AMPA-receptor trafficking and injury-induced cell death

European Journal of Neuroscience

Volumn 32, Issue 2, 2010, Pages 290-297

  Beattie, Michael S ^a   Ferguson, Adam R ^a   Bresnahan, Jacqueline C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell death; Cell imaging; Cns injury; Excitability synapse; Glia neuron interaction

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BRAIN INJURY; CELL METABOLISM; DEGENERATIVE DISEASE; EXCITOTOXICITY; HUMAN; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; ANIMAL; CELL DEATH; CENTRAL NERVOUS SYSTEM; INJURY; METABOLISM; PHYSIOLOGY; REVIEW; SYNAPSE;

ANIMALS; CELL DEATH; CENTRAL NERVOUS SYSTEM; GLUTAMIC ACID; HUMANS; NEURONAL PLASTICITY; PROTEIN TRANSPORT; RECEPTORS, AMPA; SYNAPSES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78951473274     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07343.x     Document Type: Article

References (68)

1. Adesnik, H., Nicoll, R.A. & England, P.M. (2005) Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron, 48, 977-985.
2. Agrawal, S.K. & Fehlings, M.G. (1997) Role of NMDA and non-NMDA ionotropic glutamate receptors in traumatic spinal cord axonal injury. J. Neurosci., 17, 1055-1063.
3. Balosso, S., Ravizza, T., Pierucci, M., Calcagno, E., Invernizzi, R., Di Giovanni, G., Esposito, E. & Vezzani, A. (2009) Molecular and functional interactions between tumor necrosis factor-alpha receptors and the glutamatergic system in the mouse hippocampus: implications for seizure susceptibility. Neuroscience, 161, 293-300.
4. Baumbauer, K.M., Huie, J.R., Hughes, A.J. & Grau, J.W. (2009) Timing in the absence of supraspinal input ii: regularly spaced stimulation induces a lasting alteration in spinal function that depends on the NMDA receptor, BDNF release, and protein synthesis. J. Neurosci., 29, 14383-14393.
5. Beattie, M.S. (2004) Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol Med, 10, 580-583.
6. Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M., Beattie, M.S. & Malenka, R.C. (2002) Control of synaptic strength by glial TNF alpha. Science, 295, 2282-2285.
7. Bernardino, L., Xapelli, S., Silva, A.P., Jakobsen, B., Poulsen, F.R., Oliveira, C.R., Vezzani, A., Malva, J.O. & Zimmer, J. (2005) Modulator effects of interleukin-1 beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci., 25, 6734-6744.
8. Blanchard, B.J., Chen, A., Rozeboom, L.M., Stafford, K.A., Weigele, P. & Ingram, V.M. (2004) Efficient reversal of Alzheimer's disease fibril formation and elimination of neurotoxicity by a small molecule. Proc. Natl Acad. Sci. USA, 101, 14326-14332.
9. Bruce, A.J., Boling, W., Kindy, M.S., Peschon, J., Kraemer, P.J., Carpenter, M.K., Holtsberg, F.W. & Mattson, M.P. (1996) Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat. Med., 2, 788-794.
10. Centonze, D., Muzio, L., Rossi, S., Cavasinni, F., De Chiara, V., Bergami, A., Musella, A., D'Amelio, M., Cavallucci, V., Martorana, A., Bergamaschi, A., Cencioni, M.T., Diamantini, A., Butti, E., Comi, G., Bernardi, G., Cecconi, F., Battistini, L., Furlan, R. & Martino, G. (2009) Inflammation Triggers Synaptic Alteration and Degeneration in Experimental Autoimmune Encephalomyelitis. J. Neurosci., 29, 3442-3452.
11. Chen, H.S. & Lipton, S.A. (2006) The chemical biology of clinically tolerated NMDA receptor antagonists. J. Neurochem., 97, 1611-1626.
12. Choi, D.W. (1992) Excitotoxic Cell-Death. J. Neurobiol., 23, 1261-1276.
13. Derkach, V.A., Oh, M.C., Guire, E.S. & Soderling, T.R. (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci., 8, 101-113.
14. Domercq, M., Brambilla, L., Pilati, E., Marchaland, J., Volterra, A. & Bezzi, P. (2006) P2Y1 receptor-evoked glutamate exocytosis from astrocytes - Control by tumor necrosis factor-alpha and prostaglandins. J. Biol. Chem., 281, 30684-30696.
15. Edgerton, V.R., Tillakaratne, N.J.K., Bigbee, A.J., de Leon, R.D. & Roy, R.R. (2004) Plasticity of the spinal neural circuitry after injury. Annu. Rev. Neurosci., 27, 145-167.
16. Emch, G.S., Hermann, G.E. & Rogers, R.C. (2000) TNF-alpha activates solitary nucleus neurons responsive to gastric distension. Am. J. Physiol. Gastrointest. Liver Physiol., 279, G582-G586.
17. Ferguson, A.R., Bolding, K.A., Huie, J.R., Hook, M.A., Santillano, D.R., Miranda, R.C. & Grau, J.W. (2008) Group I metabotropic glutamate receptors control metaplasticity of spinal cord learning through a Protein kinase C-Dependent mechanism. J. Neurosci., 28, 11939-11949.
18. Ferguson, A.R., Christensen, R.N., Gensel, J.C., Miller, B.A., Sun, F., Beattie, E.C., Bresnahan, J.C. & Beattie, M.S. (2008) Cell death after spinal cord injury is exacerbated by rapid TNF alpha-Induced trafficking of GluR2-Lacking AMPARs to the plasma membrane. J. Neurosci., 28, 11391-11400.
19. Gainey, M.A., Hurvitz- Wolff, J.R., Lambo, M.E. & Turrigiano, G.G. (2009) Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J. Neurosci., 29, 6479-6489.
20. Genovese, T., Mazzon, E., Crisafulli, C., Di Paola, R., Muia, C., Bramanti, P. & Cuzzocrea, S. (2006) Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther., 316, 1006-1016.
21. Gensel, J.C., Tovar, C.A., Hamers, F.P.T., Deibert, R.J., Beattie, M.S. & Bresnahan, J.C. (2006) Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J. Neurotrauma, 23, 36-54.
22. Grossman, S.D., Rosenberg, L.J. & Wrathall, J.R. (2001) Relationship of altered glutamate receptor subunit mRNA expression to acute cell loss after spinal cord contusion. Exp. Neurol., 168, 283-289.
23. Grossman, S.D., Rosenberg, L.J. & Wrathall, J.R. (2001) Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp. Neurol., 168, 273-282.
24. Hermann, G.E., Rogers, R.C., Bresnahan, J.C. & Beattie, M.S. (2001) Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamatemediated cell death in the rat spinal cord. Neurobiol. Dis., 8, 590-599.
25. 2+ Permeability of Ka-Ampa Gated Glutamate Receptor Channels Depends on Subunit Composition. Science, 252, 851-853.
26. Jourdain, P., Bergersen, L.H., Bhaukaurally, K., Bezzi, P., Santello, M., Domercq, M., Matute, C., Tonello, F., Gundersen, V. & Volterra, A. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci., 10, 331-339.
27. Kaneko, M., Stellwagen, D., Malenka, R.C. & Stryker, M.P. (2008) Tumor necrosis factor-alpha mediates one component of competitive, experiencedependent plasticity in developing visual cortex. Neuron, 58, 673-680.
28. Kigerl, K.A., Gensel, J.C., Ankeny, D.P., Alexander, J.K., Donnelly, D.J. & Popovich, P.G. (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci., 29, 13435-13444.
29. Kleen, J.K. & Holmes, G.L. (2008) Brain inflammation initiates seizures. Nat. Med., 14, 1309-1310.
30. Krueger, J.M., Rector, D.M., Roy, S., Van Dongen, H.P.A., Belenky, G. & Panksepp, J. (2008) Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci., 9, 910-919.
31. Lai, C., Xie, C.S., McCormack, S.G., Chiang, H.C., Michalak, M.K., Lin, X., Chandran, J., Shim, H., Shimoji, M., Cookson, M.R., Huganir, R.L., Rothstein, J.D., Price, D.L., Wong, P.C., Martin, L.J., Zhu, J.J. & Cai, H.B. (2006) Amyotrophic lateral sclerosis 2-deficiency leads to neuronal degeneration in amyotrophic lateral sclerosis through altered AMPA receptor trafficking. J. Neurosci., 26, 11798-11806.
32. Larsson, M. & Broman, J. (2008) Translocation of GluR1-containing AMPA receptors to a spinal nociceptive synapse during acute noxious stimulation. J. Neurosci., 28, 7084-7090.
33. Lebrun-Julien, F., Duplan, L., Pernet, V., Osswald, I., Sapieha, P., Bourgeois, P., Dickson, K., Bowie, D., Barker, P.A. & Di Polo, A. (2009) Excitotoxic Death of Retinal Neurons In Vivo Occurs via a Non-Cell-Autonomous Mechanism. J. Neurosci., 29, 5536-5545.
34. Leonoudakis, D., Zhao, P. & Beattie, E.C. (2008) Rapid tumor necrosis factor alpha-induced exocytosis of glutamate receptor 2-lacking AMPA receptors to extrasynaptic plasma membrane potentiates excitotoxicity. J. Neurosci., 28, 2119-2130.
35. Li, J., Ramenaden, E.R., Peng, J., Koito, H., Volpe, J.J. & Rosenberg, P.A. (2008) Tumor necrosis factor alpha mediates lipopolysaccharide-induced microglial toxicity to developing oligodendrocytes when astrocytes are present. J. Neurosci., 28, 5321-5330.
36. Liu, B.S., Liao, M.X., Mielke, J.G., Ning, K., Chen, Y.H., Li, L., El Hayek, Y.H., Gomez, E., Zukin, R.S., Fehlings, M.G. & Wan, Q. (2006) Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J. Neurosci., 26, 5309-5319.
37. Malinow, R. & Malenka, R.C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci., 25, 103-126.
38. Marchand, F., Tsantoulas, C., Singh, D., Grist, J., Clark, A.K., Bradbury, E.J. & McMahon, S.B. (2009) Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur. J. Pain, 13, 673-681.
39. Marsden, K.C., Beattie, J.B., Friedenthal, J. & Carroll, R.C. (2007) NMDA receptor activation potentiates inhibitory transmission through GABA receptor-associated protein-dependent exocytosis of GABA(A) receptors. J. Neurosci., 27, 14326-14337.
40. Matute, C., Alberdi, E., Domercq, M., Perez-Cerda, F., Perez-Samartin, A. & Sanchez- Gomez, M.V. (2001) The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci., 24, 224-230.
41. McDonald, J.W., Althomsons, S.P., Hyrc, K.L., Choi, D.W. & Goldberg, M.P. (1998) Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med., 4, 291-297.
42. Panter, S.S. & Faden, A.I. (1992) Pretreatment with Nmda antagonists limits release of excitatory amino-acids following traumatic brain injury. Neurosci. Lett., 136, 165-168.
43. Park, E., Velumian, A.A. & Fehlings, M.G. (2004) The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J. Neurotrauma, 21, 754-774.
44. Pitt, D., Werner, P. & Raine, C.S. (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med., 6, 67-70.
45. Riazi, K., Galic, M.A., Kuzmiski, J.B., Ho, W., Sharkey, K.A. & Pittman, Q.J. (2008) Microglial activation and TNF alpha production mediate altered CNS excitability following peripheral inflammation. Proc. Natl Acad. Sci. USA, 105, 17151-17156.
46. Rossi, D., Brambilla, L., Valori, C.F., Crugnola, A., Giaccone, G., Capobianco, R., Mangieri, M., Kingston, A.E., Bloc, A., Bezzi, P. & Volterra, A. (2005) Defective tumor necrosis factor-alpha-dependent control of astrocyte glutamate release in a transgenic mouse model of Alzheimer disease. J. Biol. Chem., 280, 42088-42096.
47. Rothstein, J.D., DykesHoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kuncl, R.W., Kanai, Y., Hediger, M.A., Wang, Y.F., Schielke, J.P. & Welty, D.F. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron, 16, 675-686.
48. Schafers, M., Sorkin, L.S., Geis, C. & Shubayev, V.I. (2003) Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci. Lett., 347, 179-182.
49. Schafers, M., Svensson, C.I., Sommer, C. & Sorkin, L.S. (2003) Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J. Neurosci., 23, 2517-2521.
50. Schafers, M., Sommer, C., Geis, C., Hagenacker, T., Vandenabeele, P. & Sorkin, L.S. (2008) Selective Stimulation of Either Tumor Necrosis Factor Receptor Differentially Induces Pain Behavior in Vivo and Ectopic Activity in Sensory Neurons in Vitro. Neuroscience, 157, 414-423.
51. Shi, S.H., Hayashi, Y., Esteban, J.A. & Malinow, R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell, 105, 331-343.
52. Sierra, A., Gottfried- Blackmore, A.C., McEwen, B.S. & Bulloch, K. (2007) Microglia derived from aging mice exhibit an altered inflammatory profile. Glia, 55, 412-424.
53. Stellwagen, D. & Malenka, R.C. (2006) Synaptic scaling mediated by glial TNF-alpha. Nature, 440, 1054-1059.
54. Stellwagen, D., Beattie, E.C., Seo, J.Y. & Malenka, R.C. (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci., 25, 3219-3228.
55. Su, Z., Yuan, Y., Chen, J., Cao, L., Zhu, Y., Gao, L., Qiu, Y. & He, C. (2009) Reactive astrocytes in glial scar attract olfactory ensheathing cells migration by secreted TNF-alpha in spinal cord lesion of rat. PLoS ONE, 4, e8141.
56. Svensson, C.I., SchSfers, M., Jones, T.L., Powell, H. & Sorkin, L.S. (2005) Spinal blockade of TNF blocks spinal nerve ligation-induced increases in spinal P-p38. Neurosci. Lett., 379, 209-213.
57. Tobinick, E.L. & Gross, H. (2008) Rapid cognitive improvement in Alzheimer's disease following perispinal etanercept administration. J. Neuroinflammation, 5, doi: 10.1186/1742-2094-5-2.
58. Turrigiano, G.G. (2006) More than a sidekick: glia and homeostatic synaptic plasticity. Trends Mol Med, 12, 458-460.
59. Turrigiano, G. (2007) Homeostatic signaling: the positive side of negative feedback. Curr. Opin. Neurobiol., 17, 318-324.
60. Turrigiano, G.G. (2008) The Self-Tuning Neuron: synaptic Scaling of Excitatory Synapses. Cell, 135, 422-435.
61. Vesce, S., Rossi, D., Brambilla, L. & Volterra, A. (2007) Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int. Rev. Neurobiol., 82, 57-71.
62. Walters, M.R., Kaste, M., Lees, K.R., Diener, H.C., Hommel, M., De Keyser, J., Steiner, H. & Versavel, M. (2005) The AMPA antagonist ZK 200775 in patients with acute ischaemic stroke: a double-blind, multicentre, placebocontrolled safety and tolerability study. Cerebrovasc. Dis., 20, 304-309.
63. Wang, C.X., Nuttin, B., Heremans, H., Dom, R. & Gybels, J. (1996) Production of tumor necrosis factor in spinal cord following traumatic injury in rats. J. Neuroimmunol., 69, 151-156.
64. Wang, X.H., Arcuino, G., Takano, T., Lin, J., Peng, W.G., Wan, P.L., Li, P.J., Xu, Q.W., Liu, Q.S., Goldman, S.A. & Nedergaard, M. (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat. Med., 10, 821-827.
65. Watkins, T.A., Emery, B., Mulinyawe, S. & Barres, B.A. (2008) Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron, 60, 555-569.
66. Wolpaw, J.R. (2006) The education and re-education of the spinal cord. Prog. Brain. Res., 157, 261-282.
67. Wrathall, J.R., Teng, Y.D. & Choiniere, D. (1996) Amelioration of functional deficits from spinal cord trauma with systemically administered NBQX, an antagonist of non-N-methyl-D-aspartate receptors. Exp. Neurol., 137, 119-126.
68. Yu, Z.F., Cheng, G.J., Wen, X.M., Wu, G.D., Lee, W.T. & Pleasure, D. (2002) Tumor necrosis factor alpha increases neuronal vulnerability to excitotoxic necrosis by inducing expression of the AMPA-glutamate receptor subunit GluR1 via an acid sphingomyelinase- and NF-kappa B-dependent mechanism. Neurobiol. Dis., 11, 199-213.