Successful inhibition of excitotoxic neuronal damage and microglial activation after delayed application of interleukin-1 receptor antagonist

Journal of Neuroscience Research

Volumn 86, Issue 15, 2008, Pages 3314-3321

  Vogt, Cornelia ^a   Hailer, Nils P ^b   Ghadban, Chalid ^a   Korf, Horst Werner ^a   Dehghani, Faramarz ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Excitatory amino acid; N methyl D aspartate; Neuroprotection; Propidium iodide; Rat

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; LECTIN; N METHYL DEXTRO ASPARTIC ACID; NEURON SPECIFIC NUCLEAR PROTEIN; PROPIDIUM IODIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN INJURY; BRAIN SLICE; CELL ACTIVATION; CELL COUNT; CELL DAMAGE; CELL DEATH; CELL LABELING; CELL POPULATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EXCITOTOXICITY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITION KINETICS; MICROGLIA; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; TIME; TISSUE CULTURE;

ANIMALS; ASTROCYTES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; MICROGLIA; MICROSCOPY, CONFOCAL; N-METHYLASPARTATE; NERVE DEGENERATION; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTOXINS; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, INTERLEUKIN-1; TIME;

EID: 57049150620     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21792     Document Type: Article

References (37)

1. Bartholdi D, Schwab ME. 1997. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci 9:1422-1438.
2. Black RA, Kronheim SR, Merriam JE, March CJ, Hopp TP. 1989. A pre-aspartate-specific protease from human leukocytes that cleaves prointerleukin-1 beta. J Biol Chem 264:5323-5326.
3. Bruce AJ, Sakhi S, Schreiber SS, Baudry M. 1995. Development of kainic acid and N-methyl-D-aspartic acid toxicity in organotypic hippocampal cultures. Exp Neurol 132:209-219.
4. Burns K, Martinon F, Tschopp J. 2003. New insights into the mechanism of IL-1beta maturation. Curr Opin Immunol 15:26-30.
5. Coogan A, O'Connor JJ. 1997. Inhibition of NMDA receptor-mediated synaptic transmission in the rat dentate gyrus in vitro by IL-1 beta. Neuroreport 8:2107-2110.
6. Craft JM, Watterson DM, Hirsch E, Van Eldik LJ. 2005. Interleukin 1 receptor antagonist knockout mice show enhanced microglial activation and neuronal damage induced by intracerebroventricular infusion of human beta-amyloid. J Neuroinflamm 2:15.
7. Dehghani F, Hischebeth GT, Wirjatijasa F, Kohl A, Korf HW, Hailer NP. 2003. The immunosuppressant mycophenolate mofetil attenuates neuronal damage after excitotoxic injury in hippocampal slice cultures. Eur J Neurosci 18:1061-1072.
8. Dehghani F, Conrad A, Kohl A, Korf HW, Hailer NP. 2004. Clodronate inhibits the secretion of proinflammatory cytokines and NO by isolated microglial cells and reduces the number of proliferating glial cells in excitotoxically injured organotypic hippocampal slice cultures. Exp Neurol 189:241-251.
9. Dusart I, Schwab ME. 1994. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6:712-724.
10. Emsley HC, Smith CJ, Georgiou RF, Vail A, Hopkins SJ, Rothwell NJ, Tyrrell PJ. 2005. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J Neurol Neurosurg Psychiatry 76:1366-1372.
11. Eriksson C, Nobel S, Winblad B, Schultzberg M. 2000. Expression of interleukin 1 alpha and beta, and interleukin 1 receptor antagonist mRNA in the rat central nervous system after peripheral administration of lipopolysaccharides. Cytokine 12:423-431.
12. Gahwiler BH. 1988. Organotypic cultures of neural tissue. Trends Neurosci 11:484-489.
13. Gelderd JB, Hall NR, O'Grady MP, Oliver J, Ferrer C, Anderson JA. 1996. The effects of interleukin-1 receptor antagonist protein (IRAP) infusion following spinal cord transection in rats. Mol Chem Neuropathol 27:167-183.
14. Giulian D, Li J, Leara B, Keenen C. 1994. Phagocytic microglia release cytokines and cytotoxins that regulate the survival of astrocytes and neurons in culture. Neurochem Int 25:227-233.
15. Gueorguieva I, Clark SR, McMahon CJ, Scarth S, Rothwell NJ, Tyrell PJ, Hopkins SJ, Rowland M. 2007. Pharmacokinetic modelling of interleukin-1 receptor antagonist in plasma and cerebrospinal fluid of patients following subarachnoid haemorrhage. Br J Clin Pharmacol (in press).
16. Hailer NP, Järhult JD, Nitsch R. 1996. Resting microglial cells in vitro: analysis of morphology and adhesion molecule expression in organotypic hippocampal slice cultures. Glia 18:319-331.
17. Hailer NP, Wirjatijasa F, Roser N, Hischebeth GT, Korf HW, Dehghani F. 2001. Astrocytic factors protect neuronal integrity and reduce microglial activation in an in vitro model of N-methyl-D-aspartate-induced excitotoxic injury in organotypic hippocampal slice cultures. Eur J Neurosci 14:315-326.
18. Hailer NP, Vogt C, Korf HW, Dehghani F. 2005. Interleukin-1beta 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.
19. Hazuda D, Webb RL, Simon P, Young P. 1989. Puri.cation and characterization of human recombinant precursor interleukin 1 beta. J Biol Chem 264:1689-1693.
20. Janes KA, Gaudet S, Albeck JG, Nielsen UB, Lauffenburger DA, Sorger PK. 2006. The response of human epithelial cells to TNF involves an inducible autocrine cascade. Cell 124:1225-1239.
21. Kohl A, Dehghani F, Korf HW, Hailer NP. 2003. The bisphosphonate clodronate depletes microglial cells in excitotoxically injured organotypic hippocampal slice cultures. Exp Neurol 181:1-11.
22. Kreutz S, Koch M, Ghadban C, Korf HW, Dehghani F. 2007. Cannabinoids and neuronal damage: differential effects of THC, AEA and 2-AG on activated microglial cells and degenerating neurons in excitotoxically lesioned rat organotypic hippocampal slice cultures. Exp Neurol 203:246-257.
23. Laake JH, Haug FM, Wieloch T, Ottersen OP. 1999. A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Brain Res Protoc 4:173-184.
24. Loscher CE, Mills KH, Lynch MA. 2003. Interleukin-1 receptor antagonist exerts agonist activity in the hippocampus independent of the interleukin-1 type I receptor. J Neuroimmunol 137:117-124.
25. Masada T, Hua Y, Xi G, Yang GY, Hoff JT, Keep RF. 2001. Attenuation of intracerebral hemorrhage and thrombin-induced brain edema by overexpression of interleukin-1 receptor antagonist. J Neurosurg 95:680-686.
26. Mulcahy NJ, Ross J, Rothwell NJ, Loddick SA. 2003. Delayed administration of interleukin-1 receptor antagonist protects against transient cerebral ischaemia in the rat. Br J Pharmacol 140:471-476.
27. Nesic O, Xu GY, McAdoo D, High KW, Hulsebosch C, Perez-Pol R. 2001a. IL-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J Neurotrauma 18:947-956.
28. Nesic O, Xu GY, McAdoo D, High KW, Hulsebosch C, Perez-Pol R. 2001b. IL-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J Neurotrauma 18:947-956.
29. Newell DW, Hsu SS, Papermaster V, Malouf AT. 1993. Colchicine is selectively neurotoxic to dentate granule cells in organotypic cultures of rat hippocampus. Neurotoxicology 14:375-380.
30. Noraberg J, Kristensen BW, Zimmer J. 1999. Markers for neuronal degeneration in organotypic slice cultures. Brain Res Brain Res Protoc 3:278-290.
31. Panegyres PK, Hughes J. 1998. The neuroprotective effects of the recombinant interleukin-1 receptor antagonist rhIL-1ra after excitotoxic stimulation with kainic acid and its relationship to the amyloid precursor protein gene. J Neurol Sci 154:123-132.
32. Pinteaux E, Rothwell NJ, Boutin H. 2006. Neuroprotective actions of endogenous interleukin-1 receptor antagonist (IL-1ra) are mediated by glia. Glia 53:551-556.
33. Pozzo Miller LD, Mahanty NK, Connor JA, Landis DM. 1994. Spontaneous pyramidal cell death in organotypic slice cultures from rat hippocampus is prevented by glutamate receptor antagonists. Neuroscience 63:471-487.
34. Stoppini L, Buchs PA, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
35. Strasser U, Fischer G. 1995. Quantitative measurement of neuronal degeneration in organotypic hippocampal cultures after combined oxygen/ glucose deprivation. J Neurosci Methods 57:177-186.
36. 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-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692-8700.
37. Viviani B, Gardoni F, Bartesaghi S, Corsini E, Facchi A, Galli CL, Di Luca M, Marinovich M. 2006. Interleukin-1 beta released by gp120 drives neural death through tyrosine phosphorylation and trafficking of NMDA receptors. J Biol Chem 281:30212-30222.