Journal of the Neurological Sciences
Volume 296, Issue 1 , Pages 1-6 , 15 September 2010

Why mesial temporal lobe epilepsy with hippocampal sclerosis is progressive: Uncontrolled inflammation drives disease progression?

  • Tianhua Yang

      Affiliations

    • Department of Neurology, West China Hospital, Si Chuan University, Cheng du, Sichuan, China
    • ,
  • Dong Zhou

      Affiliations

    • Department of Neurology, West China Hospital, Si Chuan University, Cheng du, Sichuan, China
    • Corresponding Author InformationCorresponding author. Department of Neurology, West China Hospital, Sichuan University, 610041 Chengdu, Sichuan, China. Tel.: +86 13980008088; fax: +86 28 85423550.
    • ,
  • Hermann Stefan

      Affiliations

    • Department of Neurology, Center of Epilepsy (ZEE), University of Erlangen-Nuremberg, Erlangen, Germany

Received 12 January 2010 ,Revised 28 May 2010 ,Accepted 2 June 2010.

References 

  1. Pitka¨nen A, Sutula TP. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal lobe epilepsy. Lancet Neurol. 2002;1:173–181
  2. Luby M, Spencer DD, Kim JM, deLanerolle N, McCarthy G. Hippocampal MRI volumetrics and temporal lobe substrates in medial temporal lobe epilepsy. Magn Reson Imaging. 1995;13:1065–1071
  3. Cascino GD. Neuroimaging in epilepsy: diagnostic strategies in partial epilepsy. Semin Neurol. 2008;28:523–532
  4. Stefan H, Hildebrandt M, Kerling F, Kasper BS, Hammen T, Dörfler A, et al. Clinical prediction of postoperative seizure control: structural, functional findings and disease histories. J Neurol Neurosurg Psychiatry. 2009;80:196–200
  5. Helmstaedter C, Kurthen M, Lux S, Reuber M, Elger CE. Chronic epilepsly and cognition: a longitudinal study in temporal lobe epilepsy. Ann Neurol. 2003;54:425–432
  6. Marques CM, Caboclo LOSF, Noffs MHS, Carrete H, Yacubian EMT. Progressive cognitive decline in patients with temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia. 2006;47(Suppl. 4):100–101
  7. Lynch M, Sayin U, Bownds J, Janumpalli S, Sutula T. Long-term consequences of early postnatal seizures on hippocampal learning and plasticity. Eur J Neurosci. 2000;12:2252–2264
  8. Niessen HG, Angenstein F, Vielhaber S, Frisch C, Kudin A, Elger CE, et al. Volumetric magnetic resonance imaging of functionally relevant structural alterations in chronic epilepsy after pilocarpineinduced status epilepticus in rats. Epilepsia. 2005;46:1021–1026
  9. Jiang W, Duong TM, de Lanerolle NC. The neuropathology of hyperthermic seizures in the rat. Epilepsia. 1999;40:5–19
  10. Liu Z, Yang Y, Silveira DC, Sarkisian MR. Consequences of recurrent seizures during early brain development. Neuroscience. 1999;92:1443–1454
  11. Williams PA, White AM, Clark S, Ferraro DJ, Swiercz W, Staley KJ, et al. Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci. 2009;29:2103–2112
  12. Engel J. The timing of surgical intervention for mesial temporal lobe epilepsy: a plan for a randomized clinical trial. Arch Neurol. 1999;56:1338–1341
  13. Engel J. Surgery for seizures. N Engl J Med. 1996;334:647–652
  14. Blümcke I, Beck H, Lie AA, Wiestler OD. Molecular neuropathology of human mesial temporal lobe epilepsy. Epilepsy Res. 1999;36:205–223
  15. Kalviainen R, Salmenpera T, Partanen K, Vainio P, Riekkinen P, Pitkänen A. Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology. 1998;50:1377–1382
  16. Gilliam FG, Maton BM, Martin RC, Sawrie SM, Faught RE, Hugg JW, et al. Hippocampal 1H-MRSI correlates with severity of depression symptoms in temporal lobe epilepsy. Neurology. 2007;68:364–368
  17. Shamim S, Hasler G, Liew C, Sato S, Theodore WH. Temporal lobe epilepsy, dapression, and hippocampal volume. Epilepsia. 2009;50(5):1067–1071
  18. Bernhardt BC, Worsley KJ, Besson P, Concha L, Lerch JP, Evans AC, et al. Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy. Neuroimage. 2008;42:515–524
  19. Sutula TP. Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res. 2004;60:161–171
  20. Bonilha L, Rorden C, Appenzeller S, Coan AC, Cendes F, Li LM. Gray matter atrophy associated with duration of temporal lobe epilepsy. Neuroimage. 2006;32:1070–1079
  21. Tasch E, Cendes F, Dubeau F, Andermann F, Arnold DL. Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol. 1999;45:568–576
  22. Bernasconi N, Natsume J, Bernasconi A. Progression in temporal lobe epilepsy: differential atrophy in mesial temporal structures. Neurology. 2005;65:223–228
  23. Theodore WH, Bhatia S, Hatta J, Fazilat S, DeCarli C, Bookheimer SY, et al. Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures. Neurology. 1999;52:132–136
  24. Fuerst D, Shah J, Shah A, Watson C. Hippocampal sclerosis is a progressive disorder: a longitudinal volumetric MRI study. Ann Neurol. 2003;53:413–416
  25. Bernhardt BC, Worsley KJ, Kim H, Evans AC, Bernasconi A, Bernasconi N. Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology. 2009;72:1747–1754
  26. Bernhardt BC, Worsley KJ, Bernasconi A, Bernasconi N. Temporal lobe epilepsy is associated with progressive neocortical thinning: a longitudinal study. Epilepsia. 2008;49(Suppl. 7):388
  27. Cascino GD. Temporal lobe epilepsy is a progressive neurologic disorder time means neurons!. Neurology. 2009;72:1718–1719
  28. Zipp F, Aktas O. The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci. 2006;29:518–527
  29. Popovich PG, Longbrake EE. Can the immune system be harnessed to repair the CNS?. Nat Rev Neurosci. 2008;9:481–493
  30. Jankowsky JL, Patterson PH. The role of cytokines and growth factors in seizures and their sequelae. Prog Neurobiol. 2001;63:125–149
  31. Turrin NP, Rivest S. Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol Dis. 2004;16:321–324
  32. Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia. 2005;46:1724–1743
  33. Bailey SL, Carpentier PA, McMahon EJ, Begolka WS, Miller SD. Innate and adaptive immune responses of the central nervous system. Crit Rev Immunol. 2006;26:149–188
  34. Irwin MR, Wang M, Ribeiro D, Cho HJ, Olmstead R, Breen EC, et al. Sleep loss activates cellular inflammatory signaling. Biol Psychiatry. 2008;64:538–540
  35. Black PH. Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav Immun. 2002;16:622–653
  36. Crespel A, Coubes P, Rousset MC, Brana C, Rougier A, Rondouin G, et al. Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res. 2002;952:159–169
  37. Nguyen MD, Julien JP, Rivest S. Innate immunity: the missing link in neuroprotection and neurodegeneration?. Nat Rev Neurosci. 2002;3:216–227
  38. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci. 2001;2:734–744
  39. Gehrmann J, Matsumoto Y, Kreutzberg GW. Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev. 1995;20:269–287
  40. Beach TG, Woodhurst WB, MacDonald DB, Jones MW. Reactive microglia in hippocampal sclerosis associated with human temporal lobe epilepsy. Neurosci Lett. 1995;191:27–30
  41. Jung KH, Chu K, Lee ST, Kim JH, Kang KM, Song EC, et al. Region-specific plasticity in the epileptic rat brain: A hippocampal and extrahippocampal analysis. Epilepsia. 2009;50:537–549
  42. Rodgers KM, Hutchinson MR, Northcutt A, Maier SF, Watkins LR, Barth DS. The cortical innate immune response increases local neuronal excitability leading to seizures. Brain. 2009;132:2478–2486
  43. Ravizza Teresa, Gagliardi Barbara, Noé Francesco, Boer Karin, Aronica Eleonora, Vezzania Annamaria. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis. 2008;29:142–160
  44. 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
  45. De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, et al. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci. 2000;12:2623–2633
  46. 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
  47. Fedele DE, Gouder N, Guttinger M, Gabernet L, Scheurer L, Rulicke T, et al. Astrogliosis in epilepsy leads to overexpression of adenosine kinase, resulting in seizure aggravation. Brain. 2005;128:2383–2395
  48. Crespel A. Inflammatory reactions in human temporal lobe epilepsy with hippocampal sclerosis. Epilepsia. 2006;47(Suppl. 3):258–259
  49. Schröder W, Hinterkeuser S, Seifert G, Schramm J, Jabs R, Wilkin GP, et al. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia. 2000;41(Suppl 6):S181–S184
  50. Aronica E, Boer K, van Vliet EA, Redeker S, Baayen JC, Spliet WG, et al. Complement activation in experimental and human temporal lobe epilepsy. Neurobiol Dis. 2007;26:497–511
  51. Vezzani A, Ravizza T, Balosso S, Aronica E. Glia as a source of cytokines: implications for neuronal excitability and survival. Epilepsia. 2008;49:24–32
  52. Vezzani A, Balosso S, Ravizza T. The role of cytokines in the pathophysiology of epilepsy. Brain Behav Immun. 2008;22:797–803
  53. Sims KD, Robinson MB. Expression patterns and regulation of glutarnate transporters in the developing and adult nervous system. Crit Rev Neurobiol. 1999;13:169–197
  54. Magistretti PJ, Pellerin L. The contribution of astrocytes to the 18F-2-deoxyglucose signal in PET activation studies. Mol Psychiatry. 1996;1:445–452
  55. Humpel C, Hoffer B, Stromberg 1, Bektesh S, Collins F, Olson L. Neurons of the hippocampal formation express glial cell line derived neurotrophic factor messenger RNA in response to kainate-induced excitation. Neuroscience. 1994;59:791–795
  56. Kokaia Z, Airaksinen MS, Nanobashvili A, Larsson E, Kujamäki E, Lindvall O, et al. GDNF family ligands and receptors are differentially regulated after brain insults in the rat. Eur J Neurosci. 1999;11:1202–1216
  57. Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, et al. Interleukin-1β 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
  58. Ravizza T, Lucas SM, Balosso S, Bernardino L, Ku G, Noe F, et al. Inactivation of caspase-1 in rodent brain: a novel anticonvulsive strategy. Epilepsia. 2006;47:1160–1168
  59. van Vliet EA, da Costa Araújo 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
  60. Uva L, Librizzi L, Marchi N, Noe F, Bongiovanni R, Vezzani A, et al. Acute induction of epileptiform discharges by pilocarpine in the in vitro isolated guinea-pig brain requires enhancement of blood-brain barrier permeability. Neuroscience. 2008;151:303–312
  61. Fabene PF, Navarro Mora G, Martinello M, Rossi B, Merigo F, Ottoboni L, et al. A role for leukocyte–endothelial adhesion mechanisms in epilepsy. Nat Med. 2008;14:1377–1383
  62. Ransohoff RM, Kivisakk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol. 2003;3:569–581
  63. Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ. Microglial activation and TNF-α production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci USA. 2008;105:17151–17156
  64. Kanemoto K, Kawasaki J, Miyamoto T, Obayashi H, Nishimura M. Interleukin (IL)-1b, IL-1a, and IL-1 receptor antagonist gene polymorphisms in patients with temporal lobe epilepsy. Ann Neurol. 2000;47:571–574
  65. Giulian D, Li J, Li X, George J, Rutecki PA. The impact of microglia-derived cytokines upon gliosis in the CNS. Dev Neurosci. 1994;16:128–136
  66. Marchi N, Fan QY, Ghosh C, Fazio V, Bertolini F, Betto G, et al. Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol Dis. 2009;33:171–181
  67. Ravizza T, Noé F, Zardoni D, Vaghi V, Sifringer M, Vezzani A. Interleukin converting enzyme inhibition impairs kindling epileptogenesis in rats by blocking astrocytic IL-1β production. Neurobiol Dis. 2008;31:327–333
  68. McNamara JO. Cellular and molecular basis of epilepsy. J Neurosci. 1994;14:3413–3425
  69. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci. 1997;17:3727–3738
  70. Koh S, Storey TW, Santos TC, Mian AY, Cole AJ. Early-life seizures in rats increase susceptibility to seizure-induced brain injury in adulthood. Neurology. 1999;53:915–921
  71. Ridet JL, Malhotra SK, Privat A, Gage FH. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997;20:570–577
  72. Ledeboer A, Breve´ JJ, Poole S, Tilders FJ, Van Dam AM. Interleukin-10, interleukin-4, and transforming growth factor-beta differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia. 2000;30:134–142
  73. Lee TS, Mane S, Eid T, Zhao H, Lin A, Guan Z, et al. Gene expression in temporal lobe epilepsy is consistent with increased release of glutamate by astrocytes. Mol Med. 2007;13:1–13
  74. Cole-Edwards KK, Bazan NG. Lipid signaling in experimental epilepsy. Neurochem Res. 2007;30:847–853
  75. Zhang HJ, Sun RP, Lei GF, Yang L, Liu CX. Cyclooxygenase-2 inhibitor inhibits hippocampal synaptic reorganization in pilocarpine-induced status epilepticus rats. J Zhejiang Univ Sci B. 2008;9:903–915
  76. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, et al. CXCR4-activated astrocyte glutamate release via TNFalpha, amplification by microglia triggers neurotoxicity. Nat Neurosci. 2001;4:702–710
  77. Tilleux S, Berger J, Hermans E. Induction of astrogliosis by activated microglia is associated with a down-regulation of metabotropic glutamate receptor 5. J Neuroimmunol. 2007;189:23–30
  78. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, et al. An astrocytic basis of epilepsy. Nat Med. 2005;11:973–981
  79. D'Ambrosio R. The role of glial membrane ion channels in seizures and epileptogenesis. Pharmacol Ther. 2004;103:95–108
  80. Samland H, Huitron-Resendiz S, Masliah E, Criado J, Henriksen SJ, Campbell IL. Profound increase in sensitivity to glutamatergic but not cholinergic agonistinduced seizures in transgenic mice with astrocyte production of IL-6. J Neurosci Res. 2003;73:176–187
  81. Cunningham AJ, Murray CA, O'Neill LA, Lynch MA, O'Connor JJ. Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit longterm potentiation in the rat dentate gyrus in vitro. Neurosci Lett. 1996;203:17–20
  82. 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 U S A. 1995;92:11294–11298
  83. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A. 1993;90:10061–10065
  84. Balosso S, Maroso M, Sanchez-Alavez M, Ravizza T, Frasca A, Bartfai T, et al. A novel non-transcriptional pathway mediates the proconvulsive effects of interleukin-1 beta. Brain. 2008;131:3256–3265
  85. Nitsch R, Pohl EE, Smorodchenko A, Infante-Duarte C, Aktas O, Zipp F. Directimpact of T cells on neurons revealed by two photon microscopy in living brain tissue. J Neurosci. 2004;24:2458–2464
  86. Perry VH, Cunningham C, Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol. 2007;7:161–167
  87. Nguyen MD, D'Aigle T, Gowing G, Julien JP, Rivest S. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J Neurosci. 2004;24:1340–1349
  88. Plata-Salamán CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Romanovitch AE, et al. 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
  89. Zimmer LA, Ennis M, Shipley MT. Soman-induced seizures rapidly activate astrocytes and microglia in discrete brain regions. J Comp Neurol. 1997;378:482–492
  90. Avignone E, Ulmann L, Levavasseur F, Rassendren F, Audinat E. Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci. 2008;28:9133–9144
  91. Mihaly A, Bozoky B. Immunohistochemical localization of extravasated serum albumin in the hippocampus of human subjects with partial and generalized epilepsies and epileptiform convulsions. Acta Neuropathol (Berl). 1984;65:25–34
  92. Oztas B, Kaya M, Kucuk M, Tugran N. Influence of hypoosmolality on the blood-brain barrier permeability during epileptic seizures. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:701–704
  93. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, et al. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci. 2004;24:7829–7836
  94. Tomkins O, Friedman O, Ivens S, Reiffurth C, Major S, Dreier JP, et al. Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiol Dis. 2007;25:367–377
  95. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, et al. TGF-b receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain. 2007;130:535–547
  96. O'Kane RL, Martínez-López I, DeJoseph MR, Viña JR Hawkins & RA. Na(+)-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the bloodbrain barrier. A mechanism for glutamate removal. J Biol Chem. 1999;274:31891–31895
  97. Grant GA, Meno JR, Nguyen TS, Stanness KA, Janigro D, Winn RH. Adenosine-induced modulation of excitatory amino acid transport across isolated brain arterioles. J Neurosurg. 2003;98:554–560
  98. Oliveira MS, Furian AF, Royes LF, Fighera MR, Fiorenza NG, Castelli M, et al. Cyclooxygenase-2/PGE2 pathway facilitates pentylenetetrazol-induced seizures. Epilepsy Res. 2008;79:14–21
  99. Holtman L, van Vliet EA, van Schaik R, Queiroz CM, Aronica E, Gorter JA. Effects of SC58236, a selective COX-2 inhibitor, on epileptogenesis and spontaneous seizures in a rat model for temporal lobe epilepsy. Epilepsy Res. 2009;84:56–66
  100. Rosi S, Ramirez-Amaya V, Vazdarjanova A, Esparza EE, Larkin PB, Fike JR, et al. Accuracy of hippocampal network activity is disrupted by neuroinflammation: rescue by memantine. Brain. 2009;

PII: S0022-510X(10)00250-9

doi: 10.1016/j.jns.2010.06.002

Journal of the Neurological Sciences
Volume 296, Issue 1 , Pages 1-6 , 15 September 2010

Article Tools

* Image Usage & Resolution