Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 21-27 , 25 January 2010

Tumor necrosis factor-α impairs the recovery of synaptic transmission from hypoxia in rat hippocampal slices

Received 7 August 2009 ,Revised 15 October 2009 ,Accepted 5 November 2009.

References 

  1. Arrigoni E, Crocker AJ, Saper CB, Greene RW, Scammell TE. Deletion of presynaptic adenosine A1 receptors impairs the recovery of synaptic transmission after hypoxia. Neuroscience. 2005;132:575–580
  2. Barone FC, Arvin B, White RF, Miller A, Webb CL, Willette RN, et al. Tumor necrosis factor-alpha. A mediator of focal ischemic brain injury. Stroke. 1997;28:1233–1244
  3. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, et al. SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J. Pharmacol. Exp. Ther. 2001;296:312–321
  4. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, et al. 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
  5. Blomqvist P, Wieloch T. Ischemic brain damage in rats following cardiac arrest using a long-term recovery model. J. Cereb. Blood Flow Metab. 1985;5:420–431
  6. Bon CL, Garthwaite J. Adenosine acting on A1 receptors protects NO-triggered rebound potentiation and LTP in rat hippocampal slices. J. Neurophysiol. 2002;87:1781–1789
  7. Brust TB, Cayabyab FS, Zhou N, MacVicar BA. p38 mitogen-activated protein kinase contributes to adenosine A1 receptor-mediated synaptic depression in area CA1 of the rat hippocampus. J. Neurosci. 2006;26:12427–12438
  8. Butler MP, O'Connor JJ, Moynagh PN. Dissection of tumor-necrosis factor-alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP. Neuroscience. 2004;124:319–326
  9. Centonze D, Saulle E, Pisani A, Bernardi G, Calabresi P. Adenosine-mediated inhibition of striatal GABAergic synaptic transmission during in vitro ischaemia. Brain. 2001;124:1855–1865
  10. 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
  11. Chavez-Valdez R, Wills-Karp M, Ahlawat R, Cristofalo EA, Nathan A, Gauda EB. Caffeine modulates TNF-alpha production by cord blood monocytes: the role of adenosine receptors. Pediatr. Res. 2009;65:203–208
  12. Chen ZF, Schottler F, Arlinghaus L, Kassell NF, Lee KS. Hypoxic neuronal damage in the absence of hypoxic depolarization in rat hippocampal slices: the role of glutamate receptors. Brain Res. 1996;708:82–92
  13. Coppi E, Pugliese AM, Stephan H, Muller CE, Pedata F. Role of P2 purinergic receptors in synaptic transmission under normoxic and ischaemic conditions in the CA1 region of rat hippocampal slices. Purinergic Signal. 2007;3:203–219
  14. Cumiskey D, Butler MP, Moynagh PN, O'Connor 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
  15. Cunningham AJ, Murray CA, O'Neill LA, Lynch MA, O'Connor JJ. Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci. Lett. 1996;203:17–20
  16. de Mendonca A, Ribeiro JA. Long-term potentiation observed upon blockade of adenosine A1 receptors in rat hippocampus is N-methyl-d-aspartate receptor-dependent. Neurosci. Lett. 2000;291:81–84
  17. de Mendonca A, Sebastiao AM, Ribeiro JA. Adenosine: does it have a neuroprotective role after all?. Brain Res. Brain Res. Rev. 2000;33:258–274
  18. Doolette DJ, Kerr DI. Hyperexcitability in CA1 of the rat hippocampal slice following hypoxia or adenosine. Brain Res. 1995;677:127–137
  19. Feng Y, LeBlanc MH. Effect of agmatine on the time course of brain inflammatory cytokines after injury in rat pups. Ann. N. Y. Acad. Sci. 2003;1009:152–156
  20. Fujiwara N, Higashi H, Shimoji K, Yoshimura M. Effects of hypoxia on rat hippocampal neurones in vitro. J. Physiol. 1987;384:131–151
  21. Gervitz LM, Lutherer LO, Davies DG, Pirch JH, Fowler JC. Adenosine induces initial hypoxic–ischemic depression of synaptic transmission in the rat hippocampus in vivo. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001;280:R639–R645
  22. Hsu KS, Ho WC, Huang CC, Tsai JJ. Transient removal of extracellular Mg(2+) elicits persistent suppression of LTP at hippocampal CA1 synapses via PKC activation. J. Neurophysiol. 2000;84:1279–1288
  23. Izumi Y, Katsuki H, Benz AM, Zorumski CF. Oxygen deprivation produces delayed inhibition of long-term potentiation by activation of NMDA receptors and nitric oxide synthase. J. Cereb. Blood Flow Metab. 1998;18:97–108
  24. Kim JH, Park YK, Kim JH, Kwon TH, Chung HS. Transient recovery of synaptic transmission is related to rapid energy depletion during hypoxia. Neurosci. Lett. 2006;400:1–6
  25. Lee HT, Xu H, Nasr SH, Schnermann J, Emala CW. A1 adenosine receptor knockout mice exhibit increased renal injury following ischemia and reperfusion. Am. J. Physiol. Renal. Physiol. 2004;286:F298–F306
  26. Liang YC, Huang CC, Hsu KS. A role of p38 mitogen-activated protein kinase in adenosine A1 receptor-mediated synaptic depotentiation in area CA1 of the rat hippocampus. Mol. Brain. 2008;1:13
  27. Lipton P, Whittingham TS. Reduced ATP concentration as a basis for synaptic transmission failure during hypoxia in the in vitro guinea-pig hippocampus. J. Physiol. 1982;325:51–65
  28. Liu T, Clark RK, McDonnell PC, Young PR, White RF, Barone FC, et al. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke. 1994;25:1481–1488
  29. MacEwan DJ. TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal. 2002;14:477–492
  30. Markus T, Cronberg T, Cilio C, Pronk C, Wieloch T, Ley D. Tumor necrosis factor receptor-1 is essential for LPS-induced sensitization and tolerance to oxygen-glucose deprivation in murine neonatal organotypic hippocampal slices. J. Cereb. Blood Flow Metab. 2009;29:73–86
  31. Mayne M, Shepel PN, Jiang Y, Geiger JD, Power C. Dysregulation of adenosine A1 receptor-mediated cytokine expression in peripheral blood mononuclear cells from multiple sclerosis patients. Ann. Neurol. 1999;45:633–639
  32. Murakami Y, Saito K, Hara A, Zhu Y, Sudo K, Niwa M, et al. Increases in tumor necrosis factor-alpha following transient global cerebral ischemia do not contribute to neuron death in mouse hippocampus. J. Neurochem. 2005;93:1616–1622
  33. Ozawa H, Shioda S, Dohi K, Matsumoto H, Mizushima H, Zhou CJ, et al. Delayed neuronal cell death in the rat hippocampus is mediated by the mitogen-activated protein kinase signal transduction pathway. Neurosci. Lett. 1999;262:57–60
  34. Pickering M, Cumiskey D, O'Connor JJ. Actions of TNF-alpha on glutamatergic synaptic transmission in the central nervous system. Exp. Physiol. 2005;90:663–670
  35. Pincheira R, Castro AF, Ozes ON, Idumalla PS, Donner DB. Type 1 TNF receptor forms a complex with and uses Jak2 and c-Src to selectively engage signaling pathways that regulate transcription factor activity. J. Immunol. 2008;181:1288–1298
  36. Pugliese AM, Coppi E, Spalluto G, Corradetti R, Pedata F. A3 adenosine receptor antagonists delay irreversible synaptic failure caused by oxygen and glucose deprivation in the rat CA1 hippocampus in vitro. Br. J. Pharmacol. 2006;147:524–532
  37. Renauld AE, Spengler RN. Tumor necrosis factor expressed by primary hippocampal neurons and SH-SY5Y cells is regulated by alpha(2)-adrenergic receptor activation. J. Neurosci. Res. 2002;67:264–274
  38. Rex CS, Kramar EA, Colgin LL, Lin B, Gall CM, Lynch G. Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J. Neurosci. 2005;25:5956–5966
  39. Sajjadi FG, Takabayashi K, Foster AC, Domingo RC, Firestein GS. Inhibition of TNF-alpha expression by adenosine: role of A3 adenosine receptors. J. Immunol. 1996;156:3435–3442
  40. Saleshando G, O'Connor JJ. SB203580, the p38 mitogen-activated protein kinase inhibitor blocks the inhibitory effect of beta-amyloid on long-term potentiation in the rat hippocampus. Neurosci. Lett. 2000;288:119–122
  41. Scherbel U, Raghupathi R, Nakamura M, Saatman KE, Trojanowski JQ, Neugebauer E, et al. Differential acute and chronic responses of tumor necrosis factor-deficient mice to experimental brain injury. Proc. Natl. Acad. Sci. U. S. A. 1999;96:8721–8726
  42. Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience. 1991;40:599–636
  43. Scholz KP, Miller RJ. Presynaptic inhibition at excitatory hippocampal synapses: development and role of presynaptic Ca2+ channels. J. Neurophysiol. 1996;76:39–46
  44. Sebastiao AM, de Mendonca A, Moreira T, Ribeiro JA. Activation of synaptic NMDA receptors by action potential-dependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation. J. Neurosci. 2001;21:8564–8571
  45. Seta K, Kim HW, Ferguson T, Kim R, Pathrose P, Yuan Y, et al. Genomic and physiological analysis of oxygen sensitivity and hypoxia tolerance in PC12 cells. Ann. N. Y. Acad. Sci. 2002;971:379–388
  46. Shen Y, Li R, Shiosaki K. Inhibition of p75 tumor necrosis factor receptor by antisense oligonucleotides increases hypoxic injury and beta-amyloid toxicity in human neuronal cell line. J. Biol. Chem. 1997;272:3550–3553
  47. Souza LF, Horn AP, Gelain DP, Jardim FR, Lenz G, Bernard EA. Extracellular inosine modulates ERK 1/2 and p38 phosphorylation in cultured Sertoli cells: possible participation in TNF-alpha modulation of ERK 1/2. Life Sci. 2005;77:3117–3126
  48. Sperlagh B, Zsilla G, Baranyi M, Illes P, Vizi ES. Purinergic modulation of glutamate release under ischemic-like conditions in the hippocampus. Neuroscience. 2007;149:99–111
  49. Stellwagen D, Malenka RC. Synaptic scaling mediated by glial TNF-alpha. Nature. 2006;440:1054–1059
  50. 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
  51. Sugino T, Nozaki K, Takagi Y, Hattori I, Hashimoto N, Moriguchi T, et al. Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus. J. Neurosci. 2000;20:4506–4514
  52. Sun XC, Li WB, Li QJ, Zhang M, Xian XH, Qi J, et al. Limb ischemic preconditioning induces brain ischemic tolerance via p38 MAPK. Brain Res. 2006;1084:165–174
  53. Tancredi V, D'Arcangelo G, Grassi F, Tarroni P, Palmieri G, Santoni A, et al. Tumor necrosis factor alters synaptic transmission in rat hippocampal slices. Neurosci. Lett. 1992;146:176–178
  54. Taylor CP, Weber ML, Gaughan CL, Lehning EJ, LoPachin RM. Oxygen/glucose deprivation in hippocampal slices: altered intraneuronal elemental composition predicts structural and functional damage. J. Neurosci. 1999;19:619–629
  55. Tha KK, Okuma Y, Miyazaki H, Murayama T, Uehara T, Hatakeyama R, et al. Changes in expressions of proinflammatory cytokines IL-1beta, TNF-alpha and IL-6 in the brain of senescence accelerated mouse (SAM) P8. Brain Res. 2000;885:25–31
  56. Walton KM, DiRocco R, Bartlett BA, Koury E, Marcy VR, Jarvis B, et al. Activation of p38MAPK in microglia after ischemia. J. Neurochem. 1998;70:1764–1767
  57. Wang Q, Wu J, Rowan MJ, Anwyl R. Beta-amyloid inhibition of long-term potentiation is mediated via tumor necrosis factor. Eur. J. NeuroSci. 2005;22:2827–2832
  58. Wu LG, Saggau P. Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron. 1994;12:1139–1148
  59. Wu LG, Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 1994;14:645–654
  60. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 1995;270:1326–1331
  61. Yang L, Lindholm K, Konishi Y, Li R, Shen Y. Target depletion of distinct tumor necrosis factor receptor subtypes reveals hippocampal neuron death and survival through different signal transduction pathways. J. Neurosci. 2002;22:3025–3032
  62. Zhu PJ, Krnjevic K. Adenosine release is a major cause of failure of synaptic transmission during hypoglycaemia in rat hippocampal slices. Neurosci. Lett. 1993;155:128–131
  63. Zola-Morgan S, Squire LR, Amaral DG. 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

PII: S0165-5728(09)00461-5

doi: 10.1016/j.jneuroim.2009.11.002

Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 21-27 , 25 January 2010