Protein expression profiling of inflammatory mediators in human temporal lobe epilepsy reveals co-activation of multiple chemokines and cytokines

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Kan, Anne A ^a   de Jager, Wilco ^b   de Wit, Marina ^a   Heijnen, Cobi ^b   van Zuiden, Mirjam ^b   Ferrier, Cyrill ^b   van Rijen, Peter ^b   Gosselaar, Peter ^b   Hessel, Ellen ^a   van Nieuwenhuizen, Onno ^b   de Graan, Pierre N E ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Immune system; Network analysis; Temporal lobe epilepsy

Indexed keywords

ALPHA INTERFERON; CHEMOKINE; CYTOKINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; INTERLEUKIN 22; INTERLEUKIN 25; INTERLEUKIN 27; INTERLEUKIN 5; INTERLEUKIN 7; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SCATTER FACTOR; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ADULT; AGED; ARTICLE; ASTROCYTE; AUTOPSY; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FOLLOW UP; HIPPOCAMPAL SCLEROSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MESIAL TEMPORAL LOBE EPILEPSY; MICROGLIA; MIDDLE TEMPORAL GYRUS; NEOCORTEX; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84865522903     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-207     Document Type: Article

References (108)

1. Leonardi M, Ustun TB. The global burden of epilepsy. Epilepsia 2002, 43(Suppl 6):21-25.
2. Engel J. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 2001, 42(6):796-803. 10.1046/j.1528-1157.2001.10401.x, 11422340.
3. Kwan P, Brodie MJ. Clinical trials of antiepileptic medications in newly diagnosed patients with epilepsy. Neurology 2003, 60:S2-S12.
4. Cascino GD. When drugs and surgery don't work. Epilepsia 2008, 49(Suppl 9):79-84.
5. Proper EA, Oestreicher AB, Jansen GH, Veelen CW, van Rijen PC, Gispen WH, de Graan PN. Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 2000, 123(Pt 1):19-30.
6. Houser CR. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv Neurol 1999, 79:743-761.
7. Rakhade SN, Jensen FE. Epileptogenesis in the immature brain: emerging mechanisms. Nat Rev Neurol 2009, 5:380-391. 10.1038/nrneurol.2009.80, 2822660, 19578345.
8. Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 2005, 46:1724-1743. 10.1111/j.1528-1167.2005.00298.x, 16302852.
9. Vezzani A, French J, Bartfai T, Baram TZ. The role of inflammation in epilepsy. Nat Rev Neurol 2011, 7:31-40. 10.1038/nrneurol.2010.178, 3378051, 21135885.
10. van Gassen KL, de Wit M, Koerkamp MJ, Rensen MG, van Rijen PC, Holstege FC, Lindhout D, de Graan PN. Possible role of the innate immunity in temporal lobe epilepsy. Epilepsia 2008, 49:1055-1065. 10.1111/j.1528-1167.2007.01470.x, 18076643.
11. Lee TS, Mane S, Eid T, Zhao H, Lin A, Guan Z, Kim JH, Schweitzer J, King-Stevens D, Weber P, Spencer SS, Spencer DD, de Lanerolle NC. Gene expression in temporal lobe epilepsy is consistent with increased release of glutamate by astrocytes. Mol Med 2007, 13:1-13. 1869627, 17515952.
12. Ravizza T, Gagliardi B, Noe 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. 10.1016/j.nbd.2007.08.012, 17931873.
13. Liimatainen S, Fallah M, Kharazmi E, Peltola M, Peltola J. Interleukin-6 levels are increased in temporal lobe epilepsy but not in extra-temporal lobe epilepsy. J Neurol 2009, 256:796-802. 10.1007/s00415-009-5021-x, 19252806.
14. Yamamoto A, Schindler CK, Murphy BM, Bellver-Estelles C, So NK, Taki W, Meller R, Simon RP, Henshall DC. Evidence of tumor necrosis factor receptor 1 signaling in human temporal lobe epilepsy. Exp Neurol 2006, 202:410-420. 10.1016/j.expneurol.2006.07.003, 16919273.
15. Li G, Bauer S, Nowak M, Norwood B, Tackenberg B, Rosenow F, Knake S, Oertel WH, Hamer HM. Cytokines and epilepsy. Seizure 2011, 20:249-256. 10.1016/j.seizure.2010.12.005, 21216630.
16. Friedman A, Dingledine R. Molecular cascades that mediate the influence of inflammation on epilepsy. Epilepsia 2011, 52(Suppl 3):33-39.
17. Murdoch C, Finn A. Chemokine receptors and their role in inflammation and infectious diseases. Blood 2000, 95:3032-3043.
18. Fabene PF, Bramanti P, Constantin G. The emerging role for chemokines in epilepsy. J Neuroimmunol 2010, 224:22-27. 10.1016/j.jneuroim.2010.05.016, 20542576.
19. 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. 10.1046/j.1460-9568.2000.00140.x, 10947836.
20. Fabene PF, Navarro MG, 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. 10.1038/nm.1878, 2710311, 19029985.
21. Zeng LH, Rensing NR, Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci 2009, 29:6964-6972. 10.1523/JNEUROSCI.0066-09.2009, 2727061, 19474323.
22. Louboutin JP, Chekmasova A, Marusich E, Agrawal L, Strayer DS. Role of CCR5 and its ligands in the control of vascular inflammation and leukocyte recruitment required for acute excitotoxic seizure induction and neural damage. FASEB J 2011, 25:737-753. 10.1096/fj.10-161851, 3023386, 20940264.
23. 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. 10.1016/j.nbd.2008.10.002, 3045783, 19010416.
24. Huang X, Zhang H, Yang J, Wu J, McMahon J, Lin Y, Cao Z, Gruenthal M, Huang Y. Pharmacological inhibition of the mammalian target of rapamycin pathway suppresses acquired epilepsy. Neurobiol Dis 2010, 40:193-199. 10.1016/j.nbd.2010.05.024, 2926303, 20566381.
25. 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. 10.1038/nm.2127, 20348922.
26. Vezzani A. Inflammation and epilepsy. Epilepsy Curr 2005, 5:1-6. 10.1111/j.1535-7597.2005.05101.x, 1176317, 16059445.
27. Savarin-Vuaillat C, Ransohoff RM. Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce?. Neurotherapeutics 2007, 4:590-601. 10.1016/j.nurt.2007.07.004, 17920540.
28. Schwartz M. The emergence of a new science of the mind: immunology benefits the mind. Mol Psychiatry 2010, 15:337-338. 10.1038/mp.2010.22, 20332791.
29. McClelland S, Flynn C, Dube C, Richichi C, Zha Q, Ghestem A, Esclapez M, Bernard C, Baram TZ. Neuron-restrictive silencer factor-mediated hyperpolarization-activated cyclic nucleotide gated channelopathy in experimental temporal lobe epilepsy. Ann Neurol 2011, 70:454-464. 10.1002/ana.22479, 3177145, 21905079.
30. Kan AA, van Erp S, Derijck AA, de Wit M, Hessel EV, O'Duibhir E, de Jager W, van Rijen PC, Gosselaar PH, de Graan PN, Pasterkamp RJ. Genome-wide microRNA profiling of human temporal lobe epilepsy identifies modulators of the immune response. Cell Mol Life Sci 2012, Epub ahead of print.
31. Debets RM, van Veelen CW, van Huffelen AV, van Emde BW. Presurgical evaluation of patients with intractable partial epilepsy: the Dutch epilepsy surgery program. Acta Neurol Belg 1991, 91:125-140.
32. Boer K, Spliet WG, van Rijen PC, Redeker S, Troost D, Aronica E. Evidence of activated microglia in focal cortical dysplasia. J Neuroimmunol 2006, 173:188-195. 10.1016/j.jneuroim.2006.01.002, 16483671.
33. Choi J, Nordli DR, Alden TD, DiPatri A, Laux L, Kelley K, Rosenow J, Schuele SU, Rajaram V, Koh S. Cellular injury and neuroinflammation in children with chronic intractable epilepsy. J Neuroinflammation 2009, 6:38. 10.1186/1742-2094-6-38, 2811703, 20021679.
34. Wyler AR, Dohan FC, Schweitzer JB, Berry AD. A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. Journal of Epilepsy 1992, 5:220-225.
35. Engel J, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures 1993, 609-621. New York: Raven.
36. Hulse RE, Kunkler PE, Fedynyshyn JP, Kraig RP. Optimization of multiplexed bead-based cytokine immunoassays for rat serum and brain tissue. J Neurosci Methods 2004, 136:87-98. 10.1016/j.jneumeth.2003.12.023, 2801052, 15126049.
37. de Jager W, Te VH, Prakken BJ, Kuis W, Rijkers GT. Simultaneous detection of 15 human cytokines in a single sample of stimulated peripheral blood mononuclear cells. Clin Diagn Lab Immunol 2003, 10:133-139. 145264, 12522051.
38. de Jager W, Prakken BJ, Bijlsma JW, Kuis W, Rijkers GT. Improved multiplex immunoassay performance in human plasma and synovial fluid following removal of interfering heterophilic antibodies. J Immunol Methods 2005, 300:124-135. 10.1016/j.jim.2005.03.009, 15896801.
39. Romijn HJ, van Uum JF, Breedijk I, Emmering J, Radu I, Pool CW. Double immunolabeling of neuropeptides in the human hypothalamus as analyzed by confocal laser scanning fluorescence microscopy. J Histochem Cytochem 1999, 47:229-236. 10.1177/002215549904700211, 9889258.
40. Marengo E, Robotti E, Bobba M, Gosetti F. The principle of exhaustiveness versus the principle of parsimony: a new approach for the identification of biomarkers from proteomic spot volume datasets based on principal component analysis. Anal Bioanal Chem 2010, 397:25-41. 10.1007/s00216-009-3390-8, 20091299.
41. Loup F, Picard F, Yonekawa Y, Wieser HG, Fritschy JM. Selective changes in GABAA receptor subtypes in white matter neurons of patients with focal epilepsy. Brain 2009, 132:2449-2463. 10.1093/brain/awp178, 19574438.
42. Notenboom RG, Hampson DR, Jansen GH, van Rijen PC, van Veelen CW, van Nieuwenhuizen O, de Graan PN. Up-regulation of hippocampal metabotropic glutamate receptor 5 in temporal lobe epilepsy patients. Brain 2006, 129:96-107.
43. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, Schrama LH, van Veelen CW, van Rijen PC, van Nieuwenhuizen O, Gispen WH, de Graan PNE. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 2002, 125:32-43. 10.1093/brain/awf001, 11834591.
44. Aliashkevich AF, Yilmazer-Hanke D, Van Roost D, Mundhenk B, Schramm J, Blumcke I. Cellular pathology of amygdala neurons in human temporal lobe epilepsy. Acta Neuropathol 2003, 106:99-106. 10.1007/s00401-003-0707-0, 12684832.
45. Zattoni M, Mura ML, Deprez F, Schwendener RA, Engelhardt B, Frei K, Fritschy JM. Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J Neurosci 2011, 31:4037-4050. 10.1523/JNEUROSCI.6210-10.2011, 21411646.
46. Dinarello CA. The interleukin-1 family: 10 years of discovery. FASEB J 1994, 8:1314-1325.
47. Rigau V, Morin M, Rousset MC, de Bock F, Lebrun A, Coubes P, Picot MC, Baldy-Moulinier M, Bockaert J, Crespel A, Lerner-Natoli M. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007, 130:1942-1956. 10.1093/brain/awm118, 17533168.
48. Nakahara H, Konishi Y, Beach TG, Yamada N, Makino S, Tooyama I. Infiltration of T lymphocytes and expression of icam-1 in the hippocampus of patients with hippocampal sclerosis. Acta Histochem Cytochem 2010, 43:157-162. 10.1267/ahc.10022, 3015053, 21245982.
49. dos Santos AC, Barsante MM, Arantes RM, Bernard CC, Teixeira MM, Carvalho-Tavares J. CCL2 and CCL5 mediate leukocyte adhesion in experimental autoimmune encephalomyelitis-an intravital microscopy study. J Neuroimmunol 2005, 162:122-129. 10.1016/j.jneuroim.2005.01.020, 15833367.
50. Vezzani A, Moneta D, Richichi C, Aliprandi M, Burrows SJ, Ravizza T, Perego C, De Simoni MG. Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 2002, 43(Suppl 5):30-35.
51. Auvin S, Shin D, Mazarati A, Sankar R. Inflammation induced by LPS enhances epileptogenesis in immature rat and may be partially reversed by IL1RA. Epilepsia 2010, 51(Suppl 3):34-38. 2910518, 20618397.
52. Heida JG, Pittman QJ. Causal links between brain cytokines and experimental febrile convulsions in the rat. Epilepsia 2005, 46:1906-1913. 10.1111/j.1528-1167.2005.00294.x, 16393156.
53. Vezzani A, Moneta D, Conti M, Richichi C, Ravizza T, De Luigi A, De Simoni MG, Sperk G, Andell-Jonsson S, Lundkvist J, 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. 10.1073/pnas.190206797, 17235, 11016948.
54. Biber K, de Jong EK, van Weering HR, Boddeke HW. Chemokines and their receptors in central nervous system disease. Curr Drug Targets 2006, 7:29-46. 10.2174/138945006775270196, 16454698.
55. Michaelson MD, Mehler MF, Xu H, Gross RE, Kessler JA. Interleukin-7 is trophic for embryonic neurons and is expressed in developing brain. Dev Biol 1996, 179:251-263. 10.1006/dbio.1996.0255, 8873768.
56. Moors M, Vudattu NK, Abel J, Kramer U, Rane L, Ulfig N, Ceccatelli S, Seyfert-Margolies V, Fritsche E, Maeurer MJ. Interleukin-7 (IL-7) and IL-7 splice variants affect differentiation of human neural progenitor cells. Genes Immun 2010, 11:11-20. 10.1038/gene.2009.77, 19847194.
57. Ishizaki Y, Kira R, Fukuda M, Torisu H, Sakai Y, Sanefuji M, Yukaya N, Hara T. Interleukin-10 is associated with resistance to febrile seizures: Genetic association and experimental animal studies. Epilepsia 2009, 50:761-767. 10.1111/j.1528-1167.2008.01861.x, 19055487.
58. Levin SG, Godukhin OV. Protective effects of interleukin-10 on the development of epileptiform activity evoked by transient episodes of hypoxia in rat hippocampal slices. Neurosci Behav Physiol 2007, 37:467-470. 10.1007/s11055-007-0036-1, 17505796.
59. Kurreeman FA, Schonkeren JJ, Heijmans BT, Toes RE, Huizinga TW. Transcription of the IL10 gene reveals allele-specific regulation at the mRNA level. Hum Mol Genet 2004, 13:1755-1762. 10.1093/hmg/ddh187, 15198994.
60. Zhou Z, Peng X, Insolera R, Fink DJ, Mata M. Interleukin-10 provides direct trophic support to neurons. J Neurochem 2009, 110:1617-1627. 10.1111/j.1471-4159.2009.06263.x, 2737090, 19575707.
61. Guyon A, Nahon JL. Multiple actions of the chemokine stromal cell-derived factor-1alpha on neuronal activity. J Mol Endocrinol 2007, 38:365-376. 10.1677/JME-06-0013, 17339399.
62. Kleinschek MA, Owyang AM, Joyce-Shaikh B, Langrish CL, Chen Y, Gorman DM, Blumenschein WM, McClanahan T, Brombacher F, Hurst SD, Kastelein RA. IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med 2007, 204:161-170. 10.1084/jem.20061738, 2118427, 17200411.
63. Alt C, Laschinger M, Engelhardt B. Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-protein-dependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis. Eur J Immunol 2002, 32:2133-2144. 10.1002/1521-4141(200208)32:8<2133::AID-IMMU2133>3.0.CO;2-W, 12209625.
64. Columba-Cabezas S, Serafini B, Ambrosini E, Aloisi F. Lymphoid chemokines CCL19 and CCL21 are expressed in the central nervous system during experimental autoimmune encephalomyelitis: implications for the maintenance of chronic neuroinflammation. Brain Pathol 2003, 13:38-51.
65. Sonobe Y, Takeuchi H, Kataoka K, Li H, Jin S, Mimuro M, Hashizume Y, Sano Y, Kanda T, Mizuno T, Suzumura A. Interleukin-25 expressed by brain capillary endothelial cells maintains blood-brain barrier function in a protein kinase Cepsilon-dependent manner. J Biol Chem 2009, 284:31834-31842. 10.1074/jbc.M109.025940, 2797254, 19776017.
66. Dogan RN, Long N, Forde E, Dennis K, Kohm AP, Miller SD, Karpus WJ. CCL22 regulates experimental autoimmune encephalomyelitis by controlling inflammatory macrophage accumulation and effector function. J Leukoc Biol 2011, 89:93-104. 10.1189/jlb.0810442, 3004518, 20940325.
67. Galimberti D, Fenoglio C, Comi C, Scalabrini D, De Riz M, Leone M, Venturelli E, Cortini F, Piola M, Monaco F, Bresolin N, Scarpini E. MDC/CCL22 intrathecal levels in patients with multiple sclerosis. Mult Scler 2008, 14:547-549. 10.1177/1352458507084268, 18208895.
68. Sweeney CM, Lonergan R, Basdeo SA, Kinsella K, Dungan LS, Higgins SC, Kelly PJ, Costelloe L, Tubridy N, Mills KH, Fletcher JM. IL-27 mediates the response to IFN-beta therapy in multiple sclerosis patients by inhibiting Th17 cells. Brain Behav Immun 2011, 25:1170-1181. 10.1016/j.bbi.2011.03.007, 21420486.
69. Fitzgerald DC, Rostami A. Therapeutic potential of IL-27 in multiple sclerosis?. Expert Opin Biol Ther 2009, 9:149-160. 10.1517/14712590802646936, 19236245.
70. Muller M, Carter SL, Hofer MJ, Manders P, Getts DR, Getts MT, Dreykluft A, Lu B, Gerard C, King NJ, Campbell IL. CXCR3 signaling reduces the severity of experimental autoimmune encephalomyelitis by controlling the parenchymal distribution of effector and regulatory T cells in the central nervous system. J Immunol 2007, 179:2774-2786.
71. Sorensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 1999, 103:807-815. 10.1172/JCI5150, 408141, 10079101.
72. Kohler RE, Comerford I, Townley S, Haylock-Jacobs S, Clark-Lewis I, McColl SR. Antagonism of the chemokine receptors CXCR3 and CXCR4 reduces the pathology of experimental autoimmune encephalomyelitis. Brain Pathol 2008, 18:504-516.
73. Camacho-Arroyo I, Lopez-Griego L, Morales-Montor J. The role of cytokines in the regulation of neurotransmission. Neuroimmunomodulation 2009, 16:1-12. 10.1159/000179661, 19077440.
74. Mendoza-Fernandez V, Andrew RD, Barajas-Lopez C. Interferon-alpha inhibits long-term potentiation and unmasks a long-term depression in the rat hippocampus. Brain Res 2000, 885:14-24. 10.1016/S0006-8993(00)02877-8, 11121525.
75. Salzmann A, Perroud N, Crespel A, Lambercy C, Malafosse A. Candidate genes for temporal lobe epilepsy: a replication study. Neurol Sci 2008, 29:397-403. 10.1007/s10072-008-1060-9, 19066720.
76. Peltola J, Keranen T, Rainesalo S, Hurme M. Polymorphism of the interleukin-1 gene complex in localization-related epilepsy. Ann Neurol 2001, 50:275-276.
77. Dominici R, Cattaneo M, Malferrari G, Archi D, Mariani C, Grimaldi LM, Biunno I. Cloning and functional analysis of the allelic polymorphism in the transcription regulatory region of interleukin-1 alpha. Immunogenetics 2002, 54:82-86. 10.1007/s00251-002-0445-9, 12037600.
78. Akita H, Takagi N, Ishihara N, Takagi K, Murotomi K, Funakoshi H, Matsumoto K, Nakamura T, Takeo S. Hepatocyte growth factor improves synaptic localization of the NMDA receptor and intracellular signaling after excitotoxic injury in cultured hippocampal neurons. Exp Neurol 2008, 210:83-94. 10.1016/j.expneurol.2007.10.001, 18001712.
79. Tonges L, Ostendorf T, Lamballe F, Genestine M, Dono R, Koch JC, Bahr M, Maina F, Lingor P. Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo. J Neurochem 2011, 117:892-903. 10.1111/j.1471-4159.2011.07257.x, 21443522.
80. Dube 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. 10.1523/JNEUROSCI.0551-10.2010, 2906240, 20519523.
81. 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.
82. 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. 10.1093/brain/awn271, 2724908, 18952671.
83. Cammalleri M, Martini D, Ristori C, Timperio AM, Bagnoli P. Vascular endothelial growth factor up-regulation in the mouse hippocampus and its role in the control of epileptiform activity. Eur J Neurosci 2011, 33:482-498. 10.1111/j.1460-9568.2010.07529.x, 21198982.
84. Nicoletti JN, Shah SK, McCloskey DP, Goodman JH, Elkady A, Atassi H, Hylton D, Rudge JS, Scharfman HE, Croll SD. Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 2008, 151:232-241. 10.1016/j.neuroscience.2007.09.083, 2212620, 18065154.
85. McCloskey DP, Croll SD, Scharfman HE. Depression of synaptic transmission by vascular endothelial growth factor in adult rat hippocampus and evidence for increased efficacy after chronic seizures. J Neurosci 2005, 25:8889-8897. 10.1523/JNEUROSCI.2577-05.2005, 1415170, 16192378.
86. Li Q, Oshige H, Zhen Y, Yamahara T, Oishi T, Seno T, Kawaguchi T, Numa Y, Kawamoto K. Interleukin-5 and interleukin-10 are produced in central nervous system tumor cysts. J Clin Neurosci 2009, 16:437-440. 10.1016/j.jocn.2008.04.022, 19147361.
87. Liva SM, de Vellis J. IL-5 induces proliferation and activation of microglia via an unknown receptor. Neurochem Res 2001, 26:629-637. 10.1023/A:1010983119125, 11523538.
88. Ringheim GE. Mitogenic effects of interleukin-5 on microglia. Neurosci Lett 1995, 201:131-134. 10.1016/0304-3940(95)12153-6, 8848235.
89. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986, 136:2348-2357.
90. Nunnari G, Xu Y, Acheampong EA, Fang J, Daniel R, Zhang C, Zhang H, Mukhtar M, Pomerantz RJ. Exogenous IL-7 induces Fas-mediated human neuronal apoptosis: potential effects during human immunodeficiency virus type 1 infection. J Neurovirol 2005, 11:319-328. 10.1080/13550280500187005, 16162475.
91. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M, Giuliani F, Arbour N, Becher B, Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007, 13:1173-1175. 10.1038/nm1651, 17828272.
92. Morin-Brureau M, Lebrun A, Rousset MC, Fagni L, Bockaert J, de Bock F, Lerner-Natoli M. Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: role of VEGF signaling pathways. J Neurosci 2011, 31:10677-10688. 10.1523/JNEUROSCI.5692-10.2011, 21775611.
93. Suidan GL, Dickerson JW, Chen Y, McDole JR, Tripathi P, Pirko I, Seroogy KB, Johnson AJ. CD8 T cell-initiated vascular endothelial growth factor expression promotes central nervous system vascular permeability under neuroinflammatory conditions. J Immunol 2010, 184:1031-1040. 10.4049/jimmunol.0902773, 2896014, 20008293.
94. 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. 10.1523/JNEUROSCI.1751-04.2004, 15356194.
95. Bittigau P, Ikonomidou C. Glutamate in neurologic diseases. J Child Neurol 1997, 12:471-485. 10.1177/088307389701200802, 9430311.
96. Marchi N, Angelov L, Masaryk T, Fazio V, Granata T, Hernandez N, Hallene K, Diglaw T, Franic L, Najm I, Janigro D. Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 2007, 48:732-742. 10.1111/j.1528-1167.2007.00988.x, 17319915.
97. van Vliet EA, da Costa AS, 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. 10.1093/brain/awl318, 17124188.
98. Croll SD, Goodman JH, Scharfman HE. Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. Adv Exp Med Biol 2004, 548:57-68. 2504497, 15250585.
99. Vezzani A, Aronica E, Mazarati A, Pittman QJ. Epilepsy and brain inflammation. Exp Neurol 2011, Epub ahead of print.
100. Lukasiuk K, Dabrowski M, Adach A, Pitkanen A. Epileptogenesis-related genes revisited. Prog Brain Res 2006, 158:223-241.
101. Peltola J, Palmio J, Korhonen L, Suhonen J, Miettinen A, Hurme M, Lindholm D, Keranen T. Interleukin-6 and interleukin-1 receptor antagonist in cerebrospinal fluid from patients with recent tonic-clonic seizures. Epilepsy Res 2000, 41:205-211. 10.1016/S0920-1211(00)00140-6, 10962211.
102. Bauer S, Cepok S, Todorova-Rudolph A, Nowak M, Koller M, Lorenz R, Oertel WH, Rosenow F, Hemmer B, Hamer HM. Etiology and site of temporal lobe epilepsy influence postictal cytokine release. Epilepsy Res 2009, 86:82-88. 10.1016/j.eplepsyres.2009.05.009, 19520550.
103. Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci 2005, 6:775-786.
104. Frost RA, Nystrom GJ, Lang CH. Epinephrine stimulates IL-6 expression in skeletal muscle and C2C12 myoblasts: role of c-Jun NH2-terminal kinase and histone deacetylase activity. Am J Physiol Endocrinol Metab 2004, 286:E809-E817. 10.1152/ajpendo.00560.2003, 14722032.
105. Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 2002, 16:1335-1347. 10.1096/fj.01-0876rev, 12205025.
106. Pacifici R, Paris L, Di Carlo S, Bacosi A, Pichini S, Zuccaro P. Cytokine production in blood mononuclear cells from epileptic patients. Epilepsia 1995, 36:384-387. 10.1111/j.1528-1157.1995.tb01013.x, 7607117.
107. Lenz JC, Rockstroh JK. Vicriviroc, a new CC-chemokine receptor 5 inhibitor for treatment of HIV: properties, promises and challenges. Expert Opin Drug Metab Toxicol 2010, 6:1139-1150. 10.1517/17425255.2010.510833, 20712521.
108. Sayana S, Khanlou H. Maraviroc: a new CCR5 antagonist. Expert Rev Anti Infect Ther 2009, 7:9-19. 10.1586/14787210.7.1.9, 19622053.