Innate and adaptive immunity during epileptogenesis and spontaneous seizures: Evidence from experimental models and human temporal lobe epilepsy

Neurobiology of Disease

Volumn 29, Issue 1, 2008, Pages 142-160

  Ravizza, Teresa ^a   Gagliardi, Barbara ^a   Noé, Francesco ^a   Boer, Karin ^b   Aronica, Eleonora ^b   Vezzani, Annamaria ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Astrocytes; Cytokines; Epileptogenesis; Hippocampal sclerosis; Interleukin 1; Microglia

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; B LYMPHOCYTE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; EPILEPTIC STATE; EPILEPTOGENESIS; FEMALE; FOREBRAIN; GRANULOCYTE; HIPPOCAMPAL SCLEROSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; NATURAL KILLER CELL; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE; T LYMPHOCYTE; TEMPORAL LOBE EPILEPSY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL COUNT; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; IMMUNITY; INTERLEUKIN-1BETA; MALE; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-1; SEIZURES; STILBAMIDINES; TIME FACTORS;

EID: 36549071601     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.08.012     Document Type: Article

References (72)

1. Abraham C.S., Deli M.A., Joo F., Megyeri P., and Torpier G. Intracarotid tumor necrosis factor-alpha administration increases the blood-brain barrier permeability in cerebral cortex of the newborn pig: quantitative aspects of double-labelling studies and confocal laser scanning analysis. Neurosci. Lett. 208 (1996) 85-88
2. Allan S.M., Tyrrell P.J., and Rothwell N.J. Interleukin-1 and neuronal injury. Nat. Rev., Immunol. 5 (2005) 629-640
3. Anthony D.C., Bolton S.J., Fearn S., and Perry V.H. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 120 (1997) 435-444
4. Arida R.M., Scorza F.A., Peres C.A., and Cavalheiro E.A. The course of untreated seizures in the pilocarpine model of epilepsy. Epilepsy Res. 34 (1999) 99-107
5. Aronica E., Gorter J.A., Jansen G.H., van Veelen C.W., van Rijen P.C., Leenstra S., Ramkema M., Scheffer G.L., Scheper R.J., and Troost D. Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumors. Neuroscience 118 (2003) 417-429
6. Aronica E., Boer K., van Vliet E.A., Redeker S., Baayen J.C., Spliet W.G., van Rijen P.C., Troost D., da Silva F.H., Wadman W.J., and Gorter J. Complement activation in experimental and human temporal lobe epilepsy. Neurobiol. Dis. 26 (2006) 497-511
7. Aronica E., Gorter J.A., Redeker S., van Vliet E.A., Ramkema M., Scheffer G.L., Scheper R.J., van der Valk P., Leenstra S., Baayen J.C., Spliet W.G., and Troost D. Localization of breast cancer resistance protein (BCRP) in microvessel endothelium of human control and epileptic brain. Epilepsia 46 (2005) 849-857
8. Balosso S., Ravizza T., Perego C., Peschon J., Campbell I.L., De Simoni M.G., and Vezzani A. Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors. Ann. Neurol. 57 (2005) 804-812
9. Beattie E.C., Stellwagen D., Morishita W., Bresnahan J.C., Ha B.K., Von Zastrow M., Beattie M.S., and Malenka R.C. Control of synaptic strength by glial TNFalpha. Science 295 (2002) 2282-2285
10. Bernardino L., Xapelli S., Silva A.P., Jakobsen B., Poulsen F.R., Oliveira C.R., Vezzani A., Malva J.O., and Zimmer J. Modulator effects of interleukin 1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 25 (2005) 6734-6744
11. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., Vescovi A., Bagetta G., Kollias G., Meldolesi J., and Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4 (2001) 702-710
12. Borregaard N., and Cowland J.B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89 (1997) 3503-3521
13. Cassatella M.A. Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73 (1999) 369-509
14. Crespel A., Coubes P., Rousset M.C., Brana C., Rougier A., Rondouin G., Bockaert J., Baldy-Moulinier M., and Lerner-Natoli M. Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res. 952 (2002) 159-169
15. Darlington C.L. Astrocytes as targets for neuroprotective drugs. Curr. Opin. Investig. Drugs 6 (2005) 700-703
16. De Simoni M.G., Perego C., Ravizza T., Moneta D., Conti M., Marchesi F., De Luigi A., Garattini S., and Vezzani A. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur. J. Neurosci. 12 (2000) 2623-2633
17. de Vries H.E., Blom-Roosemalen M.C., van Oosten M., de Boer A.G., van Berkel T.J., Breimer D.D., and Kuiper J. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J. Neuroimmunol. 64 (1996) 37-43
18. Del Maschio A., Zanetti A., Corada M., Rival Y., Ruco L., Lampugnani M.G., and Dejana E. Polymorphonuclear leukocyte adhesion triggers the disorganization of endothelial cell-to-cell adherens junctions. J. Cell Biol. 135 (1996) 451-497
19. Dinarello C.A. Biologic basis for interleukin-1 in disease. Blood 87 (1996) 2095-2147
20. Dinkel K., MacPherson A., and Sapolsky R.M. Novel glucocorticoid effects on acute inflammation in the CNS. J. Neurochem. 84 (2003) 705-716
21. Dubé C., Vezzani A., Behrens M., Bartfai T., and Baram T.Z. Interleukin-1beta contributes to the generation of experimental febrile seizures. Ann. Neurol. 57 (2005) 152-155
22. Dudek F.E., Hellier J.L., Williams P.A., Ferraro D.J., and Staley K.J. The course of cellular alterations associated with the development of spontaneous seizures after status epilepticus. Prog. Brain Res. 135 (2002) 53-65
23. Eriksson C., Van Dam A.M., Lucassen P.J., Bol J.G., Winblad B., and Schultzberg M. Immunohistochemical localization of interleukin-1beta, interleukin-1 receptor antagonist and interleukin-1beta converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 93 (1999) 9915-9930
24. Fellin T., Gomez-Gonzalo M., Gobbo S., Carmignoto G., and Haydon P.G. Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J. Neurosci. 26 (2006) 9312-9322
25. Ferrari C.C., Depino A.M., Prada F., Muraro N., Campbell S., Podhajcer O., Perry V.H., Anthony D.C., and Pitossi F.J. Reversible demyelination, blood-brain barrier breakdown, and pronounced neutrophil recruitment induced by chronic IL-1 expression in the brain. Am. J. Pathol. 165 (2004) 1827-3187
26. Fujikawa D.G. The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res. 725 (1996) 11-22
27. Fujiwara N., and Kobayashi K. Macrophages in inflammation. Curr. Drug Targets Inflamm. Allergy 4 (2005) 281-286
28. Giometto B., Bozza F., Faresin F., Alessio L., Mingrino S., and Tavolato B. Immune infiltrates and cytokines in gliomas. Acta Neurochir (Wien). 138 (1996) 50-56
29. Gorter J.A., van Vliet E.A., Aronica E., Breit T., Rauwerda H., Lopes da Silva F.H., and Wadman W.J. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J. Neurosci. 26 (2006) 11083-110110
30. Hampton M.B., Kettle A.J., and Winterbourn C.C. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92 (1998) 3007-3017
31. Heida J.G., and Pittman Q.J. Causal links between brain cytokines and experimental febrile convulsions in the rat. Epilepsia 46 (2005) 1906-1913
32. Hendriks J.J., Teunissen C.E., de Vries H.E., and Dijkstra C.D. Macrophages and neurodegeneration. Brain Res. Brain Res. Rev. 48 (2005) 185-195
33. Hu S., Sheng W.S., Ehrlich L.C., Peterson P.K., and Chao C.C. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation 7 (2000) 153-159
34. Jankowsky J.L., and Patterson P.H. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 63 (2001) 125-149
35. Kadhim H., Tabarki B., De Prez C., and Sebire G. Cytokine immunoreactivity in cortical and subcortical neurons in periventricular leukomalacia: are cytokines implicated in neuronal dysfunction in cerebral palsy?. Acta Neuropathol. (Berl). 105 (2003) 209-216
36. Maldonado M., Baybis M., Newman D., Kolson D.L., Chen W., McKhann II G., Gutmann D.H., and Crino P.B. Expression of ICAM-1, TNF-alpha, NF kappa B, and MAP kinase in tubers of the tuberous sclerosis complex. Neurobiol. Dis. 14 (2003) 279-290
37. Marchi N., Guiso G., Caccia S., Rizzi M., Gagliardi B., Noe F., Ravizza T., Bassanini S., Chimenti S., Battaglia G., and Vezzani A. Determinants of drug brain uptake in a rat model of seizure-associated malformations of cortical development. Neurobiol. Dis. 24 (2006) 429-442
38. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., and Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34 (1993) 985-995
39. Naldini A., and Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm. Allergy 4 (2005) 3-8
40. Nguyen M.D., Julien J.P., and Rivest S. Innate immunity: the missing link in neuroprotection and neurodegeneration?. Nat. Rev. Neurosci. 3 (2002) 216-227
41. Oby E., and Janigro D. The blood-brain barrier and epilepsy. Epilepsia 47 (2006) 1761-1774
42. Pardo C.A., Vining E.P., Guo L., Skolasky R.L., Carson B.S., and Freeman J.M. The pathology of Rasmussen syndrome: stages of cortical involvement and neuropathological studies in 45 hemispherectomies. Epilepsia 45 (2004) 516-526
43. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, New York
44. Piani D., Frei K., Do K.Q., Cuenod M., and Fontana A. Murine brain macrophages induced NMDA receptor mediated neurotoxicity in vitro by secreting glutamate. Neurosci. Lett. 133 (1991) 159-162
45. Pitkanen A., and Sutula T.P. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 1 (2002) 173-181
46. Plata-Salaman C.R., Ilyin S.E., Turrin N.P., Gayle D., Flynn M.C., Romanovitch A.E., Kelly M.E., Bureau Y., Anisman H., and McIntyre D.C. Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res. Mol Brain Res. 75 (2000) 248-258
47. Poirier J.L., Capek R., and De Koninck Y. Differential progression of Dark Neuron and Fluoro-Jade labelling in the rat hippocampus following pilocarpine-induced status epilepticus. Neuroscience 97 (2000) 59-68
48. Ravizza T., Boer K., Redeker S., Spliet W.G., van Rijen P.C., Troost D., Vezzani A., and Aronica E. The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol. Dis. 24 (2006) 128-143
49. Ravizza T., Lucas S.M., Balosso S., Bernardino L., Ku G., Noe F., Malva J., Randle J.C., Allan S., and Vezzani A. Inactivation of caspase-1 in rodent brain: a novel anticonvulsive strategy. Epilepsia 47 (2006) 1160-1168
50. Ravizza T., and Vezzani A. Status epilepticus induces time-dependent neuronal and astrocytic expression of interleukin-1 receptor type I in the rat limbic system. Neuroscience 137 (2006) 301-308
51. Roggendorf W., Strupp S., and Paulus W. Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol. (Berl). 92 (1996) 288-293
52. Schmitz C., and Hof P.R. Design-based stereology in neuroscience. Neuroscience 130 (2005) 813-831
53. Schmued L.C., Albertson C., and Slikker Jr. W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751 (1997) 37-46
54. Schwarcz R., and Pellicciari R. Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J. Pharmacol Exp Ther. 303 (2002) 1-10
55. Seiffert E., Dreier J.P., Ivens S., Bechmann I., Tomkins O., Heinemann U., and Friedman A. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J. Neurosci. 24 (2004) 7829-7836
56. Serafini B., Rosicarelli B., Magliozzi R., Stigliano E., Capello E., Mancardi G.L., and Aloisi F. Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells. J. Neuropathol Exp. Neurol. 65 (2006) 124-141
57. Sheng J.G., Boop F.A., Mrak R.E., and Griffin W.S. Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1 alpha immunoreactivity. J. Neurochem. 63 (1994) 1872-1879
58. Shinoda S., Skradski S.L., Araki T., Schindler C.K., Meller R., Lan J.Q., Taki W., Simon R.P., and Henshall D.C. Formation of a tumour necrosis factor receptor 1 molecular scaffolding complex and activation of apoptosis signal-regulating kinase 1 during seizure-induced neuronal death. Eur. J. Neurosci. 17 (2003) 2065-2076
59. Stellwagen D., Beattie E.C., Seo J.Y., and Malenka R.C. Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci. 25 (2005) 3219-3228
60. Tian G.F., Azmi H., Takano T., Xu Q., Peng W., Lin J., Oberheim N., Lou N., Wang X., Zielke H.R., Kang J., and Nedergaard M. An astrocytic basis of epilepsy. Nat. Med. 11 (2005) 973-981
61. Turrin N.P., and Rivest S. Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol. Dis. 16 (2004) 321-334
62. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., and Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 9 (1983) 315-335
63. van Vliet E.A., da Costa Araujo S., Redeker S., van Schaik R., Aronica E., and Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain (2006)
64. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., and De Simoni M.G. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J. Neurosci. 19 (1999) 5054-5065
65. Vezzani A., and Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46 (2005) 1724-1743
66. Vezzani A., and Baram T.Z. New roles for interleukin-1β in the mechanisms of epilepsy. Epilepsy Curr. 7 (2007) 45-50
67. Vezzani A., Moneta D., Conti M., Richichi C., Ravizza T., De Luigi A., De Simoni M.G., Sperk G., Andell-Jonsson S., Lundkvist J., Iverfeldt K., and Bartfai T. Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 11534-11539
68. Vezzani A., Moneta D., Richichi C., Aliprandi M., Burrows S.J., Ravizza T., Perego C., and De Simoni M.G. Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 43 Suppl 5 (2002) 30-35
69. Viviani B., Bartesaghi S., Gardoni F., Vezzani A., Behrens M.M., Bartfai T., Binaglia M., Corsini E., Di Luca M., Galli C.L., and Marinovich M. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J. Neurosci. 23 (2003) 8692-8700
70. Wieser H.G. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45 (2004) 695-714
71. Ye Z.C., and Sontheimer H. Cytokine modulation of glial glutamate uptake: a possible involvement of nitric oxide. Neuroreport 7 (1996) 2181-2185
72. Zucker D.K., Wooten G.F., and Lothman E.W. Blood-brain barrier changes with kainic acid-induced limbic seizures. Exp. Neurol. 79 (1983) 422-433