Layer-specific gene expression in epileptogenic type II focal cortical dysplasia: Normal-looking neurons reveal the presence of a hidden laminar organization

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Rossini, Laura ^a   Medici, Valentina ^a   Tassi, Laura ^b   Cardinale, Francesco ^b   Tringali, Giovanni ^a   Bramerio, Manuela ^b   Villani, Flavio ^a   Spreafico, Roberto ^a   Garbelli, Rita ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

^b OSPEDALE NIGUARDA CA GRANDA   (Italy)

Author keywords

Dysmorphic neurons; Epilepsy; Focal cortical dysplasia; Layer specific genes; Neuronal migration

Indexed keywords

CUX1 PROTEIN, HUMAN; DNA BINDING PROTEIN; ENOLASE; ETV1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MAP2 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MTOR PROTEIN, HUMAN; NR4A2 PROTEIN, HUMAN; NUCLEAR PROTEIN; NUCLEAR RECEPTOR RELATED FACTOR 1; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; REPRESSOR PROTEIN; ROR2 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; VIMENTIN;

ADOLESCENT; ADULT; CHILD; FEMALE; HUMAN; INFANT; MALE; MALFORMATION OF CORTICAL DEVELOPMENT GROUP I; METABOLISM; MIDDLE AGED; NERVE CELL; PARIETAL LOBE; PATHOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; DNA-BINDING PROTEINS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; INFANT; MALE; MALFORMATIONS OF CORTICAL DEVELOPMENT, GROUP I; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; NEURONS; NUCLEAR PROTEINS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PARIETAL LOBE; PHOSPHOPYRUVATE HYDRATASE; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; REPRESSOR PROTEINS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; VIMENTIN; YOUNG ADULT;

EID: 84921435661     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-2-45     Document Type: Article

References (52)

1. Taylor DC, Falconer MA, Bruton CJ, Corsellis JA: Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry 1971, 34: 369-387. 10.1136/jnnp.34.4.369
2. Blumcke 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, et al.: The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011, 52: 158-174. 10.1111/j.1528-1167.2010.02777.x
3. Thom M, Martinian L, Sen A, Cross JH, Harding BN, Sisodiya SM: Cortical neuronal densities and lamination in focal cortical dysplasia. Acta Neuropathol 2005, 110: 383-392. 10.1007/s00401-005-1062-0
4. Alonso-Nanclares L, Garbelli R, Sola RG, Pastor J, Tassi L, Spreafico R, DeFelipe J: Microanatomy of the dysplastic neocortex from epileptic patients. Brain 2005, 128: 158-173.
5. Englund C, Folkerth RD, Born D, Lacy JM, Hevner RF: Aberrant neuronal-glial differentiation in Taylor-type focal cortical dysplasia (type IIA/B). Acta Neuropathol 2005, 109: 519-533. 10.1007/s00401-005-1005-9
6. Sisodiya SM, Fauser S, Cross JH, Thom M: Focal cortical dysplasia type II: biological features and clinical perspectives. Lancet Neurol 2009, 8: 830-843. 10.1016/S1474-4422(09)70201-7
7. Yasin SA, Latak K, Becherini F, Ganapathi A, Miller K, Campos O, Picker SR, Bier N, Smith M, Thom M, Anderson G, Helen Cross J, Harkness W, Harding B, Jacques TS: Balloon cells in human cortical dysplasia and tuberous sclerosis: isolation of a pathological progenitor-like cell. Acta Neuropathol 2010, 120: 85-96. 10.1007/s00401-010-0677-y
8. Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB: A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012, 135: 1348-1369. 10.1093/brain/aws019
9. Miyata H, Chiang AC, Vinters HV: Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. Ann Neurol 2004, 56: 510-519. 10.1002/ana.20234
10. Ljungberg MC, Bhattacharjee MB, Lu Y, Armstrong DL, Yoshor D, Swann JW, Sheldon M, D'Arcangelo G: Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann Neurol 2006, 60: 420-429. 10.1002/ana.20949
11. Lamparello P, Baybis M, Pollard J, Hol EM, Eisenstat DD, Aronica E, Crino PB: Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain 2007, 130: 2267-2276. 10.1093/brain/awm175
12. Hua Y, Crino PB: Single cell lineage analysis in human focal cortical dysplasia. Cereb Cortex 2003, 13: 693-699. 10.1093/cercor/13.6.693
13. Hevner RF: Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development. J Neuropathol Exp Neurol 2007, 66: 101-109. 10.1097/nen.0b013e3180301c06
14. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD: Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 2007, 8: 427-437. 10.1038/nrn2151
15. Ferrere A, Vitalis T, Gingras H, Gaspar P, Cases O: Expression of Cux-1 and Cux-2 in the developing somatosensory cortex of normal and barrel-defective mice. Anat Rec A: Discov Mol Cell Evol Biol 2006, 288: 158-165.
16. Watakabe A, Ichinohe N, Ohsawa S, Hashikawa T, Komatsu Y, Rockland KS, Yamamori T: Comparative analysis of layer-specific genes in Mammalian neocortex. Cereb Cortex 2007, 17: 1918-1933. 10.1093/cercor/bhl102
17. Moroni RF, Inverardi F, Regondi MC, Watakabe A, Yamamori T, Spreafico R, Frassoni C: Expression of layer-specific markers in the adult neocortex of BCNU-Treated rat, a model of cortical dysplasia. Neuroscience 2009, 159: 682-691. 10.1016/j.neuroscience.2008.12.064
18. Moroni RF, Cipelletti B, Inverardi F, Regondi MC, Spreafico R, Frassoni C: Development of cortical malformations in BCNU-treated rat, model of cortical dysplasia. Neuroscience 2011, 175: 380-393.
19. Ferland RJ, Batiz LF, Neal J, Lian G, Bundock E, Lu J, Hsiao YC, Diamond R, Mei D, Banham AH, Brown PJ, Vanderburg CR, Joseph J, Hecht JL, Folkerth R, Guerrini R, Walsh CA, Rodriguez EM, Sheen VL: Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum Mol Genet 2009, 18: 497-516.
20. Garbelli R, Rossini L, Moroni RF, Watakabe A, Yamamori T, Tassi L, Bramerio M, Russo GL, Frassoni C, Spreafico R: Layer-specific genes reveal a rudimentary laminar pattern in human nodular heterotopia. Neurology 2009, 73: 746-753. 10.1212/WNL.0b013e3181af3397
21. Hadjivassiliou G, Martinian L, Squier W, Blumcke I, Aronica E, Sisodiya SM, Thom M: The application of cortical layer markers in the evaluation of cortical dysplasias in epilepsy. Acta Neuropathol 2010, 120: 517-528. 10.1007/s00401-010-0686-x
22. Rossini L, Moroni RF, Tassi L, Watakabe A, Yamamori T, Spreafico R, Garbelli R: Altered layer-specific gene expression in cortical samples from patients with temporal lobe epilepsy. Epilepsia 2011, 52: 1928-1937. 10.1111/j.1528-1167.2011.03246.x
23. Saito T, Hanai S, Takashima S, Nakagawa E, Okazaki S, Inoue T, Miyata R, Hoshino K, Akashi T, Sasaki M, Goto Y, Hayashi M, Itoh M: Neocortical layer formation of human developing brains and lissencephalies: consideration of layer-specific marker expression. Cereb Cortex 2011, 21: 588-596. 10.1093/cercor/bhq125
24. Arai A, Saito T, Hanai S, Sukigara S, Nabatame S, Otsuki T, Nakagawa E, Takahashi A, Kaneko Y, Kaido T, Saito Y, Sugai K, Sasaki M, Goto Y, Itoh M: Abnormal maturation and differentiation of neocortical neurons in epileptogenic cortical malformation: unique distribution of layer-specific marker cells of focal cortical dysplasia and hemimegalencephaly. Brain Res 2012, 1470: 89-97.
25. Sakakibara T, Sukigara S, Saito T, Otsuki T, Takahashi A, Kaneko Y, Kaido T, Saito Y, Sato N, Kimura Y, Nakagawa E, Sugai K, Sasaki M, Goto Y, Itoh M: Delayed maturation and differentiation of neurons in focal cortical dysplasia with the transmantle sign: analysis of layer-specific marker expression. J Neuropathol Exp Neurol 2012, 71: 741-749. 10.1097/NEN.0b013e318262e41a
26. Tassi L, Garbelli R, Colombo N, Bramerio M, Lo Russo G, Deleo F, Milesi G, Spreafico R: Type I focal cortical dysplasia: surgical outcome is related to histopathology. Epileptic Disord 2010, 12: 181-191. doi: 10.1684/epd.2010.0327
27. Garbelli R, Munari C, De Biasi S, Vitellaro-Zuccarello L, Galli C, Bramerio M, Mai R, Battaglia G, Spreafico R: Taylor's cortical dysplasia: a confocal and ultrastructural immunohistochemical study. Brain Pathol 1999, 9: 445-461. 10.1111/j.1750-3639.1999.tb00534.x
28. Hirokawa J, Watakabe A, Ohsawa S, Yamamori T: Analysis of area-specific expression patterns of RORbeta, ER81 and Nurr1 mRNAs in rat neocortex by double in situ hybridization and cortical box method. PLoS One 2008, 3: e3266. 10.1371/journal.pone.0003266
29. Colombo N, Tassi L, Deleo F, Citterio A, Bramerio M, Mai R, Sartori I, Cardinale F, Lo Russo G, Spreafico R: Focal cortical dysplasia type IIa and IIb: MRI aspects in 118 cases proven by histopathology. Neuroradiology 2012, 54: 1065-1077. 10.1007/s00234-012-1049-1
30. Tassi L, Garbelli R, Colombo N, Bramerio M, Russo GL, Mai R, Deleo F, Francione S, Nobili L, Spreafico R: Electroclinical, MRI and surgical outcomes in 100 epileptic patients with type II FCD. Epileptic Disord 2012, 14: 257-266.
31. 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: Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 2002, 125: 1719-1732. 10.1093/brain/awf175
32. Chassoux F, Devaux B, Landre E, Turak B, Nataf F, Varlet P, Chodkiewicz JP, Daumas-Duport C: Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain 2000, 123(Pt 8):1733-1751.
33. Palmini A, Najm I, Avanzini G, Babb T, Guerrini R, Foldvary-Schaefer N, Jackson G, Luders HO, Prayson R, Spreafico R, Vinters HV: Terminology and classification of the cortical dysplasias. Neurology 2004, 62: S2-S8.
34. Wang WZ, Hoerder-Suabedissen A, Oeschger FM, Bayatti N, Ip BK, Lindsay S, Supramaniam V, Srinivasan L, Rutherford M, Mollgard K, Clowry GJ, Molnar Z: Subplate in the developing cortex of mouse and human. J Anat 2010, 217: 368-380. 10.1111/j.1469-7580.2010.01274.x
35. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C: Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 2003, 25: 139-151. 10.1159/000072263
36. Fauser S, Haussler U, Donkels C, Huber S, Nakagawa J, Prinz M, Schulze-Bonhage A, Zentner J, Haas CA: Disorganization of neocortical lamination in focal cortical dysplasia is brain-region dependent: evidence from layer-specific marker expression. Acta Neuropathol Commun 2013, 1: 47-5960-1-47.
37. Muhlebner A, Coras R, Kobow K, Feucht M, Czech T, Stefan H, Weigel D, Buchfelder M, Holthausen H, Pieper T, Kudernatsch M, Blumcke I: Neuropathologic measurements in focal cortical dysplasias: validation of the ILAE 2011 classification system and diagnostic implications for MRI. Acta Neuropathol 2012, 123: 259-272. 10.1007/s00401-011-0920-1
38. Lui JH, Hansen DV, Kriegstein AR: Development and evolution of the human neocortex. Cell 2011, 146: 18-36. 10.1016/j.cell.2011.06.030
39. Bystron I, Blakemore C, Rakic P: Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 2008, 9: 110-122. 10.1038/nrn2252
40. Hansen DV, Lui JH, Parker PR, Kriegstein AR: Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464: 554-561. 10.1038/nature08845
41. Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, Corbeil D, Riehn A, Distler W, Nitsch R, Huttner WB: OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 2010, 13: 690-699. 10.1038/nn.2553
42. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR: Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409: 714-720. 10.1038/35055553
43. Haubensak W, Attardo A, Denk W, Huttner WB: Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A 2004, 101: 3196-3201. 10.1073/pnas.0308600100
44. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C: G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 2005, 47: 353-364. 10.1016/j.neuron.2005.06.032
45. Cepeda C, Andre VM, Levine MS, Salamon N, Miyata H, Vinters HV, Mathern GW: Epileptogenesis in pediatric cortical dysplasia: the dysmature cerebral developmental hypothesis. Epilepsy Behav 2006, 9: 219-235. 10.1016/j.yebeh.2006.05.012
46. Heng JI, Chariot A, Nguyen L: Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci 2010, 33: 38-47. 10.1016/j.tins.2009.09.003
47. Reiner O, Sapir T: Polarity regulation in migrating neurons in the cortex. Mol Neurobiol 2009, 40: 1-14. 10.1007/s12035-009-8065-0
48. Guerrini R, Dobyns WB, Barkovich AJ: Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci 2008, 31: 154-162. 10.1016/j.tins.2007.12.004
49. Costa-Mattioli M, Monteggia LM: mTOR complexes in neurodevelopmental and neuropsychiatric disorders. Nat Neurosci 2013, 16: 1537-1543. 10.1038/nn.3546
50. Chen J, Tsai V, Parker WE, Aronica E, Baybis M, Crino PB: Detection of human papillomavirus in human focal cortical dysplasia type IIB. Ann Neurol 2012, 72: 881-892. 10.1002/ana.23795
51. Liu S, Lu L, Cheng X, Xu G, Yang H: Viral infection and focal cortical dysplasia. Ann Neurol 2013. doi: 10.1002/ana.24037
52. Colciaghi F, Finardi A, Frasca A, Balosso S, Nobili P, Carriero G, Locatelli D, Vezzani A, Battaglia G: Status epilepticus-induced pathologic plasticity in a rat model of focal cortical dysplasia. Brain 2011, 134: 2828-2843. 10.1093/brain/awr045