Preconditioning effects of tumor necrosis factor-α and glutamate on calcium dynamics in rat organotypic hippocampal cultures

Journal of Neuroimmunology

Volumn 234, Issue 1-2, 2011, Pages 27-39

  Watters, Orla ^a   Pickering, Mark ^a   O'connor, John J ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Calcium; Glutamate; Hippocampus; Organotypic cultures; Preconditioning; Tumor necrosis factor alpha

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CALCIUM ION; GLUTAMIC ACID; INFLIXIMAB; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EXPOSURE; DRUG MECHANISM; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; IN VITRO STUDY; INCUBATION TIME; ISCHEMIC PRECONDITIONING; MALE; MOLECULAR DYNAMICS; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELL DEATH; CELL SURVIVAL; DRUG ADMINISTRATION SCHEDULE; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; IMIDAZOLES; MALE; NONLINEAR DYNAMICS; ORGAN CULTURE TECHNIQUES; PROPIDIUM; PYRIDINES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; VALINE;

EID: 79955665513     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.01.008     Document Type: Article

References (65)

1. Albensi B.C., Mattson M.P. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 2000, 35:151-159.
2. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
3. Arundine M., Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003, 34:325-337.
4. Barber P.A., Auer R.N., Buchan A.M., Sutherland G.R. Understanding and managing ischemic stroke. Can. J. Physiol. Pharmacol. 2001, 79:283-296.
5. Barone F.C., White R.F., Spera P.A., Ellison J., Currie R.W., Wang X., Feuerstein G.Z. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 1998, 29:1937-1950. discussion 1950-1.
6. Batchelor S., Thompson E.O., Miller L.A. Retrograde memory after unilateral stroke. Cortex 2008, 44:170-178.
7. Batini C., Guegan M., Palestini M., Thomasset M., Vigot R. Upregulation of Calbindin-D-28k immunoreactivity by excitatory amino acids. Arch. Ital. Biol. 1997, 135:385-397.
8. Beal M.F. Mechanisms of excitotoxicity in neurologic diseases. FASEB J. 1992, 6:3338-3344.
9. Benveniste E.N., Benos D.J. TNF-alpha- and IFN-gamma-mediated signal transduction pathways: effects on glial cell gene expression and function. FASEB J. 1995, 9:1577-1584.
10. Bernardino L., Xapelli S., Silva A.P., Jakobsen B., Poulsen F.R., Oliveira C.R., Vezzani A., Malva J.O., Zimmer J. Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 2005, 25:6734-6744.
11. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
12. Blondeau N., Widmann C., Lazdunski M., Heurteaux C. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J. Neurosci. 2001, 21:4668-4677.
13. Bullock R., Zauner A., Woodward J., Young H.F. Massive persistent release of excitatory amino acids following human occlusive stroke. Stroke 1995, 26:2187-2189.
14. Castillo J., Moro M.A., Blanco M., Leira R., Serena J., Lizasoain I., Davalos A. The release of tumor necrosis factor-alpha is associated with ischemic tolerance in human stroke. Ann. Neurol. 2003, 54:811-819.
15. Chaparro-Huerta V., Rivera-Cervantes M.C., Flores-Soto M.E., Gomez-Pinedo U., Beas-Zarate C. Proinflammatory cytokines and apoptosis following glutamate-induced excitotoxicity mediated by p38 MAPK in the hippocampus of neonatal rats. J. Neuroimmunol. 2005, 165:53-62.
16. Cheng B., Christakos S., Mattson M.P. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 1994, 12:139-153.
17. Choi D.W. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 1987, 7:369-379.
18. Cumiskey D., Butler M.P., Moynagh P.N., O'Connor J.J. Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-alpha on long-term potentiation. Brain Res. 2007, 1136:13-19.
19. de Erausquin G.A., Manev H., Guidotti A., Costa E., Brooker G. Gangliosides normalize distorted single-cell intracellular free Ca2+ dynamics after toxic doses of glutamate in cerebellar granule cells. Proc. Natl Acad. Sci. USA 1990, 87:8017-8021.
20. De Simoni A., Griesinger C.B., Edwards F.A. Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J. Physiol. 2003, 550:135-147.
21. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
22. Dolga A.M., Granic I., Blank T., Knaus H.G., Spiess J., Luiten P.G., Eisel U.L., Nijholt I.M. TNF-alpha-mediates neuroprotection against glutamate-induced excitotoxicity via NF-kappaB-dependent up-regulation of K2.2 channels. J. Neurochem. 2008, 107:1158-1167.
23. Fukunaga K., Miyamoto E. Role of MAP kinase in neurons. Mol. Neurobiol. 1998, 16:79-95.
24. Furukawa K., Mattson M.P. The transcription factor NF-kappaB mediates increases in calcium currents and decreases in NMDA- and AMPA/kainate-induced currents induced by tumor necrosis factor-alpha in hippocampal neurons. J. Neurochem. 1998, 70:1876-1886.
25. Ginis I., Jaiswal R., Klimanis D., Liu J., Greenspon J., Hallenbeck J.M. TNF-alpha-induced tolerance to ischemic injury involves differential control of NF-kappaB transactivation: the role of NF-kappaB association with p300 adaptor. J. Cereb. Blood Flow Metab. 2002, 22:142-152.
26. Glazner G.W., Mattson M.P. Differential effects of BDNF, ADNF9, and TNFalpha on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Exp. Neurol. 2000, 161:442-452.
27. Gottlieb M., Matute C. Expression of ionotropic glutamate receptor subunits in glial cells of the hippocampal CA1 area following transient forebrain ischemia. J. Cereb. Blood Flow Metab. 1997, 17:290-300.
28. Hartley D.M., Kurth M.C., Bjerkness L., Weiss J.H., CHOI D.W. Glutamate receptor-induced 45Ca2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 1993, 13:1993-2000.
29. Irving E.A., Barone F.C., Reith A.D., Hadingham S.J., Parsons A.A. Differential activation of MAPK/ERK and p38/SAPK in neurones and glia following focal cerebral ischaemia in the rat. Brain Res. Mol. Brain Res. 2000, 77:65-75.
30. Kato H., Liu Y., Araki T., Kogure K. MK-801, but not anisomycin, inhibits the induction of tolerance to ischemia in the gerbil hippocampus. Neurosci. Lett. 1992, 139:118-121.
31. Kirino T. Ischemic tolerance. J. Cereb. Blood Flow Metab. 2002, 22:1283-1296.
32. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K., et al. 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 1990, 528:21-24.
33. Kruman I.I., Mattson M.P. Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis. J. Neurochem. 1999, 72:529-540.
34. Lee B., Butcher G.Q., Hoyt K.R., Impey S., Obrietan K. Activity-dependent neuroprotection and cAMP response element-binding protein (CREB): kinase coupling, stimulus intensity, and temporal regulation of CREB phosphorylation at serine 133. J. Neurosci. 2005, 25:1137-1148.
35. Lin C.H., Chen P.S., Gean P.W. Glutamate preconditioning prevents neuronal death induced by combined oxygen-glucose deprivation in cultured cortical neurons. Eur. J. Pharmacol. 2008, 589:85-93.
36. Liu T., Clark R.K., Mcdonnell P.C., Young P.R., White R.F., Barone F.C., Feuerstein G.Z. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke 1994, 25:1481-1488.
37. Liu J., Ginis I., Spatz M., Hallenbeck J.M. Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide. Am. J. Physiol. Cell Physiol. 2000, 278:C144-C153.
38. Malenka R.C. Synaptic plasticity in the hippocampus: LTP and LTD. Cell 1994, 78:535-538.
39. Marchetti L., Klein M., Schlett K., Pfizenmaier K., Eisel U.L. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-d-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J. Biol. Chem. 2004, 279:32869-32881.
40. Matsushima K., Hakim A.M. Transient forebrain ischemia protects against subsequent focal cerebral ischemia without changing cerebral perfusion. Stroke 1995, 26:1047-1052.
41. Mayer M.L., Miller R.J. Excitatory amino acid receptors, second messengers and regulation of intracellular Ca2+ in mammalian neurons. Trends Pharmacol. Sci. 1990, 11:254-260.
42. Moncayo J., de Freitas G.R., Bogousslavsky J., Altieri M., van Melle G. Do transient ischemic attacks have a neuroprotective effect?. Neurology 2000, 54:2089-2094.
43. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 2003, 26:536-542.
44. Park K.M., Bowers W.J. Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell. Signal. 2010, 22:977-983.
45. Pickering M., Cumiskey D., O'Connor J.J. Actions of TNF-alpha on glutamatergic synaptic transmission in the central nervous system. Exp. Physiol. 2005, 90:663-670.
46. Pradillo J.M., Hurtado O., Romera C., Cardenas A., Fernandez-Tome P., Alonso-Escolano D., Lorenzo P., Moro M.A., Lizasoain I. TNFR1 mediates increased neuronal membrane EAAT3 expression after in vivo cerebral ischemic preconditioning. Neuroscience 2006, 138:1171-1178.
47. Pringle A.K., Thomas S.J., Signorelli F., Iannotti F. Ischaemic pre-conditioning in organotypic hippocampal slice cultures is inversely correlated to the induction of the 72kDa heat shock protein (HSP72). Brain Res. 1999, 845:152-164.
48. Raingeaud J., Gupta S., Rogers J.S., Dickens M., Han J., Ulevitch R.J., Davis R.J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 1995, 270:7420-7426.
49. Rivera-Cervantes M.C., Torres J.S., Feria-Velasco A., Armendariz-Borunda J., Beas-Zarate C. NMDA and AMPA receptor expression and cortical neuronal death are associated with p38 in glutamate-induced excitotoxicity in vivo. J. Neurosci. Res. 2004, 76:678-687.
50. Rosenberg G.A. Ischemic brain edema. Prog. Cardiovasc. Dis. 1999, 42:209-216.
51. Saha R.N., Liu X., Pahan K. Up-regulation of BDNF in astrocytes by TNF-alpha: a case for the neuroprotective role of cytokine. J. Neuroimmune Pharmacol. 2006, 1:212-222.
52. Saha R.N., Ghosh A., Palencia C.A., Fung Y.K., Dudek S.M., Pahan K. TNF-alpha preconditioning protects neurons via neuron-specific up-regulation of CREB-binding protein. J. Immunol. 2009, 183:2068-2078.
53. Sairanen, 2001 Mediators of inflammation in cerebral ischemia: roles of cytokine amd cyclooxygenase-2 activation. Expression of interleukin-β, tumor necrosis factor-α, their receptors, and cyclooxygenase-2 in experimental and clinical brain infarction. Academic dissertation for faculty of medicine, University of Helsinki.
54. Schmidt-Kastner R., Freund T.F. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 1991, 40:599-636.
55. Soriano F.X., Papadia S., Hofmann F., Hardingham N.R., Bading H., Hardingham G.E. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J. Neurosci. 2006, 26:4509-4518.
56. Stoppini L., Buchs P.A., Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 1991, 37:173-182.
57. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 2004, 14:311-317.
58. Tuttolomondo A., di Sciacca R., di Raimondo D., Serio A., D'Aguanno G., La Placa S., Pecoraro R., Arnao V., Marino L., Monaco S., Natale E., Licata G., Pinto A. Plasma levels of inflammatory and thrombotic/fibrinolytic markers in acute ischemic strokes: relationship with TOAST subtype, outcome and infarct site. J. Neuroimmunol. 2009, 215:84-89.
59. Wang X., Li X., Erhardt J.A., Barone F.C., Feuerstein G.Z. Detection of tumor necrosis factor-alpha mRNA induction in ischemic brain tolerance by means of real-time polymerase chain reaction. J. Cereb. Blood Flow Metab. 2000, 20:15-20.
60. Wang J.Y., Shum A.Y., Ho Y.J. Oxidative neurotoxicity in rat cerebral cortex neurons: synergistic effects of H2O2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J. Neurosci. Res. 2003, 72:508-519.
61. Wegener S., Gottschalk B., Jovanovic V., Knab R., Fiebach J.B., Schellinger P.D., Kucinski T., Jungehulsing G.J., Brunecker P., Muller B., Banasik A., Amberger N., Wernecke K.D., Siebler M., Rother J., Villringer A., Weih M. Transient ischemic attacks before ischemic stroke: preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke 2004, 35:616-621.
62. Weih M., Kallenberg K., Bergk A., Dirnagl U., Harms L., Wernecke K.D., Einhaupl K.M. Attenuated stroke severity after prodromal TIA: a role for ischemic tolerance in the brain?. Stroke 1999, 30:1851-1854.
63. Wittenberg G.M., Tsien J.Z. An emerging molecular and cellular framework for memory processing by the hippocampus. Trends Neurosci. 2002, 25:501-505.
64. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 1986, 6:2950-2967.
65. Zou J.Y., Crews F.T. TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NF kappa B inhibition. Brain Res. 2005, 1034:11-24.