Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity

Nature Medicine

Volumn 4, Issue 3, 1998, Pages 291-297

  Mcdonald, John W ^a   Althomsons, Sandy P ^a   Hyrc, Krzysztof L ^a   Choi, Dennis W ^a   Goldberg, Mark P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL HYPOXIA; CONTROLLED STUDY; FOREBRAIN; MOUSE; NEUROTOXICITY; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANOXIA; ANTIOXIDANTS; BRAIN ISCHEMIA; CELL DEATH; CELLS, CULTURED; GLUTAMIC ACID; GROWTH SUBSTANCES; KAINIC ACID; MALE; MICE; MICROINJECTIONS; OLIGODENDROGLIA; PROSENCEPHALON; RATS; RATS, INBRED STRAINS; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; SIGNAL TRANSDUCTION; TIME FACTORS;

ANIMALIA;

EID: 0031952612     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm0398-291     Document Type: Article

References (60)

1. Bunge, R.P. et al. Observations on the pathology of human spinal cord injury: A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. in Advances in Neurology (ed. Seil, F.J.) 59, 75-89 (Raven Press, New York, 1993).
2. Gledhill, R.F., Harrison, B.M. & McDonald, W.I. Demyelination after acute spinal cord compression. Exp. Neurol. 38, 472-487 (1973).
3. Hirano, A, Levine, S. & Zimmerman, H.M. Experimental cyanide encephalopathy: Electron microscopic observations of early lesions in white matter. J. Neuropathol. Exp. Neurol. 26, 200-213 (1967).
4. Okeda, R. et al. The pathogenesis of carbon monoxide encephalopathy in the acute phase-physiological and morphological correlation. Acta Neuropathol. 54, 1-10 (1981).
5. Fisher, C.M. Lacunes: Small, deep cerebral infarcts. Neurology 15, 774-784 (1965).
6. Plum, F., Posner, J.B. & Hain, R.F. Delayed neurological deterioration after anoxia. Arch. Intern. Med. 110, 56-63 (1962).
7. Ginsberg, M.D. Delayed neurological deterioration following hypoxia. in Advances in Neurology (ed. Fahn, S.) 26, 21-45 (Raven Press, New York, 1979).
8. Banker, B.Q. & Larroche, J-C. Periventricular leukomalacia of infancy. Arch. Neurol. 7, 32-56 (1962).
9. Rivkin, M.J. & Volpe, J.J. Hypoxic-ischemic brain injury in the newborn. Semin. Neurol. 13, 30-90 (1993).
10. Pantoni, L, Garcia, J.H. & Gutierrez, J.A. Cerebral white matter is highly vulnerable to ischemia. Stroke 27, 1641-1647 (1996).
11. Raine, C.S. The Norton Lecture: A review of the oligodendrocyte in the multiple sclerosis lesion. J. Neuroimmunol. 77, 135-152 (1997).
12. Benveniste, H., Drejer, J. Schousboe, A. & Diemer, N.H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral dialysis. J. Neurochem. 43, 1369-1374 (1984).
13. Rothman, S.M. & Olney, J.W. Excitotoxicity and the NMDA receptor. Trends Neurosci. 10, 299 (1987).
14. Choi, D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623 (1988).
15. Steinhauser, C. & Gallo, V. News on glutamate receptors in glial cells. Trends Neurosci. 19, 339-345 (1996).
16. 2+ responses in cortical oligodendrocyte progenitors and CG-4 cells. J. Neurosci. Res. 42, 124-130 (1995).
17. David, J.C. et. al. AMPA receptor activation is rapidly toxic to cortical astrocytes when desensitization is blocked. J. Neurosci. 16, 200-209 (1995).
18. Yamada, K.A. & Rothman, S.M. Diazoxide blocks glutamate desensitization and prolongs excitatory postsynaptic currents in rat hippocampal neurons. J. Physiol. (Lond.)458, 409-123 (1992).
19. Patneau, O.K., Vyklicky, L. & Mayer, M.L. Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate J. Neurosci. 13, 3496-3509 (1993).
20. Yoshioka, A. et al. α-Amino-3-hydroxy-5-methyl-4-isoxazoleproprionate (AMPA) receptors mediate excitotoxicity in the oligodendroglial lineage. Neurochemistry 64, 2442-2448 (1995).
21. Oka, A, Belliveau, M.J., Rosenberg, P.A. & Volpe, J.J. Vulnerability of oligodendroglia to glutamate: Pharmacology, mechanisms, and prevention, J. Neurosci. 13, 1441-1453 (1993).
22. Chot, D.W., Maulucci-Gedde, M. & Kriegstein, R., Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 357-368 (1987).
23. Frandsen, A. & Schousboe, A. Development of excitatory amino acid induced cytotoxicity in cultured neurons. Int. J. Dev. Neurosci. 8, 209-216 (1990).
24. Zhong, J. et al. Expression of mRNAs encoding subunits of the N-methyl-D-aspartate receptor in cultured cortical neurons. Mol. Pharmacol. 45, 846-853 (1994).
25. Wahl, P., Honore, T., Drejer, J. & Schousboe, A. Development of binding sites for excitatory amino acids in cultured cerebral cortex neurons. Int. J. Dev. Neurosci. 9, 287-296 (1991).
26. McDonald, J.W. & Johnston, M.V. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res. Rev. 15, 41-70 (1990).
27. McCarthy, K.D. & de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902 (1980).
28. Barres, B.A. et al. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46 (1992).
29. Ishii, S. & Volpe, J.J. Establishment of a culture system for the study of oligodendroglial development: Complementary effects of boiled serum and astrocyte extract. Dev. Neurosci. 14, 230-237 (1992).
30. Barres, B.A., Schmid, R., Sendnter, M. & Raff, M.C. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 283-295 (1993).
31. Oh, L.Y. & Yong, V.W. Astrocytes promote process outgrowth by adult human oligodendrocytes in vitro through the interaction between bFGF and astrocyte extracellular matrix. Glia 17, 237-253 (1996).
32. McDonald, J.W. et al. Cyclosporine induces neuronal apoptosis and selective oligodendrocyte death in cortical cultures. Ann. Neurol. 40, 750-758 (1996).
33. Wolswijk, G. & Noble, M. Identification of an adult-specific glial progenitor cell. Development 105, 387-400 (1989).
34. Miller, R.H. Oligodendrocyte origins. Trends Neurosci. 19, 92-96 (1996).
35. Petralia, R.S. & Wenthold, R.J. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318, 329-354 (1992).
36. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (1985).
37. Louis, J.C., Magal, E., Takayama, S. & Varon, S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 259, 689-692 (1993).
38. D'Souza, S.D., Alinauskas, K.A. & Antel, J.P. Ciliary neurotrophic factor selectively protects human oligodendrocytes from tumor necrosis factor-mediated injury. J. Neurosci. Res. 43, 289-298 (1996).
39. Noble, M. & Mayer-Proschel, M. On the track of cell survival pharmaceuticals in the oligodendrocyte type-2 lineage. Perspect. Dev. Neurobiol. 3, 121-131 (1996).
40. Kahn, M.A. & De Vellis, J. Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia 12, 87-98 (1994).
41. Rosenberg, P.A., Amin, S. & Leitner, M. Glutamate uptake disguises neurotoxic potency of glutamate agonists in cerebral cortex in dissociated cell culture. J. Neurosci. 12, 56-61 (1992).
42. Bridges, R.J. et al. Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereomer. J. Med. Chem. 34, 717-725 (1991).
43. Cotdberg, M.P. & Choi, D.W. Combined oxygen and glucose deprivation in cortical cell culture: Calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. 13, 3510-3524 (1993).
44. Friedman, B. et al. In situ demonstration of mature oligodendrocytes and their processes: An immunocytochemical study with a new monoclonal antibody, Rip. Glia 2, 380-390 (1989).
45. Koh, J.Y., Goldberg, M.P., Hartley, D.M. & Choi, D.W. Non-NMDA receptor-mediated neurotoxicity in cortical culture. J. Neurosci. 10, 693-705 (1990).
46. Kaku, D.A., Goldberg, M.P. & Choi, D.W. Antagonism of non-NMDA receptors augments the neuroprotective effect of NMDA receptor blockade in cortical cultures subjected to prolonged deprivation of oxygen and glucose. Brain Res. 554, 344-347 (1991).
47. Ratan, R.R., Murphy, T.H. & Baraban, J.M. Oxidative stress induces apoptosis in embryonic cortical neurons. J. Neurochem. 62, 37-379 (1994).
48. McDonald et al. Susceptibility to apoptosis is enhanced in immature cortical neurons. Brain Res. 759, 228-232 (1997).
49. Yoshioka, A., Bacskai, B. & Pleasure, D. Pathophysiology of oligodendroglial excitotoxicity. J. Neurosci. Res. 46, 427-437 (1996).
50. Kerr, J.F.R., Wyllie, A.M. & Currie, A.R. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257 (1972).
51. Bonfoco, E. et al Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166 (1995).
52. Gwag, B.J. et al Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience 68, 615-619 (1995).
53. Coyle, J.T., Molliver, M.E. & Kuhar, M.J. In situ injection of kainic acid: A new method for selectively lesioning neuronal cell bodies while sparing axons of passage. J. Comp. Neurol. 180, 301-324 (1978).
54. Dusart, I., Marty, S. & Peschanski, M. Demyelination, and remyelination by Schwann cells and oligodendrocytes after kainate-induced neuronal depletion in the central nervous system. Neuroscience 51, 137-148 (1992).
55. Zaczek, R., Simonton, S. & Coyle, J.T. Local and distant neuronal degeneration following intrastriatal injection of kainic acid. J. Neuropathol. Exp. Neurol. 39, 245-264 (1980).
56. Waxman, S.G. Conduction in myelinated, unmyelinated, and demyelinated fibers. Arch, Neurol. 34, 585-598 (1977).
57. Sheardown, M.J., Suzdak, P.D. & Nordholm, L. AMPA, but not NMDA, receptor antagonism is neuroprotective in gerbil global ischaemia, even when delayed 24h, Eur J. Pharmacol. 236, 347-353 (1993).
58. Wrathall, J.R., Bouzoukis, J. & Choiniere, D. Effect of kynurenate on functional deficits resulting from traumatic spinal cord injury. Eur. J. Pharm. 218, 273-281 (1992).
59. Wrathall, J.R., Choiniere, D. & Teng, Y.D. Dose-dependent reduction of tissue loss and functional impairment after spinal cord trauma with the AMPA/kainate antagonist NBQX. J. Neurosci. 14, 6598-6607 (1994).
60. Matute C., Sanchez-Gomez M.V., Martinez-Millan L. & Miledi R. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc. Natl. Acad. Sci. 94, 8830-8835 (1997).