Journal of Neurocytology

, Volume 33, Issue 3, pp 345–357 | Cite as

A fourth type of neuroglial cell in the adult central nervous system

  • Alan Peters

Abstract

Labeling central nervous tissue from mature animals with antibodies to NG2 chondroitin sulfate proteoglycan reveals the existence of large numbers of NG2 positive cells, at least some of which are oligodendroglial progenitors. It is generally agreed that these cells differ from the classically defined neuroglia, since they are antigenetically different from astrocytes, oligodendrocytes, or microglial cells. Although the NG2 positive cells have been well characterized in light microscopic preparations, examination of the labeled cells by electron microscopy have not led to general agreement about their morphological features. The basic reason for this is that it is difficult to obtain good preservation of the fine structure of NG2 labeled neurons. Since these NG2 positive cells are abundant in the central nervous system, it was decided to examine routinely prepared tissue from the brains of mature monkeys and rats by electron microscopy to determine if there is a neuroglial cell type whose presence has been overlooked. It soon became evident that there is a fourth type of neuroglial cell. These cells have pale, irregular shaped nuclei with a thin rim of heterochromatin beneath the nuclear envelope, and they have pale cytoplasm. Superficially they resemble astrocytes, which is the probable reason why the presence of this fourth type of neuroglial cell has been largely overlooked. However, the fourth type of neuroglial cell, here referred to as a ß neuroglial cell, has no intermediate filaments in its cytoplasm, the mitochondria are thinner than those of astrocytes, centrioles are frequently encountered in their cytoplasm, and when they are adjacent to capillaries they are always separated from the basal membrane by an astrocytic processes.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Reference

  1. BERGLES, D. E., ROBERTS, J. D. B., SOMOGYI, P. & JAHR, C. E. (2000) Glutamatergic synapses on oligo-dendrocyte precursor cells in hippocampus. Nature 405, 187–191.PubMedGoogle Scholar
  2. BU, J., AKHTAR, N. & NISHIYAMA, A. (2001) Transient expression of NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 34, 296–310.PubMedGoogle Scholar
  3. BUTT, A. M., DUNCAN, A., FRASER HORNBY, M., KIRVELL, S. L., HUNTER, A., LEVINE, J. M. & BERRY, M. (1999) Cells expressing the NG2antigen contact nodes of Ranvier in adult CNS white matter. Glia 26, 84–91.PubMedGoogle Scholar
  4. BUTT, A. M., KIFF, J., HUBBARD, P. & BERRY, M. (2002) Synantocytes: New functions for novel NG2 expresssing glia. Journal of Neurocytology 31, 551–565.PubMedGoogle Scholar
  5. BUTT, A. M. & NISHIYAMA, A. (2002) Editorial to Novel NG-2 glia. Journal of Neurocytology 31, 421–422.Google Scholar
  6. CENCI DI BELLO, I., DAWSON, M. R. L., LEVINE, J. M. & REYNOLDS, R. (1999) Generation of oligoden-droglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. Journal of Neurocytology 28, 365–381.PubMedGoogle Scholar
  7. CHANG, A., NISHIYAMA, A., PETERSON, J., PRINEAS, J. & TRAPP, B. D. (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. Journal of Neuroscience 20, 6404–6412.PubMedGoogle Scholar
  8. FULTON, B. P., BURNE, J. F. & RAFF, M. C. (1992) Visualization of 2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake. Journal of Neuroscience 12, 4816–4833.PubMedGoogle Scholar
  9. HORNER, P. J., THALLMAIR, M. & GAGE, F. H. (2002) Defining the NG2-expressing cell of the adult CNS. Journal of Neurocytology 31, 481–495.PubMedGoogle Scholar
  10. JENNINGS, A. R., KIRILAK, Y. & CARROLL, W. (2002) In situ characterisation of oligodendrocyte progenitor cells.A fourth type of neuroglial cell 357 in adult mammalian optic nerve. Journal of Neurocytology 31, 27–39.PubMedGoogle Scholar
  11. KAPLAN, M. S. & HINDS, J. W. (1980) Gliogenesis of astocytes and oligodendrocytes in the neocortical grey and white matter of the adult rat; electron microscopic analysis of light autoradiographs. Journal of Comparative Neurology 193, 711–727.PubMedGoogle Scholar
  12. LEVINE, J. M. & CARD, J. P. (1987) Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: Association with smooth protoplasmic astrocytes. Journal of Neuroscience 7, 2711–2720.PubMedGoogle Scholar
  13. LEVINE, J. M., REYNOLDS, R. & FAWCETT, J. W. (2001) The oligodendrocyte precursor cell in health and disease. Trends in Neuroscience 24,39–47.Google Scholar
  14. LEVINE, J. M., STINCONE, F. & LEE, Y. S. (1993) Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7, 307–321.PubMedGoogle Scholar
  15. LEVISON, S. W., YOUNG, G. M. & GOLDMAN, J. E. (1999) Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. Journal of Neuroscience Research 57, 435–446.PubMedGoogle Scholar
  16. LIN, S.-C. & BERGLES, D. E. (2002) Physiological characteristics of NG2-expressing glial cells. Journal of Neurocytology 31, 537–549.PubMedGoogle Scholar
  17. LIN, S.-C. & BERGLES, D. E. (2003) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nature Neuroscience 7,24–32.PubMedGoogle Scholar
  18. NISHIYAMA, A., CHANG, A. & TRAPP, B. D. (1999) NG2 glial cells: Anovel glial cell population in the adult brain. Journal of Neuropathology Experimental of Neurology 58, 1113–1124.Google Scholar
  19. NISHIYAMA, A., LIN, X.-H., GIESE, N., HELDIN, C.-H. & STALLCUP, W. B. (1996) Colocalization of NG2proteoglycan and PDGFa receptor on O2Aprogenitor cells in the developing rat brain. Journal of Neuroscience 43, 299–314.Google Scholar
  20. NISHIYAMA, A., YU, M., DRAZBA, J. A. & TUOHY, V. K. (1997) Normal and reactive NG2 glial cells are distinct from resting and activated microglia. Journal of Neuroscience Research 48, 299–312.PubMedGoogle Scholar
  21. NISHIYAMA, A., WATANABE, M., YANG, Z. & BU, J. (2002) Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. Journal of Neurocytology 31, 437–455.PubMedGoogle Scholar
  22. ONG, W. Y. & LEVINE, J. M. (1999)A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in normal and kainate-lesioned rat hippocampus. Journal of Neuroscience 92,83–95.Google Scholar
  23. PETERS, A., PALAY, S. L. & WEBSTER, DEF. H. (1991) The fine structure of the nervous system. Neurons and their Supporting Cells. 3 edition. New York: Oxford University Press.Google Scholar
  24. PETERS, A. & SETHARES, C. (2004) Oligodendrocytes, their progenitors, and other neuroglial cells in the aging primate cerebral cortex. Cerebral CortexAccepted for publication.Google Scholar
  25. REYNERS, H., GIANFELICI DE REYNERS, E. & MAISIN, J.-R. (1982) The beta astrocyte: Anewly recognized radiosensitive glial cell type in the cerebral cortex. Journal of Neurocytology 11, 967–983.PubMedGoogle Scholar
  26. REYNERS, H., GIANFELICI DE REYNERS, E., REGNIERS, L., & MAISIN, J.-R. (1986) A glial progenitor cell in the cerebral cortex of the adult rat. Journal of Neurocytology 15,53–61.PubMedGoogle Scholar
  27. REYNOLDS, R. & HARDY, R. (1997) Oligodendroglial pro-genitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. Journal of Neuroscience Research4 7, 455–470.Google Scholar
  28. SCOLDING, N., FRANKLIN, R., STEVENS, S., HELDIN, C.-H. COMPSTON, A. & NEWCOMBE, J. (1998) Oligodendrocyte progenitors are present in the normal adult human CNS and in lesions of multiple sclerosis. Brain 121, 2221–2228.PubMedGoogle Scholar
  29. SKOFF, R. P. (1975) The fine structure of pulse labeled ( 3 H-thymidine cells) in degenerating rat optic nerve. Journal of Comparative Neurology 161, 595–612.PubMedGoogle Scholar
  30. STALLCUP, W. B. (2002) The NG2 proteoglycan: Past insights and future prospects. Journal of Neurocytology 31, 423–435.PubMedGoogle Scholar
  31. YE, P., BAGNELL, R. & D'ERCOLE, A. J. (2003) Mouse NG2 + oligodendrocyte precursors express mRNA for proteolipid protein but not its DM-20 variant: A study of laser microdissection-captured NG + cells. Journal of Neuroscience 23, 4401–4405.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Alan Peters
    • 1
  1. 1.Boston University School of MedicineDepartment of Anatomy and NeurobiologyBostonUSA

Personalised recommendations