Role of cortical dysplasia in epileptogenesis following prolonged febrile seizure

Epilepsia

Volumn 51, Issue 9, 2010, Pages 1809-1819

  Park, Kyung Il ^a   Chu, Kon ^b,c,d   Jung, Keun Hwa ^b,d   Kim, Jin Hee ^b   Kang, Kyung Muk ^b   Lee, Soon Tae ^b,d   Park, Hee Kwon ^b,d   Kim, Manho ^b,d   Lee, Sang Kun ^b,c,d   Roh, Jae Kyu ^b,d  

^a Inje University College of Medicine   (South Korea)

^b Adult Stem Cell Research   (South Korea)

^c Seoul National University Hospital   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

Cortical dysplasia; Epileptogenesis; Febrile convulsion; Hippocampal sclerosis; Synaptogenesis; Temporal lobe epilepsy

Indexed keywords

METHYLAZOXYMETHANOL; SODIUM CHLORIDE; METHYLAZOXYMETHANOL ACETATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DENSITY; CONTROLLED STUDY; CORTICAL DYSPLASIA; DENTATE GYRUS; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAPHY; EPILEPTOGENESIS; FEBRILE CONVULSION; FEMALE; GLIA CELL; GLIOSIS; HIPPOCAMPAL SCLEROSIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MORPHOLOGICAL ADAPTATION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RAT; RISK FACTOR; SEIZURE; SPONTANEOUS RECURRENT SEIZURE; SYNAPTOGENESIS; TEMPORAL LOBE EPILEPSY; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; SCLEROSIS; SEIZURES, FEBRILE; SPRAGUE DAWLEY RAT; STATISTICS AND NUMERICAL DATA; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; METHYLAZOXYMETHANOL ACETATE; MOSSY FIBERS, HIPPOCAMPAL; RATS; RATS, SPRAGUE-DAWLEY; SCLEROSIS; SEIZURES, FEBRILE; SYNAPSES;

EID: 77956319446     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2010.02676.x     Document Type: Article

References (72)

1. Amano S, Ihara N, Uemura S, Yokoyama M, Ikeda M, Serikawa T, Sasahara M, Kataoka H, Hayase Y, Hazama F 1996) Development of a novel rat mutant with spontaneous limbic-like seizures. Am J Pathol 149 : 329 336.
2. Baraban SC, Schwartzkroin PA 1995) Electrophysiology of CA1 pyramidal neurons in an animal model of neuronal migration disorders: prenatal methylazoxymethanol treatment. Epilepsy Res 22 : 145 156.
3. Baraban SC, Schwartzkroin PA 1996) Flurothyl seizure susceptibility in rats following methylazoxymethanol treatment. Epilepsy Res 23 : 189 194.
4. Baraban SC, Wenzel HJ, Hochman DW, Schwartzkroin PA 2000) Characterization of heterotopic cell clusters in the hippocampus of rats exposed to methylazoxymethanol in utero. Epilepsy Res 39 : 87 102.
5. Bender RA, Dubé C, Gonzalez-Vega R, Mina EW, Baram TZ 2003) Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures. Hippocampus 13 : 399 412.
6. Brandt C, Ebert U, Löscher W 2004) Epilepsy induced by extended amygdala-kindling in rats: lack of clear association between development of spontaneous seizures and neuronal damage. Epilepsy Res 62 : 135 156.
7. Brewster A, Bender RA, Chen Y, Dubé C, Eghbal-Ahmadi M, Baram TZ 2002) Developmental febrile seizures modulate hippocampal gene expression of hyperpolarization-activated channels in an isoform- and cell-specific manner. J Neurosci 22 : 4591 4599.
8. Castro PA, Cooper EC, Lowenstein DH, Baraban SC 2001) Hippocampal heterotopia lack functional Kv4.2 potassium channels in the methylazoxymethanol model of cortical malformations and epilepsy. J Neurosci 21 : 6626 6634.
9. Chang YC, Kuo YM, Huang AM, Huang CC 2005) Repetitive febrile seizures in rat pups cause long-lasting deficits in synaptic plasticity and NR2A tyrosine phosphorylation. Neurobiol Dis 18 : 466 475.
10. Chen ZL, Strickland S 1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91 : 917 925.
11. Chevassus-au-Louis N, Ben-Ari Y, Vergnes M 1998a) Decreased seizure threshold and more rapid rate of kindling in rats with cortical malformation induced by prenatal treatment with methylazoxymethanol. Brain Res 812 : 252 255.
12. Chevassus-Au-Louis N, Congar P, Represa A, Ben-Ari Y, Gaïarsa JL 1998b) Neuronal migration disorders: heterotopic neocortical neurons in CA1 provide a bridge between the hippocampus and the neocortex. Proc Natl Acad Sci USA 95 : 10263 10268.
13. Chu K, Jung KH, Lee ST, Kim JH, Kang KM, Kim HK, Lim JS, Park HK, Kim M, Lee SK, Roh JK 2008) Erythropoietin reduces epileptogenic processes following status epilepticus. Epilepsia 49 : 1723 1732.
14. Coggeshall RE, Lekan HA 1996) Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364 : 6 15.
15. Colacitti C, Sancini G, DeBiasi S, Franceschetti S, Caputi A, Frassoni C, Cattabeni F, Avanzini G, Spreafico R, Di Luca M, Battaglia G 1999) Prenatal methylazoxymethanol treatment in rats produces brain abnormalities with morphological similarities to human developmental brain dysgeneses. J Neuropathol Exp Neurol 58 : 92 106.
16. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M, Bernard C 2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4 : 52 62.
17. Cronin J, Dudek FE 1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 22 : 181 184.
18. Dubé C, Yu H, Nalcioglu O, Baram TZ 2004) Serial MRI after experimental febrile seizures: altered T2 signal without neuronal death. Ann Neurol 56 : 709 714.
19. Dubé C, Brunson KL, Eghbal-Ahmadi M, Gonzalez-Vega R, Baram TZ 2005) Endogenous neuropeptide Y prevents recurrence of experimental febrile seizures by increasing seizure threshold. J Mol Neurosci 25 : 275 284.
20. Dubé C, Richichi C, Bender RA, Chung G, Litt B, Baram TZ 2006) Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 129 : 911 922.
21. Dudek FE, Sutula TP 2007) Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res 163 : 755 773.
22. Falconer MA, Serafetinides E, Corsellis J 1964) Etiology and pathogenesis of temporal lobe epilepsy. Arch Neurol 10 : 233 248.
23. Falconer MA 1971) Genetic and related aetiological factors in temporal lobe epilepsy. Epilepsia 12 : 13 31.
24. Fauser S, Huppertz HJ, Bast T, Strobl K, Pantazis G, Altenmueller DM, Feil B, Rona S, Kurth C, Rating D, Korinthenberg R, Steinhoff BJ, Volk B, Schulze-Bonhage A 2006) Clinical characteristics in focal cortical dysplasia: a retrospective evaluation in a series of 120 patients. Brain 129 : 1907 1916.
25. Fleck MW, Hirotsune S, Gambello MJ, Phillips-Tansey E, Suares G, Mervis RF, Wynshaw-Boris A, McBain CJ 2000) Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J Neurosci 20 : 2439 2450.
26. French JA, Williamson PD, Thadani VM, Darcey TM, Mattson RH, Spencer SS, Spencer DD 1993) Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann Neurol 34 : 774 780.
27. Germano IM, Zhang YF, Sperber EL, Moshé SL 1996) Neuronal migration disorders increase susceptibility to hyperthermia induced seizures in developing rats. Epilepsia 379 : 902 910.
28. Germano IM, Sperber EF 1998) Transplancentally induced neuronal migration disorders: an animal model for the study of the epilepsies. J Neurosci Res 51 : 473 488.
29. Germano IM, Sperber EF, Ahuja S, Moshe SL 1998) Evidence of enhanced kindling and hippocampal neuronal injury in immature rats with neuronal migration disorders. Epilepsia 39 : 1253 1260.
30. Gomez-Anson B, Thom M, Moran N, Stevens J, Scaravili F 2000) Imaging and radiographic-pathological correlation in histologically-proven cases of focal cortical dysplasia and other glial and neuronoglial malformative lesions in adults. Neuroradiology 42 : 157 167.
31. Grabs D, Bergmann M, Schuster T, Fox PA, Brich M, Gratzl M 1994) Differential expression of synaptophysin and synaptoporin during pre and postnatal development of the rat hippocampal network. Eur J Neurosci 6 : 1765 1771.
32. Hamati-Haddad A, Abou-Khalil B 1998) Epilepsy diagnosis and localization in patients with antecedent childhood febrile convulsions. Neurology 50 : 917 922.
33. Harrington EP, Möddel G, Najm IM, Baraban SC 2007) Altered glutamate receptor - transporter expression and spontaneous seizures in rats exposed to methylazoxymethanol in utero. Epilepsia 48 : 158 168.
34. Hauser WA 1997) Incidence and prevalence. In Engel J Jr%., Pedley TA (Eds) Epilepsy: a comprehensive textbook. Lippincott-Raven, Philadelphia, pp. 47 57.
35. Hesdorffer DC, Chan S, Tian H, Allen Hauser W, Dayan P, Leary LD, Hinton VJ 2008) Are MRI-detected brain abnormalities associated with febrile seizure type? Epilepsia 49 : 765 771.
36. Johnson EW, Dubovsky J, Rich SS, O'Donovan CA, Orr HT, Anderson VE, Gil-Nagel A, Ahmann P, Dokken CG, Schneider DT, Weber JL 1998) Evidence for a novel gene for familial febrile convulsions, FEB2, linked to chromosome 19p in an extended family from the Midwest. Hum Mol Genet 7 : 63 67.
37. Jung KH, Chu K, Kim M, Jeong SW, Song YM, Lee ST, Kim JY, Lee SK, Roh JK 2004) Continuous cytosine-b-d-arabinofuranoside infusion reduces ectopic granule cells in adult rat hippocampus with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Eur J Neurosci 19 : 3219 3226.
38. Kugler SL, Stenroos ES, Mandelbaum DE, Lehner T, McKoy VV, Prossick T, Sasvari J, Swannick K, Katz J, Johnson WG 1998) Hereditary febrile seizures: phenotype and evidence for a chromosome 19p locus. Am J Med Genet 79 : 354 361.
39. Lévesque MF, Nakasato N, Vinters HV, Babb TL 1991) Surgical treatment of limbic epilepsy associated with extrahippocampal lesions: the problem of dual pathology. J Neurosurg 75 : 364 370.
40. Lynch M, Sutula T 2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83 : 693 704.
41. Manford M, Hart YM, Sander JW, Shorvon SD 1992) National General Practice Study of Epilepsy (NGPSE): partial seizure patterns in a general population. Neurology 42 : 1911 1917.
42. Mathern GW, Cifuentes F, Leite JP, Pretorius JK, Babb TL 1993) Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol 87 : 326 339.
43. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK 1995) The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118 : 105 118.
44. Mohamed A, Wyllie E, Ruggieri P, Kotagal P, Babb T, Hilbig A, Wylie C, Ying Z, Staugaitis S, Najm I, Bulacio J, Foldvary N, Lüders H, Bingaman W 2001) Temporal lobe epilepsy due to hippocampal sclerosis in pediatric candidates for epilepsy surgery. Neurology 56 : 1643 1649.
45. Morimoto K, Fahnestock M, Racine RJ 2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73 : 1 60.
46. Najm IM, Ying Z, Babb T, Mohamed A, Hadam J, LaPresto E, Wyllie E, Kotagal P, Bingaman W, Foldvary N, Morris H, Lüders HO 2000) Epileptogenicity correlated with increased N-methyl-D-aspartate receptor subunit NR2A/B in human focal cortical dysplasia. Epilepsia 41 : 971 976.
47. Nelson KB, Ellenberg JH 1976) Predictors of epilepsy in children who have experienced febrile seizures. N Engl J Med 295 : 1029 1033.
48. Nohria V, Lee N, Tien RD, Heinz ER, Smith JS, DeLong GR, Skeen MB, Resnick TJ, Crain B, Lewis DV 1994) Magnetic resonance imaging evidence of hippocampal sclerosis in progression: a case report. Epilepsia 35 : 1332 1336.
49. Okazaki MM, Evenson DA, Nadler JV 1995) Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 352 : 515 534.
50. Peiffer A, Thompson J, Charlier C, Otterud B, Varvil T, Pappas C, Barnitz C, Gruenthal K, Kuhn R, Leppert M 1999) A locus for febrile seizures (FEB3) maps to chromosome 2q23-24. Ann Neurol 46 : 671 678.
51. Porter BE, Judkins AR, Clancy RR, Duhaime A, Dlugos DJ, Golden JA 2003) Dysplasia: a common finding in intractable pediatric temporal lobe epilepsy. Neurology 61 : 365 368.
52. Proper EA, Oestreicher AB, Jansen GH, Veelen CW, van Rijen PC, Gispen WH, de Graan PN 2000) Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmacoresistant temporal lobe epilepsy. Brain 123 : 19 30.
53. Sancini G, Franceschetti S, Battaglia G, Colacitti C, Di Luca M, Spreafico R, Avanzini G 1998) Dysplastic neocortex and subcortical heterotopias in methylazoxymethanol-treated rats: an intracellular study of identified pyramidal neurones. Neurosci Lett 246 : 181 185.
54. Scantlebury MH, Ouellet PL, Psarropoulou C, Carmant L 2004) Freeze lesion-induced focal cortical dysplasia predisposes to atypical hyperthermic seizures in the immature rat. Epilepsia 45 : 592 600.
55. Scantlebury MH, Gibbs SA, Foadjo B, Lema P, Psarropoulou C, Carmant L 2005) Febrile seizures in the predisposed brain: a new model of temporal lobe epilepsy. Ann Neurol 58 : 41 49.
56. Shinnar S 1998) Prolonged febrile seizures and mesial temporal sclerosis. Ann Neurol 43 : 411 412.
57. Singec I, Knoth R, Ditter M, Hagemeyer CE, Rosenbrock H, Frotscher M, Volk B 2002) Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. J Comp Neurol 452 : 139 153.
58. Sisodiya SM, Free SL, Stevens JM, Fish DR, Shorvon SD 1995) Widespread cerebral structural changes in patients with cortical dysgenesis and epilepsy. Brain 118 : 1039 1050.
59. Smith BN, Dudek FE 2001) Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol 85 : 1 9.
60. Smyth MD, Barbaro NM, Baraban SC 2002) Effects of antiepileptic drugs on induced epileptiform activity in the rat model of dysplasia. Epilepsy Res 50 : 251 264.
61. Sperber EF, Haas KZ, Stanton PK, Moshe SL 1991) Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Brain Res Dev Brain Res 60 : 88 93.
62. Sutula T, Zhang P, Lynch M, Sayin U, Golarai G, Rod R 1998) Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J Comp Neurol 390 : 578 594.
63. Takase K, Shigeto H, Suzuki SO, Kikuchi H, Ohyagi Y, Kira J 2008) Prenatal freeze lesioning produces epileptogenic focal cortical dysplasia. Epilepsia 49 : 997 1010.
64. Tassi L, Colombo N, Garbelli R, Francione S, Lo Russo G, Mai R, Cardinale F, Cossu M, Ferrario A, Galli C, Bramerio M, Citterio A, Spreafico R 2002) Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 125 : 1719 1732.
65. Toth Z, Yan XX, Haftoglou S, Ribak CE, Baram TZ 1998) Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model. J Neurosci 18 : 4285 4294.
66. Tsai ML, Leung LS 2006) Decrease of hippocampal GABA B receptor-mediated inhibition after hyperthermia-induced seizures in immature rats. Epilepsia 47 : 277 287.
67. VanLandingham KE, Heinz ER, Cavazos JE, Lewis DV 1998) Magnetic resonance imaging evidence of hippocampal injury after prolonged focal febrile convulsions. Ann Neurol 43 : 413 426.
68. Wallace SJ 1972) Aetiological aspects of febrile convulsions: pregnancy and perinatal factors. Arch Dis Child 47 : 171 178.
69. Wallace RH, Berkovic SF, Howell RA, Sutherland GR, Mulley JC 1996) Suggestion of a major gene for familial febrile convulsions mapping to 8q13-21. J Med Genet 33 : 308 312.
70. Wenzel HJ, Robbins CA, Tsai LH, Schwartzkroin PA 2001) Abnormal morphological and functional organization of the hippocampus in a p35 mutant model of cortical dysplasia associated with spontaneous seizures. J Neurosci 21 : 983 998.
71. Wyllie E, Comair YG, Kotagal P, Bulacio J, Bingaman W, Ruggieri P 1998) Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 44 : 740 748.
72. Ying Z, Babb TL, Comair YG, Bingaman W, Bushey M, Touhalisky K 1998) Induced expression of NMDAR2 proteins and differential expression of NMDAR1 splice variants in dysplastic neurons of human epileptic neocortex. J Neuropathol Exp Neurol 57 : 47 62.