronal pathway patterning. J Comp Neurol 185:1–22PubMedGoogle Scholar
  65. Skoff RP, Knapp PE, Bartlett WP (1986) Astrocytic diversity in the optic nerve: a cytoarchitectural study. In: Federoff S, Vernadakis A (eds) Astrocytes. Development, morphology, and regional specialization of astrocytes. Academic Press, Orlando, Florida, pp 269–289Google Scholar
  66. Small RK, Riddle P, Noble M (1987) Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328:155–157PubMedGoogle Scholar
  67. Stagaard M, Møllgård K (1989) The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry. Anat Embryol 180:17–28PubMedGoogle Scholar
  68. Stagaard Janas M, Nowakowski RS, Møllgård K (1991) Glial cell differentiation in neuron-free and neuron-rich regions. II. Early appearance of S-100 protein positive astrocytes in human fetal hippocampus. Anat Embryol 184:559–569PubMedGoogle Scholar
  69. Stagaard M, Nowakowski RS, Møllgård K (1990) S-100 immunoreactivity is differentially localized during the development of neuron-free and neuron-rich areas (abstract). Eur J Neurosci [Suppl 3]:223Google Scholar
  70. Valentino KL, Jones EG, Kane SA (1983) Expression of GFAP immunoreactivity during development of long fiber tracts in the rat CNS. Dev Brain Res 9:317–336Google Scholar
  71. Vanselow J, Thanos S, Godement P, Henke-Fahle S, Bonhoefer F (1989) Spatial arrangement of radial glia and ingrowing retinal axons in the chick optic tecum during development. Dev Brain Res 45:15–27Google Scholar
  72. 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 289:74–88PubMedGoogle Scholar
  73. 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 109:3063–3071PubMedGoogle Scholar
  74. Woodhams PL, Bascó LE, Jajós F, Cisillág A, Balázs R (1981) Radial glia in the developing mouse cerebral cortex and hippocampus. Anat Embryol 163:331–343PubMedGoogle Scholar
  75. 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

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Mette Stagaard Janas
    • 1
  • Richard S. Nowakowski
    • 2
  • Ole B. F. Terkelsen
    • 1
  • 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

Personalised recommendations