Are developmental dysplastic lesions epileptogenic?

Epilepsia

Volumn 53, Issue SUPPL. 1, 2012, Pages 35-44

  Schwartzkroin, Philip A ^a   Wenzel, H Jürgen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Eker rat; Granule cell dispersion; Methylazoxymethanol; Nodular heterotopia; p35 knockout mouse; Tuber

Indexed keywords

METHYLAZOXYMETHANOL;

BRAIN NERVE CELL; CELL MIGRATION; CORTICAL DYSPLASIA; CYTOPATHOLOGY; DENTATE GYRUS; DNA DAMAGE; EKER RAT; ELECTROENCEPHALOGRAM; EPILEPTOGENESIS; EXPERIMENTAL MODEL; GENE; GENE MUTATION; HIPPOCAMPUS; HUMAN; KNOCKOUT MOUSE; NONHUMAN; P35 GENE; PRIORITY JOURNAL; RAT STRAIN; REVIEW; TUBEROUS SCLEROSIS; WILD TYPE;

ANIMALS; CARCINOGENS; DISEASE MODELS, ANIMAL; EPILEPSY; FEMALE; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; METHYLAZOXYMETHANOL ACETATE; MICE; MICE, KNOCKOUT; PHOSPHOTRANSFERASES; PREGNANCY; RATS; TUBEROUS SCLEROSIS;

EID: 84861390501     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2012.03473.x     Document Type: Review

References (76)

1. Aboian MS, Wong-Kisiel LC, Rank M, Wetjen NM, Wirrell EC, Witte RJ,. (2011) SISCOM in children with tuberous sclerosis complex-related epilepsy. Pediatr Neurol 45: 83-88.
2. Albertson AJ, Yang J, Hablitz JJ,. (2011) Decreased hyperpolarization- activated currents in Layer V pyramidal neurons enhances excitability in focal cortical dysplasia. J Neurophysiol 106: 2189 -2200.
3. Andre VM, Cepeda C, Vinters HV, Huynh M, Mathern GW, Levine MS,. (2010) Interneurons, GABA(A) currents, and subunit composition of the GABA(A) receptor in type I and type II cortical dysplasia. Epilepsia 51 (Suppl. 3): 166-170.
4. Aronica E, Zurolo E, Iyer A, de Groot M, Anink J, Carbonell C, van Vliet EA, Baayen JC, Boison D, Gorter JA,. (2011) Upregulation of adenosine kinase in astrocytes in experimental and human temporal lobe epilepsy. Epilepsia 52: 1645-1655.
5. Avoli M, Bernasconi A, Mattia D, Olivier A, Hwa GG,. (1999) Epileptiform discharges in the human dysplastic neocrotex: in vitro physiology and pharmacology. Ann Neurol 46: 816-826.
6. 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.
7. Baraban SC, Schwartzkroin PA,. (1996) Flurothyl seizure susceptibility in rats following prenatal methylazoxymethanol treatment. Epilepsy Res 23: 189-194.
8. Blümcke I, Schewe JC, Normann S, Brustle O, Schramm J, Elger CE, Wiestler OD,. (2001) Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy. Hippocampus 11: 311-321.
9. Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R,. (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc task force of the ILAE Diagnostic Methods Commission. Epilepsia 52: 158-174.
10. Boonyapisit K, Najm I, Klem G, Ying Z, Burrier C, LaPresto E, Nair D, Bingaman W, Prayson R, Luders H,. (2003) Epileptogenicity of focal malformations due to abnormal cortical development: direct electrocorticographic- histopathologic correlations. Epilepsia 44: 69-76.
11. Calcagnotto ME, Paredes MF, Tihan T, Barbaro NM, Baraban SC,. (2005) Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia. J Neurosci 25: 9649-9657.
12. Castro PA, Pleasure SJ, Baraban SC,. (2002) Hippocampal heterotopia with molecular and electrophysiological properties of neocortical neurons. Neuroscience 114: 961-972.
13. Cepeda C, Hurst RS, Flores-Hernández J, Hernández- Echeagaray E, Klapstein GJ, Boylan MK, Calvert CR, Jocoy EL, Nguyen OK, André VM, Vinters HV, Ariano MA, Levine MS, Mathern GW,. (2003) Morphological and electrophysiological characterization of abnormal cell types in pediatric cortical dysplasia. J Neurosci Res 72: 472-486.
14. Cepeda C, André VM, Yamazaki I, Hauptman JS, Chen JY, Vinters HV, Mathern GW, Levine MS,. (2010) Comparative study of cellular and synaptic abnormalities in brain tissue samples from pediatric tuberous sclerosis complex and cortical dysplasia type II. Epilepsia 51 (Suppl. 3): 160-165.
15. Chae T, Kwon YT, Bronson R, Dikkes P, Li E, Tsai L-H,. (1997) Mice lacking p35, a neuronal specific activator of cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18: 29-42.
16. Chassoux F, Rodrigo S, Semah F, Beuvon F, Landre E, Devaux B, Turak B, Mellerio C, Meder JF, Roux FX, Daumas-Duport C, Merlet P, Dulac O, Chiron C,. (2010) FDG-PET improves surgical outcome in negative MRI-Yaylor-type focal cortical dysplasias. Neurology 75: 2168-2175.
17. Chassoux F, Landre E, Mellerio C, Turak B, Mann MW, Daumas-Duport C, Chiron C, Devaux B,. (2012) Type II focal cortical dysplasia: electro-clinical phenotype and surgical outcome related to imaging. Epilepsia 53: 349-358.
18. Chevassus-au-Louis N, Rafiki A, Jorquera I, Ben-Ari Y, Represa A,. (1998) Neocortex in the hippocampus: an anatomical and functional study of CA1 heterotopias after prenatal treatment with methylazoxymethanol in rats. J Comp Neurol 394: 520-536.
19. Chevassus-au-Louis N, Baraban SC, Gaiarsa JL, Ben-Ari Y,. (1999a) Cortical malformations and epilepsy: new insights from animal models. Epilepsia 40: 811-1821.
20. Chevassus-au-Louis N, Jorquera I, Ben-Ari Y, Represa A,. (1999b) Abnormal connections in the malformed cortex of rats with prenatal treatment with methylazoxymethanol may support hyperexcitability. Dev Neurosci 21: 385-392.
21. Colacitti C, Sancini G, Franceschetti S, Cattabeni F, Avanzini G, Spreafico R, DiLuca M, Battaglia G,. (1998) Altered connections between neocortical and heterotopic areas in methylazoxymethanol-treated rat. Epilepsy Res 32: 49-62.
22. Curatolo P, Verdecchia M, Mombardieri R,. (2002) Tuberous sclerosis complex: a review of neurological aspects. Eur J Paediatr Neurol 6: 15-23.
23. Dabora SL, Franz DN, Ashwal S, Sagalowsky A, DiMario FJ Jr, Miles D, Cutler D, Krueger D, Uppot RN, Rabenou R, Camposano S, Paolini J, Fennessy F, Lee N, Woodrum C, Manola J, Garber J, Thiele EA,. (2011) Multicenter phase 2 trial of sirolimus for tuberous sclerosis: kidney angiomyolipomas and other tumors regress and VEGF-D levels decrease. PLoS ONE 6: e23379.
24. D'Antuono M, Louvel J, Kohling R, Mattia D, Bernasconi A, Olivier A, Turak B, Devaux A, Pumain R, Avoli M,. (2004) GABA(A) receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 127: 1626-1640.
25. Duveau V, Madhusudan A, Caleo M, Knuesel I, Fritschy JM,. (2010) Impaired reelin processing and secretion by Cajal-Retzius cells contributes to granule cell dispersioin in a mouse model of temporal lobe epilepsy. Hippocampus 21: 935-944.
26. Feliciano DM, Su T, Lopez J, Platel JC, Bordey A,. (2011) Single-cell Tsc1 knockout during corticogenesis generates tuber-like lesions and reduces seizure threshold in mice. J Clin Invest 121: 1596-1607.
27. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA,. (1995) Physiologic and morphologic charactersitics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36: 543-558.
28. Franz DN, Leonard J, Tudor C, Chuck G, Care M, Sethuraman G, Dinopoulos A, Thomas G, Crone KR,. (2006) Rapamycin causes regression of astrocytomas in tuberous sclerosis complex. Ann Neurol 59: 490-498.
29. Frotscher M, Chai X, Bock HH, Haas CA, Forster E, Zhao S,. (2009) Role of reelin in the development and maintenance of cortical lamination. J Neural Transm 116: 1451-1455.
30. Garbelli R, Zucca I, Milesi G, Mastropeitro A, D'Incerti L, Tassi L, Colombo N, Marras C, Villani F, Minati L, Spreafico R,. (2011) Combined 7-T MRI and histopathologic study of normal and dysplastic samples from patients with TLE. Neurology 76: 1177-1185.
31. Guerrini R,. (2005) Genetic malformations of the cerebral cortex and epilepsy. Epilepsia 46 (Suppl. 1): 32-37.
32. Haas CA, Frotscher M,. (2010) Reelin deficiency causes granule cell dispersion in epilepsy. Exp Brain Res 200: 141-149.
33. Harrington EP, Moddel 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. Jacobs KM, Hwang BJ, Prince DA,. (1999) Focal epleptogenesis in a rat model of polymicrogyria. J Neurophysiol 81: 159-173.
35. Jones DL, Baraban SC,. (2009) Inhibitory inputs to hippocampal interneurons are reorganized in Lis1 mutant mice. J Neurophysiol 102: 648-658.
36. 11C]methyl-L-tryptophan positron emission tomography (PET). J Child Neurol 20: 429-438.
37. Knight LS, Wenzel HJ, Schwartzkroin PA,. (2012) Inhibition and interneuron distribution in the dentate gyrus of p35 knockout mice. Epilepisa 53(Suppl. 1): 161-179.
38. Koh S, Jayakar P, Dunoyer C, Whiting SE, Resnick TJ, Alvarez LA, Morrison G, Ragheb J, Prats A, Dean P, Gillman J, Duchowny MS,. (2000) Epilepsy surgery in children with tuberous sclerosis complex: presurgical evaluation and outcome. Epilepsia 41: 1206-1213.
39. Lerner JT, Salamon N, Hauptman JS, Velasco TR, Hemb M, Wu JY, Sankar R, Donald Shields W, Engel J Jr, Fried I, Cepeda C, Andre VM, Levine MS, Miyata H, Yong WH, Vinters HV, Mathern GW,. (2009) Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: a critical review and the UCLA experience. Epilepsia 50: 1310-1335.
40. Madhavan D, Weiner HL, Carlson C, Devinsky O, Kuzniecky R,. (2007) Local epileptogenic networks in tuberous sclerosis complex: a case review. Epilepsy Behav 11: 140-146.
41. Major P, Rakowski S, Simon MV, Cheng M-L, Eskandar E, Baron J, Leeman BA, Frosch MP, Thiele EA,. (2009) Are cortical tubers epileptogenic? Evidence from electrocorticography. Epilepsia 50: 147-154.
42. Moddel G, Jacobson B, Ying Z, Janigro D, Bingaman W, Gonzalez-Marinez J, Kellinghaus C, Prayson RA, Najm I,. (2005) The NMDA receptor NR2B subunit contributes to epileptogenesis in human cortical dysplasia. Brain Res 1046: 10-23.
43. Patel LS, Wenzel HJ, Schwartzkroin PA,. (2004) Physiological and morphological characterizationof dentate granule cells in the p35 knockout mouse hippocampus: evidence for an epileptic circuit. J Neurosci, 24: 9005-9014.
44. Pierce JP, McCloskey DP, Scharfman HE,. (2011) Morphometry of hilar ectopic granule cells in the rat. J Comp Neurol 519: 1196-1218.
45. Poluch S, Jablonska B, Juliano SL,. (2008) Alteration of interneuron migration in a ferret model of cortical dysplasia. Cereb Cortex 18: 78-92.
46. Roper N,. (2009) Surgical treatment of the extratemporal epilepsies. Epilepsia 50 (Suppl. 8): 69-74.
47. Roper SN, Eisenschenk S, King MA,. (1999) Reduced density of parvalbumin- and calbindin D28-immunoreactive neurons in experimental cortical dysplasia. Epilepsy Res 37: 63-71.
48. Sarkisian MR, Rattan S, D'Mello SR, LoTurco JJ,. (1999) Characterization of seizures in the flathead rat: a new genetic model of epilepsy in early postnatal development. Epilepsia 40: 394-400.
49. Sarkisian MR, Frenkel M, Li W, Oborski JA, LoTurco JJ,. (2001) Altered interneuron development in the cerebral cortex of the flathead mutant. Cereb Cortex 11: 734-743.
50. Scharfman H, Goodman J, McCloskey D,. (2007) Ectopic granule cells of the rat dentate gyrus. Dev Neurosci 29: 14-27.
51. Schwartzkroin PA, Roper SN, Wenzel HJ,. (2004) Cortical dysplasia and epilepsy: animal models. Adv Exp Med Biol 548: 145-174.
52. Sheen VL, Jansen A, Chen MH, Parrini E, Morgan T, Ravenscroft R, Ganesh V, Underwood T, Wiley J, Leventer R, Vaid RR, Ruiz DE, Hutchins GM, Menasha J, Willner J, Geng Y, Gripp KW, Nicholson L, Berry-Kravis E, Bodell A, Apse K, Hill RS, Dubeau F, Andermann F, Barkovich J, Andermann E, Shugart YY, Thomas P, Viri M, Veggiotti P, Robertson S, Guerrini R, Walsh CA,. (2005) Filamin A mutations cause periventricular nodular heterotopia with Ehlers-Danlos syndrome. Neurology 64: 254-2562.
53. Sosunov AA, Wu X, Weiner HL, Mikell CG, Goodman RR, Crino PD, McKhann GM 2nd,. (2008) Tuberous sclerosis: a primary pathology of astrocytes? Epilepsia 49 (Suppl. 2): 53-62.
54. Tassi L, Colombo N, Garbelli R, Francione S, LoRusso 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: 719-732.
55. Tsai L-H, Delalle I, Caviness JS Jr, Chae T, Harlow E,. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371: 419-423.
56. Tschuluun N, Wenzel HJ, Katleba K, Schwartzkroin PA,. (2005) Initiation and spread of epileptiform discharges in the methylazoxymethanol acetate rat model of cortical dysplasia: functional and structural connectivity between CA1 heterotopia and hippocampus/neocortex. Neuroscience 133: 327-342.
57. Tschuluun N, Wenzel HJ, Schwartzkroin PA,. (2007) Irradiation exacerbates cortical cytopathology in the Eker rat model of Tuberous Sclerosis Complex, but does not induce hyperexcitability. Epilepsy Res 73: 53-64.
58. Tschuluun N, Wenzel HJ, Doisy ET, Schwartzkroin PA,. (2011) Initiation of epileptiform activity in a rat model of periventricular nodular heterotopia. Epilepsia 52: 2304-2314.
59. Uhlmann EJ, Wong M, Baldwin RL, Bajenaru ML, Onda H, Kwiatkowski DJ, Yamada K, Gutmann DH,. (2002) Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann Neurol 52: 285-296.
60. Urbach H, Scheffler B, Heinrichsmeier T, von Oertzen J, Kral T, Wellmer J, Schramm J, Wiestler OK, Blumcke I,. (2002) Focal cortical dysplasia of Taylor's balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome. Epilepsia 43: 33-40.
61. Wagner J, Urbach H, Neihusmann P, von Lehe M, Elger CE, Wellmer J,. (2011) Focal cortical dysplasia type IIb: completeness of cortical, not subcortical resection is necessary for seizure freedom. Epilepsia 52: 1418-1424.
62. Wang Y, Greenwood JS, Calcagnotto ME, Kirsch HE, Barbaro NM, Baraban SC,. (2007) Neocortical hyperexcitability in a human case of tuberous sclerosis complex and mice lacking neuronal expression of TSC1. Ann Neurol 61: 139-152.
63. Weiner HL,. (2004) Tuberous sclerosis and multiple tubers: localizing the epileptogenic zone. Epilepsia, 45 (Suppl. 4): 41-42.
64. Wenzel HJ, Schwartzkroin PA,. (2006) Morphologic approaches to the characterization of epilepsy models. In, Pitkanen A, Schwartzkroin PA, Moshe SL, (Eds) Models of seizures and epilepsy. Elsevier/Academic Press, San Diego, pp. 629-651.
65. Wenzel HJ, Robbins CA, Tsai L-H, 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.
66. Wenzel HJ, Patel LS, Robbins CA, Emmi A, Yeung RS, Schwartzkroin PA,. (2004) Morphology of cerebral lesions in the Eker rat model of tuberous sclerosis. Acta Neuropathol 108: 97-108.
67. Wenzel HJ, Tamse CT, Schwartzkroin PA,. (2006) Dentate development in organotypic hippocampal slice cultures from p35 knock-out mice. Dev Neurosci 29: 99-112.
68. Wierschke S, Lehmann TN, Dehnicke C, Horn P, Nitsch R, Deisz RA,. (2010) Hyperpolarization -activated cation currents in human epileptogenic neocortex. Epilepsia 51: 404-414.
69. Wong M,. (2010) Mammalian target of rapamycin (mTOR) inhibition as a potential antiepileptogenic therapy: from tuberous sclerosis to common acquired epilepsies. Epilepsia 51: 27-36.
70. Xiang H, Chen HX, Yu XX, King MA, Roper SN,. (2006) Reduced excitatory drive in interneurons in an animal model of cortical dysplasia. J Neurophysiol 96: 569-578.
71. Yeung RS, Xiao GH, Everitt JI, Jin F, Walker CL,. (1995) Allelic loss at the tuberous sclerosis 2 locus in spontaneous tumors in the Eker rat. Mol Carcinog 14: 28-36.
72. Yeung RS, Katsetos CD, Klein-Szanto A,. (1997) Subependymal astrocytic hamartomas in the Eker rat model of tuberous sclerosis. Am J Pathol 151: 1477-1486.
73. Zeng LH, Bero AW, Zhang B, Holtzman DM, Wong M,. (2010) Modulation of astrocyte glutamate transporters decreases seizures in a mouse model of tuberous sclerosis complex. Neurobiol Dis 37: 764-771.
74. Zhou FW, Roper SN,. (2011) Altered firing fates and patterns in interneurons in experimental cortical dysplasia. Cereb Cortex 21: 1645-1658.
75. Zhu WJ, Roper SN,. (2000) Reduced inhibition an animal model of cortical dysplasia. J Neurosci 20: 8925-8931.
76. Zilles K, Qu M, Schleicher A, Luhmann HJ,. (1998) Characterization of neuronal migration disorders in neocortical structures: quantitative receptor autoradiography of ionotropic glutamate, GABA(A) and GABA(B) receptors. Eur J Neurosci 10: 3095-3106.