Hypoxic injury of isolated axons is independent of ionotropic glutamate receptors

Neurobiology of Disease

Volumn 25, Issue 2, 2007, Pages 284-290

  Underhill, Suzanne M ^a   Goldberg, Mark P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA kainate; Axon; Calpain; Excitotoxicity; Glutamate; Ischemia; NMDA; Oxygen glucose deprivation; White matter

Indexed keywords

AMPA RECEPTOR ANTAGONIST; CALCIUM; CALPAIN; GLUCOSE; GLUTAMATE RECEPTOR AGONIST; GLUTAMIC ACID; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR ANTAGONIST; OXYGEN; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; AXONAL INJURY; BIOLOGICAL MODEL; BRAIN ISCHEMIA; CALCIUM TRANSPORT; CELL ISOLATION; CELL LABELING; CONTROLLED STUDY; EXCITOTOXICITY; EXTRACELLULAR CALCIUM; HYPOXIA; IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NEUROFILAMENT; NEUROLOGIC DISEASE; NONHUMAN; NONMYELINATED NERVE; PERIKARYON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SODIUM TRANSPORT; WHITE MATTER;

ANIMALS; ANOXIA; AXONS; CALCIUM; CALCIUM SIGNALING; CALPAIN; CELL CULTURE TECHNIQUES; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GLUCOSE; GLUTAMIC ACID; HYPOXIA-ISCHEMIA, BRAIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROTOXINS; RECEPTORS, GLUTAMATE; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; WALLERIAN DEGENERATION;

EID: 33846330653     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.09.011     Document Type: Article

References (45)

1. Agrawal S.K., and Fehlings M.G. Role of NMDA and non-NMDA ionotropic glutamate receptors in traumatic spinal cord axonal injury. Neurosci. J. 17 (1997) 1055-1063
2. Bjartmar C., and Trapp B.D. Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences. Curr. Opin. Neurol. 14 (2001) 271-278
3. Brown A.M., Wender R., and Ransom B.R. Metabolic substrates other than glucose support axon function in central white matter. J. Neurosci. Res. 66 (2001) 839-843
4. Campenot R.B. Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. Dev. Biol. 93 (1982) 13-21
5. David J.C., Yamada K.A., Bagwe M.R., and Goldberg M.P. AMPA receptor activation is rapidly toxic to cortical astrocytes when desensitization is blocked. J. Neurosci. 16 (1996) 200-209
6. Dewar D., Yam P., and McCulloch J. Drug development for stroke: importance of protecting cerebral white matter. Eur. J. Pharmacol. 375 (1999) 41-50
7. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., and Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28 (2000) 41-51
8. Fern R., and Moller T. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J. Neurosci. 20 (2000) 34-42
9. Fern R., Ransom B.R., and Waxman S.G. Voltage-gated calcium channels in CNS white matter: role in anoxic injury. J. Neurophysiol. 74 1 (1995) 369-377
10. Follett P.L., Rosenberg P.A., Volpe J.J., and Jensen F.E. NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci. 20 (2000) 9235-9241
11. Gallo V., Patneau D.K., Mayer M.L., and Vaccarino F.M. Excitatory amino-acid receptors in glial progenitor cells-Molecular and functional-properties. Glia 11 (1994) 94-101
12. Garthwaite G., Brown G., Batchelor A.M., Goodwin D.A., and Garthwaite J. Mechanisms of ischaemic damage to central white matter axons: a quantitative histological analysis using rat optic nerve. Neuroscience 94 (1999) 1219-1230
13. Goldberg M.P., and Choi D.W. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. 13 (1993) 3510-3524
14. Hasbani M.J., Hyrc K.L., Faddis B.T., Romano C., and Goldberg M.P. Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp. Neurol. 154 (1998) 241-258
15. Hasbani M.J., Viquez N.M., and Goldberg M.P. NMDA receptors mediate hypoxic spine loss in cultured neurons. NeuroReport 12 (2001) 2731-2735
16. Ivins K.J., Bui E.T., and Cotman C.W. Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis. Neurobiol. Dis. 5 (1998) 365-378
17. Jiang Q., and Stys P.K. Calpain inhibitors confer biochemical, but not electrophysiological, protection against anoxia in rat optic nerves. J. Neurochem. 74 (2000) 2101-2107
18. Kanellopoulos G.K., Xu X.M., Hsu C.Y., Lu X., Sundt T.M., and Kouchoukos N.T. White matter injury in spinal cord ischemia: protection by AMPA/kainate glutamate receptor antagonism. Stroke 31 (2000) 1945-1952
19. Karadottir R., Cavelier P., Bergersen L.H., and Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438 (2005) 1162-1166
20. Li S., Jiang Q., and Stys P.K. Important role of reverse Na(+)-Ca(2+) exchange in spinal cord white matter injury at physiological temperature. J. Neurophysiol. 84 (2000) 1116-1119
21. Matute C., Sanchez-Gomez M.V., Martinez-Millan L., and Miledi R. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8830-8835
22. McCracken E., Fowler J., Dewar D., Morrison S., and McCulloch J. Grey matter and white matter ischemic damage is reduced by the competitive AMPA receptor antagonist, SPD 502. J. Cereb. Blood Flow Metab. 22 (2002) 1090-1097
23. McDonald J.W., Althomsons S.P., Hyrc K.L., Choi D.W., and Goldberg M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med. 4 (1998) 291-297
24. Meller D., Eysel U.T., and Schmidt-Kastner R. Transient immunohistochemical labelling of rat retinal axons during Wallerian degeneration by a monoclonal antibody to neurofilaments. Brain Res. 648 (1994) 162-166
25. Micu I., Jiang Q., Coderre E., Ridsdale A., Zhang L., Woulfe J., Yin X., Trapp B.D., Mcrory J.E., Rehak R., Zamponi G.W., Wang W., and Stys P.K. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439 (2006) 988-992
26. Ouardouz M., Nikolaeva M.A., Coderre E., Zamponi G.W., Mcrory J.E., Trapp B.D., Yin X.H., Wang W.L., Woulfe J., and Stys P.K. Depolarization-induced Ca2+ release in ischemic spinal cord white matter involves L-type Ca2+ channel activation of ryanodine receptors. Neuron 40 (2003) 53-63
27. Ouardouz M., Zamponi G.W., Barr W., Kiedrowski L., and Stys P.K. Protection of ischemic rat spinal cord white matter: Dual action of KB-R7943 on Na+/Ca2+ exchange and L-type Ca2+ channels. Neuropharmacology 48 (2005) 566-575
28. Pitt D., Werner P., and Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6 (2000) 67-70
29. Rosenberg P.A., Li Y., Ali S., Altiok N., Back S.A., and Volpe J.J. Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J. Neurochem. 73 (1999) 476-484
30. Salter M.G., and Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438 (2005) 1167-1171
31. Sasaki T., Kishi M., Saito M., Tanaka T., Higuchi N., Kominami E., Katunuma N., and Murachi T. Inhibitory effect of di- and tripeptidyl aldehydes on calpains and cathepsins. J. Enzyme Inhib. 3 (1990) 195-201
32. Stys P.K. General mechanisms of axonal damage and its prevention. J. Neurol. Sci. 233 (2005) 3-13
33. Stys P.K., and Lopachin R.M. Mechanisms of calcium and sodium fluxes in anoxic myelinated central nervous system axons. Neuroscience 82 (1998) 21-32
34. Stys P.K., Ransom B.R., Waxman S.G., and Davis P.K. Role of extracellular calcium in anoxic injury of mammalian central white matter. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 4212-4216
35. Taylor A., Rhee S., and Jeon N. Microfluidic chambers for cell migration and neuroscience research. Methods Mol. Biol. 321 (2006) 167-177
36. Tekkok S.B., and Goldberg M.P. Ampa/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J. Neurosci. 21 (2001) 4237-4248
37. Utzschneider D.A., Thio C., Sontheimer H., Ritchie J.M., Waxman S.G., and Kocsis J.D. Action-potential conduction and sodium-channel content in the optic-nerve of the myelin-deficient rat. Proc. R. Soc. Lond., Ser. B Biol. Sci. 254 (1993) 245-250
38. Volpe J.J. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50 (2001) 553-562
39. Waxman S.G., Ransom B.R., and Stys P.K. Non-synaptic mechanisms of Ca(2+)-mediated injury in CNS white matter. Trends Neurosci. 14 (1991) 461-468
40. Waxman S.G., Black J.A., Ransom B.R., and Stys P.K. Protection of the axonal cytoskeleton in anoxic optic nerve by decreased extracellular calcium. Brain Res. 614 (1993) 137-145
41. Waxman S.G., Black J.A., Ransom B.R., and Stys P.K. Anoxic injury of rat optic nerve: ultrastructural evidence for coupling between Na+ influx and Ca(2+)-mediated injury in myelinated CNS axons. Brain Res. 644 (1994) 197-204
42. Wilke S., Thomas R., Allcock N., and Fern R. Mechanism of acute ischemic injury of oligodendroglia in early myelinating white matter: the importance of astrocyte injury and glutamate release. J. Neuropathol. Exp. Neurol. 63 (2004) 872-881
43. Wolf J.A., Stys P.K., Lusardi T., Meaney D., and Smith D.H. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J. Neurosci. 21 (2001) 1923-1930
44. Wrathall J.R., Choiniere D., and 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 (1994) 6598-6607
45. Yoshioka A., Hardy M., Younkin D.P., Grinspan J.B., Stern J.L., and Pleasure D. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors mediate excitotoxicity in the oligodendroglial lineage. J. Neurochem. 64 (1995) 2442-2448