TNFα potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: Neuroprotection by NFκB inhibition

Brain Research

Volumn 1034, Issue 1-2, 2005, Pages 11-24

  Zou, Jian Y ^a   Crews, Fulton T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Glutamate excitotoxicity; Glutamate transport; Hippocampus; TNF

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR ANTAGONIST; ANTIOXIDANT; BUTYLCRESOL; DIZOCILPINE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PROLYLTHREONYLASPARTIC ACID SYNAPTOTAGMIN CONJUGATE; PROPIDIUM IODIDE; PROTEIN INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CELL DEATH; CONTROLLED STUDY; CYTOARCHITECTURE; DENTATE GYRUS; ENTORHINAL CORTEX; FLUORESCENCE; HIPPOCAMPUS; MOLECULAR INTERACTION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 13844270562     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.11.014     Document Type: Article

References (69)

1. Y. Adamchik, M.V. Frantseva, M. Weisspapir, P.L. Carlen, and J.L. Perez Velazquez Methods to induce primary and secondary traumatic damage in organotypic hippocampal slice cultures Brain Res., Brain Res. Protoc. 5 2000 153 158
2. B. Ahlemeyer, S. Kolker, Y. Zhu, G.F. Hoffmann, and J. Krieglstein Increase in glutamate-induced neurotoxicity by activated astrocytes involves stimulation of protein kinase C J. Neurochem. 82 2002 504 515
3. S.M. Allan, and N.J. Rothwell Cytokines and acute neurodegeneration Nat. Rev., Neurosci. 2 2001 734 744
4. S.J. An, T.C. Kang, S.K. Park, I.K. Hwang, S.S. Cho, M.H. Chung, and M.H. Won Oxidative DNA damage and alteration of glutamate transporter expressions in the hippocampal Ca1 area immediately after ischemic insult Mol. Cells 13 2002 476 480
5. J.L. Arriza, W.A. Fairman, J.I. Wadiche, G.H. Murdoch, M.P. Kavanaugh, and S.G. Amara Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex J. Neurosci. 14 1994 5559 5569
6. F.C. Barone, B. Arvin, R.F. White, A. Miller, C.L. Webb, R.N. Willette, P.G. Lysko, and G.Z. Feuerstein Tumor necrosis factor-alpha. A mediator of focal ischemic brain injury Stroke 28 1997 1233 1244
7. E.C. Beattie, D. Stellwagen, W. Morishita, J.C. Bresnahan, B.K. Ha, M. Von Zastrow, M.S. Beattie, and R.C. Malenka Control of synaptic strength by glial TNFalpha Science 295 2002 2282 2285
8. A. Belmadani, J.Y. Zou, M.J. Schipma, E.J. Neafsey, and M.A. Collins Ethanol pre-exposure suppresses HIV-1 glycoprotein 120-induced neuronal degeneration by abrogating endogenous glutamate/Ca2+-mediated neurotoxicity Neuroscience 104 2001 769 781
9. E.N. Benveniste, and D.J. Benos TNF-alpha- and IFN-gamma-mediated signal transduction pathways: effects on glial cell gene expression and function FASEB J. 9 1995 1577 1584
10. C. Brana, C. Benham, and L. Sundstrom A method for characterising cell death in vitro by combining propidium iodide staining with immunohistochemistry Brain Res., Brain Res. Protoc. 10 2002 109 114
11. I.Y. Chung, and E.N. Benveniste Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta J. Immunol. 144 1990 2999 3007
12. F.T. Crews Alcohol and neurodegeneration CNS Drug Rev. 5 1999 379 394
13. N.C. Danbolt Glutamate uptake Prog. Neurobiol. 65 2001 1 105
14. F. de Bock, B. Derijard, J. Dornand, J. Bockaert, and G. Rondouin The neuronal death induced by endotoxic shock but not that induced by excitatory amino acids requires TNF-alpha Eur. J. Neurosci. 10 1998 3107 3114
15. S. Diekmann, R. Nitsch, and T.G. Ohm The organotypic entorhinal- hippocampal complex slice culture of adolescent rats. A model to study transcellular changes in a circuit particularly vulnerable in neurodegenerative disorders J. Neural Transm., Suppl. 44 1994 61 71
16. H. Fillit, W.H. Ding, L. Buee, J. Kalman, L. Altstiel, B. Lawlor, and G. Wolf-Klein Elevated circulating tumor necrosis factor levels in Alzheimer's disease Neurosci. Lett. 129 1991 318 320
17. S.M. Fine, R.A. Angel, S.W. Perry, L.G. Epstein, J.D. Rothstein, S. Dewhurst, and H.A. Gelbard Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia J. Biol. Chem. 271 1996 15303 15306
18. M. Finley, D. Fairman, D. Liu, P. Li, A. Wood, and S. Cho Functional validation of adult hippocampal organotypic cultures as an in vitro model of brain injury Brain Res. 1001 2004 125 132
19. M. Frotscher, S. Zafirov, and B. Heimrich Development of identified neuronal types and of specific synaptic connections in slice cultures of rat hippocampus Prog. Neurobiol. 45 1995 143 164
20. G. Gegelashvili, Y. Dehnes, N.C. Danbolt, and A. Schousboe The high-affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signalling mechanisms Neurochem. Int. 37 2000 163 170
21. G. Gegelashvili, M.B. Robinson, D. Trotti, and T. Rauen Regulation of glutamate transporters in health and disease Prog. Brain Res. 132 2001 267 286
22. Y. Goodman, and M.P. Mattson Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid beta-peptide toxicity J. Neurochem. 66 1996 869 872
23. J.J. Haddad Redox regulation of pro-inflammatory cytokines and IkappaB-alpha/NF-kappaB nuclear translocation and activation Biochem. Biophys. Res. Commun. 296 2002 847 856
24. Y. Han, T. He, D.R. Huang, C.A. Pardo, and R.M. Ransohoff TNF-alpha mediates SDF-1 alpha-induced NF-kappa B activation and cytotoxic effects in primary astrocytes J. Clin. Invest. 108 2001 425 435
25. G.E. Hardingham, Y. Fukunaga, and H. Bading Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways Nat. Neurosci. 5 2002 405 414
26. M. Hayashi, S. Araki, N. Arai, S. Kumada, M. Itoh, K. Tamagawa, M. Oda, and Y. Morimatsu Oxidative stress and disturbed glutamate transport in spinal muscular atrophy Brain Dev. 24 2002 770 775
27. K. Hemmer, L. Fransen, H. Vanderstichele, E. Vanmechelen, and P. Heuschling An in vitro model for the study of microglia-induced neurodegeneration: involvement of nitric oxide and tumor necrosis factor-alpha Neurochem. Int. 38 2001 557 565
28. G.E. Hermann, R.C. Rogers, J.C. Bresnahan, and M.S. Beattie Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord Neurobiol. Dis. 8 2001 590 599
29. J.B. Hoek, and J.G. Pastorino Ethanol, oxidative stress, and cytokine-induced liver cell injury Alcohol 27 2002 63 68
30. I.E. Holopainen, and H.B. Lauren Neuronal activity regulates GABAA receptor subunit expression in organotypic hippocampal slice cultures Neuroscience 118 2003 967 974
31. S. Hu, W.S. Sheng, L.C. Ehrlich, P.K. Peterson, and C.C. Chao Cytokine effects on glutamate uptake by human astrocytes Neuroimmunomodulation 7 2000 153 159
32. B. Kaltschmidt, M. Uherek, B. Volk, P.A. Baeuerle, and C. Kaltschmidt Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease Proc. Natl. Acad. Sci. U. S. A. 94 1997 2642 2647
33. A. Khoruts, L. Stahnke, C.J. McClain, G. Logan, and J.I. Allen Circulating tumor necrosis factor, interleukin-1 and interleukin-6 concentrations in chronic alcoholic patients Hepatology 13 1991 267 276
34. J.H. Laake, F.M. Haug, T. Wieloch, and O.P. Ottersen A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence Brain Res., Brain Res. Protoc. 4 1999 173 184
35. S.L. Liao, and C.J. Chen Differential effects of cytokines and redox potential on glutamate uptake in rat cortical glial cultures Neurosci. Lett. 299 2001 113 116
36. A.P. Lieberman, P.M. Pitha, H.S. Shin, and M.L. Shin Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus Proc. Natl. Acad. Sci. U. S. A. 86 1989 6348 6352
37. T. Liu, R.K. Clark, P.C. McDonnell, P.R. Young, R.F. White, F.C. Barone, and G.Z. Feuerstein Tumor necrosis factor-alpha expression in ischemic neurons Stroke 25 1994 1481 1488
38. U. Martens, and A. Wree Distribution of [3H]MK-801, [3H]AMPA and [3H]Kainate binding sites in rat hippocampal long-term slice cultures isolated from external afferents Anat. Embryol. (Berl.) 203 2001 491 500
39. M.P. Mattson, and S. Camandola NF-kappaB in neuronal plasticity and neurodegenerative disorders J. Clin. Invest. 107 2001 247 254
40. M.P. Mattson, Y. Goodman, H. Luo, W. Fu, and K. Furukawa Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration J. Neurosci. Res. 49 1997 681 697
41. M. Mayne, W. Ni, H.J. Yan, M. Xue, J.B. Johnston, M.R. Del Bigio, J. Peeling, and C. Power Antisense oligodeoxynucleotide inhibition of tumor necrosis factor-alpha expression is neuroprotective after intracerebral hemorrhage Stroke 32 2001 240 248
42. M. Mogi, M. Harada, H. Narabayashi, H. Inagaki, M. Minami, and T. Nagatsu Interleukin (IL)-1 beta, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease Neurosci. Lett. 211 1996 13 16
43. M.C. Morganti-Kossman, P.M. Lenzlinger, V. Hans, P. Stahel, E. Csuka, E. Ammann, R. Stocker, O. Trentz, and T. Kossmann Production of cytokines following brain injury: beneficial and deleterious for the damaged tissue Mol. Psychiatry 2 1997 133 136
44. H. Nawashiro, D. Martin, and J.M. Hallenbeck Inhibition of tumor necrosis factor and amelioration of brain infarction in mice J. Cereb. Blood Flow Metab. 17 1997 229 232
45. D.R. New, S.B. Maggirwar, L.G. Epstein, S. Dewhurst, and H.A. Gelbard HIV-1 Tat induces neuronal death via tumor necrosis factor-alpha and activation of non-N-methyl-d-aspartate receptors by a NFkappaB-independent mechanism J. Biol. Chem. 273 1998 17852 17858
46. J. Noraberg, B.W. Kristensen, and J. Zimmer Markers for neuronal degeneration in organotypic slice cultures Brain Res., Brain Res. Protoc. 3 1999 278 290
47. J.W. Olney, D.F. Wozniak, and N.B. Farber Excitotoxic neurodegeneration in Alzheimer disease. New hypothesis and new therapeutic strategies Arch. Neurol. 54 1997 1234 1240
48. W. Pan, and A.J. Kastin Increase in TNFalpha transport after SCI is specific for time, region, and type of lesion Exp. Neurol. 170 2001 357 363
49. C.L. Poitry-Yamate, L. Vutskits, and T. Rauen Neuronal-induced and glutamate-dependent activation of glial glutamate transporter function J. Neurochem. 82 2002 987 997
50. I. Rahman Regulation of nuclear factor-kappa B, activator protein-1, and glutathione levels by tumor necrosis factor-alpha and dexamethasone in alveolar epithelial cells Biochem. Pharmacol. 60 2000 1041 1049
51. J. Robertson, J.M. Beaulieu, M.M. Doroudchi, H.D. Durham, J.P. Julien, and W.E. Mushynski Apoptotic death of neurons exhibiting peripherin aggregates is mediated by the proinflammatory cytokine tumor necrosis factor-alpha J. Cell Biol. 155 2001 217 226
52. M.B. Robinson, and L.A. Dowd Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system Adv. Pharmacol. 37 1997 69 115
53. S.M. Rothman, and J.W. Olney Excitotoxicity and the NMDA receptor-still lethal after eight years Trends Neurosci. 18 1995 57 58
54. J. Sassoon, M. Daniels, and D.R. Brown Astrocytic regulation of NMDA receptor subunit composition modulates the toxicity of prion peptide PrP106-126 Mol. Cell Neurosci. 25 2004 181 191
55. L.C. Schmued, C. Albertson, and W. Slikker Jr. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration Brain Res. 751 1997 37 46
56. M.K. Sharief, B. McLean, and E.J. Thompson Elevated serum levels of tumor necrosis factor-alpha in Guillain-Barre syndrome Ann. Neurol. 33 1993 591 596
57. K.D. Sims, and M.B. Robinson Expression patterns and regulation of glutamate transporters in the developing and adult nervous system Crit. Rev. Neurobiol. 13 1999 169 197
58. L. Stoppini, P.A. Buchs, and D. Muller A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods 37 1991 173 182
59. R.A. Swanson, J. Liu, J.W. Miller, J.D. Rothstein, K. Farrell, B.A. Stein, and M.C. Longuemare Neuronal regulation of glutamate transporter subtype expression in astrocytes J. Neurosci. 17 1997 932 940
60. M. Takahashi, B. Billups, D. Rossi, M. Sarantis, M. Hamann, and D. Attwell The role of glutamate transporters in glutamate homeostasis in the brain J. Exp. Biol. 200 Pt 2 1997 401 409
61. M. Tamatani, Y.H. Che, H. Matsuzaki, S. Ogawa, H. Okado, S. Miyake, T. Mizuno, and M. Tohyama Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons J. Biol. Chem. 274 1999 8531 8538
62. H.D. Venters, R. Dantzer, and K.W. Kelley Tumor necrosis factor-alpha induces neuronal death by silencing survival signals generated by the type I insulin-like growth factor receptor Ann. N. Y. Acad. Sci. 917 2000 210 220
63. H.D. Venters, S.R. Broussard, J.H. Zhou, R.M. Bluthe, G.G. Freund, R.W. Johnson, R. Dantzer, and K.W. Kelley Tumor necrosis factor(alpha) and insulin-like growth factor-I in the brain: is the whole greater than the sum of its parts? J. Neuroimmunol. 119 2001 151 165
64. X. Wang, T.L. Yue, F.C. Barone, R.F. White, R.C. Gagnon, and G.Z. Feuerstein Concomitant cortical expression of TNF-alpha and IL-1 beta mRNAs follows early response gene expression in transient focal ischemia Mol. Chem. Neuropathol. 23 1994 103 114
65. J. Xu, G. Fan, S. Chen, Y. Wu, X.M. Xu, and C.Y. Hsu Methylprednisolone inhibition of TNF-alpha expression and NFkB activation after spinal cord injury in rats Brain Res. Mol. Brain Res. 59 1998 135 142
66. Z. Yu, G. Cheng, X. Wen, G.D. Wu, W.T. Lee, and D. Pleasure 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-kappaB-dependent mechanism Neurobiol. Dis. 11 2002 199 213
67. X. Zhao, B. Bausano, B.R. Pike, J.K. Newcomb-Fernandez, K.K. Wang, E. Shohami, N.C. Ringger, S.M. DeFord, D.K. Anderson, and R.L. Hayes TNF-alpha stimulates caspase-3 activation and apoptotic cell death in primary septo-hippocampal cultures J. Neurosci. Res. 64 2001 121 131
68. J. Zimmer, and B.H. Gahwiler Growth of hippocampal mossy fibers: a lesion and coculture study of organotypic slice cultures J. Comp. Neurol. 264 1987 1 13
69. J. Zimmer, B.W. Kristensen, B. Jakobsen, and J. Noraberg Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures Amino Acids 19 2000 7 21