Altered spatial distribution of PV-cortical cells and dysmorphic neurons in the somatosensory cortex of BCNU-treated rat model of cortical dysplasia

Epilepsia

Volumn 49, Issue 5, 2008, Pages 872-887

  Moroni, Ramona Frida ^a   Inverardi, Francesca ^a   Regondi, Maria Cristina ^a   Panzica, Ferruccio ^a   Spreafico, Roberto ^a   Frassoni, Carolina ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Cortical dysplasia; Epilepsy; GABAergic neurons; Immunocytochemistry; Rat

Indexed keywords

CALBINDIN; CARMUSTINE; PARVALBUMIN; SM1311 ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORTICAL DYSPLASIA; CYTOARCHITECTURE; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; NERVE CELL LESION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CARMUSTINE; CLASSICAL LISSENCEPHALIES AND SUBCORTICAL BAND HETEROTOPIAS; DISEASE MODELS, ANIMAL; EPILEPSY; FEMALE; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALFORMATIONS OF CORTICAL DEVELOPMENT; MATERNAL-FETAL EXCHANGE; NEURONS; PARVALBUMINS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX;

EID: 43249087976     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2007.01440.x     Document Type: Article

References (79)

1. Acampora D, Mazan S, Avantaggiato V, Barone P, Tuorto F, Lallemand Y, Brulet P, Simeone A 1996) Epilepsy and brain abnormalities in mice lacking the Otx1 gene. Nat Genet 14 : 218 222.
2. Alonso-Nanclares L, Garbelli R, Sola RG, Pastor J, Tassi L, Spreafico R, DeFelipe J 2005) Microanatomy of the dysplastic neocortex from epileptic patients. Brain 128 : 158 173.
3. Barkovich AJ, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns WB 2005) A developmental and genetic classification for malformations of cortical development. Neurology 65 : 1873 1887.
4. Battaglia G, Pagliardini S, Saglietti L, Cattabeni F, Di Luca M, Bassanini S, Setola V 2003) Neurogenesis in cerebral heterotopia induced in rats by prenatal methylazoxymethanol treatment. Cereb Cortex 13 : 736 748.
5. Benardete EA, Kriegstein AR 2002) Increased excitability and decreased sensitivity to GABA in an animal model of dysplastic cortex. Epilepsia 43 : 970 982.
6. 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.
7. Carretta D, Santarelli M, Sbriccoli A, Pinto F, Catini C, Minciacchi D 2004) Spatial analysis reveals alterations of parvalbumin- and calbindin-positive local circuit neurons in the cerebral cortex of mutant mdx mice. Brain Res 1016 : 1 11.
8. Carter SK, Schabel FM, Jr., Broder LE, Johnston TP 1972) 1,3-Bis(2-chloroethyl)-1-nitrosourea (bcnu) and other nitrosoureas in cancer treatment: a review. Adv Cancer Res 16 : 273 332.
9. Caviness VS, Jr., Yorke CH Jr. 1976) Interhemispheric neocortical connections of the corpus callosum in the reeler mutant mouse: a study based on anterograde and retrograde methods. J Comp Neurol 170 : 449 459.
10. Celio MR 1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35 : 375 475.
11. Chen ZF, Schottler F, Bertram E, Gall CM, Anzivino MJ, Lee KS 2000) Distribution and initiation of seizure activity in a rat brain with subcortical band heterotopia. Epilepsia 41 : 493 501.
12. Chevassus-au-Louis N, Jorquera I, Ben-Ari Y, Represa A 1999) Abnormal connections in the malformed cortex of rats with prenatal treatment with methylazoxymethanol may support hyperexcitability. Dev Neurosci 21 : 385-392.
13. Cepeda C, Andre VM, Levine MS, Salamon N, Miyata H, Vinters HV, Mathern GW 2006) Epileptogenesis in pediatric cortical dysplasia: the dysmature cerebral developmental hypothesis. Epilepsy Behav 9 : 219 235.
14. Cipelletti B, Avanzini G, Vitellaro-Zuccarello L, Franceschetti S, Sancini G, Lavazza T, Acampora D, Simeone A, Spreafico R, Frassoni C 2002) Morphological organization of somatosensory cortex in Otx(-/-) mice. Neuroscience 115 : 657 667.
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. Colombo N, Tassi L, Galli C, Citterio A, Lo Russo G, Scialfa G, Spreafico R 2003) Focal cortical dysplasias: MR imaging, histopathologic and clinical correlations in surgically treated patients with epilepsy. Am J Neuroradiol 24 : 724 733.
17. Crino PB, Duhaime AC, Baltuch G, White R 2001) Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia. Neurology 56 : 906 913.
18. D'Arcangelo G 2005) The reeler mouse: anatomy of a mutant. Int Rev Neurobiol 71 : 383 417.
19. DeFelipe J, Garcia SR, Marco P, Del Rio MR, Pulido P, Ramon Y, Cajal S 1993) Selective changes in the microorganization of the human epileptogenic neocortex revealed by parvalbumin immunoreactivity. Cereb Cortex 3 : 39 48.
20. DeFelipe J 1999) Chandelier cells and epilepsy. Brain 122 : 1807 1822.
21. Drabløs F, Feyzi E, Aas PA, Vaagbo CB, Kavli B, Bratlie MS, Pena-Diaz J, Otterlei M, Slupphaug G, Krokan HE 2004) Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair 3 : 1389 1407.
22. Duyckaerts C, Godefroy G, Hauw JJ 1994) Evaluation of neuronal numerical density by Dirichlet tessellation. J Neurosci Methods 51 : 47 69.
23. Duyckaerts C, Godefroy G 2000) Voronoi tessellation to study the numerical density and the spatial distribution of neurones. J Chem Neuroanat 20 : 83 92.
24. Eriksson SH, Free SL, Malmgren K, Nordborg C 2003) Evaluation of nerve cell distribution in cerebral cortex: a proposal for a new method applied to patients with epilepsy. J Neurosci Methods 128 : 151 157.
25. Engel J Jr. 1996) Excitation and inhibition in epilepsy. Can J Neurol Sci 23 : 167 174.
26. Ewend MG, Elbabaa S, Carey LA 2005) Current treatment paradigms for the management of patients with brain metastases. Neurosurgery 57 : S66 S77.
27. Ferrer I 1993) Experimentally induced cortical malformations in rats. Childs Nerv Syst 9 : 403 407.
28. Ferrer I, Alcàntara S, Zùjar MJ, Cinòs C 1993) Structure and pathogenesis of cortical nodules induced by prenatal X-irradiation in the rat. Acta Neuropathol 85 : 205 212.
29. Ferrer I, Olover B, Russi A, Casas R, Rivera R 1994) Parvalbumin and calbindin-D28k immunocytochemistry in human neocortical epileptic foci. J Neurol Sci 123 : 18 25.
30. Frassoni C, Inverardi F, Coco S, Ortino B, Grumelli C, Pozzi D, Verderio C, Matteoli M 2005) Analysis of SNAP-25 immunoreactivity in hippocampal inhibitory neurons during development in culture and in situ. Neuroscience 131 : 813 823.
31. Fleck MW, Hirotsune S, Gambello M, 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.
32. Garbelli R, Munari C, De Biasi S, Vitellaro-Zuccarello L, Galli C, Bramerio M, Mai R, Battaglia G, Spreafico R 1999) Taylor's cortical dysplasia: a confocal and ultrastructural immunohistochemical study. Brain Pathol 9 : 445 461.
33. Garbelli R, Meroni A, Magnaghi G, Beolchi MS, Ferrario A, Tassi L, Bramerio M, Spreafico R 2006) Architectural (Type IA) focal cortical dysplasia and parvalbumin immunostaining in temporal lobe epilepsy. Epilepsia 47 : 1074 1078.
34. Germano IM, Zhang YF, Sperber EF, Moshé SL 1996) Neuronal migration disorders increase susceptibility to hyperthermia-induced seizures in developing rats. Epilepsia 37 : 902 910.
35. Germano IM, Sperber EF 1998) Transplacentally induced neuronal migration disorders: an animal model for the study of the epilepsies. J Neurosci Res 51 : 473 488.
36. Graber KD, Kharazia VK, Parada I, Prince DA 1999) Parvalbumin-containing interneurons are spared in the undercut model of post-traumatic epileptogenesis. Epilepsia 40 (Suppl7 31.
37. Guerrini R, Sicca F, Parmeggiani L 2003) Epilepsy and malformations of the cerebral cortex. Epileptic Disord 5 : S9 S26.
38. Hannan AJ, Servotte S, Katsnelson A, Sisodiya S, Blakemore C, Squier M, Molnár Z 1999) Characterization of nodular neuronal heterotopia in children. Brain 122 : 219 238.
39. 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.
40. Hildebrandt M, Pieper T, Winkler P, Kolodziejczyk D, Holthausen H, Blümcke I 2005) Neuropathological spectrum of cortical dysplasia in children with severe focal epilepsies. Acta Neuropathol 110 : 1 11.
41. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A 1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19 : 333 339.
42. Hoffman SN, Salin PA, Prince DA 1994) Chronic neocortical epileptogenesis in vitro. J Neurophysiol 71 : 1762 1773.
43. Jacobs KM, Gutnick MJ, Price DA 1996) Hyperexcitability in a model of cortical maldevelopment. Cereb Cortex 6 : 514 523.
44. Jacobs KM, Kharazia VN, Prince DA 1999) Mechanisms underlying epileptogenesis in cortical malformations. Epilepsy Res 36 : 165 188.
45. Janota I, Polkey CE 1992) Cortical dysplasia in epilepsy. In Pedley TA, Meldrum BS (Eds) Recent advances in epilepsy. Chuchill Livingstone, London, pp. 37 49.
46. Jansen LA, Uhlmann EJ, Crino PB, Gutmann DH, Wong M 2005) Epileptogenesis and reduced inward rectifier potassium current in tuberous sclerosis complex-1-deficient astrocytes. Epilepsia 46 : 1871 1880.
47. Kellinghaus C, Kunieda T, Ying Z, Pan A, Luders HO, Najm IM 2004) Severity of histopathologic abnormalities and in vivo epileptogenicity in the in utero radiation model of rats is dose dependent. Epilepsia 42 : 1221 1227.
48. Lawson JA, Birchansky S, Pacheco E, Jayakar P, Resnick TJ, Dean P, Duchowny MS 2005) Distinct clinicopathologic subtypes of cortical dysplasia of Taylor. Neurology 64 : 55 61.
49. Lee KS, Schottler F, Collins JL, Lanzino G, Couture D, Rao A, Hiramatsu KI, Goto Y, Hong SC, Caner H, Yamamoto H, Chen ZF, Bertram E, Berr S, Omary R, Scrable H, Jackson T, Goble J, Eisenman L 1997) A genetic animal model of human neocortical heterotopia associated with seizures. J Neurosci 17 : 6236 6242.
50. Marco P, Sola RG, Pulido P, Alijarde MT, Sanchez A, Ramon Y, Cajal S, DeFelipe J 1996) Inhibitory neurons in the human epileptogenic temporal neocortex. An immunocytochemical study. Brain 119 : 1327 1347.
51. Marín-Padilla M, Tsai RJ, King MA, Roper SN 2003) Altered corticogenesis and neuronal morphology in irradiation-induced cortical dysplasia: a Golgi-Cox study. J Neuropathol Exp Neurol 62 : 1129 1143.
52. Mizuguchi M, Takashima S, Yamanouchi H, Nakazato Y, Mitani H, Hino O 2000) Novel cerebral lesions in the Eker rat model of tuberous sclerosis: cortical tuber and anaplastic ganglioglioma. J Neuropathol Exp Neurol 59 : 188 196.
53. Moroni R, Regondi MC, Inverardi F, Garbelli R, Spreafico R, Frassoni C 2005) BCNU-treated rat as a model of cortical dysplasia. In National Congress of the Italian Society for Neuroscience, October 1-4, 2005, Ischia, Italy. p. 647.
54. Palmini A, Najm I, Avanzini G, Babb T, Guerrini R, Foldvary-Schaefer N, Jackson G, Lüders HO, Prayson R, Sprafico R, Vinters HV 2004) Terminology and classification of the cortical dysplasias. Neurology 62 : S2 S8.
55. Pantò MR, Zappalà A, Tuorto F, Cicirata F 2004) Role of the Otx1 gene in cell differentiation of mammalian cortex. Eur J Neurosci 19 : 2893 2902.
56. Patrylo PR, Browning RA, Cranick S 2006) Reeler homozygous mice exhibit enhanced susceptibility to epileptiform activity. Epilepsia 47 : 257 266.
57. Penschuck S, Fladstad P, Didriksen M, Leist M, Michael-Titus AT 2006) Decrease in parvalbumin-expressing neurons in the hippocampus and increased phencyclidine-induced locomotor activity in the rat methylazoxymethanol (MAM) model of schizophrenia. Eur J Neurosci 23 : 279 284.
58. Prince DA, Tseng GF 1993) Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol 69 : 1276 1291.
59. Roberts MR, Bittman K, Li WW, French R, Mitchell B, LoTurco JJ, D'Mello SR 2000) The flathead mutation causes CNS-specific developmental abnormalities and apoptosis. J Neurosci 20 : 2295 2306.
60. Rakic P 1988) Specification of cerebral cortical areas. Science 241 : 170 176.
61. Roper SN 1998) In utero irradiation of rats as a model of human cerebrocortical dysgenesis: a review. Epilepsy Res 32 : 63 74.
62. Roper SN, Eisenschenk S, King MA 1999) Reduced density of parvalbumin- and calbindin D28k-immunoreactive neurons in experimental cortical dysplasia. Epilepsy Res 37 : 63 71.
63. Rosen GD, Press DM, Sherman GF, Galaburda AM 1992) The development of induced cerebrocortical microgyria in the rat. J Neuropathol Exp Neurol 51 : 601 611.
64. Rosen GD, Jacobs KM, Prince DA 1998) Effects of neonatal freeze lesions on expression of parvalbumin in rat neocortex. Cereb Cortex 8 : 753 761.
65. Sánchez MP, Frassoni C, Álvarez-Bolado G, Spreafico R, Fairén A 1992) Distribution of calbindin and parvalbumin in the developing somatosensory cortex and its primordium in the rat: an immunocytochemical study. J Neurocytol 21 : 717 736.
66. 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.
67. Sancini G, Franceschetti S, Lavazza T, Panzica F, Cipelletti B, Frassoni C, Spreafico R, Acampora D, Avanzini G 2001) Potentially epileptogenic dysfunction of cortical NMDA- and GABA-mediated neurotransmission in Otx1-/- mice. Eur J Neurosci 14 : 1065 1074.
68. 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.
69. 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.
70. Schwarz P, Stichel CC, Luhmann HJ 2000) Characterization of neuronal migration disorders in neocortical structures: loss or preservation of inhibitory interneurons? Epilepsia 41 : 781 787.
71. Spreafico R, Pasquier B, Minotti L, Garbelli R, Kahane P, Grand S, Benabid AL, Tassi L, Avanzini G, Battaglia G, Munari C 1998) Immunocytochemical investigation on dysplastic human tissue from epileptic patients. Epilepsy Res 32 : 34 48.
72. Spreafico R, Tassi L, Colombo N, Bramerio SM, Galli C, Garbelli R, Ferrario A, Lo Russo G, Munari C 2000) Inhibitory circuits in human dysplastic tissue. Epilepsia 41 : S168 S173.
73. 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.
74. Thom M, Harding BN, Lin WR, Martinian L, Cross, Sisodiya SM 2003) Cajal-Retzius cells, inhibitory interneuronal populations and neuropeptide Y expression in focal cortical dysplasia and microdysgenesis. Acta Neuropathol 105 : 561 569.
75. Trotter SA, Kapur J, Anzivino MJ, Lee KS 2006) GABAergic synaptic inhibition is reduced before seizure onset in a genetic model of cortical malformation. J Neurosci 26 : 10756 10767.
76. 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.
77. Walker MD, Alexander E Jr., Hunt WE, MacCarty CS, Mahaley MS Jr., Mealey J Jr., Norrell HA, Owens G, Ransohoff J, Wilson CB, Gehan EA, Strike TA 1978) Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial. J Neurosurg 49 : 333 343.
78. Yeung RS, Katsetos CD, Klein-Szanto A 1997) Subependymal astrocytic hamartomas in the Eker rat model of tubero sclerosis. Am J Pathol 151 : 1477.
79. Zamecnik J, Krsek P, Druga R, Marusic P, Benes V, Tichy M, Komarek V 2006) Densities of parvalbumin-immunoreactive neurons in non-malformed hippocampal sclerosis-temporal neocortex and in cortical dysplasias. Brain Res Bull 68 : 474 481.