Journal of Neurocytology

, Volume 31, Issue 6–7, pp 457 ppl=–467 | Cite as

Cytology and lineage of NG2-positive glia

  • M. Berry
  • P. Hubbard
  • A. M. Butt


We present evidence that NG2+ glia are an integral part of an oligodendrocyte/synantocyte (OS) lineage stream the progenitors of which begin to produce both glial phenotypes at about birth. The NG2 CSPG is differentially distributed within the OS lineage, being expressed in progenitors and synantocytes but not in oligodendrocytes. All cells in the OS lineage, except the primordial stem cells, express O4. The oligodendrocyte line reacts with CD9, but synantocytes are CD9−. Nonetheless, synantocytes are morphologically complex and specialised glia which contact axolemma in myelinated fibres at nodes of Ranvier and synaptic terminals, and form >99% of all NG2+ glia in the adult CNS. Thus, the other NG2+ phenotype, the adult oligodendrocyte progenitor cell (AOPC), constitutes a small population of <1% of all NG2+ glia in the mature CNS. AOPC are a heterogeneous set of cells probably originating from multiple sources which, by definition, produce oligodendrocytes in the adult to replace loss after trauma, demyelination and normal ‘wear and tear’. The definitive functions of synantocytes remain undefined.


  1. Belachew, S., Aguirre, A. A., Wang, H., Vautier, F., Yuan, X., Anderson, S., Kirby, M.& Gallo, V.(2002) Cyclin-dependent kinase-2 controls oligodendrocyte progenitor cell cycle progression and is down-regulated in adult oligodendrocyte progenitors. Journal of Neuroscience 22, 8553–8562.Google Scholar
  2. Bergles, D. E., Roberts, J. D., Somogyi, P.& Jahr, C. E.(2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405, 187–191.Google Scholar
  3. Berry, M., Butt, A. M., Wilkin, G.& Perry, V. H.(2002) Structure and function of glia in the central nervous system. In Greenfield's Neuropathology, 7th ed.(edited by Lantos, D.& Graham, D. I.), Chap. 2, pp. 75–121. London: Arnold.Google Scholar
  4. Berry, M., Sandvig, A., Barrett, L. B., Butt, A. M.& Logan, A.(2003) Reactive glia and scar derived CNS axon growth inhibitors. Glia(in press).Google Scholar
  5. Black, J. A.& Waxman, S. G.(1988) The perinodal astrocyte. Glia 1, 169–183.Google Scholar
  6. Butt, A. M.& Berry, M.(2000) Oligodendrocytes and the control of myelination in vivo: New insights from the rat anterior medullary velum. Journal of Neuroscience Research 59, 477–488.Google Scholar
  7. Butt, A. M., Duncan, A.& Berry, M.(1994) Astrocyte associations with nodes of Ranvier: Ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve. Journal of Neurocytology 23, 486–499.Google Scholar
  8. Butt, A. M., Duncan, A., Hornby, F. M., Kirvell, S. L., Hunter, A., Levine, J. M.& Berry, M.(1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26, 84–91.Google Scholar
  9. Butt, A. M.& Ransom, B. R.(1993) Morphology of astrocytes during development in the intact rat optic nerve. The Journal of Comparative Neurology 338, 141–158.Google Scholar
  10. Butt, A. M., Kiff, J., Hubbard, P.& Berry, M.(2003) Synantocytes: New fnctions for novel NG2 expressing glia. Journal of Neurocytology 31, 551–565.Google Scholar
  11. Caporaso, G. L.& Chao, M. V.(2001) Telomerase and oligodendrocyte differentiation. Journal of Neurobiology 49, 224–234.Google Scholar
  12. Casaccia-Bonnefil, P., Hardy, R. J., Teng, K. K., Levine, J. M., Koff, A.& Chao, M. V.(1999) Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Development 126, 4027–4037.Google Scholar
  13. 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.Google Scholar
  14. Chen, M. S., Huber, A. B., Van Der Haar, M. E., Frank, M., Schnell, L., Spillmann, A. A., Christ, F.& Schwab, M. E.(2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434–439.Google Scholar
  15. Dawson, M. R. L., Levine, J. M., & Reynolds, R.(2000) NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors. Journal of Neuroscience Research 61, 471–479.Google Scholar
  16. Di Bello, I. C., Dawson, M. R., Levine, J. M.& Reynolds, R.(1999) Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the adult brain stem is associated with demyelination rather than inflammation. Journal of Neurocytology 28, 365–381.Google Scholar
  17. Diers-Fenger, M., Kirchhoff, F., Kettenmann, H., Levine, J. M.& Trotter, J.(2001) AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: Isolation, differentiation, and association with radial glia. Glia 34, 213–228.Google Scholar
  18. Dou, C.& Levine, J. M.(1994) Inhibition of neurite outgrowth by the NG2 chondroitin sulphate proteoglycan. Journal of Neuroscience 14, 7616–7628.Google Scholar
  19. Fidler, P. S., Schuette, K., Asher, R. A., Dobbertin, A., Thornton, S. R., Callepatino, Y., Muir, E., Levine, J. M., Geller, H. M., Rogers, J. H., Faissner, A.& Fawcett, J. W.(1999) Comparing astrocyte cell lines that are inhibitory or permissive for axon growth: The major axon inhibitory proteoglycan is NG2. Journal of Neuroscience 19, 8778–8788.Google Scholar
  20. Ffrench-Constant, C., Miller, R. H., Kruse, J., Schachner, M.& Raff, M. C.(1986) Molecular specialisation of astrocyte processes at nodes of Ranvier. Journal of Cell Biology 102, 844–852.Google Scholar
  21. Ffrench-Constant, C., Miller, R. H., Burne, J. F.& Raff, M. C.(1988) Evidence that migratory oligodendrocyte-type 2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. Journal of Neurocytology 17, 13–25.Google Scholar
  22. Fulton, B. P., Burne, J. F.& Raff, M. C.(1992) Visualisation of O-2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake. Journal Neuroscience 12, 4816–4833.Google Scholar
  23. Gallo, V., Zhou, J. M., Mcbain, C. J., Wright, P., Knutson, P. L.& Armstrong, R. C.(1996) Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate-mediated K+channel block. Journal of Neuroscience 16, 2659–2670.Google Scholar
  24. Gard, A. L.& Pfeiffer, S. E.(1990) Two proliferative stages of the oligodendrocyte lineage (A2B5+O4?and O4?GalC?) under different mitogenic control. Neuron 5, 615–625.Google Scholar
  25. Gensert, J. M.& Golman, J. E.(2001) Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. Journal of Neurobiology 48, 75–86.Google Scholar
  26. Gensert, J. M.& Golman, J. E.(1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19, 197–203.Google Scholar
  27. Genoud, S., Lappe-Siefke, C., Goebbels, S., Radtke, F., Aguet, M., Scherer, S. S., Suter, U., Nave, K. A.& Mantei, N.(2002) Notch1 control of oligodendrocyte differentiation in the spinal cord. Journal of Cell Biology 158, 709–718.Google Scholar
  28. Greenwood, K.& Butt, A. M.(2003) Evidence that perinatal and adult NG2 expressing glia are not conventional oligodendrocyte progenitors and do not depend on axons for survival. Molecular and Cellular Neuroscience(in press).Google Scholar
  29. Guilian, D., Johnson, B., Krebs, J. F., Tapscott, M. J.& Honda, S.(1991) A growth factor from neuronal cell lines stimulates myelin protein synthesis in mammalian brain. Journal of Neuroscience 11, 327–336.Google Scholar
  30. Hall, A., Giese, N. A.& Richardson, W. D.(1996) Spinal cord oligodendrocytes develop from ventrallyderived progenitor cells that express PDGF alphareceptors. Development 122, 4085–4094.Google Scholar
  31. Hardy, R.& Reynolds, R.(1991) Proliferation and differentiation potential of rat forebrain oligodendroglial progenitors both in vitroand in vivo. Development 111, 1061–1080.Google Scholar
  32. Hardy, R.& Reynolds, R.(1993) Neuron-oligodendroglia interactions during central nervous system development. Journal of Neuroscience Research 36, 121–126.Google Scholar
  33. Hartman, B. K., Agrawal, H. C., Agrawal, D.& Kalmbach, S.(1982) Development and maturation of central myelin: Comparison of immunohistochemical localization of proteolipid protein and basic protein in myelin and oligodendrocytes. Proceedings of the National Academy of Sciences USA 79, 4217–4220.Google Scholar
  34. Hildebrand, C.(1971) Ultrastructural and lightmicroscopic studies of the nodal region in large myelinated fibres of developing feline spinal cord white matter. 1. The nodes of Ranvier. Acta Physiologica Scandivica, Supplement 364, 81–101.Google Scholar
  35. Hildebrand, C.& Waxman, S. G.(1984) Postnatal differentiation of rat optic nerve fibres: Electron microscopic observations of the development of nodes of Ranvier and axoglia relations. Journal of Comparative Neurology 224, 25–37.Google Scholar
  36. Horner, P. J., Power, A. E., Kempermann, G., Kuhn, H. G., Palmer, T. D.& Winkler, J.(2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. The Journal of Neuroscience 20, 2218–2228.Google Scholar
  37. Jones, L. L., Yamaguchi, Y., Stallcup, W. B.& Tuszynski, M. H.(2002) NG2 is a major chondroitin sulphate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. Journal of Neuroscience 22, 2792–2803.Google Scholar
  38. Kierstead, H. S., Levine, J. M.& Blakemore, W. F.(1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22, 161–170.Google Scholar
  39. Levine, J. M.(1994) Increased expression of chondroitinsulphate proteoglycan after brain injury. Journal of Neuroscience 14, 4716–4730.Google Scholar
  40. 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.Google Scholar
  41. Levine, J. M.& Goldman, J. E.(1988a) Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. Journal of Comparative Neurology 277, 441–455.Google Scholar
  42. Levine, J. M.& Goldman, J. E.(1988b) Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebellum. Journal of Neuroscience 8, 3992–4006.Google Scholar
  43. Levine, J. M.& Reynolds, R.(1999) Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Experimental Neurology 160, 333–347.Google Scholar
  44. Levine, J. M., Reynolds, R.& Fawcett, J. W.(2001) The oligodendrocyte precursor cell in health and disease. Trends in Neurosciences 24, 39–47.Google Scholar
  45. Levine, A., Stincone, F.& Lee, Y. S.(1993) Development and differentiation of glia precursor cells in the rat cerebellum. Glia 7, 307–321.Google Scholar
  46. Levison, S. W.& Goldman, J. E.(1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201–212.Google Scholar
  47. Li, G., Crang, A. J., Rundle, J. L.& Blakemore, W. F.(2002) Oligodendrocyte progenitor in the adult rat CNS express myelin oligodendrocyte glycoprotein (MOG). Brain Pathology 12, 463–471.Google Scholar
  48. Lin, S.-C.& Bergles, D. E.(2003) Physiological characteristics of NG2-expressing glial cells. Journal of Neurocytology 31(6/7), 537–549.Google Scholar
  49. Ling, E.-A., Paterson, J. A., Privat, A., Mori, S.& Leblond, C. P.(1973) Investigation of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats. Journal of Comparative Neurology 149, 43–72.Google Scholar
  50. Ling, E.-A.& Leblond, C. P.(1973) Investigation of glial cells in semithin sections. II. Variation with age in the numbers of the various glial cell types in rat cortex and corpus callosum. Journal of Comparative Neurology 149, 73–81.Google Scholar
  51. Lu, Q. R., Yuk, D., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., Mcmahon, A. P., Stiles, C. D.& Rowitch, D. H.(2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in themammaliancentral nervous system. Neuron 25, 317–329.Google Scholar
  52. Ludwin, S. K.(1979) An autoradiographic study of cellular proliferation in remyelination of the central nervous system. American Journal of Pathology 95, 683–696.Google Scholar
  53. Mallon, B. S., Shick, H. E., Kidd, G. J.& Macklin, W. B.(2002) Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. Journal of Neuroscience 22, 876–885.Google Scholar
  54. Martin, S., Levine, A. K., Chen, Z. J., Ughrin, Y.& Levine, J. M.(2001) Deposition of NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. Journal of Neuroscience 21, 8119–8128.Google Scholar
  55. McTigue, D. M., Wei, P.& Stokes, B. T.(2001) Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. Journal of Neuroscience 21, 3392–3400.Google Scholar
  56. Miller, R. H., Fulton, B. P.& Raff, M. C.(1989) A novel type of glial cell associated with nodes of Ranvier in rat optic nerve. European Journal Neuroscience 1, 172–180.Google Scholar
  57. Mori, S.& Leblond, C. P.(1970) Electronmicroscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. Journal of Comparative Neurology 139, 1–30.Google Scholar
  58. Nishiyama, A.(2001) NG2 cells in the brain: A novel glial cell population. Human Cell 14, 77–82.Google Scholar
  59. Nishiyama, A., Watanabe, M., Yang, Z.& Bu, J.(2003) Identity, distribution and development of NG2+expressing glial cells. Journal of Neurocytology. 31, 437–455.Google Scholar
  60. Nishiyama, A., Chang, A.& Trapp, B. D.(1999) NG2+glia cells: A novel glial cell population in the adult brain. Journal of Neuropathology and Experimental Neurologyl 58, 1113–1124.Google Scholar
  61. Nishiyama, A., Lin, X.-H., Giese, N. Heldin, C.-H.& Stallcup, W. B.(1996a) Co-localisation of NG2 proteoglycan and PDGF α-receptor on O2A progenitor cells in the developing rat brain. Journal of Neuroscience Research 43, 299–314.Google Scholar
  62. Nishiyama, A., Lin, X.-H., Giese, N., Heldin, C.-H.& Stallcup, W. B.(1996b) Interaction between NG2 proteoglycan and PDGF α-receptor on O2A progenitor cells is required for optimal response of PDGF. Journal of Neuroscience Research 43, 299–314.Google Scholar
  63. 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 48, 299–312.Google Scholar
  64. 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.Google Scholar
  65. Noll, E.& Miller, R. H.(1993) Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral mid-line region in the embryonic rat spinal cord. Development 118, 563–573.Google Scholar
  66. Ong, Y. W.& Levine J. M.(1999)Alight and electron microscopic study of NG2 chondroitin sulphate proteoglycan positive oligodendrocyte precursor cells in the normal and kainate lesioned rat hippocampus. Neuroscience 92, 83–95.Google Scholar
  67. Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E.& Stallcup, W. B.(2001) NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Developmental Dynamics 222, 218–227.Google Scholar
  68. Ozerdem, U., Monosov, E.& Stallcup, W. B.(2002) NG2 proteoglycan expressed by pericytes in pathological microvasculature. Microvascular Research 63, 129–134.Google Scholar
  69. Pouly, S., Prat, A., Blain, M., Olivier, A.& Antel, J.(2001) NG2 immunoreactivity on human brain endothelial cells. Acta Neuropathologica 102, 313–320.Google Scholar
  70. Pringle, N. P., Mughar, H. S., Collarini, E. J.& Richardson, W. D.(1992) PDGF receptors in the rat CNS: During late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115, 535–551.Google Scholar
  71. Pringle, N. P.& Richardson, W. D.(1993) A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 117, 525–533.Google Scholar
  72. Privat, A.(1975) Postnatal gliogenesis in the mammalian brain. International Reviews of Cytology 40, 281–323.Google Scholar
  73. Privat, A.& Leblond, C. P.(1972) The subependymal layer and neighboring region of the brain of the young rat. Journal of Comparative Neurology 146, 277–302.Google Scholar
  74. Raff, M. C., Miller, R. H.& Noble, M.(1983) A glial progenitor cell that develops in vitrointo an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 3909–3906.Google Scholar
  75. Raff, M. C., Abnet, E. R.& Fog-Seang, J.(1985) Reconstruction of a developmental clock in vitro: A critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell 42, 61–69.Google Scholar
  76. RamÓn-Moliner, E.(1958) A study of neuroglia. The problem of transitional forms. Journal of Comparative Neurology 110, 157–171.Google Scholar
  77. Ramon Y Cajal, S.(1909) Histologie du système nerveux de l'homme et des vertébrés. p. 238. Paris: Maloine.Google Scholar
  78. Reyners, H., Gianfelici De Reyners, E.& Maisin, J.-R.(1982) The beta astrocyte: A newly recognised radiosensitive glial cell type in the cerebral cortex. Journal of Neurocytology 11, 967–983.Google Scholar
  79. 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.Google Scholar
  80. Reynolds, R.& Hardy, R.(1997) Oligodendroglial progenitors labelled with O4 antibody persist in the adult rat cerebral cortex in vivo. Journal of Neuroscience Research 47, 455–470.Google Scholar
  81. Reynolds, R.& Wilkin, G. P.(1988) Development of microglial cells in rat cerebellum. II. An in situimmunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 102, 409–425.Google Scholar
  82. Reynolds, R., Dawson, M., Polito, A., Di Bello, I. C., Papadopoulos, D., Pham-Dinh, D.& Levine, J.(2003) The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS. Journal of Neurocytology 31(6/7), 523–535.Google Scholar
  83. Richardson, W. D., Pringle, N., Moseley, M. J., Westermark, B.& Dubois-Dalcq, M.(1988) A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53, 309–319.Google Scholar
  84. Sasahara, M., Fries, J. W. U., Raines, E. W., Gown, A. M., Westrum, L. E., Frosch, M. P., Bonthron, D. T., Ross, R.& Collins, T.(1991) PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 64, 217–227.Google Scholar
  85. Shi, J., Marinovich, A.& Barres, B. A.(1998) Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. Journal of Neuroscience 18, 4627–4636.Google Scholar
  86. Skoff, R. P.(1990) Gliogenesis in the rat optic nerve: Astrocytes are generated in a single wave before oligodendrocytes. Developmental Biology 139, 149–168.Google Scholar
  87. Skoff, R. P.& Vaughn, J. E.(1971) An autoradiographic study of cellular proliferation inthe degenerating opticnerve. Journal of Comparative Neurology 141, 133–156.Google Scholar
  88. Smart, I.& Leblond, C. P.(1961) Evidence for division and transformation of neuroglia cells in the mouse brain, as derived from radioautography after injection of thymidine-H3. Journal of Comparative Neurology 116, 349–368.Google Scholar
  89. Stensaas, L. J.(1977) The ultrastructure of astrocytes, oligodendrocytes and microglia in the optic nerve of urodele amphibians (A. punctatum, T. pyrrhogaster, T. viridescens). Journal of Neurocytology 6, 269–286.Google Scholar
  90. Tanaka, K., Nogawa, S., Ito, D., Suzuki, S., Dembo, T., Kosakai, A.& Fukuuchi, Y.(2001) Activation of NG2-positive oligodendrocyte progenitor cells during post-ischemic reperfusion in the rat brain. Neuroreport 12, 2169–2174.Google Scholar
  91. Tang, X., Davies, J. E.& Davies, S. J. A.(2002) Changes in distribution, cell associations, and protein expression levels ofNG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar. Journal of Neuroscience Research. Online ISSN: 1097–4547 Print ISSN: 0360–4012.Google Scholar
  92. Temple, S.& Raff, M. C.(1986) Clonal analysis of oligodendrocyte development in culture: Evidence for a developmental clock that counts cell divisions. Cell 44, 773–779.Google Scholar
  93. Terada, N., Baracskay, K., Kinter, M., Melrose, S., Brophy, P. J., Boucheix, C., Bjartmar, C., Kidd, G.& Trapp, B. D.(2002) The tetraspanin protein, CD9, is expressed by progenitor cells committed to oligodendrogenesis and is linked to beta 1 integrin, CD81, and Tspan-2. Glia 40, 350–359.Google Scholar
  94. Trapp, B. D., Nishiyama, A., Cheng, D.& Macklin, W.(1997) Differentiation and death of premyelinating oligodendrocytes in the developing rodent brain. Journal of Cell Biology 137, 459–468.Google Scholar
  95. Ughrin, Y. M., Chen, Z. J.& Levine, J. M.(2003) Multiple regions of NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. Journal of neuroscience 23, 175–186.Google Scholar
  96. Wang, S., Sdrulla, A. D., Disibio, G., Bush, G., Nofziger, D., Hicks, C., Weinmaster, G.& Barres, B.(1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63–75.Google Scholar
  97. Warf, B. C., Fok-Seang, J.& Miller, R. H.(1991) Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. Journal of Neuroscience 11, 2477–2488.Google Scholar
  98. Warrington, A. E., Barbarese, E.& Pfeiffer, E. S.(1993) Differential myelinogenic capacity of specific developmental stages of the oligodendrocytes lineage upon transplantation into hypomyelinating hosts. Journal of Neuroscience Research 34, 1–13.Google Scholar
  99. Watanabe, M., Toyama, Y.& Nishiyama, A.(2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. Journal of Neuroscience Research 69, 826–836.Google Scholar
  100. Yeh, H. J., Ruit, K. G., Wang, Y. X., Parks, W. C., Snider, W. D.& Deuel, T. F.(1991) PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell 64, 209–216.Google Scholar
  101. Zhang, S.-C., Lundberg, C., Lipsitz, D., O'connor, L. T.& Duncan, I. D.(1998) Generation of oligodendroglial progenitors from neural stem cells. Journal of Neurocytology 27, 475–489.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • M. Berry
    • 1
  • P. Hubbard
    • 1
  • A. M. Butt
    • 1
  1. 1.Neural Damage and Repair, Centre for Neuroscience Research, Hodgkin BuildingGKT School of Biomedical SciencesLondonUK

Personalised recommendations