Interleukin-1β but not tumor necrosis factor-α potentiates neuronal damage by quinolinic acid: protection by an adenosine A2A receptor antagonist

Journal of Neuroscience Research

Volumn 85, Issue 5, 2007, Pages 1077-1085

  Stone, Trevor W ^a,b   Behan, Wilhelmina M H ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cytokines; Excitotoxicity; Hippocampus; Interleukin 1 ; Kynurenic acid; Kynurenines; Quinolinic acid; TNF ; Tumor necrosis factor

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; ADENOSINE A2A RECEPTOR ANTAGONIST; INTERLEUKIN 1BETA; QUINOLINIC ACID; TUMOR NECROSIS FACTOR ALPHA; ADENOSINE A2A RECEPTOR; NEUROPROTECTIVE AGENT; NEUROTOXIN; TRIAZINE DERIVATIVE; TRIAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN INFECTION; BRAIN ISCHEMIA; CELL DAMAGE; CONTROLLED STUDY; DRUG ACTIVITY; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; BRAIN INJURY; CELL PROTECTION; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; IMMUNOLOGY; METABOLISM; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; WISTAR RAT;

ANIMALS; BRAIN INJURIES; BRAIN ISCHEMIA; CYTOPROTECTION; DRUG SYNERGISM; HIPPOCAMPUS; INTERLEUKIN-1BETA; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PYRAMIDAL CELLS; QUINOLINIC ACID; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A2A; TRIAZINES; TRIAZOLES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34147218086     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21212     Document Type: Article

References (92)

1. 2A receptors in rat brain. Eur J Pharmacol 411:205-210.
2. Allan SM. 2002. Varied actions of proinflammatory cytokines on excitotoxic cell death in the rat CNS. J Neurosci Res 67:428-434.
3. Allan SM, Lawrence CB, Rothwell NJ. 1998. Interleukin-18 and interleukin-1 receptor antagonist do not affect glutamate release or calcium entry in rat striatal synaptosomes. Mol Psychiatry 3:178-182.
4. Angstwurm K, Freyer D, Dirnagl U, Hanisch UK, Schumann RR, Einhaupl KM, Weber JR. 1998. Tumour necrosis factor alpha induces only minor inflammatory changes in the CNS, but augments experimental meningitis. Neuroscience 86:627-634.
5. 2+ accumulation. Proc Natl Acad Sci U S A 92:9328-9332.
6. Barone FC, Arvin B, White RF, Miller A, Webb CL, Willette RN, Lysko PG, Feuerstein GZ. 1997. Tumor necrosis factor-alpha - a mediator of focal ischemic brain injury. Stroke 28:1233-1244.
7. Behan WMH, Stone TW. 2000. Role of kynurenines in the neurotoxic actions of kainic acid. Br J Pharmacol 129:1764-1770.
8. 2A receptor antagonists. Br J Pharmacol 135:1435-1442.
9. Behan WMH, MacDonald M, Darlington LG, Stone TW. 1999. Oxidative stress as a mechanism for quinolinic acid-induced hippocampal damage: protection by melatonin and deprenyl. Br J Pharmacol 128: 1754-1760.
10. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, Vezzani A, Malva JO, Zimmer J. 2005. Modulator effects of interleukin-1β and TNF-α on AMPA-induced excitotoxicity in mouse organotypic slice cultures. J Neurosci 25:6734-6744.
11. Blight AR, Leroy EC Jr, Heyes MP. 1997. Quinolinic acid accumulation in injured spinal cord: time course, distribution, and species differences between rat and guinea pig. J Neurotrauma 14:89-98.
12. Botchkina GI, Meistrell ME, Botchkina IL, Tracey KJ. 1997. Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol Med 3:765-781.
13. Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP. 1996. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med 7:788-794.
14. Canellada A, Cano E, Sanchez-Ruiloba L, Zafra F, Redondo JM. 2006. Calcium-dependent expression of TNF-α in neural cells is mediated by the calcineurin/NFAT pathway. Mol Cell Neurosci 31:692-701.
15. Carlson NG, Wieggel WA, Chen JA, Bacchi A, Rogers SW, Gahring LC. 1999. Inflammatory cytokines, IL-1, IL-1β, IL-6 and TNF-α impart neuroprotection to an excitotoxin through distinct pathways. J Immunol 163:3963-3968.
16. Cheng B, Christakos S, Mattson MP. 1994. Tumor necrosis factors protect neurons against metabolic excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12:139-153.
17. Chiarugi A, Calvani M, Meli E, Traggiai E, Moroni F. 2001. Synthesis and release of neurotoxic kynurenine metabolites by human monocyte-derived macrophages. J Neuroimmunol 120:190-198.
18. Chung IY, Benveniste EN. 1990. Tumor necrosis factor-alpha production by astrocytes - induction by lipopolysaccharide, IFN-gamma, and IL1-β. J Immunol 144:2999-3007.
19. 2a receptors in the rat hippocampus. Brain Res 649:208-216.
20. De A, Krueger JM, Simasko SM. 2003. Tumour necrosis alpha increases cytosolic calcium responses to AMPA and KCl in primary cultures of rat hippocampal neurons. Brain Res 981:133-142.
21. Dimopoulos N, Piperi C, Salonicioti A, Mitropoulos P, Kallai E, Liappas I, Lea RW, Kalofoutis A. 2006. Indices of low-grade inflammation correlate with early cognitive deterioration in an elderly Greek population. Neurosci Lett 398:118-123.
22. Eriksson C, Tehranian R, Iverfeldt K, Winblad W, Schultzberg M. 2000. Increased expression of mRNA encoding interleukin-1β and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration. J Neurosci Res 60:266-279.
23. Espey MG, Chernyshev ON, Reinhard JF, Namboodiri MAA, Colton CA. 1997. Activated human microglia produce the excitotoxin quinolinic acid. Neuroreport 8:431-434.
24. Galarraga E, Surmeier DJ, Kitai ST. 1990. Quinolinate and kainate neurotoxicity in neostriatal cultures is potentiated by coculturing with neocortical neurons. Brain Res 512:269-276.
25. Gao Y, Phillis JW. 1994. CGS 15943, an adenosine A2 receptor antagonist, reduces cerebral ischemic injury in the mongolian gerbil. Life Sci 55:PL61-PL65.
26. Giulian D, Vaca K, Noonan CA. 1990. Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 250:1593-1596.
27. Glazner GW, Mattson MP. 2000. Differential effects of BDNF, ADNF9, and TNF-alpha on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Exp Neurol 161: 442-452.
28. Gregersen R, Lambertsen K, Finsen B. 2000. Microglia and macrophages are the major source of TNF in permanent middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 20:53-65.
29. Grundy RJ, Rothwell NJ, Allan SM. 2002. Site-specific actions of interleukin-1 on excitotoxic cell death in rat striatum. Brain Res 926:142-148.
30. Hailer NP, Vogt C, Korf HW, Dehghani F. 2005. Interleukin-1 beta exacerbates and interleukin-1 receptor antagonist attenuates neuronal injury and microglial activation after excitotoxic damage in organotypic hippocampal slice cultures. Eur J Neurosci 21:2347-2360.
31. 2A receptor agonists reduce ischemia/reperfusion injury of rat liver mainly by inhibiting leukocyte activation. J Pharmacol Exp Therap 294:1034-1042.
32. Hermann GE, Rogers RC, Bresnahan JC, Beattie MS. 2001. Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol Dis 8:590-599.
33. Heyes MP, Nowak TS Jr. 1990. Delayed increases in regional brain quinolinic acid follow transient ischemia in the gerbil. J Cereb Blood Flow Metab 10:660-667.
34. Heyes MP, Rubinow D, Lane C, Markey SP. 1989. Cerebrospinal fluid quinolinic acid concentrations are increased in acquired immune deficiency syndrome. Ann Neurol 26:275-277.
35. Heyes MP, Mefford IN, Quearry BJ, Dedhia M, Lackner A. 1990. Increased ratio of quinolinic acid to kynurenic acid in cerebrospinal fluid of D retrovirus-infected rhesus macaques: relationship to clinical and viral status. Ann Neurol 27:666-675.
36. Heyes MR, Brew BJ, Martin A, Price RW, Salazar AM, Sidtis JJ, Yergey JA, Mourdian MM, Sadler AE, Keilp J, Rubmow D, Markey SP. 1991. Quinolinic acid in cerebrospinal fluid and serum in HIV-1 infection: relationhip to clinical and neurologic status. Ann Neurol 29:202-209.
37. Heyes MP, Jordan EK, Lee K, Saito K, Frank JA, Snoy PJ, Markey SP, Gravell M. 1992a. Relationship of neurologic status in macaques infected with the simian immunodeficiency virus to cerebrospinal fluid quinolinic acid and kynurenic acid. Brain Res 570:237-250.
38. Heyes MP, Saito K, Markey SP. 1992b. Human macrophages convert L-trptophan into the neurotoxin quinolinic acid. Biochem J 283:633-635.
39. Heyes MP, Achim CL, Wiley CA, Major EO, Saito K, Markey SP. 1996. Human microglia convert L-tryptophan into the neurotoxin quinolinic acid. Biochem J 320:595-597.
40. 2A receptor agonists and antagonists. Neuroscience 85:229-237.
41. 2A receptor antagonist. Brain Res 800:328-335.
42. Kerr SJ, Armati PJ, Guillemin GJ, Brew BJ. 1998. Chronic exposure of human neurones to quinolinic acid results in neuronal changes consistent with AIDS dementia complex. AIDS 12:355-363.
43. Khaspekov L, Kida E, Victorov I, Mossakowski MJ. 1989. Neurotoxic effect induced by quinolinic acid in dissociated cell-culture of mouse hippocampus. J Neurosci Res 22:150-157.
44. 2+ increase in cultured cortical astrocytes. Bram Res 893:237-243.
45. Lawrence CB, Allan SM, Rothwell NJ. 1998. Interleukin-1 beta and the interleukin-1 receptor antagonist act in the striatum to modify excitotoxic brain damage in the rat. Eur J Neurosci 10:1188-1195.
46. Lieberman AP, Pitha PM, Shin HS, Shin ML. 1989. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci U S A 86:6348-6352.
47. 2A adenosine receptor. Drug Dev Res 64:172-177.
48. Mascarucci P, Pergo C, Terrazzino S, De Simoni MG. 1998. Glutamate release in the tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1β. Neuroscience 86:1285-1290.
49. Meistrell ME, Botchkina GI, Wang H, Di Santo E, Cockcroft KM, Bloom O, Vishnubhakat JM, Ghezzi P, Tracey KJ. 1997. Tumour necrosis factor is a brain damaging cytokine in cerebral ischemia. Shock 8:341-348.
50. Moffett JR, Espey MG, Gaudet SJ, Namboodiri MAA. 1993. Antibodies to quinolinic acid reveal localization in select immune cells rather than neurons or astroglia. Brain Res 623:337-340.
51. Moffett JR, Espey MG, Namboodiri MAA. 1994. Antibodies to quinolinic acid and the determination of its cellular-distribution within the rat immune-system. Cell Tissue Res 278:461-469.
52. 2A receptors by SCH 58261 results in neuroprotective effects in cerebral ischemia in rats. Neuroreport 9:3955-3959.
53. 2+-permeable alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA)/kainate (Ca-A/K) channels in a subset of hippocampal pyramidal neurons. Exp Neurol 193:384-393.
54. 2a adenosine receptor. Mol Pharmacol 48:970-974.
55. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. London: Academic Press.
56. Pearson VL, Rothwell NJ, Tolmond S. 1999. Excitotoxic brain damage in the rat induced interleukin-1β protein in microglia and astrocytes: correlation with the progression of cell death. Glia 25:311-323.
57. Pelidou SH, Scultzberg M, Iverfeldt K. 2002. Increased sensitivity to NMDA receptor-induced excitotoxicity in cerebellar granule cells from interleukin-1 receptor type-1-deficient mice. J Neuroimmunol 133: 108-115.
58. Pemberton LA, Kerrm SJ, Smythe G, Brew BJ. 1997. Quinolinic acid production by macrophages stimulated with IFN-gamma, TNF-alpha and IFN-alpha. J Interferon Cytokine Res 17:589-595.
59. Perry RT, Collins JS, Wiener H, Acton R, Go RCP. 2001. The role of TNF and its receptor in Alzheimer's disease. Neurobiol Aging 22:873-883.
60. Platenik J, Stopka P, Vejrazka M, Stipek S. 2001. Quinolinic acid-iron(II) complexes: slow autoxidation, but enhanced hydroxyl radical production in the Fenton reaction. Free Radical Res 34:445-459.
61. Pringle AK, Niyadurupola N, Johns P, Anthony DC, Iannotti F. 2001. Interleukin-1β exacerbates hypoxia-induced neuronal damage, but attenuates toxicity produced by simulated ischemia and excitotoxicity in rat organotypic hippocampal slice cultures. Neurosci Lett 305:29-32.
62. Radesater AC, Johansson S, Oberg C, Luthman J. 2003. The vitamin-E analog trolox and the NMDA antagonist MK-801 protect pyramidal neurons in hippocampal slice cultures from IL-1 beta-induced neurodegeneration. Neurotox Res 5:433-441.
63. Rios C, Santamaria A. 1991. Quinolinic acid is a potent lipid peroxidant in rat-brain homogenates. Neurochem Res 16:1139-1143.
64. Royo NC, Wahl F, Stutzmann JM. 1999. Kinetics of polymorphonuclear neutrophil infiltration after a traumatic brain injury in rat. Neuroreport 10:1363-1367.
65. Saito K, Nowak TS Jr, Markey SP, Heyes MP. 1992. Delayed increases in kynurenine pathway metabolism in damaged brain regions following transient cerebral ischemia. J Neurochem 60:180-192.
66. Saito K, Suyama K, Nishida K, Sei Y, Basile AS. 1996. Early increases in TNF-alpha, IL-6 and IL-1 beta levels following transient cerebral ischemia in gerbil brain. Neurosci Lett 206:149-152.
67. Santamaria A, Jimenez-Capdeville ME, Camacho A, Rodriguez-Martinez E, Flores A, Galvan-Arzate S. 2001a. In vivo hydroxyl radical formation after quinolinic acid infusion into rat corpus striatum. Neuroreport 12:2693-2696.
68. Santamaria A, Galvan-Arzate S, Lisy V, Ali SF, Duhart HM, Osorio-Rico L, Rios C, Stastny F. 2001b. Quinolinic acid induces oxidative stress in rat brain synaptosomes. Neuroreport 12:871-874.
69. Schwarcz R, Whetsell WO Jr, Mangano RM. 1983. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science 219:316-318.
70. 2A receptor agonist CGS21680. Drug Dev Res 39:108-114.
71. Shen Y, Li R, Shiosaki K. 1997. 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 272:3550-3553.
72. Shohami E, Gallily R, Mechoulam R, Bass R, Ben-Hur T. 1997. Cytokine production in the brain following closed head injury: dexanabinol (HU-211) is a novel TNF-α inhibitor and an effective neuroprotectant. J Neuroimmunol 72:169-177.
73. Sipe KJ, Srisawasdi D, Dantzer R, Kelley KW, Weyhenmeyer JA. 1996. An endogenous 55kDa TNF receptor mediates cell death in a neural cell line. Brain Res Mol Brain Res 38:222-232.
74. Stipek S, Stastny F, Platenik J, Crkovska J, Zima T. 1997. The effect of quinolinate on rat brain lipid peroxidation is dependent on iron. Neurochem Int 30:233-237.
75. Stone TW. 1993. Neuropharmacology of quinolinic and kynurenic acids. Pharm Rev 45:309-379.
76. Stone TW. 2001. Kynurenines in the CNS: from obscurity to therapeutic importance. Progr Neurobiol 64:185-218.
77. Stone TW. 2002. Purines and neuroprotection. Adv Exp Biol Med 513:249-280.
78. Stone TW, Darlington LG. 2002. Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 1:609-620.
79. Stone TW, Perkins MN. 1981. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol 72:411-412.
80. Strijbos PJLM, Rothwell NJ. 1995. Interleukin-1β attenuates excitatory amino acid induced neurodegeneration in vitro - involvement of nerve growth factor. J Neurosci 15:3468-3474.
81. Stroemer RP, Rothwell NJ. 1998. Exacerbation of ischemic brain damage by localised striatal injection of interleukin-1β in the rat. J Cereb Blood Flow Metab 18:833-839.
82. Tarkowski E, Blennow K, Wallin A, Tarkowski A. 1999. Intracerebral production of TNF-α, a local neuroprotective agent, in Alzheimer's disease and vascular dementia. J Clin Immunol 19:223-230.
83. Thornton P, Pinteaux E, Gibson RM, Allan SM, Rothwell NJ. 2006. Interleukin-1-induced neurotoxicity is mediated by glia and requires caspase activation and free radical release. J Neurochem 98:258-266.
84. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M. 2003. Interleukin-1 beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692-8700.
85. 2A receptor agonist and antagonist. Eur J Pharmacol 287:295-302.
86. Wang CX, Shuaib A. 2002. Involvement of inflammatory cytokines in central nervous system injury. Prog Neurobiol 67:161-172.
87. Whetsell WO Jr, Schwarcz R. 1989. Prolonged exposure to submicromolar concentrations of quinolinic acid causes excitotoxic damage in organotypic cultures of rat corticostriatal system. Neurosci Lett 97:271-275.
88. Wilde GJC, Pringle AK, Sundstrom LE, Mann DA, Iannotti F. 2000. Attenuation and augmentation of ischaemia-related neuronal death by TNF-α in vitro. Eur J Neurosci 12:3863-3870.
89. Yu ACH, Lau LT. 2000. Expression of interleukin-1 alpha, tumor necrosis factor alpha and interleukin-6 genes in astrocytes under ischemic injury. Neurochem Int 36:369-377.
90. Yu ZF, Cheng GJ, Wen XM, Wu GD, Lee WT, Pleasure D. 2002. TNF-α 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 11:199-213.
91. Zhu Y, Saito K, Murakami Y, Asano M, Iwakura Y, Seishima M. 2006. Early increase in mRNA levels of pro-inflammatory cytokines and their interactions in the mouse hippocampus after transient global ischemia. Neurosci Lett 393:122-126.
92. Zou JY, Crews FT. 2005. TNF-α potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NFκB inhibition. Brain Res 1034:11-24.