Status epilepticus induces time-dependent neuronal and astrocytic expression of interleukin-1 receptor type I in the rat limbic system

Interleukin-1beta is rapidly synthesized by glia after the induction of seizures. Recent evidence shows that endogenous IL-1beta has proconvulsant actions mediated by interleukin-1 receptor type I. This receptor also mediates interleukin-1beta effects on neuronal susceptibility to neurotoxic insults. In this study, we investigated the basal and seizure-induced expression of interleukin-1 receptor type I in rat forebrain to identify the cells targeted by interleukin-1beta during epileptic activity. Self-sustained limbic status epilepticus was induced in rats by electrical stimulation of the ventral hippocampus. Interleukin-1 receptor type I immunoreactivity was barely detectable in neurons in control brain tissue. During status epilepticus, interleukin-1 receptor type I was induced in the hippocampal neurons firstly, and several hours later in astrocytes localized in limbic and extralimbic areas. Neuronal interleukin-1 receptor type I expression in the hippocampus outlasted the duration of spontaneous electroencephalographic seizure and was not observed in degenerating neurons. Astrocytic expression occurred transiently, between six and 18 h after the induction of status epilepticus and was invariably found in regions of neuronal damage. These time-dependent, cell- and region-specific changes in interleukin-1 receptor type I expression during status epilepticus suggest that interleukin-1 receptor type I in neurons mediates interleukin-1beta-induced fast changes in hippocampal excitability while interleukin-1 receptor type I receptors in astrocytes may mediate interleukin-1beta effects on neuronal survival in hostile conditions.

[1]  C. Plata-salamán,et al.  Interleukin-1β System (Ligand, Receptor Type I, Receptor Accessory Protein and Receptor Antagonist), TNF-α, TGF-β1 and Neuropeptide Y mRNAs in Specific Brain Regions During Bacterial LPS-Induced Anorexia , 1998, Brain Research Bulletin.

[2]  N. Rothwell,et al.  Cytokines and acute neurodegeneration , 2001, Nature Reviews Neuroscience.

[3]  F. Poulsen,et al.  Modulator Effects of Interleukin-1β and Tumor Necrosis Factor-α on AMPA-Induced Excitotoxicity in Mouse Organotypic Hippocampal Slice Cultures , 2005, The Journal of Neuroscience.

[4]  A. Vezzani,et al.  Functional Role of Inflammatory Cytokines and Antiinflammatory Molecules in Seizures and Epileptogenesis , 2002, Epilepsia.

[5]  B. C. Wise,et al.  Arachidonic acid lipoxygenation may mediate interleukin‐1 stimulation of nerve growth factor secretion in astroglial cultures , 1993, Journal of neuroscience research.

[6]  M. Gayle,et al.  Interleukin 1 signaling occurs exclusively via the type I receptor. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Rothwell,et al.  Interleukin-1 receptor antagonist inhibits neuronal damage caused by fluid percussion injury in the rat , 1995, Brain Research.

[8]  G. Sperk,et al.  Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy , 1995, Neuroscience.

[9]  A. Coogan,et al.  The p38 mitogen-activated protein kinase inhibitor SB203580 antagonizes the inhibitory effects of interleukin-1β on long-term potentiation in the rat dentate gyrus in vitro , 1999, Neuroscience.

[10]  W. Friedman Cytokines Regulate Expression of the Type 1 Interleukin-1 Receptor in Rat Hippocampal Neurons and Glia , 2001, Experimental Neurology.

[11]  C L Galli,et al.  Interleukin-1β Enhances NMDA Receptor-Mediated Intracellular Calcium Increase through Activation of the Src Family of Kinases , 2003, The Journal of Neuroscience.

[12]  T. Hirabayashi,et al.  Reduced postischemic apoptosis in the hippocampus of mice deficient in interleukin‐1 , 2002, The Journal of comparative neurology.

[13]  J. Krebs,et al.  Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  H. Togari,et al.  Interleukin-1β induces the expression of lipocortin 1 mRNA in cultured rat cortical astrocytes , 2001, Neuroscience Research.

[15]  Yasuyoshi Watanabe,et al.  Pyrogenic cytokines injected into the rat cerebral ventricle induce cyclooxygenase‐2 in brain endothelial cells and also upregulate their receptors , 2001, The European journal of neuroscience.

[16]  H. Scharfman,et al.  Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. , 2004, Advances in experimental medicine and biology.

[17]  C. Garlanda,et al.  Dynamic induction of the long pentraxin PTX3 in the CNS after limbic seizures: evidence for a protective role in seizure-induced neurodegeneration , 2001, Neuroscience.

[18]  C. Dinarello Interleukin-1 and interleukin-1 antagonism. , 1991, Blood.

[19]  M. Wong,et al.  Localization of interleukin 1 type I receptor mRNA in rat brain. , 1994 .

[20]  William Slikker,et al.  Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration , 1997, Brain Research.

[21]  N. Rothwell,et al.  Cytokines and the nervous system II: actions and mechanisms of action , 1995, Trends in Neurosciences.

[22]  M. Satoh,et al.  Localization of type I interleukin-1 receptor mRNA in the rat brain. , 1994, Brain research. Molecular brain research.

[23]  M. Curtis,et al.  Calcium-binding protein immunoreactivity in the piriform cortex of the guinea-pig: Selective staining of subsets of non-gabaergic neurons by calretinin , 1998, Neuroscience.

[24]  C. Plata-salamán,et al.  Kindling modulates the IL-1β system, TNF-α, TGF-β1, and neuropeptide mRNAs in specific brain regions , 2000 .

[25]  C. Gall,et al.  Interleukin-1 beta increases basic fibroblast growth factor mRNA expression in adult rat brain and organotypic hippocampal cultures. , 1994, Brain research. Molecular brain research.

[26]  E. Furshpan,et al.  Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[28]  D. Srinivasan,et al.  Cell Type-Specific Interleukin-1β Signaling in the CNS , 2004, The Journal of Neuroscience.

[29]  S. Garattini,et al.  Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus , 2000, The European journal of neuroscience.

[30]  N. Rothwell,et al.  Interleukin-1 beta attenuates excitatory amino acid-induced neurodegeneration in vitro: involvement of nerve growth factor , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. A. Colivicchi,et al.  Interleukin-1β activates forebrain glial cells and increases nitric oxide production and cortical glutamate and GABA release in vivo: implications for Alzheimer's disease , 1999, Neuroscience.

[32]  D. Giulian,et al.  Brain glia release factors with opposing actions upon neuronal survival , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  M. Satoh,et al.  Effects of kainic acid on messenger RNA levels of IL-1β, IL-6, TNFα and LIF in the rat brain , 1991 .

[34]  Edward H Bertram,et al.  Self-sustaining limbic status epilepticus induced by ‘continuous’ hippocampal stimulation: electrographic and behavioral characteristics , 1989, Epilepsy Research.

[35]  N. Rothwell,et al.  Neuroprotective Effects of Human Recombinant Interleukin-1 Receptor Antagonist in Focal Cerebral Ischaemia in the Rat , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  M. Minami,et al.  Type 2 interleukin-1 receptor mRNA is induced by kainic acid in the rat brain. , 1997, Brain research. Molecular brain research.

[37]  M. Lynch,et al.  Lipopolysaccharide‐induced increase in signalling in hippocampus is abrogated by IL‐10 – a role for IL‐1β? , 2004, Journal of neurochemistry.

[38]  P. Patterson,et al.  The role of cytokines and growth factors in seizures and their sequelae , 2001, Progress in Neurobiology.

[39]  A. Vezzani,et al.  Interleukin-1β Immunoreactivity and Microglia Are Enhanced in the Rat Hippocampus by Focal Kainate Application: Functional Evidence for Enhancement of Electrographic Seizures , 1999, The Journal of Neuroscience.

[40]  G. Sperk,et al.  Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Klaus Resch,et al.  The Interleukin-1 Receptor Accessory Protein (IL-1RAcP) Is Essential for IL-1-induced Activation of Interleukin-1 Receptor-associated Kinase (IRAK) and Stress-activated Protein Kinases (SAP Kinases)* , 1997, The Journal of Biological Chemistry.

[42]  J. Velíšková,et al.  Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development , 2003, Neurobiology of Disease.

[43]  H. Sontheimer,et al.  Cytokine modulation of glial glutamate uptake: a possble involvement of nitric oxide , 1996, Neuroreport.

[44]  S. Allan,et al.  Interleukin‐1 in the Brain , 2003 .

[45]  Shuxian Hu,et al.  Cytokine Effects on Glutamate Uptake by Human Astrocytes , 2000, Neuroimmunomodulation.

[46]  C. Finch,et al.  Glial Fibrillary Acidic Protein Transcription Responses to Transforming Growth Factor‐β1 and Interleukin‐1β Are Mediated by a Nuclear Factor‐1‐Like Site in the Near‐Upstream Promoter , 1999, Journal of neurochemistry.