Experimental Models for Astrocyte Activation and Fibrous Gliosis

  • Lawrence F. Eng
Part of the NATO ASI Series book series (volume 2)

Abstract

Astrocytes are thought to perform a variety of metabolic and structural functions depending on the developmental, normal, or disease state of the central nervous system (CNS). In response to CNS injury or trauma, astrocytes proliferate and increase in size; their cytoplasmic processes become larger and more tortuous; and there is a substantial increase in the number of intermediate glial filaments and glial fibrillary acidic protein (GFAP) content. The mechanism of reactive GFAP accumulation is an area of active inquiry. It could result from decreased degradation. Rapid proteolytic degradation of GFAP in a continuous human glioma cell line grown in culture and as a solid tumor (1) and in rodent optic nerve and spinal cord has been reported (2, 3). Alternatively, increased synthesis of GFAP, as a result of translation of pre-existing GFAP mRNA, or de novo transcription of GFAP mRNA are possible explanations for this observation. Since glial filament production appears to play a role in CNS scarring and astrocyte differentiation, studies of GFAP activation and of cytoskeletal and metabolic functions of GFAP in astrocytes have been areas of investigation in our laboratory since we first reported and suggested that GFAP was a constituent of glial filaments (4, 5). If reactive fibrous gliosis could be inhibited or delayed in trauma and disease, the other cell types, oligodendroglia and neurons, might have the opportunity to respond and re-establish in a more normal manner; conversely, a highly anaplastic astrocytoma might be induced to differentiate.

Keywords

Dementia Hydrocortisone Tuberculosis Retina Histamine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bigbee, J. W., Bigner, D. D., Pegram, C., and Eng, L. F. (1983). Study of glial fibrillary acidic pro tein in a human glioma cell line grown in culture and as a solid tumor. J. Neurochem., 40, 460–467.PubMedCrossRefGoogle Scholar
  2. 2.
    Dearmond, S. J., fajardo, M., Naughton, S. A., and Eng, L. F. (1983). Degradation of glial fibrillary acidic protein by a calcium dependent proteinase: an electroblot study. Brain Res., 262, 275–282.PubMedCrossRefGoogle Scholar
  3. 3.
    Schlaepfer, W. W. and Zimmerman, V.-J. P. (1981). Calcium-mediated breakdown of glial filaments and neurofilaments in rat optic nerve and spinal cord. Neurochem. Res., 6, 243–255.PubMedCrossRefGoogle Scholar
  4. 4.
    Eng, L. F., Gerstl, B., and Vanderhaeghen, J. J. (1970). A study of proteins in old multiple sclerosis plaques. Trans. Am. Soc. Neurochem., 1, 42.Google Scholar
  5. 5.
    Eng, L. F., Vanderhaeghen, J. J., Bignami, A., and Gerstl, B. (1971). An acidic protein isolated from fibrous astrocytes. Brain Res., 28, 351–354.PubMedCrossRefGoogle Scholar
  6. 6.
    Beguin, P., Shooter, E. M., and Eng, L. F. (1980). Cell-free synthesis of glial fibrillary acidic protein. Neurochem. Res., 5, 513–521.PubMedCrossRefGoogle Scholar
  7. 7.
    Bigbee, J. W. and Eng, L. F. (1982). Glial fibrillary acidic protein synthesized in vitro using messenger RNA from jimpy mouse spinal cord. Brain Res., 249, 383–386.PubMedCrossRefGoogle Scholar
  8. 8.
    Bigbee, J. W. and Eng, L. F. (1982). Analysis and comparison of in vitro synthesized glial fibrillary acidic protein with rat CNS intermediate filament proteins. J. Neurochem., 38, 130–134.PubMedCrossRefGoogle Scholar
  9. 9.
    Bigbee, J. W., Bigner, D. D., and Eng, L. F. (1983). Glial fibrillary acidic protein synthesized in vitro using messenger RNA from a human glioma cell line. J. Neuropathol. Exp. Neurol., 42, 80–86.PubMedCrossRefGoogle Scholar
  10. 10.
    Browning, E. T. (1985). Neurohormone stimulated cytoskeletal protein phosphorylation in astro cytes. Trans. Am. Soc. Neurochem., 16, 214.Google Scholar
  11. 11.
    Browning, E. T. and Ruina, M. (1984). Glial fibrillary acidic protein: norepinephrine stimulated phosphorylation in intact C-6 glioma cells. J. Neurochem., 42, 718–726.PubMedCrossRefGoogle Scholar
  12. 12.
    McCarthy, K. K., Prime, J., Harmon, T., and Pollenz, R. S. (1985). Receptor mediated phosphorylation of astroglial intermediate filament proteins in culture. J. Neurochem., 44, 723–730.PubMedCrossRefGoogle Scholar
  13. 13.
    Bignami, A., Eng, L. F., Dahl, D., and Uyeda, C. T. (1972). Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res., 43, 429–435.PubMedCrossRefGoogle Scholar
  14. 14.
    Uyeda, C. T., Eng, L. F., and Bignami, A. (1972). Immunological study of the glial fibrillary acidic protein. Brain Res., 37, 81–89.PubMedCrossRefGoogle Scholar
  15. 15.
    Eng, L. F. and Rubinstein, L. J. (1978). Contribution of immunohistochemistry to diagnostic problems of human cerebral tumors. J. Histochem. Cytochem., 26, 513–522.PubMedCrossRefGoogle Scholar
  16. 16.
    Eng, L. F. and Bigbee, J. W. (1978). Immunohistochemistry of nervous system-specific antigens. In: Advances in Neurochemistry Vol. 3, 43–98.Google Scholar
  17. 17.
    Bignami, A., Dahl, D., and Rueger, D. G. (1980). Glial fibrillary acidic (GFA) protein in normal neural cells and in pathological conditions. In: Advances in Cellular Neurobiology Vol. 1, 285–310.Google Scholar
  18. 18.
    deArmond, S. J., Eng, L. F., and Rubinstein, L. J. (1980). The application of glial fibrillary acidic (GFA) protein immunohistochemistry in neurooncology. A progress report. Pathol. Res. Pract., 168, 374–394.Google Scholar
  19. 19.
    Eng, L. F. (1980). The glial fibrillary acidic (GFA) protein. In: Proteins of the Nervous System, 2nd edition, 85–117.Google Scholar
  20. 20.
    Eng, L. F. and DeArmond, S.J. (1982). Immunocytochemical studies of astrocytes in normal development and disease. In: Advances in Cellular Neurobiology Vol. 3, 145–171.Google Scholar
  21. 21.
    Eng, L. F. and DeArmond, S. J. (1983). Immunochemistry of the glial fibrillary acidic protein. In: Progress in Neuropathology Vol. 5, 19–39.Google Scholar
  22. 22.
    Rubinstein, L. J. (1982). Tumors of the central nervous system. In: Atlas of Tumor Pathology Supplement, 2nd Ser., Fasc. 6, Armed Forces Institute of Pathology, Washington, D.C.Google Scholar
  23. 23.
    Dahl, D. and Bignami, A. (1983). The glial fibrillary acidic protein and astrocytic 10 nanometer filaments. In: Handbook of Neurochemistry, 2nd edition, Vol. 5, 127–151.Google Scholar
  24. 24.
    Eng, L. F. (1985). Glial fibrillary acidic protein: The major protein of glial intermediate filaments in differentiated astrocytes. J. Neuroimmunol., 8, 203–214.PubMedCrossRefGoogle Scholar
  25. 25.
    Hatfield, J. S., Skoff, R. P., Maisel, H., and Eng, L. F. (1984). Glial fibrillary acidic protein is localized in the lens epithelium. J. Cell Biol. 98, 1895–1898.PubMedCrossRefGoogle Scholar
  26. 26.
    Hatfield, J. S., Skoff, R. P., Maisel, H., Eng, L. F., and Bigner, D. D. (1985). The lens epithelium contains glial fibrillary acidic protein. J. Neuroimmunol., 8, 347–357.PubMedCrossRefGoogle Scholar
  27. 27.
    Chiu, F-C. and Goldman, J. E. (1985). Regulation of glial fibrillary acidic protein (GFAP) expression in CNS development and in pathological states. J. Neuroimmunol. 8, 283–292.PubMedCrossRefGoogle Scholar
  28. 28.
    Goldman, J. E. and Chiu, F-C. (1984). Growth kinetics, cell shape, and the cytoskeleton of primary astrocyte cultures. J. Neurochem., 42, 175–184.PubMedCrossRefGoogle Scholar
  29. 29.
    Chiu, F-C. and Goldman, J. E. (1984). Synthesis and turnover of cytoskeletal proteins in cultured astrocytes. J. Neurochem., 42, 166–174.PubMedCrossRefGoogle Scholar
  30. 30.
    Goldman, J. E. and Chiu, F-C. (1984). Dibutyryl cyclic AMP causes intermediate filament accumulation and actin reorganization in primary astrocytes. Brain Res., 306, 85–95.PubMedCrossRefGoogle Scholar
  31. 31.
    Morrison, R. S., DeVellis, J., Lee, Y-L., Bradshaw, R. A., and Eng, L. F. (1985). Hormone and growth factors regulate the biosynthesis of glial fibrillary acidic protein in rat brain astrocytes. J. Neurosci. Res (in press).Google Scholar
  32. 32.
    Wu, D. K., Morrison, R. S., and Devellis, J. (1985). Modulation of beta-adrenergic response in rat brain astrocytes by serum and hormones. J. Cell Physiol, 122, 73 - 80.Google Scholar
  33. 33.
    deArmond, S. J., Lee, Y-L., and Eng, L. F. (1983). Turnover of glial fibrillary acidic protein in the mouse. J. Neurochem, 41 ( Suppl. ), S3.Google Scholar
  34. 34.
    DeArmond, S. J., Lee, Y-L., Kretzschmar, H. A., and Eng, L. F. (1985). Turnover of glial filaments and neurofilaments in mouse spinal cord. J. Neurochem.(Submitted for publication).Google Scholar
  35. 35.
    Smith, M. E., Perret, V., and Eng, L. F. (1984). Metabolic studies in vitro of the CNS cytoskeletal proteins: Synthesis and degradation. Neurochem. Res. 9, 1493–1507.PubMedCrossRefGoogle Scholar
  36. 36.
    Hortega, P. del Rio and Penfield, W. (1927). Cerebral cicatrix. The reaction of neuroglia and microglia to brain wounds. Bull. Johns Hopkins Hosp., 31, 278–303.Google Scholar
  37. 37.
    Cavanagh, J. B. (1970). The proliferation of astrocytes around a needle wound in the rat brain. J. Anat., 106, 471–487.PubMedGoogle Scholar
  38. 38.
    Lapham, L. W. and Johnstone, M. A. (1964). Cytologic and cytochemical studies of neuroglia. III. The DNA content of fibrous astrocytes with implication concerning the nature of these cells. J. Neuropathol. Exp. Neurol. 23, 419–430.PubMedCrossRefGoogle Scholar
  39. 39.
    Nathaniel, E. J. H. and Nathaniel, D. R. (1977). Astroglial response to degeneration of dorsal root fibers in adult rat spinal cord. Exp. Neurol., 54, 60–76.PubMedCrossRefGoogle Scholar
  40. 40.
    Bignami, A. and Dahl, D. (1976). The astroglial response to stabbing. Immunofluorescence studies with antibodies to astrocyte-specific protein (GFA) in mammalian and submammalian vertebrates. Neuropathol. Appl. Neurobiol., 2, 99–111.CrossRefGoogle Scholar
  41. 41.
    Amaducci, L. A., Forno, K. I., and Eng, L. F. (1981). Immunohistochemical study of glial fibrillary acidic (GFA) protein astrocytes following cryogenic lesion of the rat brain. Neurosci. Lett., 21, 27 - 32.Google Scholar
  42. 42.
    Dahl, D., Cosby, C. J., and Bignami, A. (1981). Filament proteins in rat optic nerves undergoing Wallerian degeneration. Exp. Neurol., 71, 421–430.PubMedCrossRefGoogle Scholar
  43. 43.
    Dahl, D., Strocchi, P., and Bignami, A. (1982). Vimentin in the central nervous system. A study of the mesenchymal-type intermediate filament-protein in Wallerian degeneration and in postnatal rat development by two-dimensional gel electrophoresis. Differentiation, 22, 185–190.PubMedCrossRefGoogle Scholar
  44. 44.
    Norenberg, M. D. (1983). Immunohistochemistry of glutamine synthetase. In: Glutamine, Gluta-mate, and GABA in the Central Nervous System, 95–111.Google Scholar
  45. 45.
    Nathaniel, E. J. H. and Nathaniel, D. R. (1981). The reactive astrocyte. In: Advances in Cellular Neurobiology Vol. 2, 249–301.Google Scholar
  46. 46.
    Ohmichen, M. (1980). Enzyme-histochemical differentiation of neuroglia and microglia: A contribution to the cytogenesis of microglia and globoid cells. Pathol. Res. Pract., 168, 344–373.Google Scholar
  47. 47.
    Latov, N., Nilaver, G., and Zimmerman, A. (1979). Fibrillary astrocytes proliferate in response to brain injury. Dev. Biol., 72, 381 –384.PubMedCrossRefGoogle Scholar
  48. 48.
    Barrett, C. P., Guth, L., Donati, E. J., and Krikorjan, J. G. (1981). Astroglial reaction in the gray matter lumbar segments after midthoracic transection of the adult rat spinal cord. Exp. Neurol., 73, 365–377.PubMedCrossRefGoogle Scholar
  49. 49.
    Polak, M., Haymaker, W., Johnson, J. E., and D’Amelio, F. (1982). Neuroglia and their reactions. In: Histology and Histopathology of the Nervous System Vol. 1, 363–480.Google Scholar
  50. 50.
    Wekerle, H. (1984). The lesion of acute experimental autoimmune encephalomyelitis. Isolation and membrane phenotypes of perivascular infiltrates from encephalitic rat brain white matter. Lab. Invest., 51, 199–205.PubMedGoogle Scholar
  51. 51.
    Waldor, M. K., Sriram, S., Hardy, R., Herzenberg, L. A., Herzenberg, L. A., Lanier, L., Lim, M. and Steinman, L. (1985). Reversal of experimental allergic encephalomyelitis with monoclonal antibody to a T-cell subset marker. Science, 227, 415–417.PubMedCrossRefGoogle Scholar
  52. 52.
    Smith, M. E., Somera, F. P., and Eng, L. F. (1983). Immunocytochemical staining for glial fibrillar acidic protein and the metabolism of cytoskeletal proteins in experimental allergic encephalomyelitis. Brain Res., 264, 241–253.PubMedCrossRefGoogle Scholar
  53. 53.
    Brown, A. M. and Mcfarlin, D. E. (1981). Relapsing experimental allergic encephalomyelitis in the SJL/J mouse. Lab. Invest., 45, 278–284.PubMedGoogle Scholar
  54. 54.
    Smith, M. E., Somera, F. P., Swanson, K., and Eng, L. F. (1984). Glial fibrillary acidic protein in acute and chronic relapsing experimental allergic encephalomyelitis (EAE). In: Experimental Allergic Encephalomyelitis: A Useful Model for Multiple Sclerosis, 139–144.Google Scholar
  55. 55.
    Smith, M. E., Somera, F. P., and Eng, L. F. (1984). GFAP in chronic relapsing EAE in the SJL/J mouse. Trans. Am. Soc. Neurochem., 15, 154.Google Scholar
  56. 56.
    Linington, C., Suckling, A. J., Weir, M. D., and Cuzner, M. L. (1984). Changes in the metabolism of glial fibrillary acid protein (GFAP) during chronic relapsing experimental allergic encephalomyelitis in the strain 13 guinea-pig. Neurochem., Int., 6, 393–401.CrossRefGoogle Scholar
  57. 57.
    Dahl, D., Bignami, A., Weber, K., and Osborn, M. (1981). Filament proteins in rat optic nerves undergoing Wallerian degeneration. Localization of vimentin, the fibroblastic 100 Å filament protein, in normal and reactive astrocytes. Exp. Neurol., 73, 496.PubMedCrossRefGoogle Scholar
  58. 58.
    Fedoroff, S., McAuley, W. A. J., Houie, J. D., and Devon, R. M. (1984). Astrocyte cell lineage. V. Similarity of astrocytes that form in the presence of dBcAMP in cultures to reactive astrocytes in vivo. J. Neurosci. Res., 12, 15–27.CrossRefGoogle Scholar
  59. 59.
    Dixon, R. G. and Eng, L. F. (1981). Glial fibrillary acidic protein in the retina of the developing albino rat: an immunoperoxidase study of paraffin-embedded tissue. J. Comp. Neurol., 195, 305–322.CrossRefGoogle Scholar
  60. 60.
    Bignami, A. and Dahl, D. (1979). The radial glia of Müller in the rat retina and their response to injury. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. Exp. Eye Res., 28, 63–69.PubMedCrossRefGoogle Scholar
  61. 61.
    Shaw, G. and Weber, K. (1983). The structure and development of the rat retina: an immunofluorescence microscopial study using antibodies specific of intermediate filament proteins. Europ. J. Cell Biol., 30, 219–232.PubMedGoogle Scholar
  62. 62.
    Eisenfeld, A. J., Bunt-Milam, A. H., and Sarthy, P. V. (1984). Müller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest. Ophthalmol Vis. Sci, 25, 1321–1328.Google Scholar
  63. 63.
    O’Dowd, D. K. and Eng, L. F. (1979). Immunocytochemical localization of the glial fibrillary acidic (GFA) protein in the Müller cell of the human retina. Soc. Neurosci. Abstr., 5, 431.Google Scholar
  64. 64.
    Wacker, W. B., Donoso, L. A., Kalsow, C. M., Yankeelov, J. A., Jr., and Organisciak, D. T. (1977). Experimental allergic uveitis. Isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina. J. Immunol, 119, 1949.PubMedGoogle Scholar
  65. 65.
    Faure, J. P. (1980). Autoimmunity and the retina. Curr. Top Eye Res, 2, 215.PubMedGoogle Scholar
  66. 66.
    Nussenblatt, R. B., Kuwabara, T., de Monasterio, F. M., and Wacker, W. B. (1981). Santigen uveitis in primates. A new model for human disease. Arch. Ophthalmol, 99, 1090.PubMedGoogle Scholar
  67. 67.
    Mochizuki, M., Charley, J., Kuwabara, T., Nussenblatt, R. B., and Gery, I. (1983). Involvement of the pineal gland in rats with experimental autoimmune uveitis. Invest. Ophthalmol. Vis. Sci., 24, 1333–1338.Google Scholar
  68. 68.
    Mochizuki, M., Kuwabara, T., Chan, C-C., Nussenblatt, R. B., Metcalfe, D. D., and Gery, I. (1984). An association between susceptibility to experimental autoimmune uveitis and choroidal mast cell numbers. J. Immunol, 133, 1699.PubMedGoogle Scholar
  69. 69.
    Mochizuki, M., Kuwabara, T., McAllister, C., Nussenblatt, R. B., and Gery, I. (1985). Adoptive transfer of experimental autoimmune uveoretinitis in rats. Immunopathogenic mechanisms and histologic features. Invest. Ophthalmol. Vis. Sci, 26, 1–9.PubMedGoogle Scholar
  70. 70.
    Chan, C-C., Nussenblatt, R. B., Mochizuki, M., Palestine, A. G., BenEzra, D., and Gery, I. (1985). Subsets of T-lymphocytes in inflammatory sites of ocular autoimmune diseases in man and rats. Trans. Am. Soc. Neurochem, 16, 251.Google Scholar
  71. 71.
    Chan, C-C., Mochizuki, M., Nussenblatt, R. B., Palestine, A. G., McaLlister, C., Gery, I., and Benezra, D. (1985). T-lymphocyte subsets in experimental autoimmune uveitis. Clin. Immunol. Immunopathol, 35, 103–110.PubMedCrossRefGoogle Scholar
  72. 72.
    Ortiz-Ortiz, L., Nakamura, R. M., and Weigle, W. O. (1976). T cell requirement for experimental allergic encephalomyelitis induced in the rat. J. Immunol, 117, 576–579.PubMedGoogle Scholar
  73. 73.
    Lapham, L. W. (1962). Cytological and cytochemical studies of neuroglia. I. A study of the problem of amitosis in reactive protoplasmic astrocytes. Am. J. Pathol, 41, 1–21.PubMedGoogle Scholar
  74. 74.
    Skoff, R. P. (1975). The fine structure of pulse-labelled (3H-thymidine) cells in degenerating rat optic nerve. J. Comp. Neurol, 161, 595–612.PubMedCrossRefGoogle Scholar
  75. 75.
    Skoff, R. P. and Vaughn, J. E. (1971). An autoradiographic study of cellular proliferation in degenerating rat optic nerve. J. Comp. Neurol, 141, 133–156.PubMedCrossRefGoogle Scholar
  76. 76.
    Vaughn, J. E., Hinds, P. L., and Skoff, R. P. (1970). Electron microscopic studies of Wallerian degeneration in the optic nerve of the rat. I.Themultipotentialglia. J. Comp. Neurol, 140, 175–206.PubMedCrossRefGoogle Scholar
  77. 77.
    Ludwin, S. K. (1985). Reaction of oligodendrocytes and astrocytes to trauma and implantation. A combined autoradiographic and immunohistochemical study. Lab. Invest, 52, 20–30.PubMedGoogle Scholar
  78. 78.
    Mathewson, A. J. and Berry, M. (1985). Observations on the astrocyte response to a cerebral stab wound in adult rats. Brain Res, 327, 61–69.PubMedCrossRefGoogle Scholar
  79. 79.
    Das, G. D. (1974). Transplantation of embryonic neural tissue in the mammalian brain. I. Growth and differentiation of neuroblasts from various regions of the embryonic brain in the cerebellum of neonate rats. Life Sci, 4, 93–124.Google Scholar
  80. 80.
    Das, G. D., Hallas, B. H., and Das, K. G. (1980). Transplantation of brain tissue in the brain of rat. I. Growth characteristics of neocortical transplants from embryos of different ages. Am. J. Anat, 158, 135–145.PubMedCrossRefGoogle Scholar
  81. 81.
    Jaeger, C. B. and Lund, R. D. (1980). Transplantation of embryonic occipital cortex to the brain of newborn rats. An autoradiographic study of transplant histogenesis. Exp. Brain Res, 40, 265–272.PubMedCrossRefGoogle Scholar
  82. 82.
    Oblinger, M. M., Hallas, B. H., and Das, G. D. (1980). Neocortical transplants in the cerebellum of the rat: their afferents and efferents. Brain Res, 189, 228–232.PubMedCrossRefGoogle Scholar
  83. 83.
    Stenevi, U., Bjorklund, A., and Svendgaard, N.-N. (1976). Transplantation of central and peripheral monoamine neurons to the adult rat brain: techniques and conditions for survival. Brain Res, 114, 1–20.PubMedCrossRefGoogle Scholar
  84. 84.
    Nornes, H., Bjorklund, A., and Stenevi, U. (1983). Reinnervation of the denervated adult spinal cord of rats by intraspinal transplants of embryonic brain stem neurons. Cell Tissue Res, 230, 1535.Google Scholar
  85. 85.
    Bjorklund, A. and Stenevi, U. (1984). Intracerebral neural implants: neuronal replacement and reconstruction of damaged circuitries. Annual Rev. Neurosci, 7, 279–308.CrossRefGoogle Scholar
  86. 86.
    Das, G. D. (1983). Neural transplantation in the spinal cord of the adult mammal. In: Spinal Cord Reconstruction, 367–396.Google Scholar
  87. 87.
    Das, G. D. (1983). Neural transplantation in mammalian brain some conceptual and technical con siderations. In: Neural Tissue Transplantation Research, 1–64.Google Scholar
  88. 88.
    Das, G. D. (1983). Neural transplantation in the spinal cord of adult rats. Conditions, survival, cytology and connectivity of the transplants. J. Neurol. Sci, 62, 191–210.PubMedCrossRefGoogle Scholar
  89. 89.
    Kromer, L. F., Bjorklund, A., and Stenevi, U. (1983). Intracephalic neural implants in the adult rat brain. I. Growth and mature organization of brainstem, cerebellar and hippocampal implants. J. Comp. Neurol, 218, 433–459.PubMedCrossRefGoogle Scholar
  90. 90.
    Reier, P. J., Perlow, M. J., and Guth, L. (1983). Development of embryonic spinal cord transplants in the rat. Develop. Brain Res, 10, 201–219.CrossRefGoogle Scholar
  91. 91.
    Reier, P. J. (1985). Neural tissue grafts and repair of the injured spinal cord. Neuropathol. Appl. Neurobiol, 11, 81–104.PubMedCrossRefGoogle Scholar
  92. 92.
    Reier, P. J., Bregman, B. S., and Wujek, J. R. (1985). Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J. Comp., Neurol. (Submitted for publication).Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1987

Authors and Affiliations

  • Lawrence F. Eng
    • 1
    • 2
  1. 1.Department of PathologyStanford University School of MedicinePalo AltoUSA
  2. 2.Veterans Administration Medical CenterPalo AltoUSA

Personalised recommendations