A role for tumor necrosis factor-α in ischemia and ischemic preconditioning

Journal of Neuroinflammation

John J O'Connor¹  Orla Watters¹ 

[1] UCD School of Biomolecular and Biomedical Science, UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland

关键词: preconditioning;    calcium;    glutamate;    hippocampus;    ischemia;    Tumor Necrosis Factor-alpha;   

Others  :  1213221
DOI  :  10.1186/1742-2094-8-87

 received in 2011-06-03, accepted in 2011-08-02,  发布年份 2011

【 摘 要 】

During cerebral ischemia, elevation of TNF-α and glutamate to pathophysiological levels may induce dysregulation of normal synaptic processes, leading ultimately to cell death. Previous studies have shown that patients subjected to a mild transient ischemic attack within a critical time window prior to a more severe ischemic episode may show attenuation in the clinical severity of the stroke and result in a more positive functional outcome. Studies with organotypic hippocampal cultures and mixed primary hippocampal cultures have shown that prior incubation with low concentrations of glutamate and TNF-α increase the resistance of neurones to a subsequent insult from glutamate, AMPA and NMDA, while co-exposure of TNF-α and for example AMPA may have neuroprotective effects compared to cultures exposed to excitotoxic agents alone. In addition our work has shown that although glutamate and TNF-α pretreatment induces analogous levels of desensitisation of the intracellular calcium dynamics of neurons under resting conditions and in response to acute glutamate stimulation, their downstream signalling pathways involved in this response do not converge. Glutamate and TNF-α would appear to have opposing effects on resting Ca²⁺ levels which supports the proposal that they have distinct modes of preconditioning.

【 授权许可】

   
2011 Watters and O'Connor; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Suyama K: Changes of neuronal transmission in the hippocampus after transient ischemia in spontaneously hypertensive rats and the protective effects of MK-801. Stroke 1992, 23:260-266.
• [2]Jarvis CR, Anderson TR, Andrew RD: Anoxic depolarization mediates acute damage independent of glutamate in neocortical brain slices. Cereb Cortex 2001, 11:249-259.
• [3]Kohno K, Hoehn-Berlage M, Mies G, Back T, Hossmann KA: Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging 1995, 13:73-80.
• [4]Rosenberg GA: Ischemic brain edema. Prog Cardiovasc Dis 1999, 42:209-216.
• [5]Barber PA, Auer RN, Buchan AM, Sutherland GR: Understanding and managing ischemic stroke. Can J Physiol Pharmacol 2001, 79:283-296.
• [6]Martin RL, Lloyd HGE, Cowan AI: The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends in Neurosciences 1994, 17:251-257.
• [7]Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P: Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
• [8]Kogo J, Takeba Y, Kumai T, Kitaoka Y, Matsumoto N, Ueno S, Kobayashi S: Involvement of TNF-alpha in glutamate-induced apoptosis in a differentiated neuronal cell line. Brain Res 2006, 1122:201-208.
• [9]Liu T, Clark RK, McDonnell PC, Young PR, White RF, Barone FC, Feuerstein GZ: Tumor necrosis factor-alpha expression in ischemic neurons. Stroke 1994, 25:1481-1488.
• [10]Bullock R, Zauner A, Woodward J, Young HF: Massive persistent release of excitatory amino acids following human occlusive stroke. Stroke 1995, 26:2187-2189.
• [11]Davalos A, Castillo J, Serena J, Noya M: Duration of glutamate release after acute ischemic stroke. Stroke 1997, 28:708-710.
• [12]Ventura R, Harris KM: Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes. The Journal of Neuroscience 1999, 19:6897-6906.
• [13]Dziewulska D, Mossakowski MJ: Cellular expression of tumor necrosis factor a and its receptors in human ischemic stroke. Clin Neuropathol 2003, 22:35-40.
• [14]Figiel I, Dzwonek K: TNF[alpha] and TNF receptor 1 expression in the mixed neuronal-glial cultures of hippocampal dentate gyrus exposed to glutamate or trimethyltin. Brain Research 2007, 1131:17.
• [15]Dopp JM, Mackenzie-Graham A, Otero GC, Merrill JE: Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia. J Neuroimmunol 1997, 75:104-112.
• [16]Bebo BF Jr, Linthicum DS: Expression of mRNA for 55-kDa and 75-kDa tumor necrosis factor (TNF) receptors in mouse cerebrovascular endothelium: effects of interleukin-1 beta, interferon-gamma and TNF-alpha on cultured cells. J Neuroimmunol 1995, 62:161-167.
• [17]Tartaglia LA, Weber RF, Figari IS, Reynolds C, Palladino MA Jr, Goeddel DV: The two different receptors for tumor necrosis factor mediate distinct cellular responses. Proc Natl Acad Sci USA 1991, 88:9292-9296.
• [18]Dembic Z, Loetscher H, Gubler U, Pan YC, Lahm HW, Gentz R, Brockhaus M, Lesslauer W: Two human TNF receptors have similar extracellular, but distinct intracellular, domain sequences. Cytokine 1990, 2:231-237.
• [19]Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel UL: 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.
• [20]Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ: A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science 2000, 288:2351-2354.
• [21]Pinckard JK, Sheehan KC, Schreiber RD: Ligand-induced formation of p55 and p75 tumor necrosis factor receptor heterocomplexes on intact cells. J Biol Chem 1997, 272:10784-10789.
• [22]Pinckard JK, Sheehan KC, Arthur CD, Schreiber RD: Constitutive shedding of both p55 and p75 murine TNF receptors in vivo. J Immunol 1997, 158:3869-3873.
• [23]Rothe M, Wong SC, Henzel WJ, Goeddel DV: A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 1994, 78:681-692.
• [24]Song HY, Regnier CH, Kirschning CJ, Goeddel DV, Rothe M: Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc Natl Acad Sci USA 1997, 94:9792-9796.
• [25]Hsu H, Xiong J, Goeddel DV: The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 1995, 81:495-504.
• [26]Chen G, Goeddel DV: TNF-R1 signaling: a beautiful pathway. Science 2002, 296:1634-1635.
• [27]Pimentel-Muiños FX, Seed B: Regulated Commitment of TNF Receptor Signaling: A Molecular Switch for Death or Activation. Immunity 1999, 11:783-793.
• [28]MacEwan DJ: TNF receptor subtype signalling: differences and cellular consequences. Cell Signal 2002, 14:477-492.
• [29]Liu ZG, Hsu H, Goeddel DV, Karin M: Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 1996, 87:565-576.
• [30]Reddy SA, Huang JH, Liao WS: Phosphatidylinositol 3-kinase as a mediator of TNF-induced NF-kappa B activation. J Immunol 2000, 164:1355-1363.
• [31]Botchkina GI, Meistrell ME, Botchkina IL, Tracey KJ: Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol Med 1997, 3:765-781.
• [32]Schneider-Brachert W, Tchikov V, Neumeyer J, Jakob M, Winoto-Morbach S, Held-Feindt J, Heinrich M, Merkel O, Ehrenschwender M, Adam D, et al.: Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 2004, 21:415-428.
• [33]Badiola N, Malagelada C, Llecha N, Hidalgo J, Comella JX, Sabriá J, Rodríguez-Alvarez J: Activation of caspase-8 by tumour necrosis factor receptor 1 is necessary for caspase-3 activation and apoptosis in oxygen-glucose deprived cultured cortical cells. Neurobiol Dis 2009, 35:438-47.
• [34]Hughes CC, Male DK, Lantos PL: Adhesion of lymphocytes to cerebral microvascular cells: effects of interferon-gamma, tumour necrosis factor and interleukin-1. Immunology 1988, 64:677-681.
• [35]Tsao N, Hsu HP, Wu CM, Liu CC, Lei HY: Tumour necrosis factor-alpha causes an increase in blood-brain barrier permeability during sepsis. J Med Microbiol 2001, 50:812-821.
• [36]Selmaj K, Farooq M, Norton W, Raine C, Brosnan C: Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. The Journal of Immunology 1990, 144:129-135.
• [37]Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP: Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med 1996, 2:788-94.
• [38]Gary DS, Bruce-Keller AJ, Kindy MS, Mattson MP: Ischemic and excitotoxic brain injury is enhanced in mice lacking the p55 tumor necrosis factor receptor. J Cereb Blood Flow Metab 1998, 18:1283-7.
• [39]Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B: Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009, 29:1319-30.
• [40]Taoufik E, Petit E, Divoux D, Tseveleki V, Mengozzi M, Roberts ML, Valable S, Ghezzi P, Quackenbush J, Brines M, Cerami A, Probert L: TNF receptor I sensitizes neurons to erythropoietin- and VEGF-mediated neuroprotection after ischemic and excitotoxic injury. Proc Natl Acad Sci USA 2008, 105:6185-90.
• [41]Perea G, Araque A: Synaptic regulation of the astrocyte calcium signal. J Neural Transm 2005, 112:127-135.
• [42]Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, Sonobe Y, Mizuno T, Suzumura A: Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 2006, 281:21362-21368.
• [43]Boston-Howes W, Gibb SL, Williams EO, Pasinelli P, Brown RH Jr, Trotti D: Caspase-3 cleaves and inactivates the glutamate transporter EAAT2. J Biol Chem 2006, 281:14076-14084.
• [44]Sitcheran R, Gupta P, Fisher PB, Baldwin AS: Positive and negative regulation of EAAT2 by NF-kappaB: a role for N-myc in TNFalpha-controlled repression. Embo J 2005, 24:510-520.
• [45]Zou JY, Crews FT: 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.
• [46]Sparacio SM, Zhang Y, Vilcek J, Benveniste EN: Cytokine regulation of interleukin-6 gene expression in astrocytes involves activation of an NF-kappa B-like nuclear protein. J Neuroimmunol 1992, 39:231-242.
• [47]Stellwagen D, Beattie EC, Seo JY, Malenka RC: Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci 2005, 25:3219-3228.
• [48]Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Melle G: Do transient ischemic attacks have a neuroprotective effect? Neurology 2000, 54:2089-2094.
• [49]Castillo J, Moro MA, 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.
• [50]Grabb MC, Choi DW: Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 1999, 19:1657-1662.
• [51]Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, Feuerstein GZ: 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 1950-1931
• [52]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.
• [53]Matsushima K, Hakim AM: Transient forebrain ischemia protects against subsequent focal cerebral ischemia without changing cerebral perfusion. Stroke 1995, 26:1047-1052.
• [54]Pringle AK, Thomas SJ, Signorelli F, Iannotti F: Ischaemic pre-conditioning in organotypic hippocampal slice cultures is inversely correlated to the induction of the 72 kDa heat shock protein (HSP72). Brain Res 1999, 845:152-164.
• [55]Liu J, Ginis I, Spatz M, Hallenbeck JM: Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide. Am J Physiol Cell Physiol 2000, 278:C144-153.
• [56]Wang X, Li X, Erhardt JA, Barone FC, Feuerstein GZ: 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.
• [57]Saha RN, 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.
• [58]Lin CH, Chen PS, Gean PW: Glutamate preconditioning prevents neuronal death induced by combined oxygen-glucose deprivation in cultured cortical neurons. Eur J Pharmacol 2008, 589:85-93.
• [59]Saha RN, Ghosh A, Palencia CA, Fung YK, Dudek SM, Pahan K: TNF-alpha preconditioning protects neurons via neuron-specific up-regulation of CREB-binding protein. J Immunol 2009, 183:2068-2078.
• [60]Glazner GW, Mattson MP: 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.
• [61]Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, Vezzani A, Malva JO, 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.
• [62]De Simoni A, Griesinger CB, Edwards FA: Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 2003, 550:135-147.
• [63]Watters O, Pickering M, O'Connor JJ: Preconditioning effects of tumor necrosis factor-alpha and glutamate on calcium dynamics in rat organotypic hippocampal cultures. J Neuroimmunol 2011, 234:27-39.
• [64]Sotgiu S, Zanda B, Marchetti B, Fois ML, Arru G, Pes GM, Salaris FS, Arru A, Pirisi A, Rosati G: Inflammatory biomarkers in blood of patients with acute brain ischemia. Eur J Neurol 2006, 13:505-513.
• [65]Wilde GJ, Pringle AK, Sundstrom LE, Mann DA, Iannotti F: Attenuation and augmentation of ischaemia-related neuronal death by tumour necrosis factor-alpha in vitro. Eur J Neurosci 2000, 12:3863-3870.
• [66]Pradillo JM, Hurtado O, Romera C, Cardenas A, Fernandez-Tome P, Alonso-Escolano D, Lorenzo P, Moro MA, Lizasoain I: TNFR1 mediates increased neuronal membrane EAAT3 expression after in vivo cerebral ischemic preconditioning. Neuroscience 2006, 138:1171-1178.
• [67]Goldberg MP, Choi DW: Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 1993, 13:3510-3524.
• [68]Mabuchi T, Kitagawa K, Kuwabara K, Takasawa K, Ohtsuki T, Xia Z, Storm D, Yanagihara T, Hori M, Matsumoto M: Phosphorylation of cAMP response element-binding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo. J Neurosci 2001, 21:9204-9213.
• [69]Werner CG, Scartabelli T, Pancani T, Landucci E, Moroni F, Pellegrini-Giampietro DE: Differential role of mGlu1 and mGlu5 receptors in rat hippocampal slice models of ischemic tolerance. Eur J Neurosci 2007, 25:3597-3604.
• [70]Guerrini L, Blasi F, Denis-Donini S: Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci USA 1995, 92:9077-9081.
• [71]Tamatani M, Che YH, Matsuzaki H, Ogawa S, Okado H, Miyake S, Mizuno T, Tohyama M: Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 1999, 274:8531-8538.
• [72]Irving EA, Barone FC, Reith AD, Hadingham SJ, Parsons AA: 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.
• [73]Scholzke MN, Potrovita I, Subramaniam S, Prinz S, Schwaninger M: Glutamate activates NF-kappaB through calpain in neurons. Eur J Neurosci 2003, 18:3305-3310.
• [74]Chaparro-Huerta V, Rivera-Cervantes MC, Flores-Soto ME, 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.