Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity

Journal of Neuroscience Research

Volumn 71, Issue 2, 2003, Pages 237-245

  Rosenberg, Paul A ^a,b   Dai, Weimin ^a   Gan, Xiao Dong ^a   Ali, Sanjida ^a   Fu, Jennifer ^a   Back, Stephen A ^a   Sanchez, Russell M ^a   Segal, Michael M ^a   Follett, Pamela L ^a   Jensen, Frances E ^a   Volpe, Joseph J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Cerebral palsy; Excitotoxicity; Glutamate; Hypoxia; Ischemia; Periventricular leukomalacia

Indexed keywords

GLUTAMATE RECEPTOR; KAINIC ACID; MYELIN BASIC PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MYELINATION; NEUROTOXICITY; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANIMALS, NEWBORN; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SURVIVAL; CILIARY NEUROTROPHIC FACTOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG INTERACTIONS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FIBROBLAST GROWTH FACTORS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MYELIN BASIC PROTEINS; OLIGODENDROGLIA; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE;

EID: 12244302883     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10472     Document Type: Article

References (51)

1. Back SA, Gan XD, Li Y, Rosenberg PA, Volpe JJ. 1998. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 18:6241-6253.
2. Back SA, Khan R, Gan XD, Rosenberg PA, Volpe JJ. 1999. A new Alamar blue viability assay to rapidly quantify oligodendrocyte death. J Neurosci Methods 91:47-54.
3. Bansal R, Pfeiffer SE. 1989. Reversible inhibition of oligodendrocyte progenitor differentation by a monoclonal antibody against surface galactolipids. Proc Natl Acad Sci USA 86:6181-6185.
4. Barres BA, Koroshetz WJ, Swartz KJ, Chun LLY, Corey DP. 1990. Ion channel expression by white matter glia: The O2A glial progenitor cell. Neuron 4:507-524.
5. Barres BA, Lazar MA, Raff MC. 1994. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120:1097-1108.
6. Bergles DE, Roberts JDB, Somogyi P, Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
7. Choi DW. 1988. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
8. Dai WM, Egebjerg J, Lambert JD. 2001. Characteristics of AMPA receptor-mediated responses of cultured cortical and spinal cord neurones and their correlation to the expression of glutamate receptor subunits, GluR1-4. Br J Pharmacol 132:1859-1875.
9. Davis JB, Maher P. 1994. Protein kinase C activation inhibits glutamate-induced cytotoxicity in a neuronal cell line. Brain Res 652:169-173.
10. Fern R, Möller T. 2000. Rapid ischemic cell death in immature oligodendrocytes: A fatal glutamate release feedback loop. J Neurosci 20:34-42.
11. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE. 2000. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235-9241.
12. + channel block. J Neurosci 16:2659-2670.
13. -) directly from postnatal rodent cerebrum. Neuroprotocols 2:209-218.
14. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
15. Horn R, Marty A. 1988. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145-159.
16. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, Grinspan JB, Pleasure D. 2002. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 81:390-402.
17. Kavanaugh B, Beesley J, Itoh T, Itoh A, Grinspan J, Pleasure D. 2000. Neurotrophin-3 (NT-3) diminishes susceptibility of the oligodendroglial lineage to AMPA glutamate receptor-mediated excitotoxicity. J Neurosci Res 60:725-732.
18. Lerma J. 1997. Kainate reveals its targets. Neuron 19:1155-1158.
19. Levi G, Aloisi F, Wilkin GP. 1987. Differentiation of cerebellar bipotential glial precursors into oligodendrocytes in primary culture: Developmental proficle of surface antigens and mitotic activity. J Neurosci Res 18:407-417.
20. LeVine SM, Goldman JE. 1988. Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. J Comp Neurol 277:441-455.
21. Li SX, Stys PK. 2000. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 20:1190-1198.
22. Lipton SA, Rosenberg PA. 1994. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622.
23. Liu H-N, Almazan G. 1995. Glutamate induces c-fos protooncogene expression and inhibits proliferation in oligodendrocyte progenitors: Receptor characterization. Eur J Neurosci 7:2355-2363.
24. Mallard EC, Rees S, Stringer M, Cock ML, Harding R. 1998. Effects of chronic placental insufficiency on brain development in fetal sheep. Pediatr Res 43:262-270.
25. Matute C, Sanchez-Gomez MV, Martinez-Millan L, Miledi R. 1997. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci USA 94:8830-8835.
26. McCarthy KD, de nellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
27. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP. 1998a. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297.
28. McDonald JW, Levine JM, Qu Y. 1998b. Multiple classes of the oligodendrocyte lineage are highly vulnerable to excitotoxicity. Neuroreport 9:2757-2762.
29. Meldrum B, Garthwaite J. 1990. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11:379-387.
30. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytoxicity assays. J Immunol 65:55-63.
31. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ. 1993. Vulnerability of oligodendroglia to glutamate: Pharmacology, mechanisms, and prevention. J Neurosci 13:1441-1453.
32. Patneau DK, Wright PW, Winters C, Mayer ML, Gallo V. 1994. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 12:357-371.
33. Pfeiffer SE, Warrington AE, Bansal R. 1993. The oligodendrocyte and its many cellular processes. Trends Cell Biol 3:191-197.
34. Pitt D, Werner P, Raine CS. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70.
35. Puchalski RB, Louis JC, Brose N, Traynelis SF, Egeberg J, Kukekov V, Wenthold RJ, Rogers SW, Lin F, Moran T, Morrison JH, Heinemann SF. 1994. Selective RNA editing and subunit assembly of native glutamate receptors. Neuron 13:131-147.
36. Rees S, Stringer M, Just Y, Hooper SB, Harding R. 1997. The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation. Brain Res Dev Brain Res 103:103-118.
37. Rice JE, Vannucci RC, Brierley JB. 1981. The influence of immaturity on hypoxia-ischemia brain damage in the rat. Ann Neurol 9:131-141.
38. Rothman SM, Olney JW. 1986. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19:105-111.
39. Sanchez-Gomez MV, Matute C. 1996. Activation of AMPA and kainate glutamate receptors impairs the viability of oligodendrocytes in vitro. Int J Dev Biol Suppl 1:187S-188S.
40. Sanchez-Gomez MV, Matute C. 1999. AMPA and kainate receptors each mediate excitotoxicity in oligodendroglial cultures. Neurobiol Dis 6:475-485.
41. Schachner M, Kim SU, Zehnle R. 1981. Developmental expression in central and peripheral nervous system of oligodendrocyte antigen (O antigens) recognized by monoclonal antibody. Dev Biol 83:328-338.
42. Segal MM. 1994. Endogenous bursts underlie seizurelike activity in solitary excitatory hippocampal neurons in microcultures. J Neurophysiol 72:1874-1883.
43. Sontheimer H, Trotter J, Schachner M, Kettenmann H. 1989. Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 2:1135-1145.
44. Stephens GJ, Marriott DR, Djamgoz MBA, Wilkin GP. 1993. Electrophysiological and biochemical evidence for bradykinin receptors on cultured rat cortical oligodendrocytes. Neurosci Lett 153:223-226.
45. Tekkök SB, Goldberg MP. 2001. AMPA/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 21:4237-4248.
46. Volpe JJ. 2001. Hypoxic-ischemic encephalopathy: Neuropathology and pathogenesis. In: Neurology of the Newborn. Philadelphia: W.B. Saunders Co. p 296-330.
47. Wang C, Pralong WF, Schulz MF, Rougon G, Aubry JM, Pagliusi S, Robert A, Kiss JZ. 1996. Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: A critical role in regulating polysialic acidneural cell adhesion molecule expression and cell migration. J Cell Biol 135:1565-1581.
48. Wyllie DJA, Mathie A, Symonds CJ, Cull-Candy SG. 1991. Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures. J Physiol 432:235-258.
49. Yamada KA, Dubinsky JM, Rothman SM. 1989. Quantitative physiological characterization of a quinoxalinedione non-NMDA antagonist. J Neurosci 9:3230-3236.
50. Yonezawa M, Back SA, Gan X, Rosenberg PA, Volpe JJ. 1996. Cystine deprivation induces oligodendroglial death: Rescue by free radical scavengers andby a diffusible glial factor. J Neurochem 67:566-573.
51. Yoshioka A, Hardy M, Younkin DP, Grinspan JB, Stern JL, Pleasure D. 1995. α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors mediate excitotoxicity in the oligodendroglial lineage. J Neurochem 64:2442-2448.