Epilepsy and inflammation in the brain: Overview and pathophysiology

Epilepsy Currents

Volumn 14, Issue SUPPL.1, 2014, Pages 3-7

  Vezzani, Annamaria ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CYCLOOXYGENASE 2; GLUTAMIC ACID; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROTRANSMITTER; PROTEIN S100B; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL LOSS; COMPLEMENT SYSTEM; CORTICAL DYSPLASIA; ENCEPHALITIS; ENDOTHELIUM CELL; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; EXCITOTOXICITY; EXPERIMENTAL MODEL; EXTRAVASATION; FEBRILE CONVULSION; GENE DELETION; GENE OVEREXPRESSION; HUMAN; IMMUNOREACTIVITY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LYMPHOCYTE; MICROGLIA; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN PHOSPHORYLATION; RASMUSSEN SYNDROME; SEIZURE; SEIZURE THRESHOLD; TEMPORAL LOBE EPILEPSY; UPREGULATION; ETIOLOGY; NERVE CELL EXCITABILITY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84897933220     PISSN: 15357597     EISSN: 15357511     Source Type: Journal    
DOI: 10.5698/1535-7511-14.s2.3     Document Type: Article

References (59)

1. Griffin WS. Inflammation and neurodegenerative diseases. Am J Clin Nutr 2006;83:470S-474S.
2. Allan SM, Tyrrell PJ, Rothwell NJ. Interleukin-1 and neuronal injury. Nat Rev Immunol 2005;5:629-640.
3. Vezzani A, French J, Bartfai T, Baram TZ. The role of inflammation in epilepsy. Nat Rev Neurol 2011;7:31-40.
4. De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, De Luigi A, Garattini S, Vezzani A. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 2000;12:2623-2633.
5. Eriksson C, Van Dam AM, Lucassen PJ, Bol JG, Winblad B, 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 1999;93:915-930.
6. Gorter JA, van Vliet EA, Aronica E, Breit T, Rauwerda H, Lopes Da Silva FH, Wadman WJ. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 2006;26:11083-11110.
7. Plata-Salaman CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Romanovitch AE, Kelly ME, Bureau Y, Anisman H, Mcintyre DC. Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Mol Brain Res 2000;75:248-258.
8. Ravizza T, Vezzani A. Status epilepticus induces time-dependent neuronal and astrocytic expression of interleukin-1 receptor type I in the rat limbic system. Neuroscience 2006;137:301-308.
9. Shinoda S, Skradski SL, Araki T, Schindler CK, Meller R, Lan JQ, Taki W, Simon RP, Henshall DC. 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 2003;17:2065-2076.
10. Turrin NP, Rivest S. Innate immune reaction in response to seizures: Implications for the neuropathology associated with epilepsy. Neurobiol Dis 2004;16:321-334.
11. Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, De Simoni MG. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: Functional evidence for enhancement of electrographic seizures. J Neurosci 1999;19:5054-5065.
12. Jankowsky JL, Patterson PH. The role of cytokines and growth factors in seizures and their sequelae. Prog Neurobiol 2001;63:125-149.
13. Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, Vezzani A. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 2010;16:413-419.
14. Bianchi ME, Manfredi AA. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 2007;220:35-46.
15. Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: Evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008;29:142-160.
16. Fabene PF Mora GN, Martinello M, Rossi B, Merigo F, Ottoboni L, Bach S, Angiari S, Benati D, Chakir A, Zanetti L, Schio F, Osculati A, Marzola P, Nicolato E, Homeister JW, Xia L, Lowe JB, Mcever RP, Osculati F, Sbarbati A, Butcher EC, Constantin G. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 2008;14:1377-1383.
17. Boer K, Jansen F, Nellist M, Redeker S, Van Den Ouweland AM, Spliet WG, Van Nieuwenhuizen O, Troost D, Crino PB, Aronica E. Inflammatory processes in cortical tubers and subependymal giant cell tumors of tuberous sclerosis complex. Epilepsy Res 2008;78:7-21.
18. Iyer A, Zurolo E, Spliet WG, Van Rijen PC, Baayen JC, Gorter JA, Aronica E. Evaluation of the innate and adaptive immunity in type I and type II focal cortical dysplasias. Epilepsia 2010;51:1763-1773.
19. Nguyen MD, Julien JP, Rivest S. Innate immunity: The missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 2002;3:216-227.
20. Oby E, Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006;47:1761-1774.
21. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 2004;24:7829-7836.
22. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, Seiffert E, Heinemann U, Friedman A. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 2007;130:535-547.
23. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, Shapira M, Heinemann U, Friedman A, Kaufer D. Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 2009;29:8927-8935.
24. Friedman A, Kaufer D, Heinemann U. Blood-brain barrier breakdowninducing astrocytic transformation: Novel targets for the prevention of epilepsy. Epilepsy Res 2009;85:142-149.
25. van Vliet EA, Da Costa Araujo S, Redeker S, Van Schaik R, Aronica E, Gorter JA. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007;130:521-534.
26. Zurolo E, Iyer A, Maroso M, Carbonell C, Anink JJ, Ravizza T, Fluiter K, Spliet GWM, Van Rijen PC, Vezzani A, Aronica E. Activation of TLR, RAGE and HMGB1 signaling in malformations of cortical development. Brain 2011;134:1015-1032.
27. Ravizza T, Boer K, Redeker S, Spliet WG, Van Rijen PC, Troost D, Vezzani A, Aronica E. The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol Dis 2006;24:128-143.
28. Kulkarni SK, Dhir A. Cyclooxygenase in epilepsy: From perception to application. Drugs Today (Barc) 2009;45:135-154.
29. Aronica E, Boer K, van Vliet EA, Redeker S, Baayen JC, Spliet WG, Van Rijen PC, Troost D, Da Silva FH, Wadman WJ, Gorter JA. Complement activation in experimental and human temporal lobe epilepsy. Neurobiol Dis 2007;26:497-511.
30. Desjardins P, Sauvageau A, Bouthillier A, Navarro D, Hazell AS, Rose C, Butterworth RF. Induction of astrocytic cyclooxygenase-2 in epileptic patients with hippocampal sclerosis. Neurochem Int 2003;42:299-303.
31. Vezzani A, Granata T. Brain inflammation in epilepsy: Experimental and clinical evidence. Epilepsia 2005;46:1724-1743.
32. Dubé CM, Ravizza T, Hamamura M, Zha Q, Keebaugh A, Fok K, Andres AL, Nalcioglu O, Obenaus A, Vezzani A, Baram TZ. Epileptogenesis provoked by prolonged experimental febrile seizures: Mechanisms and biomarkers. J Neurosci 2010;30:7484-7494.
33. Samland H, Huitron-Resendiz S, Masliah E, Criado J, Henriksen SJ, Campbell IL. Profound increase in sensitivity to glutamatergic- but not cholinergic agonist-induced seizures in transgenic mice with astrocyte production of IL-6. J Neurosci Res 2003;73:176-187.
34. Akassoglou K, Probert L, Kontogeorgos G, Kollias G. Astrocyte-specific but not neuron-specific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J Immunol 1997;158:438-445.
35. Probert L, Akassoglou K, Pasparakis M, Kontogeorgos G, Kollias G. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor alpha. Proc Natl Acad Sci USA 1995;92:11294-11298.
36. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA 1993;90:10061-10065.
37. Riazi K, Galic MA, Pittman QJ. Contributions of peripheral inflammation to seizure susceptibility: Cytokines and brain excitability. Epilepsy Res 2010;89:34-42.
38. Balosso S, Maroso M, Sanchez-Alavez M, Ravizza T, Frasca A, Bartfai T, Vezzani A. A novel non-transcriptional pathway mediates the proconvulsive effects of interleukin-1beta. Brain 2008;131:3256-3265.
39. Xiong ZQ, Qian W, Suzuki K, Mcnamara JO. Formation of complement membrane attack complex in mammalian cerebral cortex evokes seizures and neurodegeneration. J Neurosci 2003;23:955-960.
40. Oliveira MS, Furian AF, Royes LF, Fighera MR, Fiorenza NG, Castelli M, Machado P, Bohrer D, Veiga M, Ferreira J, Cavalheiro EA, Mello CF. Cyclooxygenase- 2/PGE2 pathway facilitates pentylenetetrazol-induced seizures. Epilepsy Res 2008;79:14-21.
41. Vezzani A, Moneta D, Richichi C, Aliprandi M, Burrows SJ, Ravizza T, Perego C, De Simoni MG. Functional role of inflammatory cytokines and anti-inflammatory molecules in seizures and epileptogenesis. Epilepsia 2002;43:S30-35.
42. Kim HJ, Chung JI, Lee SH, Jung YS, Moon CH, Baik EJ. Involvement of endogenous prostaglandin F2alpha on kainic acid-induced seizure activity through FP receptor: The mechanism of proconvulsant effects of COX-2 inhibitors. Brain Res 2008;1193:153-161.
43. Marchi N, Fan Q, Ghosh C, Fazio V, Bertolini F, Betto G, Batra A, Carlton E, Najm I, Granata T, Janigro D. Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol Dis 2009;33:171-181.
44. Spigolon G, Veronesi C, Bonny C, Vercelli A. c-Jun N-terminal kinase signaling pathway in excitotoxic cell death following kainic acidinduced status epilepticus. Eur J Neurosci 2010;31:1261-1272.
45. Vezzani A, Moneta D, Conti M, Richichi C, Ravizza T, De Luigi A, De Simoni MG, Sperk G, Andell-Jonsson S, Lundkvist J, Iverfeldt K, Bartfai T. Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc Natl Acad Sci USA 2000;97:11534-11539.
46. Ravizza T, Lucas SM, Balosso S, Bernardino L, Ku G, Noé F, Malva J, Randle JC, Allan S, Vezzani A. Inactivation of caspase-1 in rodent brain: A novel anticonvulsive strategy. Epilepsia 2006;47:1160-1168.
47. Maroso M, Balosso S, Ravizza T, Iori V, Wright CI, French J, Vezzani A. ICE/Caspase-1 inhibition reduces acute seizures and drug resistant chronic epileptic activity in mice. Neurotherapeutics 2011;8: 304-315.
48. Dubé C, Vezzani A, Behrens M, Bartfai T, Baram TZ. Interleukin-1beta contributes to the generation of experimental febrile seizures. Ann Neurol 2005;57:152-155.
49. Heida JG, Pittman QJ. Causal links between brain cytokines and experimental febrile convulsions in the rat. Epilepsia 2005;46:1906-1913.
50. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M. Interleukin- 1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 2003;23:8692-8700.
51. Viviani B, Gardoni F, Marinovich M. Cytokines and neuronal ion channels in health and disease. Int Rev Neurobiol 2007;82:247-263.
52. Hu S, Sheng WS, Ehrlich LC, Peterson PK, Chao CC. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation 2000;7:153-159.
53. Ye ZC, Sontheimer H. Cytokine modulation of glial glutamate uptake: A possible involvement of nitric oxide. Neuroreport 1996;7:2181-2185.
54. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: Amplification by microglia triggers neurotoxicity. Nat Neurosci 2001;4:702-710.
55. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Wang X, Zielke HR, Kang J, Nedergaard M. An astrocytic basis of epilepsy. Nat Med 2005;11:973-981.
56. Fellin T, Gomez-Gonzalo M, Gobbo S, Carmignoto G, Haydon PG. Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci 2006;26:9312-9322.
57. Wang S, Cheng Q, Malik S, Yang J. Interleukin-1beta inhibits gammaaminobutyric acid type A (GABA(A)) receptor current in cultured hippocampal neurons. J Pharmacol Exp Ther 2000;292:497-504.
58. Zeise ML, Espinoza J, Morales P, Nalli A. Interleukin-1beta does not increase synaptic inhibition in hippocampal CA3 pyramidal and dentate gyrus granule cells of the rat in vitro. Brain Res 1997;768:341-344.
59. Vezzani A, Baram TZ. New roles for interleukin-1beta in the mechanism of epilepsy. Epilepsy Curr 2007;7:45-50.