Myoloid-related protein 8, an endogenous ligand of toll-like receptor 4, Is involved in epileptogenesis of mesial temporal lobe epilepsy via activation of the nuclear factor-κb pathway in astrocytes

Molecular Neurobiology

Volumn 49, Issue 1, 2014, Pages 337-351

  Gan, Na ^a   Yang, Lifen ^a   Omran, Ahmed ^a,b   Peng, Jing ^a   Wu, Liwen ^a   He, Fang ^a   Zhang, Ciliu ^a   Xiang, Qiulian ^a   Kong, Huimin ^a   Ma, Yupin ^a   Ashhab, Muhammad Usman ^a   Deng, Xiaolu ^a   Yin, Fei ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Suez Canal University Faculty of Medicine   (Egypt)

Author keywords

Interleukin 1 ; Mesial temporal lobe epilepsy; Myeloid related protein 8; Nuclear factor kappa B; Toll like receptor 4

Indexed keywords

CARBAMAZEPINE; ETIRACETAM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LAMOTRIGINE; MEMBRANE PROTEIN; MYELOID RELATED PROTEIN 8; OXCARBAZEPINE; PHENOBARBITAL; TOLL LIKE RECEPTOR 4; TOPIRAMATE; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT THERAPY; ASTROCYTE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; EPILEPTOGENESIS; FEMALE; GENETIC TRANSFECTION; HIPPOCAMPUS; HUMAN; MALE; MESIAL TEMPORAL LOBE EPILEPSY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVIEW; SCHOOL CHILD; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ASTROCYTES; CALGRANULIN A; CELLS, CULTURED; CHILD; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; LIGANDS; MALE; NF-KAPPA B; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84894381253     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8522-7     Document Type: Review

References (88)

1. Sander JW (2003) The epidemiology of epilepsy revisited. Curr Opin Neurol 16:165-170
2. Rakhade SN, Jensen FE (2009) Epileptogenesis in the immature brain: emerging mechanisms. Nat Rev Neurol 5:380-391
3. Friedman MJ, Sharieff GQ (2006) Seizures in children. Pediatr Clin North Am 53:257-277
4. Cascino GD (2008) When drugs and surgery don't work. Epilepsia 49:79-84
5. Turrin NP, Rivest S (2004) Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol Dis 16:321-334
6. Vezzani A, Granata T (2005) Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46:1724-1743
7. Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A (2008) Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29:142-160
8. Choi J, Nordli DR Jr, Alden TD, DiPatri A Jr, Laux L, Kelley K, Rosenow J, Schuele SU, Rajaram V, Koh S (2009) Cellular injury and neuroinflammation in children with chronic intractable epilepsy. J Neuroinflammation 6:38
9. Peng J, Omran A, Ashhab MU, Kong H, Gan N, He F, Yin F (2013) Expression Patterns of miR-124, miR-134, miR-132, and miR-21 in an Immature Rat Model and Children with Mesial Temporal Lobe Epilepsy. J Mol Neurosci doi: 10.1007/s12031-013-9953-3.
10. Ashhab MU, Omran A, Kong H, Gan N, He F, Peng J, Yin F (2013) Expressions of Tumor Necrosis Factor-Alpha and MicroRNA-155 in Immature Rat Model of Status Epilepticus and Children with Mesial Temporal Lobe Epilepsy. J Mol Neurosci [Epub ahead of print]. doi: 10.1007/s12031-013-0013-9
11. Pitkanen A, Sutula TP (2002) Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 1:173-181
12. Galic MA, Riazi K, Henderson AK, Tsutsui S, Pittman QJ (2009) Viral-like brain inflammation during development causes increased seizure susceptibility in adult rats. Neurobiol Dis 36:343-351
13. Rasmussen T, Olszewski J, Lloyd-Smith D (1958) Focal seizures due to chronic localized encephalitis. Neurology 8:435-445
14. Cojocaru IM, Cojocaru M (2010) Reactions of the immune system in epilepsy. Maedica (Buchar) 3:201-206
15. Choi J, Min HJ, Shin JS (2011) Increased levels of HMGB1 and pro-inflammatory cytokines in children with febrile seizures. J Neuroinflammation 8:135
16. Berg AT, Shinnar S (1996) Unprovoked seizures in children with febrile seizures: short-term outcome. Neurology 47:562-568
17. Shinnar S (2003) Febrile seizures and mesial temporal sclerosis. Epilepsy Curr 3:115-118
18. Bsibsi M, Ravid R, Gveric D, van Noort JM (2002) Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61:1013-1021
19. Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, Vezzani A (2010) Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 16:413-419
20. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, van der Poll T, Sorg C, Roth J (2007) Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13:1042-1049
21. Hayashi T, Nakamura T, Takaoka A (2011) Pattern recognition receptors. Nihon Rinsho Meneki Gakkai Kaishi 34:329-345
22. Mencin A, Kluwe J, Schwabe RF (2009) Toll-like receptors as targets in chronic liver diseases. Gut 58:704-720
23. Burkhardt K, Schwarz S, Pan C, Stelter F, Kotliar K, Von Eynatten M, Sollinger D, Lanzl I, Heemann U, Baumann M (2009) Myeloid-related protein 8/14 complex describes microcirculatory alterations in patients with type 2 diabetes and nephropathy. Cardiovasc Diabetol 8:10
24. Achouiti A, Vogl T, Urban CF, Röhm M, Hommes TJ, van Zoelen MA, Florquin S, Roth J, van 't Veer C, de Vos AF, van der Poll T (2012) Myeloid-related protein-14 contributes to protective immunity in gram-negative pneumonia derived sepsis. PLoS Pathog 8:e1002987
25. Maiseyeu A, Badgeley MA, Kampfrath T, Mihai G, Deiuliis JA, Liu C, Sun Q, Parthasarathy S, Simon DI, Croce K, Rajagopalan S (2012) In vivo targeting of inflammation-associated myeloid-related protein 8/14 via gadolinium immunonanoparticles. Arterioscler Thromb Vasc Biol 32:962-970
26. Ziegler G, Prinz V, Albrecht MW, Harhausen D, Khojasteh U, Nacken W, Endres M, Dirnagl U, Nietfeld W, Trendelenburg G (2009) Mrp-8 and -14 mediate CNS injury in focal cerebral ischemia. Biochim Biophys Acta 1792:1198-1204
27. Engel S, Schluesener H, Mittelbronn M, Seid K, Adjodah D, Wehner HD, Meyermann R (2000) Dynamics of microglial activation after human traumatic brain injury are revealed by delayed expression of macrophage-related proteins MRP8 and MRP14. Acta Neuropathol 100:313-322
28. Yonekawa K, Neidhart M, Altwegg LA, Wyss CA, Corti R, Vogl T, Grigorian M, Gay S, Lüscher TF, Maier W (2011) Myeloid related proteins activate Toll-like receptor 4 in human acute coronary syndromes. Atherosclerosis 218:486-492
29. Holzinger D, Frosch M, Kastrup A, Prince FH, Otten MH, Van Suijlekom-Smit LW, ten Cate R, Hoppenreijs EP, Hansmann S, Moncrieffe H, Ursu S, Wedderburn LR, Roth J, Foell D, Wittkowski H (2012) The Toll-like receptor 4 agonist MRP8/14 protein complex is a sensitive indicator for disease activity and predicts relapses in systemic-onset juvenile idiopathic arthritis. Ann Rheum Dis 71:974-980
30. Crespel A, Coubes P, Rousset MC, Brana C, Rougier A, Rondouin G, Bockaert J, Baldy-Moulinier M, Lerner-Natoli M (2002) Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res 952:159-169
31. Voutsinos-Porche B, Koning E, Kaplan H, Ferrandon A, Guenounou M, Nehlig A, Motte J (2004) Temporal patterns of the cerebral inflammatory response in the rat lithium-pilocarpine model of temporal lobe epilepsy. Neurobiol Dis 17:385-402
32. Lubin FD, Ren Y, Xu X, Anderson AE (2007) Nuclear factor-kB regulates seizure threshold and gene transcription following convulsant stimulation. J Neurochem 103:1381-1395
33. Chuang YC, Chen SD, Lin TK, Chang WN, Lu CH, Liou CW, Chan SH, Chang AY (2010) Transcriptional upregulation of nitric oxide synthase II by nuclear factor-kappaB promotes apoptotic neuronal cell death in the hippocampus following experimental status epilepticus. J Neurosci Res 88:1898-1907
34. Yu N, Di Q, Liu H, Hu Y, Jiang Y, Yan YK, Zhang YF, Zhang YD (2011) Nuclear factor-kappa B activity regulates brain expression of P-glycoprotein in the kainic acid-induced seizure rats. Mediators Inflamm: 670613
35. Takeda K, Akira S (2004) TLR signaling pathways. Semin Immunol 16:3-9
36. Okun E, Griffioen KJ, Mattson MP (2011) Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci 34:269-281
37. Sayyah M, Beheshti S, Shokrgozar MA, Eslami-far A, Deljoo Z, Khabiri AR, Haeri Rohani A (2005) Antiepileptogenic and nticonvulsant activity of interleukin-1 beta in amygdala-kindled rats. Exp Neurol 191:145-153
38. Akin D, Ravizza T, Maroso M, Carcak N, Eryigit T, Vanzulli I, Aker RG, Vezzani A, Onat FY (2011) IL-1β is induced in reactive astrocytes in the somatosensory cortex of rats with genetic absence epilepsy at the onset of spike-and-wave discharges, and contributes to their occurrence. Neurobiol Dis 44:259-269
39. Järvelä JT, Lopez-Picon FR, Plysjuk A, Ruohonen S, Holopainen IE (2011) Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus. J Neuroinflammation 8:29
40. Omran A, Peng J, Zhang C, Xiang QL, Xue J, Gan N, Kong H, Yin F (2012) Interleukin-1β and microRNA-146a in an immature rat model and children with mesial temporal lobe epilepsy. Epilepsia 53:1215-1224
41. Rizzi M, Perego C, Aliprandi M, Richichi C, Ravizza T, Colella D, VelískÅvá J, Moshé SL, De Simoni MG, Vezzani A (2003) Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development. Neurobiol Dis 14:494-503
42. Vezzani A, Baram TZ (2007) New roles for interleukin-1 Beta in the mechanisms of epilepsy. Epilepsy Curr 7:45-50
43. Nguyen MD, Julien JP, Rivest S (2002) Innate immunity: the missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 3:216-227
44. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294
45. Blümcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, Merschhemke M, Meencke HJ, Lehmann T, von Deimling A, Scheiwe C, Zentner J, Volk B, Romstöck J, Stefan H, Hildebrandt M (2007) A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:235-244
46. Sloviter RS (1982) A simplified Timm stain procedure compatible with formaldehyde fixation and routine paraffin embedding of rat brain. Brain Res Bull 8:771-774
47. Choi J, Koh S (2008) Role of Brain Inflammation in Epileptogenesis. Yonsei Med J 49:1-18
48. Loscher W, Schmidt D (2006) New horizons in the development of antiepileptic drugs: innovative strategies. Epilepsy Res 69:183-272
49. Stafstrom CE (2010) Mechanisms of action of antiepileptic drugs: the search for synergy. Curr Opin Neurol 23:157-163
50. Vezzani A, French J, Bartfai T, Baram TZ (2011) The role of inflammation in epilepsy. Nat Rev Neurol 7(31-40):51
51. Ravizza T, Balosso S, Vezzani A (2011) Inflammation and prevention of epileptogenesis. Neurosci Lett 497:223-230
52. Auvin S, Mazarati A, Shin D, Sankar R (2010) Inflammation enhances epileptogenesis in the developing rat brain. Neurobiol Dis 40:303-310
53. Marchi N, Fan Q, Ghosh C, Fazio V, Bertolini F, Betto G, Batra A, Carlton E, Najm I, Granata T, Janigro D (2009) Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol Dis 33:171-181
54. Abraham J, Fox PD, Condello C, Bartolini A, Koh S (2012) Minocycline attenuates microglia activation and blocks the long-term epileptogenic effects of early-life seizures. Neurobiol Dis 46:425-430
55. Wang DD, Englot DJ, Garcia PA, Lawton MT, Young WL (2012) Minocycline- and tetracycline-class antibiotics are protective against partial seizures in vivo. Epilepsy Behav 24:314-318
56. Jaworska-Adamu J, Dmowska M, Cybulska R, Krawczyk A, Pawlikowska- Pawlȩga B (2011) Investigations of hippocampal astrocytes in lipopolysaccharide-preconditioned rats in the pilocarpine model ofepilepsy. Folia Histochem Cytobiol 49:219-224
57. Lee SH, Kim BJ, Kim YB, Chung PW, Moon HS, Suh BC, Yoon WT, Jin DK, Park YS, Lee YT, Park KY (2012) IL-1β induction and IL-6 suppression are associated with aggravated neuronal damage in a lipopolysaccharide-pretreated kainic acid-induced rat pup seizure model. Neuroimmunomodulation 19:319-325
58. Granata T, Cross H, Theodore W, Avanzini G (2011) Immune-mediated epilepsies. Epilepsia 52:5-11
59. Kerkhoff C, Eue I, Sorg C (1999) The regulatory role of MRP8 (S100A8) and MRP14 (S100A9) in the transendothelial migration of human leukocytes. Pathobiology 67:230-232
60. Meeuwsen S, Bsibsi M, Persoon-Deen C, Ravid R, van Noort JM (2005) Cultured human adult microglia from different donors display stable cytokine, chemokine and growth factor gene profiles but respond differently to a pro-inflammatory stimulus. Neuroimmunomodulation 12:235-245
61. Roth J, Vogl T, Sorg C, Sunderkotter C (2003) Phagocyte-specific S100 proteins: a novel group of proinflammatory molecules. Trends Immunol 24:155-158
62. Foell D, Wittkowski H, Vogl T, Roth J (2007) S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81:28-37
63. Foell D, Roth J (2004) Proinflammatory S100 proteins in arthritis and autoimmune disease. Arthritis Rheum 50:3762-3771
64. Frosch M, Strey A, Vogl T, Wulffraat NM, Kuis W, Sunderkötter C, Harms E, Sorg C, Roth J (2000) Myeloid-related proteins 8 and 14 are specifically secreted during interaction of phagocytes and activated endothelium and are useful markers for monitoring disease activity in pauciarticular-onset juvenile rheumatoid arthritis. Arthritis Rheum 43:628-637
65. Peltier DC, Simms A, Farmer JR, Miller DJ (2010) Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J Immunol 184:7010-7021
66. Zurolo E, Iyer A, Maroso M, Carbonell C, Anink JJ, Ravizza T, Fluiter K, Spliet WG, van Rijen PC, Vezzani A, Aronica E (2011) Activation of Toll-like receptor, RAGE and HMGB1 signalling in malformations of cortical development. Brain 134:10151032
67. Gorina R, Font-Nieves M, Márquez-Kisinousky L, Santalucia T, Planas AM (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFκB signaling, MAPK, and Jak1/Stat1 pathways. GLIA 59:242-255
68. Anderson KV (2000) Toll signaling pathways in the innate immune response. Curr Opin Immunol 12:13-19
69. Akira S, Takeda K, Kaisho T (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2:675-680
70. Yan Q, Carmody RJ, Qu Z, Ruan Q, Jager J, Mullican SE, Lazar MA, Chen YH (2012) Nuclear factor-κB binding motifs specify Toll-like receptor-induced gene repression through an inducible repressosome. Proc Natl Acad Sci U S A 109:14140-14145
71. Ge Y, Xu Y, Sun W, Man Z, Zhu L, Xia X, Zhao L, Zhao Y, Wang X (2012) The molecular mechanisms of the effect of Dexamethasone and Cyclosporin A on TLR4 /NF-κB signaling pathway activation in oral lichen planus. Gene 508:157-164
72. Wang PP, Xie DY, Liang XJ, Peng L, Zhang GL, Ye YN, Xie C, Gao ZL (2012) HGF and direct mesenchymal stem cells contact synergize to inhibit hepatic stellate cells activation through TLR4/NF-kB pathway. PLoS One 7:e43408
73. Ma CX, Yin WN, Cai BW, Wu J, Wang JY, He M, Sun H, Ding JL, You C (2009) Toll-like receptor 4/nuclear factor-kappa B signaling detected in brain after early subarachnoid hemorrhage. Chin Med J (Engl) 122:1575-1581
74. Dong XQ, Yu WH, Hu YY, Zhang ZY, Huang M (2011) Oxymatrine reduces neuronal cell apoptosis by inhibiting Toll-like receptor 4/nuclear factor kappa-B-dependent inflammatory responses in traumatic rat brain injury. Inflamm Res 60:533-539
75. Lan L, Tao J, Chen A, Xie G, Huang J, Lin J, Peng J, Chen L (2013) Electroacupuncture exerts anti-inflammatory effects in cerebral ischemia-reperfusion injured rats via suppression of the TLR4/NF-κB pathway. Int J Mol Med 31:75-80
76. Lerner-Natoli M, Montpied P, Rousset MC, Bockaert J, Rondouin G (2000) Sequential expression of surface antigens and transcription factor NF-kappaB by hippocampal cells in excitotoxicity and experimental epilepsy. Epilepsy Res 41:141-154
77. Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, De Simoni MG (1999) Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 19:5054-5065
78. 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 (2000) Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc Natl Acad Sci U S A 97:11534-11539
79. Ravizza T, Boer K, Redeker S, Spliet WG, van Rijen PC, Troost D, Vezzani A, Aronica E (2006) The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol Dis 24:128-143
80. Xie C, Sun J, Qiao W, Lu D, Wei L, Na M, Song Y, Hou X, Lin Z (2011) Administration of simvastatin after kainic acid-induced status epilepticus restrains chronic temporal lobe epilepsy. PLoS One 6:e24966
81. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629-640
82. Appel SH, Beers DR, Henkel JS (2009) T cell-microglial dialog in Parkinson's disease and amyotrophic lateral sclerosis: are we listening? Trends Immunol 31:7-17
83. Volman V, Bazhenov M, Sejnowski TJ (2012) Computational models of neuron-astrocyte interaction in epilepsy. Front Comput Neurosci 6:58
84. Iyer A, Zurolo E, Prabowo A, Fluiter K, Spliet WG, van Rijen PC, Gorter JA, Aronica E (2012) MicroRNA-146a: a key regulator of astrocyte-mediated inflammatory response. PLoS One 7:e44789
85. Witcher MR, Ellis TL (2012) Astroglial networks and implications for therapeutic neuromodulation of epilepsy. Front Comput Neurosci 6:61
86. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570-577
87. Pousset F, Dantzer R, Kelley KW, Parnet P (2000) Interleukin-1 signaling in mouse astrocytes involves Akt: a study with interleukin-4 and IL-10. Eur Cytokine Netw 11:427-434
88. Couturier J, Paccalin M, Morel M, Terro F, Milin S, Pontcharraud R, Fauconneau B, Page G (2011) Prevention of the β-amyloid peptide-induced inflammatory process by inhibition of double-stranded RNA-dependent protein kinase in primary murine mixed co-cultures. J Neuroinflammation 8:72