Therapeutic strategies in multiple sclerosis. II. Long-term repair

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1390, 1999, Pages 1711-1720

  Scolding, Neil ^a,b,c  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c FRENCHAY HOSPITAL   (United Kingdom)

Author keywords

Human oligodendrocytes; Myelin repair; Oligodendrocyte precursor; Remyelination

Indexed keywords

EID: 0033615478     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0514     Document Type: Article

References (129)

1. Aloisi, F., Giampaolo, A., Russo, G., Peschle, C. & Levi, G. 1992 Developmental appearance, antigenic profile and proliferation of glial cells of the human embryonic spinal cord an immunocytochemical study using dissociated cells. Glia 5, 171-181.
2. Anonymous 1997 Have a pig's heart? Lancet 349, 219.
3. Archer, D. R., Cuddon, P. A., Lipsitz, D. & Duncan, I. D. 1997 Myelination of the canine central nervous system by glial cell transplantation: a model for repair of human myelin disease. Nature Med. 3, 54-59.
4. Armstrong, R. C., Dorn, H. H., Kufta, C. V., Friedman, E. & Dubois-Dalcq, M. E. 1992 Pre-oligodendrocytes from adult human CNS. J. Neurosci. 12, 1538-1547.
5. Asakura, K., Miller, D. J., Murray, K., Bansal, R., Pfeiffer, S. E. & Rodriguez, M. 1996a Monoclonal autoantibody SCH94.03, which promotes central nervous system remyelination, recognizes an antigen on the surface of oligodendrocytes. J. Neurosci. Res. 43, 273-281.
6. Asakura, K., Pogulis, R. J., Pease, L. R. & Rodriguez, M. 1996b A monoclonal autoantibody which promotes central nervous system remyelination is highly polyreactive to multiple known and novel antigens. J. Neuroimmunol. 65, 11-19.
7. Barnett, S. C., Franklin, R. J. M. & Blakemore, W. F. 1993 In vitro and in vivo analysis of a rat bipotential O-2A progenitor cell line containing the temperature-sensitive mutant gene of the SV40 large T antigen. Eur. J. Neurosci. 5, 1247-1260.
8. Blakemore, W. F. & Franklin, R. J. M. 1991 Transplantation of glial cells into the CNS. Trends Neurosci. 14, 323-327.
9. Bunge, M. B., Bunge, R. P. & Ris, H. 1961 Ultrastructural study of remyelination in an experimental lesion in the adult cat spinal cord. J. Biophys. Biochem. Cytol. 10, 67-94.
10. Bunge, R. P. 1987 Tissue culture observations relevant to the study of axon- Schwann cell interactions during peripheral nerve development and repair. J. Exp. Biol. 132, 21-34.
11. Cajal, S. R. 1913 Degeneration and regeneration of the nervous system (1928 edn translated and edited by R. May), pp. 734-760. Oxford University Press.
12. Carroll, W. M., Jennings, A. R. & Mastaglia, F. L. 1990 The origin of remyelinating oligodendrocytes in antiserum-mediated demyelinative optic neuropathy. Brain 113, 953-973.
13. Carson, M. J., Behringer, R. R., Brinster, R. L. & McMorris, F. A. 1993 Insulin-like growth factor 1 increases brain growth and central nervous system myelination in transgenic mice. Neuron 10, 729-740.
14. Compston, D. A. S. 1996 Remyelination of the central nervous system. Mult. Scler. 1, 388-392.
15. Compston, D. A. S., Zajicek, J., Sussman, J., Webb, A., Hall, G., Muir, D. A., Shaw, C., Wood, A. & Scolding, N. 1997 Glial lineages and myelination in the central nervous system. J. Anat. 190, 161-200.
16. Coutinho, A., Kazatchkine, M. D. & Avrameas, S. 1995 Natural autoantibodies. Curr. Opin. Immunol. 7, 812-818.
17. Crang, A. J. & Blakemore, W. F. 1991 Remyelination of demyelinated rat axons by transplanted mouse oligodendrocytes. Glia 4, 305-313.
18. Dawson, J. W. 1916 The histology of disseminated sclerosis. Edinb. Med. J. 17, 229-410.
19. Deacon, T. (and 10 others) 1997 Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nature Med. 3, 350-353.
20. Duncan, I. D. 1996 Glial cell transplantation and remyelination of the central nervous system. Neuropathol. Appl. Neurobiol. 22, 87-100.
21. Duncan, I. D. & Hoffman, R. L. 1997 Schwann cell invasion of the central nervous system of the myelin mutants. J. Anat. 190, 35-49.
22. Eddelston, M. & Mucke, L. 1993 Molecular profile of reactive astrocytes - implications for their role in neurologic disease. Neuroscience 54, 15-36.
23. Edge, A. S., Gosse, M. E. & Dinsmore, J. 1998 Xenogencic cell therapy: current progress and future developments in porcine cell transplantation. Cell Transplant. 7, 525-539.
24. Feigin, I. & Popoff, H. 1966 Regeneration of myelin in multiple sclerosis: the role of mesenchymal cells in such regeneration and in myelin formation in the peripheral nervous system. Neurology 16, 364-372.
25. Felts, P. A. & Smith, K. J. 1992 Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Res. 574, 178-192.
26. Ferguson, B., Matyszak, M. K., Esiri, M. M. & Perry, V. H. 1997 Axonal damage in acute multiple sclerosis lesions. Brain 120, 393-399.
27. ffrench Constant, C. & Raff, M. C. 1986 Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 319, 499-502.
28. Franklin, R. J. M. 1993 Reconstructing myelin-deficient environments in the CNS by glial cell transplantation. Semin. Neurosci. 5, 443-451.
29. Franklin, R. J. M. & Blakemore, W. F. 1993 Requirements for Schwann cell migration within CNS environments: a view-point. Int. J. Dev. Neurosci. 11, 641-649.
30. Franklin, R. J. M. & Blakemore, W. F. 1995 Glial-cell transplantation and plasticity in the O-2A lineage implications for CNS repair. Trends Neurosci. 18, 151-156.
31. Franklin, R. J. M. & Blakemore, W. F. 1997 Transplanting oligodendrocyte progenitors into the adult CNS. J. Anat. 190, 23-33.
32. Franklin, R. J. M., Crang, A. J., Blakemore, W. F. 1991 Transplanted type-1 astrocytes facilitate repair of demyelinating lesions by host oligodendrocytes in adult rat spinal cord. J. Neurocytol. 20, 420-430.
33. Franklin, R. J., Crang, A. J. & Blakemore, W. F. 1992 Type 1 astrocytes fail to inhibit Schwann cell remyelination of CNS axons in the absence of cells of the O-2A lineage. Dev. Neurosci. 14, 85-92.
34. Franklin, R. J. M., Bayley, S. A., Milner, R., ffrench Constant, C. & Blakemore, W. F. 1995 Differentiation of the o-2a progenitor-cell line cg-4 into oligodendrocytes and astrocytes following transplantation into glia-deficient areas of CNS while-matter. Glia 13, 39-44.
35. Franklin, R. J. M., Gilson, J. M., Franceschini, I. A. & Barnett, S. C. 1996 Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell-line into areas of demyelination in the adult CNS. Glia 17, 217-224.
36. Gage, F. H., Coates, P. W., Palmer, T. D., Kuhn, H. G., Fisher, L. J., Suhonen, J. O., Peterson, D. A., Suhr, S. T. & Ray, J. 1995 Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl Acad. Sci. USA 92, 11879-11883.
37. Greenfield, J. G. & King, L. S. 1936 Observations on the histopathology of the cerebral lesions in disseminated sclerosis. Brain 59, 445-459.
38. Griffiths, I. (and 10 others) 1998 Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610-1613.
39. Gritti, A. (and 10 others) 1996 Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16, 1091-1100.
40. Groves, A. K., Barnett, S. C., Franklin, R. J. M., Crang, A. J., Mayer, M., Blakemore, W. F. & Noble, M. 1993 Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 362, 453-455.
41. Hale, G. & Waldmann, H. 1996 Recent results using CAMPATH-1 antibodies to control GVHD and graft rejection. Bone Marrow Transplant. 17, 305-308.
42. Harrison, B. M. 1980 Remyelination by cells introduced into a stable demyelinating lesion in the central nervous system. J. Neurol. Sci. 46, 63-81.
43. Harrison, B. 1985 Schwann cell and oligodendrocyte remyelination in lysolecithin-induced lesions in irradiated rat spinal cord. J. Neurol. Sci. 67, 143-159.
44. Honmou, O., Felts, P. A., Waxman, S. G. & Kocsis, J. D. 1996 Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J. Neurosci. 16, 3199-3208.
45. Itoyama, Y., Webster, H. D., Richardson E. P. J. & Trapp, B. D. 1983 Schwann cell remyelination of demyelinated axons in spinal cord multiple sclerosis lesions. Ann. Neurol. 14, 339-346.
46. Itoyama, Y., Ohnishi, A., Tateishi, J., Kuroiwa, Y. & Webster, H. D. 1985 Spinal cord multiple sclerosis lesions in Japanese patients: Schwann cell remyelination occurs in areas that lack glial fibrillary acidic protein (GFAP). Acta Neuropathol. Berl. 65, 217-223.
47. Jeffery, N. D., Crang, A. J., O'Leary, M. T., Hodge, S. J. & Blakemore, W. F. 1999 Behavioural consequences of oligodendrocyte progenitor cell transplantation into experimental demyelinating lesions in the rat spinal cord. Eur. J. Neurosci. 11, 1508-1514.
48. Jessen, K. R. & Mirsky, R. 1997 Embryonic Schwann cell development: the biology of Schwann cell precursors and early Schwann cells. J. Anat. 191, 501-505.
49. Kennedy, P. G. E. & Fok Scang, J. 1986 Studies on the development, antigenic phenotype and function of human glial cells in tissue culture. Brain 109, 1261-1277.
50. Keown, J. 1993 The Polkinghorne report on fetal research: nice recommendations, shame about the reasoning. J. Med. Ethics 19, 114-120.
51. Kierstead, H. S. & Blakemore, W. F. 1997 Identification of postmitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J. Neuropathol. Exp. Neurol. 56, 1191-1201.
52. Kondoh, T., Pundt, L. L., Blount, J. P., Conrad, J. A. & Low, W. C. 1996 Transplantation of human fetal tissue from spontaneous abortions to a rodent model of Parkinson's disease. Cell Transplant. 5, 69-75.
53. Langford, L. A., Porter, S. & Bunge, R. P. 1988 Immortalized rat Schwann cells produce tumours in vivo. J. Neurocytol. 17, 521-529.
54. Lassmann, H., Bruck, W., Lucchinetti, C. F. & Rodriguez, M. 1997 Remyelination in multiple sclerosis. Mult. Scler. 3, 133-136.
55. Levi, A. D. O. & Bunge, R. P. 1994 Studies of myelin formation after transplantation of human Schwann cells into the severe combined immunodeficient mouse. Exp. Neurol. 130, 41-52.
56. Lipton, S. A. 1986 Blockade of electrical-activity promotes the death of mammalian retinal ganglion-cells in culture. Proc. Natl Acad. Sci. USA 83, 9774-9778.
57. Low, W. C., Eastlund, T., Verfaille, C., Hershel, M., Vurnig, B., Weese, K., Norris, B., Peterson, A. & Forbes, J. 1994 Human fetal tissue from spontaneous abortions as potential sources of donor tissue for cell transplantation therapy. Transplant. Proc. 26, 3500.
58. Ludwin, S. K. 1980 Chronic demyelination inhibits remyelination of the central nervous system. Lab. Invest. 43, 382-387.
59. Ludwin, S. 1988 Remyelination in the central nervous system and in the peripheral nervous system. Adv. Neurol. 47, 215-254.
60. McKay, J. S., Blakemore, W. F. & Franklin, R. J. 1997 The effects of the growth factor antagonist trapidil on remyelination in the CNS. Neuropathol. Appl. Neurobiol. 23, 56-58.
61. McKay, R. D. G. 1997 Stem cells in the central nervous system. Science 276, 66-71.
62. McMorris, F. A. & McKinnon, R. D. 1996 Regulation of oligodendrocyte development and CNS myelination by growth factors: prospects for therapy of demyelinating disease. Brain Pathol. 6, 313-329.
63. McMorris, F. A., Furlanetto, R. W., Mozell, R. L., Carson, M. J. & Raible, D. W. 1990 Regulation of oligodendrocyte development by insulin-like growth factors and cyclic nucleotides. Ann. NY Acad. Sci. 605, 101-109.
64. Malik, O., Scolding, N., Newcombe, J. & Compston, D. A. S. 1999 Growth factor expression and remyelination in lesions from patients with MS (Abstract.) J. Neurol. Neurosurg. Psychiat. (In the press.)
65. Martinez-Serrano, A. & Bjorklund, A. 1995 Gene transfer to the mammalian brain using neural stem cells: a focus on trophic factors, neuroregeneration, and cholinergic neuron systems. Clin. Neurosci. 3, 301-309.
66. MeyerFranke, A., Kaplan, M. R., Pfrieger, F. W. & Barres, B. A. 1995 Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15, 805-819.
67. Mirsky, R. & Jessen, K. R. 1999 The neurobiology of Schwann cells. Brain Pathol. 9, 293-311.
68. Morrissey, T. K., Bunge, R. P. & Kleitman, N. 1995a Human Schwann cells in vitro. I. Failure to differentiate and support neuronal health under co-culture conditions that promote full function of rodent cells. J. Neurobiol. 28, 171-189.
69. Morrissey, T. K., Kleitman, N. & Bunge, R. P. 1995b Human Schwann cells in vitro. II. Myelination of sensory axons following extensive purification and heregulin-induced expansion. J. Neurobiol. 28, 190-201.
70. Moreau, T., Thorpe, J., Miller, D., Moseley, I., Hale, G., Waldmann, H., Clayton, D., Wing, M., Scolding, N. & Compston, A. 1994 Preliminary evidence from magnetic resonance imaging for reduction in disease activity after lymphocyte depletion in multiple sclerosis. Lancet 344, 298-301.
71. Muir, D. A. & Compston, D. A. S. 1996 Growth factor stimulation triggers apoptotic cell death in mature oligodendrocytes. J. Neurosci. Res. 44, 1-11.
72. Noseworthy, J. H. (and 12 others) 1997 Intravenous immunoglobulin does not reverse recently acquired, apparently permanent weakness in multiple sclerosis. Ann. Neurol. 42, M115.
73. Ogata, J. & Feigin, I. 1975 Schwann cells and regenerated peripheral myelin in multiple sclerosis: an ultrastructural study. Neurology 25, 713-716.
74. Ozawa, K., Suchanek, G., Breitschopf, H., Bruck, W., Budka, H., Jellinger, K. & Lassmann, H. 1994 Patterns of oligoden-droglia pathology in multiple sclerosis. Brain 117, 1311-1322.
75. Perier, O. & Gregoire, A. 1965 Electron microscopic features of multiple sclerosis lesions. Brain 88, 937-952.
76. Platt, J. L. 1996 The immunological barriers to xenotransplantation. Crit. Rev. Immunol. 16, 331-358.
77. Polkinghorne, J. C. 1989 Review of the guidance on the research use of fetuses and fetal material. Cm 762, 1989. London: HMSO.
78. Prabhakar, S., D'Souza, S., Antel, J. P., McClaurin, J. A., Schipper, H. M. & Wang, E. 1995 Phenotypic and cell-cycle properties of human oligodendrocytes in-vitro. Brain Res. 672, 159-169.
79. Prineas, J. W. & Connell, F. 1979 Remyelination in multiple sclerosis. Ann. Neurol. 5, 22-31.
80. Prineas, J. W., Barnard, R. O., Kwon, E. E., Sharer, L. R. & Cho, E. S. 1993 Multiple sclerosis: remyelination of nascent lesions. Ann. Neurol. 33, 137-151.
81. Pundt, L. L., Kondoh, T. & Low, W. C. 1995 The fat of human glial cells following transplantation in normal rodents and rodent models of neurodegenerative disease. Brain Res. 695, 25-36.
82. Raff, M. C., Miller, R. H. & Noble, M. 1983 A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396.
83. Raine, C. S. & Cross, A. H. 1989 Axonal dystrophy as a consequence of long-term demyelination. Lab. Invest. 60, 714-725.
84. Raine, C. S. & Traugott, U. 1985 Remyelination in chronic relapsing experimental allergic encephalomyelitis and multiple sclerosis. In The pathology of the myelinated axon (ed. M. Adachi, A. Hirano & S. M. Aronson), pp. 229-275. New York: Igaku-Shoin.
85. Raine, C. S. & Wu, E. 1993 Multiple sclerosis: remyelination in acute lesions. J. Neuropathol. Exp. Neurol. 52, 199-204.
86. Ramon, C. A. & Avila, J. 1998 Olfactory ensheathing glia: properties and function. Brain Res. Bull. 46, 175-187.
87. Remy, P. (and 14 others) 1995 Clinical correlates of [F-18]fluorodopa uptake in 5 grafted parkinsonian-patients. Ann. Neurol. 38, 580-588.
88. Reynolds, B. A. & Weiss, S. 1996 Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13.
89. Reynolds, M. L. & Woolf, C. J. 1993 Reciprocal Schwann cell axon interactions. Curr. Opin. Neurobiol. 3, 683-693.
90. Rio Hortega, P. 1921 Estudios sobre la neuroglia. La glia de escasas radiciones (oligodendroglia). Biol. Real. Soc. Esp. d. Hist. Nat. January.
91. Rodriguez, M. & Lennon, V. A. 1990 Immunoglobulius promote remyelination in the central nervous system. Ann. Neurol. 27, 12-17.
92. Rodriguez, M., Lennon, V. A., Benveniste, E. N. & Merrill, J. E. 1987 Remyelination by oligodendrocytes stimulated by antiserum to spinal cord. J. Neuropathol. Exp. Neurol. 46, 84-95.
93. Rodriguez, M., Miller, D. J. & Lennon, V. A. 1996 Immunoglobulins reactive with myelin basic protein promote CNS remyelination. Neurology 46, 538-545.
94. Rosen, C. L., Bunge, R. P. & Ard, M. D. 1989 Type 1 astrocytes inhibit myelination by adult oligodendrocytes in vitro. J. Neurosci. 9, 3371-3379.
95. Rosenbluth, J. 1996 Glial transplantation in the treatment of myelin loss or deficiency. In The neurobiology of disease: contributions from neuroscience to clinical neurology (ed. H. Bostock, P. A. Kirkwood & A. H. Pullen), pp. 124-128. Cambridge University Press.
96. Rosenbluth, J., Hasegawa, M., Shirasaki, N., Rosen, C. L. & Liu, Z. 1990 Myelin formation following transplantation of normal fetal glia into myelin-deficient rat spinal cord. J. Neurocytol. 19, 718-730.
97. Rosenbluth, J., Liu, Z., Guo, D. & Schiff, R. 1993 Myelin formation by mouse glia in myelin-deficient rats treated with cyclosporine. J. Neurocytol. 22, 967-977.
98. Rudick, R. A., Cohen, J. A., Weinstock Guttman, B., Kinkel, R. P. & Ransohoff, R. M. 1997 Management of multiple sclerosis. N. Engl. J. Med. 337, 1604-1611.
99. Rutkowski J. L., Kirk, C. J., Lerner, M. A. & Tennekoon, G. I. 1995 Purification and expansion of human Schwann cells in vitro. Nature Med. 1, 80-83.
100. Sabel, B. A. 1997 Unrecognized potential of surviving neurons: within-systems plastictiy, recovery of function, and the hypothesis of minimal residual structure. Neuroscientist 3, 366-370.
101. Satoh, J. & Kim, S. U. 1994 Proliferation and differentiation of fetal human oligodendrocytes in culture. J. Neurosci. Res. 39, 260-272.
102. Scherer, S. 1999 Axonal pathology in demyelinating diseases (editorial; comment). Ann. Neurol. 45, 6-7.
103. Scolding, N. 1996 New cells for old: the ethics of using foetal cells for brain repair. Tablet 604-605.
104. Scolding, N. J. 1997 Strategies for repair and remyelination in demyelinating diseases. Curr. Opin. Neurol. 10, 193-200.
105. Scolding, N. J. 1998 Glial precursor cells in the adult human brain. Neuroscientist 4, 264-272.
106. Scolding, N. J., Rayner, P. J., Sussman, J., Shaw, C. & Compston, D. A. S. 1995 A proliferative adult human oligodendrocyte progenitor. NeuroReport 6, 441-445.
107. Scolding, N. J., Franklin, R. J. M., Stevens, S., Heldin, C. H., Compston, D. A. S. & Newcombe, J. 1998 Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 121, 2221-2228.
108. Scolding, N. J., Rayner, P. J. & Compston, D. A. S. 1999 Early oligodendrocyte progenitors and 'type-2' astrocytes are present in adult human while matter. Neuroscience 89, 1-5.
109. Seilhean, D., Gansmuller, A., Baronvan Evercooren, A., Gumpel, M. & Lachapelle, F. 1996 Myelination by transplanted human and mouse central nervous system tissue alter long-term cryopreservation. Acta Neuropathol. 91, 82-88.
110. Shi, J., Marinovich, A. & Barres, B. A. 1998 Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. J. Neurosci. 18, 4627-4636.
111. Skoff, R. P. 1996 The lineages of neuroglial cells. Neuroscientist 2, 335-344.
112. Snyder, E. Y. 1994 Grafting immortalized neurons to the CNS. Curr. Opin. Neurobiol. 4, 742-751.
113. Stangel, M., Compston, D. A. S. & Scolding, N. J. 1999 Soluble human polyclonal immunoglobulins do not influence oligodendrocyte behaviour in vitro. J. Neuroimmunol. 96, 228-233.
114. Svendsen, C. N., Clarke, D. J., Rosser, A. E. & Dunnett, S. B. 1996 Survival and differentiation of rat and human epidermal growth factor-responsive precursor cells following grafting into the lesioned adult central nervous system. Exp. Neurol. 137, 376-388.
115. Targett, M. P., Sussman, J., Scolding, N., O'Leary, M. T., Compston, D. A. S. & Blakemore, W. F. 1996 Failure to achieve remyelination of demyelinated rat axons following transplantation of glial cells obtained from the adult human brain. Neuropathol. Appl. Neurobiol. 22, 199-206.
116. Tontsch, U., Archer, D. R., DuboisDalcq, M. & Duncan, I. D. 1994 Transplantation of an oligodendrocyte cell line leading to extensive myelination. Prof. Natl Acad. Sci. USA 91, 11616-11620.
117. Trapp, B. D., Peterson, J., Ransohoff, R. M., Rudick, R. A., Mork, S. &. Bo, L. 1998 Axon transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278-285.
118. Trotter, J., Crang, J., Schachner, M. & Blakemore, W. 1991 Repair of central nervous system lesions by glial cells immortalised with an oncogene-carrying retrovirus. Schweiz. Arch. Neurol. Psychiat. 142, 102-104.
119. Utschneider, D. A., Archer, D. R., Koesis, J. D., Waxman, S. G. & Duncan, I. D. 1994 Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelin-deficient rat. Proc. Natl Acad. Sci. USA 91, 53-57.
120. Van den Berg, L. H., Bar, P. R., Sodaar, P., Mollee, I., Wokke, J. J. H. & Logtenberg, T. 1995 Selective expansion and long-term culture of human Schwann cells from sural nerve biopsies. Ann. Neurol. 38, 674-678.
121. Warrington, A. E., Barbarese, E. & Pfeiffer, S. E. 1993 Differential myelinogenic capacity of specific developmental stages of the oligodeudrocyte lineage upon transplantation into hypomyelinating hosts. J. Neurosci. Res. 34, 1-13.
122. Weiss, S., Reynolds, B. A., Vescovi, A. L., Morshead, C., Craig, C. G., Van der Kooy, D. 1996 Is there a neural stem cell in the mammalian forebrain? Trends Neurosci. 19, 387-393.
123. Wilson, H., Barnett, S. C. & Scolding, N. J. 1999 An adult human oligodendrocyte progenitor cell line. J. Neurol. Abst. (In the press.)
124. Wolswijk, G. & Noble, M. 1992 Cooperation between PDGF and FGF converts slowly dividing O-2A(adult) progenitor cells to rapidly dividing cells with characteristics of O-2A(perinatal) progenitor cells. J. Cell Biol. 118, 889-900.
125. Woodruff, R. H. & Franklin, R. J. M. 1997 Growth factors and remyelination in the CNS. Histol. Histopathol. 12, 459-466.
126. Yamamoto, T., Kawamura, J., Hashimoto, S. & Nakamura, M. 1991 Extensive, proliferation of peripheral type myelin in necrotic spinal cord lesions of multiple sclerosis. J. Neurol. Sci. 102, 163-169.
127. Yao, D. L., Liu, X., Hudson, L. D. & De Webster, H. F. 1996 Insulin-like growth factor-I given subcutaneously reduces clinical deficits, decreases lesion severity and upregulates synthesis of myelin proteins in experimental autoimmune encephalomyelitis. Life Sci. 58, 1301-1306.
128. Zhang, S. C., Ge, B. & Duncan, I. D. 1999 Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity. Proc. Natl Acad Sci. USA 96, 4089-4094.
129. Zhang, S. C., Lipsitz, D. & Duncan, I. D. 1998 Self-renewing canine oligodendroglial progenitor expanded as oligospheres. J. Neurosci. Res. 54, 181-190.