Neuronal migration disorders

Neurobiology of Disease

Volumn 38, Issue 2, 2010, Pages 154-166

  Guerrini, Renzo ^a   Parrini, Elena ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Cerebral cortex; Cortical malformation; Development; Epilepsy; Focal cortical dysplasia; Heterotopia; Lissencephaly; MRI; Neuronal migration; Polymicrogyria

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 2; ALPHA TUBULIN; BETA TUBULIN; CYCLIN DEPENDENT KINASE 5; DOUBLECORTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; FILAMIN A; PROTEIN P35; REELIN; TRANSCRIPTION FACTOR PAX6; VERY LATE ACTIVATION ANTIGEN 3; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

AGYRIA; AICARDI SYNDROME; COBBLESTONE LISSENCEPHALY; COGNITIVE DEFECT; CORTICAL DYSPLASIA; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; LANGUAGE DISABILITY; MICROGYRIA; MILLER DIEKER SYNDROME; NEURONAL MIGRATION DISORDER; NONHUMAN; PACHYGYRIA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SUBCORTICAL HETEROTOPIA;

CELL MOVEMENT; CEREBRAL CORTEX; HUMANS; MAGNETIC RESONANCE IMAGING; MUTATION; NEURONAL MIGRATION DISORDERS; NEURONS;

EID: 77951207235     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.02.008     Document Type: Review

References (136)

1. Aicardi J., Lefebvre J., Lerique-Koechlin A. A new syndrome: spasms in flexion, callosal agenesis, ocular abnormalities. Electroencephalogr. Clin. Neurophysiol. 1965, 19:609-610.
2. Aligianis I.A., Johnson C.A., Gissen P., Chen D., Hampshire D., Hoffmann K., Maina E.N., Morgan N.V., Tee L., Morton J., Ainsworth J.R., Horn D., Rosser E., Cole T.R.P., Stolte-Dijkstra I., Fieggen K., Clayton-Smith J., Mégarbané A., Shield J.P., Newbury-Ecob R., Dobyns W.B., Graham J.M., Kjaer K.W., Warburg M., Bond J., Trembath R.C., Harris L.W., Takai Y., Mundlos S., Tannahill D., Woods C.G., Maher E.R. Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome. Nat. Genet. 2005, 37:221-223.
3. Alonso-Nanclares L., Gabelli R., Sola R.G., Pastor J., Tassi L., Spreafico R., DeFelipe J. Microanatomy of the dysplastic neocortex from epileptic patients. Brain 2005, 128:158-173.
4. Araujo D., de Araujo D.B., Pontes-Neto O.M., Escorsi-Rosset S., Simao G.N., Wichert-Ana L., Velasco T.R., Sakamoto A.C., Leite J.P., Santos A.C. Language and motor FMRI activation in polymicrogyric cortex. Epilepsia 2006, 47:589-592.
5. Assadi A.H., Zhang G., Beffert U., McNeil R.S., Renfro A.L., Niu S., Quattrocchi C.C., Antalffy B.A., Sheldon M., Armstrong D.D., Wynshaw-Boris A., Herz J., D'Arcangelo G., Clark G.D. Interaction of reelin signaling and Lis1 in brain development. Nat. Genet. 2003, 35:270-276.
6. Baala L., Briault S., Etchevers H.C., Laumonnier F., Natiq A., Amiel J., Boddaert N., Picard C., Sbiti A., Asermouh A., Attié-Bitach T., Encha-Razavi F., Munnich A., Sefiani A., Lyonnet S. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat. Genet. 2007, 39:454-456.
7. Bai J., Ramos R.L., Ackman J.B., Thomas A.M., Lee R.V., LoTurco J.J. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 2003, 6:1277-1283.
8. Bai J., Ramos R.L., Paramasivam M., Siddiqi F., Ackman J.B., LoTurco J.J. The role of DCX and LIS1 in migration through the lateral cortical stream of developing forebrain. Dev. Neurosci. 2008, 30:144-156.
9. Barkovich A.J. Congenital malformations of the brain and skull. Pediatric Neuroimaging 2000, 251-381. Lippincott William and Wilkins, Philadelphia. 3rd ed. A. Barkovich (Ed.).
10. Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 2005, 65:1873-1887.
11. Becker A.J., Urbach H., Scheffler B., Baden T., Normann S., Lahl R., Pannek H.W., Tuxhorn I., Elger C.E., Schramm J., Wiestler O.D., Blümcke I. Focal cortical dysplasia of Taylor's balloon cell type: mutational analysis of the TSC1 gene indicates a pathogenic relationship to tuberous sclerosis. Ann. Neurol. 2002, 52:29-37.
12. Beltrán-Valero de Bernabé D., Currier S., Steinbrecher A., Celli J., van Beusekom E., van der Zwaag B., Kayserili H., Merlini L., Chitayat D., Dobyns W.B., Cormand B., Lehesjoki A.-E., Cruces J., Voit T., Walsh C.A., van Bokhoven H., Brunner H.G. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am. J. Hum. Genet. 2002, 71:1033-1043.
13. Beltran-Valero de Bernabé D., Voit T., Longman C., Steinbrecher A., Straub V., Yuva Y., Herrmann R., Sperner J., Korenke C., Diesen C., Dobyns W.B., Brunner H.G., van Bokhoven H., Brockington M., Muntoni F. Mutations in the FKRP gene can cause muscle-eye-brain disease and Walker-Warburg syndrome. J. Med. Genet. 2004, 41:e61.
14. Bonneau D., Toutain A., Laquerrière A., Marret S., Saugier-Veber P., Barthez M.-A., Radi S., Biran-Mucignat V., Rodriguez D., Gélot A. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann. Neurol. 2002, 51:340-349.
15. Boycott K.M., Flavelle S., Bureau A., Glass H.C., Fujiwara T.M., Wirrell E., Davey K., Chudley A.E., Scott J.N., McLeod D.R., Parboosingh J.S. Homozygous deletion of the very low density lipoprotein receptor gene causes autosomal recessive cerebellar hypoplasia with cerebral gyral simplification. Am. J. Hum. Genet. 2005, 77:477-483.
16. Brooks A.S., Bertoli-Avella A.M., Burzynski G.M., Breedveld G.J., Osinga J., Boven L.G., Hurst J.A., Mancini G.M.S., Lequin M.H., de Coo R.F., Matera I., de Graaff E., Meijers C., Willems P.J., Tibboel D., Oostra B.A., Hofstra R.M.W. Homozygous nonsense mutations in KIAA1279 are associated with malformations of the central and enteric nervous systems. Am. J. Hum. Genet. 2005, 77:120-126.
17. Burneo J.G., Kuzniecky R.I., Bebin M., Knowlton R.C. Cortical reorganization in malformations of cortical development: a magnetoencephalographic study. Neurology 2004, 63:1818-1824.
18. Cardoso C., Leventer R.J., Dowling J.J., Ward H.L., Chung J., Petras K.S., Roseberry J.A., Weiss A.M., Das S., Martin C.L., Pilz D.T., Dobyns W.B., Ledbetter D.H. Clinical and molecular basis of classical lissencephaly: mutations in the LIS1 gene (PAFAH1B1). Hum. Mutat. 2002, 19:4-15.
19. Cardoso C., Leventer R.J., Ward H.L., Toyo-oka K., Chung J., Gross A., Martin C.L., Allanson J., Pilz D.T., Olney A.H., Mutchinick O.M., Hirotsune S., Wynshaw-Boris A., Dobyns W.B., Ledbetter D.H. Refinement of a 400-kb critical region allows genotypic differentiation between isolated lissencephaly, Miller-Dieker syndrome, and other phenotypes secondary to deletions of 17p13.3. Am. J. Hum. Genet. 2003, 72:918-930.
20. Cardoso C., Boys A., Parrini E., Mignon-Ravix C., McMahon J.M., Khantane S., Bertini E., Pallesi E., Missirian C., Zuffardi O., Novara F., Villard L., Giglio S., Chabrol B., Slater H.R., Moncla A., Scheffer I.E., Guerrini R. Periventricular heterotopia, mental retardation, and epilepsy associated with 5q14.3-q15 deletion. Neurology 2008, [Electronic publication ahead of print].
21. Cohen M., Campbell R., Yaghmai F. Neuropathological abnormalities in developmental dysphasia. Ann. Neurol. 1989, 25:567-570.
22. Corbo J.C., Deuel T.A., Long J.M., LaPorte P., Tsai E., Wynshaw-Boris A., Walsh C.A. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 2002, 22:7548-7557.
23. D'Arcangelo G. Reelin mouse mutants as models of cortical development disorders. Epilepsy. Behav. 2006, 8:81-90.
24. Dabora S.L., Roberts P., Nieto A., Perez R., Jozwiak S., Franz D., Bissler J., Thiele E.A., Sims K., Kwiatkowski D.J. Association between a high-expressing interferon-gamma allele and a lower frequency of kidney angiomyolipomas in TSC2 patients. Am. J. Hum. Genet. 2002, 71:750-758.
25. des Portes V., Francis, Pinard J.M., Desguerre, Moutard M.L., Snoeck I., Meiners L.C., Capron F., Cusmai R., Ricci S., Motte J., Echenne B., Ponsot G., Dulac O., Chelly J., Beldjord C. doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum. Mol. Genet. 1998, 7:1063-1070.
26. Dobyns W.B., Guerrini R., Czapansky-Beilman D.K., Pierpont M.E., Breningstall G., Yock D.H., Bonanni P., Truwit C.L. Bilateral periventricular nodular heterotopia with mental retardation and syndactyly in boys: a new X-linked mental retardation syndrome. Neurology 1997, 49:1042-1047.
27. Dobyns W.B., Truwit C.L., Ross M.E., Matsumoto N., Pilz D.T., Ledbetter D.H., Gleeson J.G., Walsh C.A., Barkovich A.J. Differences in the gyral pattern distinguish chromosome 17-linked and X-linked lissencephaly. Neurology 1999, 53:270-277.
28. Dobyns W.B., Berry-Kravis E., Havernick N.J., Holden K.R., Viskochil D. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia. Am. J. Med. Genet. 1999, 86:331-337.
29. Dobyns W.B., Mirzaa G., Christian S.L., Petras K., Roseberry J., Clark G.D., Curry C.J.R., McDonald-McGinn D., Medne L., Zackai E., Parsons J., Zand D.J., Hisama F.M., Walsh C.A., Leventer R.J., Martin C.L., Gajecka M., Shaffer L.G. Consistent chromosome abnormalities identify novel polymicrogyria loci in 1p36.3, 2p16.1-p23.1, 4q21.21-q22.1, 6q26-q27, and 21q2. Am. J. Med. Genet. A 2008, 146A:1637-1654.
30. Duchowny M., Jayakar P., Harvey A.S., Resnick T., Alvarez L., Dean P., Levin B. Language cortex representation: effects of developmental versus acquired pathology. Ann. Neurol. 1996, 40:31-38.
31. Duchowny M., Jayakar P., Levin B. Aberrant neural circuits in malformations of cortical development and focal epilepsy. Neurology 2000, 55:423-428.
32. Dumoulin S.O., Jirsch J.D., Bernasconi A. Functional organization of human visual cortex in occipital polymicrogyria. Hum. Brain Mapp. 2007, 28:1302-1312.
33. Eash D., Waggoner D., Chung J., Stevenson D., Martin C.L. Calibration of 6q subtelomere deletions to define genotype/phenotype correlations. Clin. Genet. 2005, 67:396-403.
34. Ekşioǧlu Y.Z., Scheffer I.E., Cardenas P., Knoll J., DiMario F., Ramsby G., Berg M., Kamuro K., Berkovic S.F., Duyk G.M., Parisi J., Huttenlocher P.R., Walsh C.A. Periventricular heterotopia: an X-linked dominant epilepsy locus causing aberrant cerebral cortical development. Neuron 1996, 16:77-87.
35. Englund C., Fink A., Lau C., Pham D., Daza R.A.M., Bulfone A., Kowalczyk T., Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 2005, 25:247-251.
36. Faulkner N.E., Dujardin D.L., Tai C.Y., Vaughan K.T., O'Connell C.B., Wang Y., Vallee R.B. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell. Biol. 2000, 2:784-791.
37. Feng Y., Chen M.H., Moskowitz I.P., Mendonza A.M., Vidali L., Nakamura F., Kwiatkowski D.J., Walsh C.A. Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19836-19841.
38. Ferland R.J., Gaitanis J.N., Apse K., Tantravahi U., Walsh C.A., Sheen V.L. Periventricular nodular heterotopia and Williams syndrome. Am. J. Med. Genet. A 2006, 140:1305-1311.
39. Fink J.M., Dobyns W.B., Guerrini R., Hirsch B.A. Identification of a duplication of Xq28 associated with bilateral periventricular nodular heterotopia. Am. J. Hum. Genet. 1997, 61:379-387.
40. Friede R.L. Developmental neuropathology 1989, 577. Springer-Verlag, New York.
41. Friocourt G., Kanatani S., Tabata H., Yozu M., Takahashi T., Antypa M., Raguénès O., Chelly J., Férec C., Nakajima K., Parnavelas J.G. Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J. Neurosci. 2008, 28:5794-5805.
42. Galaburda A.M., Sherman G.F., Rosen G.D., Aboitiz F., Geschwind N. Developmental dyslexia: four consecutive patients with cortical anomalies. Ann. Neurol. 1985, 18:222-233.
43. Gawlik-Kuklinska K., Wierzba J., Wozniak A., Iliszko M., Debiec-Rychter M., Dubaniewicz-Wybieralska M., Limon J. Periventricular heterotopia in a boy with interstitial deletion of chromosome 4p. Eur. J. Med. Genet. 2008, 51:165-171.
44. Glaser T., Jepeal L., Edwards J.G., Young S.R., Favor J., Maas R.L. PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat. Genet. 1994, 7:463-471.
45. Gleeson J.G., Walsh C.A. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 2000, 23:352-359.
46. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 1998, 92:63-72.
47. Gleeson J.G., Minnerath S., Kuzniecky R.I., Dobyns W.B., Young I.D., Ross M.E., Walsh C.A. Somatic and germline mosaic mutations in the doublecortin gene are associated with variable phenotypes. Am. J. Hum. Genet. 2000, 67:574-581.
48. Gleeson J.G., Luo R.F., Grant P.E., Guerrini R., Huttenlocher P.R., Berg M.J., Ricci S., Cusmai R., Wheless J.W., Berkovic S., Scheffer I., Dobyns W.B., Walsh C.A. Genetic and neuroradiological heterogeneity of double cortex syndrome. Ann. Neurol. 2000, 47:265-269.
49. Golden, A.J., Harding, B.N., 2004. Pathology and genetics. Developmental neurophatology. ISN Neuropath Press, Basel 386 pages.
50. Guerreiro M.M., Andermann E., Guerrini R., Dobyns W.B., Kuzniecky R., Silver K., Van Bogaert P., Gillain C., David P., Ambrosetto G., Rosati A., Bartolomei F., Parmeggiani A., Paetau R., Salonen O., Ignatius J., Borgatti R., Zucca C., Bastos A.C., Palmini A., Fernandes W., Montenegro M.A., Cendes F., Andermann F. Familial perisylvian polymicrogyria: a new familial syndrome of cortical maldevelopment. Ann. Neurol. 2000, 48:39-48.
51. Guerreiro M.M., Hage S.R., Guimarães C.A., Abramides D.V., Fernandes W., Pacheco P.S., Piovesana A.M., Montenegro M.A., Cendes F. Developmental language disorder associated with polymicrogyria. Neurology 2002, 59:245-250.
52. Guerrini R., Dobyns W.B. Bilateral periventricular nodular heterotopia with mental retardation and frontonasal malformation. Neurology 1998, 51:499-503.
53. Guerrini R., Filippi T. Neuronal migration disorders, genetics, and epileptogenesis. J. Child. Neurol. 2005, 20:287-299.
54. Guerrini R., Dravet Ch., Bureau M., Mancini J., Canapicchi R., Livet M.O., Belmonte A. Diffuse and localized dysplasias of cerebral cortex: clinical presentation, outcome, and proposal for a morphologic MRI classification based on a study of 90 patients. Dysplasias of Cerebral Cortex and Epilepsy 1996, 255-269. Lippincott-Raven. Philadelphia, New York. R. Guerrini, F. Andermann, R. Canapicchi, J. Roger, B.G. Zifkin, P. Pfanner (Eds.).
55. Guerrini R., Dubeau F., Dulac O., Barkovich A.J., Kuzniecky R., Fett C., Jones-Gotman M., Canapicchi R., Cross H., Fish D., Bonanni P., Jambaqué I., Andermann F. Bilateral parasagittal parietooccipital polymicrogyria and epilepsy. Ann. Neurol. 1997, 41:65-73.
56. Guerrini R., Genton P., Bureau M., Parmeggiani A., Salas-Puig X., Santucci M., Bonanni P., Ambrosetto G., Dravet C. Multilobar polymicrogyria, intractable drop attack seizures, and sleep-related electrical status epilepticus. Neurology 1998, 51:504-512.
57. Guerrini R., Barkovich A.J., Sztriha L., Dobyns W.B. Bilateral frontal polymicrogyria: a newly recognized brain malformation syndrome. Neurology 2000, 54:909-913.
58. Guerrini R., Moro F., Andermann E., Hughes E., D'Agostino D., Carrozzo R., Bernasconi A., Flinter F., Parmeggiani L., Volzone A., Parrini E., Mei D., Jarosz J.M., Morris R.G., Pratt P., Tortorella G., Dubeau F., Andermann F., Dobyns W.B., Das S. Nonsyndromic mental retardation and cryptogenic epilepsy in women with doublecortin gene mutations. Ann. Neurol. 2003, 54:30-37.
59. Guerrini R., Mei D., Sisodiya S., Sicca F., Harding B., Takahashi Y., Dorn T., Yoshida A., Campistol J., Krämer G., Moro F., Dobyns W.B., Parrini E. Germline and mosaic mutations of FLN1 in men with periventricular heterotopia. Neurology 2004, 63:51-56.
60. Guerrini R., Moro F., Kato M., Barkovich A.J., Shiihara T., McShane M.A., Hurst J., Loi M., Tohyama J., Norci V., Hayasaa K., Kang U.J., Das S., Dobyns W.B. Expansion of the first PolyA tract of ARX causes infantile spasms and status dystonicus. Neurology 2007, 69:427-433.
61. Guerrini R., Dobyns W., Barkovich A. Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends. Neurosci. 2008, 31:154-162.
62. Guzzetta A., Bonanni P., Biagi L., Tosetti M., Montanaro D., Guerrini R., Cioni G. Reorganisation of the somatosensory system after early brain damage. Clin. Neurophysiol. 2007, 118:1110-1121.
63. Hannan A.J., Servotte S., Katsnelson A., Sisodiya S., Blakemore C., Squier M., Molnár Z. Characterization of nodular neuronal heterotopia in children. Brain 1999, 122:219-238.
64. Harding B. Gray matter heterotopia. Dysplasias of Cerebral Cortex and Epilepsy 1996, 255-269. Lippincott-Raven, Philadelphia, New York. R. Guerrini, F. Andermann, R. Canapicchi, J. Roger, B.G. Zifkin, P. Pfanner (Eds.).
65. Harding B., Copp A. Malformations of the nervous system. Greenfields Neuropathology 1997, 521-538. Edward Arnold, London-Melbourne-Auckland. J. Graham, P.L. Lantos (Eds.).
66. Hehr U., Hehr A., Uyanik G., Phelan E., Winkler J., Reardon W. A filamin A splice mutation resulting in a syndrome of facial dysmorphism, periventricular nodular heterotopia, and severe constipation reminiscent of cerebro-fronto-facial syndrome. J. Med. Genet. 2006, 43:541-544.
67. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999, 24:481-489.
68. Hirotsune S., Fleck M.W., Gambello M.J., Bix G.J., Chen A., Clark G.D., Ledbetter D.H., McBain C.J., Wynshaw-Boris A. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet. 1998, 19:333-339.
69. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 2000, 26:93-96.
70. Jin Z., Tietjen I., Bu L., Liu-Yesucevitz L., Gaur S.K., Walsh C.A., Piao X. Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum. Mol. Genet. 2007, 16:1972-1985.
71. Kakita A., Hayashi S., Moro F., Guerrini R., Ozawa T., Ono K., Kameyama S., Walsh C.A., Takahashi H. Bilateral periventricular nodular heterotopia due to filamin 1 gene mutation: widespread glomeruloid microvascular anomaly and dysplastic cytoarchitecture in the cerebral cortex. Acta Neuropathol. 2002, 104:649-657.
72. Kantarci S., Al-Gazali L., Hill R.S., Donnai D., Black G.C.M., Bieth E., Chassaing N., Lacombe D., Devriendt K., Teebi A., Loscertales M., Robson C., Liu T., MacLaughlin D.T., Noonan K.M., Russell M.K., Walsh C.A., Donahoe P.K., Pober B.R. Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat. Genet. 2007, 39:957-959.
73. Kato M., Das S., Petras K., Kitamura K., Morohashi K., Abuelo D.N., Barr M., Bonneau D., Brady A.F., Carpenter N.J., Cipero K.L., Frisone F., Fukuda T., Guerrini R., Iida E., Itoh M., Lewanda A.F., Nanba Y., Oka A., Proud V.K., Saugier-Veber P., Schelley S.L., Selicorni A., Shaner R., Silengo M., Stewart F., Sugiyama N., Toyama J., Toutain A., Vargas A.L., Yanazawa M., Zackai E.H., Dobyns W.B. Mutations of ARX are associated with striking pleiotropy and consistent genotype-phenotype correlation. Hum. Mutat. 2004, 23:147-159.
74. Keays D.A., Tian G., Poirier K., Huang G.-J., Siebold C., Cleak J., Oliver P.L., Fray M., Harvey R.J., Molnár Z., Piñon M.C., Dear N., Valdar W., Brown S.D.M., Davies K.E., Rawlins J.N.P., Cowan N.J., Nolan P., Chelly J., Flint J. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 2007, 128:45-57.
75. Kitamura K., Yanazawa M., Sugiyama N., Miura H., Iizuka-Kogo A., Kusaka M., Omichi K., Suzuki R., Kato-Fukui Y., Kamiirisa K., Matsuo M., Kamijo S., Kasahara M., Yoshioka H., Ogata T., Fukuda T., Kondo I., Kato M., Dobyns W.B., Yokoyama M., Morohashi K. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat. Genet. 2002, 32:359-369.
76. Kondo-Iida E., Kobayashi K., Watanabe M., Sasaki J., Kumagai T., Koide H., Saito K., Osawa M., Nakamura Y., Toda T. Novel mutations and genotype-phenotype relationships in 107 families with Fukuyama-type congenital muscular dystrophy (FCMD). Hum. Mol. Genet. 1999, 8:2303-2309.
77. Kuzniecky R., Andermann F., Guerrini R. Congenital bilateral perisylvian syndrome: study of 31 patients. The CBPS Multicenter Collaborative Study. Lancet 1993, 341:608-612.
78. Lamparello P., Baybis M., Pollard J., Hol E.M., Eisenstat D.D., Aronica E., Crino P.B. Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain 2007, 130:2267-2276.
79. Lange M., Winner B., Müller J.L., Marienhagen J., Schröder M., Aigner L., Uyanik G., Winkler J. Functional imaging in PNH caused by a new FilaminA mutation. Neurology 2004, 62:151-152.
80. Lee N., Radtke R.A., Gray L., Burger P.C., Montine T.J., DeLong G.R., Lewis D.V., Oakes W.J., Friedman A.H., Hoffman J.M. Neuronal migration disorders: positron emission tomography correlations. Ann. Neurol. 1994, 35:290-297.
81. Letinic K., Zoncu R., Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 2002, 417(6889):645-649.
82. Little A.S., Ng Y.T., Kerrigan J.F., Treiman D.M., Fram E., Rekate H.L. Anterior motor strip displacement in a boy with right frontal gray matter heterotopia undergoing epilepsy surgery. Epilepsy Behav. 2007, 11:241-246.
83. Longman C., Brockington M., Torelli S., Jimenez-Mallebrera C., Kennedy C., Khalil N., Feng L., Saran R.K., Voit T., Merlini L., Sewry C.A., Brown S.C., Muntoni F. Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum. Mol. Genet. 2003, 12:2853-2861.
84. Mai R., Tassi L., Cossu M., Arancione S., Lo Russo G., Gabelli R., Ferrario A., Galli C., Taroni F., Citterio A., Spreafico R. A neuropathological, stereo-EEG, and MRI study of subcortical band heterotopia. Neurology 2003, 60:1834-1838.
85. Marín-Padilla M., Parisi J.E., Armstrong D.L., Sargent S.K., Kaplan J.A. Shaken infant syndrome: developmental neuropathology, progressive cortical dysplasia, and epilepsy. Acta Neuropathol. 2002, 103:321-332.
86. Marusic P., Najm I.M., Ying Z., Prayson R., Rona S., Nair D., Hadar E., Kotagal P., Bej M.D., Wyllie E., Bingaman W., Lüders H. Focal cortical dysplasias in eloquent cortex: functional characteristics and correlation with MRI and histopathologic changes. Epilepsia 2002, 43:27-32.
87. Matsumoto N., Leventer R.J., Kuc J.A., Mewborn S.K., Dudlicek L.L., Ramocki M.B., Pilz D.T., Mills P.L., Das S., Ross M.E., Ledbetter D.H., Dobyns W.B. Mutation analysis of the DCX gene and genotype/phenotype correlation in subcortical band heterotopia. Eur. J. Hum. Genet. 2001, 9:5-12.
88. Mei D., Parrini E., Pasqualetti M., Tortorella G., Franzoni E., Giussani U., Marini C., Migliarini S., Guerrini R. Multiplex ligation-dependent probe amplification detects DCX gene deletions in band heterotopia. Neurology 2007, 68:446-450.
89. Mei D., Lewis R., Parrini E., Lazarou L., Marini C., Pilz D., Guerrini R. High frequency of genomic deletions and duplication in the LIS1 gene in lissencephaly: implications for molecular diagnosis. J. Med. Genet. 2008, 45:355-361.
90. Moro F., Pisano T., Bernardina B.D., Polli R., Murgia A., Zoccante L., Darra F., Battaglia A., Pramparo T., Zuffardi O., Guerrini R. Periventricular heterotopia in fragile X syndrome. Neurology 2006, 67:713-715.
91. Nadarajah B., Parnavelas J.G. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 2002, 3:423-432.
92. Najm I.M., Tilelli C.Q., Oghlakian R. Pathophysiological mechanisms of focal cortical dysplasia: a critical review of human tissue studies and animal models. Epilepsia 2007, 48(Suppl 2):21-32.
93. Neal J., Apse K., Sahin M., Walsh C.A., Sheen V.L. Deletion of chromosome 1p36 is associated with periventricular nodular heterotopia. Am. J. Med. Genet. A. 2006, 140:1692-1695.
94. Nowaczyk M.J., Teshima I.E., Siegel-Bartelt J., Clarke J.T. Deletion 4q21/4q22 syndrome: two patients with de novo 4q21.3q23 and 4q13.2q23 deletions. Am. J. Med. Genet. 1997, 69:400-405.
95. Ohira R., Zhang Y.H., Guo W., Dipple K., Shih S.L., Doerr J., Huang B.L., Fu L.J., Abu-Khalil A., Geschwind D., McCabe E.R.B. Human ARX gene: genomic characterization and expression. Mol. Genet. Metab. 2002, 77:179-188.
96. Okazaki S., Ohsawa M., Kuki I., Kawawaki H., Koriyama T., Ri S., Ichiba H., Hai E., Inoue T., Nakamura H., Goto Y., Tomiwa K., Yamano T., Kitamura K., Itoh M. Aristaless-related homeobox gene disruption leads to abnormal distribution of GABAergic interneurons in human neocortex: evidence based on a case of X-linked lissencephaly with abnormal genitalia (XLAG). Acta Neuropathol. 2008, 116:453-462.
97. OMIM: http://www.ncbi.nlm.nih.gov/sites/entrez?db=omim.
98. Palmini A., Najm I., Avanzini G., Babb T., Guerrini R., Foldvary-Schaefer N., Jackson G., Lüders H.O., Prayson R., Spreafico R., Vinters H.V. Terminology and classification of the cortical dysplasias. Neurology 2004, 62(6 Suppl 3):S2-S8.
99. Parrini E., Ramazzotti A., Dobyns W.B., Mei D., Moro F., Veggiotti P., Marini C., Brilstra E.H., Dalla Bernardina B., Goodwin L., Bodell A., Jones M.C., Nangeroni M., Palmeri S., Said E., Sander J.W., Striano P., Takahashi Y., Van Maldergem L., Leonardi G., Wright M., Walsh C.A., Guerrini R. Periventricular heterotopia: phenotypic heterogeneity and correlation with Filamin A mutations. Brain 2006, 129:1892-1906.
100. Piao X., Hill R.S., Bodell A., Chang B.S., Basel-Vanagaite L., Straussberg R., Dobyns W.B., Qasrawi B., Winter R.M., Innes A.M., Voit T., Ross M.E., Michaud J.L., Déscarie J.-C., Barkovich A.J., Walsh C.A. G protein-coupled receptor-dependent development of human frontal cortex. Science 2004, 303:2033-2036.
101. Piao X., Chang B.S., Bodell A., Woods K., Benzeev B., Topcu M., Guerrini R., Goldberg-Stern H., Sztriha L., Dobyns W.B., Barkovich A.J., Walsh C.A. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann. Neurol. 2005, 58:680-687.
102. Pilz D.T., Matsumoto N., Minnerath S., Mills P., Gleeson J.G., Allen K.M., Walsh C.A., Barkovich A.J., Dobyns W.B., Ledbetter D.H., Ross M.E. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum. Mol. Genet. 1998, 7:2029-2037.
103. Pilz D.T., Kuc J., Matsumoto N., Bodurtha J., Bernadi B., Tassinari C.A., Dobyns W.B., Ledbetter D.H. Subcortical band heterotopia in rare affected males can be caused by missense mutations in DCX (XLIS) or LIS1. Hum. Mol. Genet. 1999, 8:1757-1760.
104. Pinard J., Feydy A., Carlier R., Perez N., Pierot L., Burnod Y. Functional MRI in double cortex: functionality of heterotopia. Neurology 2000, 54:153-1531.
105. Poirier K., Keays D.A., Francis F., Saillour Y., Bahi N., Manouvrier S., Fallet-Bianco C., Pasquier L., Toutain A., Tuy F.P., Bienvenu T., Joriot S., Odent S., Ville D., Desguerre I., Goldenberg A., Moutard M.L., Fryns J.P., van Esch H., Harvey R.J., Siebold C., Flint J., Beldjord C., Chelly J. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Hum. Mutat. 2007, 28:1055-1064.
106. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 1993, 364:717-721.
107. Ribeiro M.d.C., Gama de Sousa S., Freitas M.M., Carrilho I., Fernandes I. Bilateral perisylvian polymicrogyria and chromosome 1 anomaly. Pediatr. Neurol. 2007, 36:418-420.
108. Richardson M.P., Koepp M.J., Brooks D.J., Coull J.T., Grasby P., Fish D.R., Duncan J.S. Cerebral activation in malformations of cortical development. Brain 1998, 121:304-12951.
109. Robin N.H., Taylor C.J., McDonald-McGinn D.M., Zackai E.H., Bingham P., Collins K.J., Earl D., Gill D., Granata T., Guerrini R., Katz N., Kimonis V., Lin J.-P., Lynch D.R., Mohammed S.N., Massey R.F., McDonald M., Rogers R.C., Splitt M., Stevens C.A., Tischkowitz M.D., Stoodley N., Leventer R.J., Pilz D.T., Dobyns W.B. Polymicrogyria and deletion 22q11.2 syndrome: window to the etiology of a common cortical malformation. Am. J. Med. Genet. A 2006, 140:2416-2425.
110. Roll P., Rudolf G., Pereira S., Royer B., Scheffer I.E., Massacrier A., Valenti M.P., Roeckel-Trevisiol N., Jamali S., Beclin C., Seegmuller C., Metz-Lutz M.N., Lemainque A., Delepine M., Caloustian C., de Saint Martin A., Bruneau N., Depetris D., Mattei M.G., Flori E., Robaglia-Schlupp A., Levy N., Neubauer B.A., Ravid R., Marescaux C., Berkovic S.F., Hirsch E., Lathrop M., Cau P., Szepetowski P. SRPX2 mutations in disorders of language cortex and cognition. Hum. Mol. Genet. 2006, 15:1195-1207.
111. Ross M.E., Swanson K., Dobyns W.B. Lissencephaly with cerebellar hypoplasia (LCH): a heterogeneous group of cortical malformations. Neuropediatrics 2001, 32:256-263.
112. Sapir T., Elbaum M., Reiner O. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J. 1997, 16:6977-6984.
113. Sarkisian M.R., Bartley C.M., Chi H., Nakamura F., Hashimoto-Torii K., Torii M., Flavell R.A., Rakic P. MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 2006, 52:789-801.
114. Scherer C., Schuele S., Minotti L., Chabardes S., Hoffmann D., Kahane P. Intrinsic epileptogenicity of an isolated periventricular nodular heterotopia. Neurology 2005, 65:495-496.
115. Sheen V.L., Dixon P.H., Fox J.W., Hong S.E., Kinton L., Sisodiya S.M., Duncan J.S., Dubeau F., Scheffer I.E., Schachter S.C., Wilner A., Henchy R., Crino P., Kamuro K., DiMario F., Berg M., Kuzniecky R., Cole A.J., Bromfield E., Biber M., Schomer D., Wheless J., Silver K., Mochida G.H., Berkovic S.F., Andermann F., Andermann E., Dobyns W.B., Wood N.W., Walsh C.A. Mutations in the X-linked filamin 1 gene cause periventricular nodular heterotopia in males as well as in females. Hum. Mol. Genet. 2001, 10:1775-1783.
116. Sheen V.L., Wheless J.W., Bodell A., Braverman E., Cotter P.D., Rauen K.A., Glenn O., Weisiger K., Packman S., Walsh C.A., Sherr E.H. Periventricular heterotopia associated with chromosome 5p anomalies. Neurology 2003, 60:1033-1036.
117. Sheen V.L., Ganesh V.S., Topcu M., Sebire G., Bodell A., Hill R.S., Grant P.E., Shugart Y.Y., Imitola J., Khoury S.J., Guerrini R., Walsh C.A. Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat. Genet. 2004, 36:69-76.
118. Sicca F., Kelemen A., Genton P., Das S., Mei D., Moro F., Dobyns W.B., Guerrini R. Mosaic mutations of the LIS1 gene cause subcortical band heterotopia. Neurology 2003, 61:1042-1046.
119. Sprecher E., Ishida-Yamamoto A., Mizrahi-Koren M., Rapaport D., Goldsher D., Indelman M., Topaz O., Chefetz I., Keren H., O'brien T.J., Bercovich D., Shalev S., Geiger D., Bergman R., Horowitz M., Mandel H. A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am. J. Hum. Genet. 2005, 77:242-251.
120. Staudt M., Krägeloh-Mann I., Holthausen H., Gerloff C., Grodd W. Searching for motor functions in dysgenic cortex: a clinical transcranial magnetic stimulation and functional magnetic resonance imaging study. J. Neurosurg. 2004, 101(1 Suppl):69-77.
121. Strømme P., Mangelsdorf M.E., Shaw M.A., Lower K.M., Lewis S.M.E., Bruyere H., Lütcherath V., Gedeon A.K., Wallace R.H., Scheffer I.E., Turner G., Partington M., Frints S.G.M., Fryns J.-P., Sutherland G.R., Mulley J.C., Gécz J. Mutations in the human ortholog of Aristaless cause X-linked mental retardation and epilepsy. Nat. Genet. 2002, 30:441-445.
122. Sztriha L., Guerrini R., Harding B., Stewart F., Chelloug N., Johansen J.G. Clinical, MRI, and pathological features of polymicrogyria in chromosome 22q11 deletion syndrome. Am. J. Med. Genet. A 2004, 127A:313-317.
123. Takanashi J., Barkovich A.J. The changing MR imaging appearance of polymicrogyria: a consequence of myelination. AJNR Am. J. Neuroradiol. 2003, 24:788-793.
124. Tassi L., Colombo N., Gabelli 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.
125. Tassi L., Colombo N., Cossu M., Mai R., Francione S., Lo Russo G., Galli C., Bramerio M., Battaglia G., Garbelli R., Meroni A., Spreafico R. Electroclinical, MRI and neuropathological study of 10 patients with nodular heterotopia, with surgical outcomes. Brain 2005, 128:321-337.
126. Uyanik G., Morris-Rosendahl D.J., Stiegler J., Klapecki J., Gross C., Berman Y., Martin P., Dey L., Spranger S., Korenke G.C., Schreyer I., Hertzberg C., Neumann T.E., Burkart P., Spaich C., Meng M., Holthausen H., Adès L., Seidel J., Mangold E., Buyse G., Meinecke P., Schara U., Zeschnigk C., Muller D., Helland G., Schulze B., Wright M.L., Kortge-Jung S., Hehr A., Bogdahn U., Schuierer G., Kohlhase J., Aigner L., Wolff G., Hehr U., Winkler J. Location and type of mutation in the LIS1 gene do not predict phenotypic severity. Neurology 2007, 69:442-447.
127. Vallee R.B., Faulkner N.E., Tai C.Y. The role of cytoplasmic dynein in the human brain developmental disease lissencephaly. Biochim. Biophys. Acta 2000, 1496:89-98.
128. van der Flier A., Sonnenberg A. Structural and functional aspects of filamins. Biochim. Biophys. Acta 2001, 1538:99-117.
129. van Reeuwijk J., Janssen M., van den Elzen C., Beltran-Valero de Bernabé D., Sabatelli P., Merlini L., Boon M., Scheffer H., Brockington M., Muntoni F., Huynen M.A., Verrips A., Walsh C.A., Barth P.G., Brunner H.G., van Bokhoven H. POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J. Med. Genet. 2005, 42:907-912.
130. van Reeuwijk J., Maugenre S., van den Elzen C., Verrips A., Bertini E., Muntoni F., Merlini L., Scheffer H., Brunner H.G., Guicheney P., van Bokhoven H. The expanding phenotype of POMT1 mutations: from Walker-Warburg syndrome to congenital muscular dystrophy, microcephaly, and mental retardation. Hum. Mutat. 2006, 27:453-459.
131. Wynshaw-Boris A., Gambello M.J. LIS1 and dynein motor function in neuronal migration and development. Genes. Dev. 2001, 15:639-651.
132. Xiang X., Osmani A.H., Osmani S.A., Xin M., Morris N.R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell. 1995, 6:297-310.
133. Yao G., Chen X.-N., Flores-Sarnat L., Barlow G.M., Palka G., Moeschler J.B., McGillivray B., Morse R.P., Korenberg J.R. Deletion of chromosome 21 disturbs human brain morphogenesis. Genet. Med. 2006, 8:1-7.
134. Ying Z., Gonzalez-Martinez J., Tilelli C., Bingaman W., Najm I. Expression of neural stem cell surface marker CD133 in balloon cells of human focal cortical dysplasia. Epilepsia 2005, 46:1716-1723.
135. Zaki M., Shehab M., El-Aleem A.A., Abdel-Salam G., Koeller H.B., Ilkin Y., Ross M.E., Dobyns W.B., Gleeson J.G. Identification of a novel recessive RELN mutation using a homozygous balanced reciprocal translocation. Am. J. Med. Genet. A 2007, 143A:939-944.
136. Zollino M., Colosimo C., Zuffardi O., Rossi E., Tosolini A., Walsh C.A., Neri G. Cryptic t(1;12)(q44;p13.3) translocation in a previously described syndrome with polymicrogyria, segregating as an apparently X-linked trait. Am. J. Med. Genet. A 2003, 117A:65-71.