Subcortical band heterotopia (SBH) in males: Clinical, imaging and genetic findings in comparison with females

Brain

Volumn 125, Issue 11, 2002, Pages 2507-2522

  D'Agostino, Maria Daniela ^a,b   Bernasconi, Andrea ^a   Das, Soma ^d   Bastos, Alexandre ^a   Valerio, Rosa M ^a,i   Palmini, André ^j   Da Costa, Jaderson Costa ^j   Scheffer, Ingrid E ^l   Berkovic, Samuel ^a,l   Guerrini, Renzo ^m   Dravet, Charlotte ⁿ   Ono, Jiro ^o   Gigli, GianLuigi ^p,q   Federico, Antonio ^q,r   Booth, Fran ^c   Bernardi, Bruno ^s   Volpi, Lilia ^s   Tassinari, Carlo Alberto ^s   Guggenheim, Mary Anne ^e   Ledbetter, David H ^d   Gleeson, Joseph G ^f   Lopes Cendes, Iscia ^k   Vossler, David G ^g   Malaspina, Elisabetta ^t   Franzoni, Emilio ^t   Sartori, Roberto J ^h   Mitchel, Michael H ^h   Mercho, Suha ^a   Dubeau, François ^a   Andermann, Frederick ^a,b   Dobyns, William B ^d   Andermann, Eva ^a,b   more..

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c HEALTH SCIENCES CENTRE   (Canada)

^d UNIVERSITY OF CHICAGO   (United States)

^e Shodair Children's Hospital   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g SWEDISH MEDICAL CENTER   (United States)

^h WALTER REED ARMY MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF SÃO PAULO   (Brazil)

^j PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^k UNIVERSITY OF CAMPINAS   (Brazil)

^l ROYAL CHILDREN'S HOSPITAL   (Australia)

^m UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁿ CENTRE SAINT PAUL   (France)

^o TOYONAKA MUNICIPAL HOSPITAL   (Japan)

^p SANTA MARIA DELLA MISERICORDIA UNIVERSITY HOSPITAL   (Italy)

^q Associazione Anni Verdi   (Italy)

^r UNIVERSITY OF SIENA   (Italy)

^s BELLARIA HOSPITAL   (Italy)

^t UNIVERSITY OF BOLOGNA   (Italy)

more..

Author keywords

DCX; Double cortex; LIS1; Male; Subcortical band heterotopia

Indexed keywords

ANTICONVULSIVE AGENT; CARBAMAZEPINE; DOUBLECORTIN; LAMOTRIGINE; PHENYTOIN; VALPROIC ACID; VIGABATRIN;

ADOLESCENT; ADULT; ANATOMY; ARTICLE; BASE MISPAIRING; CHILD; CHROMOSOME 9P; CHROMOSOME MOSAICISM; CLINICAL ARTICLE; CLINICAL FEATURE; CLINICAL TRIAL; COGNITION; FEMALE; GENE; GENE MUTATION; GENETICS; GENOTYPE PHENOTYPE CORRELATION; HETEROTOPIA; HUMAN; HUMAN TISSUE; INFANT; INTELLIGENCE QUOTIENT; KARYOTYPING; LIS1 GENE; MALE; MENTAL DEFICIENCY; META ANALYSIS; MISSENSE MUTATION; NEURORADIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SEX DIFFERENCE; SUBCORTICAL BAND HETEROTOPIA; TRISOMY;

EID: 0036845824     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awf248     Document Type: Article

References (75)

1. Andermann E, Andermann F. Genetic aspects of neuronal migration disorders. X-linked inheritance in subcortical band and periventricular nodular heterotopia; familial occurrence of bilateral perisylvian polymicrogyria. In: Guerrini R, Andermann F, Canapicchi R, Roger J, Zifkin BG, Pfanner P, editors. Dysplasias of Cerebral Cortex and Epilepsy. Philadelphia: Lippincott-Raven; 1996. p. 11-5.
2. Anton ES, Marchionni MA, Lee KF, Rakic P. Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 1997; 124: 3501-10.
3. v integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 1999; 22: 277-89.
4. Barkovich AJ, Jackson DE Jr, Boyer RS. Band heterotopias: A newly recognized neuronal migration anomaly. Radiology 1989; 171: 455-8.
5. Barkovich AJ, Guerrini R, Battaglia G, Kalifa G, N'Guyen T, Parmeggiani A, et al. Band heterotopia: Correlation of outcome with magnetic resonance imaging parameters. Ann Neurol 1994; 36: 609-17.
6. Berg MJ, Schiffitto G, Powers JM, Martinez-Capolino C, Fong CT, Myers GJ, et al. X-linked female band heterotopia-male lissencephaly syndrome. Neurology 1998; 50: 1143-6.
7. Cardoso C, Leventer RJ, Matsumoto N, Kuc JA, Ramocki MB, Mewborn SK, et al. The location and type of mutation predict malformation severity in isolated lissencephaly caused by abnormalities within the LIS1 gene. Hum Mol Genet 2000; 9: 3019-28.
8. Cardoso C, Leventer RJ, Dowling JJ, Ward HL, Chung J, Petras KS, et al. Clinical and molecular basis of classical lissencephaly: Mutations in the LIS1 gene (PAFAHIBI). [Review]. Hum Mutat 2002; 19: 4-15.
9. Chong SS, Pack SD, Roschke AV, Tanigami A, Carrozzo R, Smith AC, et al. A revision of the lissencephaly and Miller-Dieker syndrome critical regions in chromosome 17p13.3. Hum Mol Genet 1997; 6: 147-55.
10. CCTILAE. Proposal for revised clinical and electroencephalographic classification of epileptic seizures. Epilepsia 1981; 22: 489-501.
11. CCTILAE. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989; 30: 389-99.
12. D'Arcangelo G, Miao GG, Chen S-C, Soares HD, Morgan JI, Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995; 374: 719-23.
13. De Volder AG, Gadisseux J-F, Michel CJ, Maloteaux J-M, Bol AC, Grandin CB, et al. Brain glucose utilization in band heterotopia: Synaptic activity of 'double cortex'. Pediatr Neurol 1994; 11: 290-4.
14. des Portes V, Pinard JM, Smadja D, Motte J, Boespflug-Tanguy O, Moutard ML, et al. Dominant X-linked subcortical laminar heterotopia and lissencephaly syndrome (X-SCLH/LIS): Evidence for the occurrence of mutation in males and mapping of a potential locus in Xq22. J Med Genet 1997; 34: 177-83.
15. des Portes V, Pinard JM, Billuart P, Vinet MC, Koulakoff A, Carrié A, et al. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 1998a; 92: 51-61.
16. des Portes V, Francis F, Pinard JM, Desguerre I, Moutard ML, Snoeck I, et al. Doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum Mol Genet 1998b; 7: 1063-70.
17. Dobyns WB, Curry CJ, Hoyme HE, Turlington L, Ledbetter DH. Clinical and molecular diagnosis of Miller-Dieker syndrome. Am J Hum Genet 1991; 48: 584-94.
18. Dobyns WB, Reiner O, Carrozzo R, Ledbetter DH. Lissencephaly: A human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. [Review]. JAMA 1993; 270: 2838-42.
19. Dobyns WB, Andermann E, Andermann F, Czapansky-Beilman D, Dubeau F, Dulac O, et al. X-linked malformations of neuronal migration. [Review]. Neurology 1996; 47: 331-9.
20. Dobyns WB, Truwit CL, Ross ME, Matsumoto N, Pilz DT, Ledbetter DH, et al. Differences in the gyral pattern distinguish chromosome 17-linked and X-linked lissencephaly. Neurology 1999; 53: 270-7.
21. Federico A, Tomasetti P, Zollino M, Diomedi M, Dotti MT, De Stefano N, et al. Association of trisomy 9p and band heterotopia. Neurology 1999; 53: 430-2.
22. Fox JW, Lamperti ED, Eksioglu YZ, Hong SE, Feng Y, Graham DA, et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 1998; 21: 1315-25.
23. Franzoni E, Bernardi B, Marchiani V, Crisanti AF, Marchi R, Fonda C. Band brain heterotopia. Case report and literature review. [Review]. Neuropediatrics 1995; 26: 37-40.
24. Gallucci M, Bozzao A, Curatolo P, Splendiani A, Cifani A, Passariello R. MR imaging of incomplete band heterotopia. AJNR Am J Neuroradiol 1991; 12: 701-2.
25. Gigli GL, Tomassetti P, Diomedi M, Chierichetti F, Blasi C, Dotti MT, et al. Doppia corteccia, epilessia e ritardo mentale grave in un soggetto maschio con cariotipo 47XY+der(9). Boll Lega Ital Epil 1996; 95/96: 399-401.
26. Gleeson JG, Allen KM, Fox JF, Lamperti ED, Berkovic S, Scheffer I, et al. 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.
27. Gleeson JG, Minnerath SR, Fox JF, Allen KM, Luo RF, Hong SE, et al. Characterization of mutations in the gene doublecortin in patients with the double cortex syndrome. Ann Neurol 1999; 45: 146-53.
28. Gleeson JG, Luo RF, Grant PE, Guerrini R, Huttenlocher PR, Berg MJ, et al. Genetic and neuroradiological heterogeneity of double cortex syndrome. Ann Neurol 2000a; 47: 265-9.
29. Gleeson JG, Minnerath S, Kuzniecky RI, Dobyns WB, Young ID, Ross ME, et al. Somatic and germline mosaic mutations in the doublecortin gene are associated with variable phenotypes. Am J Hum Genet 2000b; 67: 574-81.
30. Gonzales JL, Russo CJ, Goldowitz D, Sweet HO, Davisson MT, Walsh CA. Birthdate and cell marker analysis of scrambler: A novel mutation affecting cortical development with a reeler-like phenotype. J Neurosci 1997; 17: 9204-11.
31. Guerrini R, Carrozzo R. Epilepsy and genetic malformations of the cerebral cortex. [Review]. Am J Med Genet 2001; 106: 160-73.
32. Harding B. Gray matter heterotopia. In: Guerrini R, Andermann F, Canapicchi R, Roger J, Zifkin BG, Pfanner P, editors. Dysplasias of Cerebral Cortex and Epilepsy. Philadelphia: Lippincott-Raven; 1996. p. 81-8.
33. Hashimoto R, Seki T, Takuma Y, Suzuki N. The 'double cortex' syndrome on MRI. Brain Dev 1993; 15: 57-9.
34. Hattori M, Adachi H, Tsujimoto M, Arai N, Inoue K. Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected]. Nature 1994; 370: 216-8.
35. Horesh D, Shapir T, Francis F, Wolf SG, Caspi M, Elbaum M, et al. Doublecortin, a stabilizer of microtubules. Hum Mol Genet 1999; 8: 1599-610.
36. Iannetti P, Raucci U, Basile LA, Spalice A, Di Biasi C, Trasimeni G, et al. Neuronal migrational disorders: Diffuse cortical dysplasia or the 'double cortex' syndrome. Acta Paediatr 1993; 82: 501-3.
37. Jacob H. Faktoren bei der entstehung der normalen und der entwicklungsgestörten hirnrinde. Z Ges Neurol Psychiat 1936; 155: 1-39.
38. Jacob H. Genetisch verschiedene gruppen entwicklungsgestörter gehirne. Z Ges Neurol Psychiat 1938; 160: 615-48.
39. Kato M, Kanai M, Soma O, Takusa Y, Kimura T, Numakura C, et al. Mutation of the doublecortin gene in male patients with double cortex syndrome: Somatic mosaicism detected by hair root analysis. Ann Neurol 2001; 50: 547-51.
40. Ketonen L, Roddy S, Lannan M. Band heterotopia. J Child Neurol 1994; 9: 384-5.
41. Landy HJ, Curless RG, Ramsay RE, Slater J, Ajmone-Marsan C, Quencer RM. Corpus callosotomy for seizures associated with band heterotopia. Epilepsia 1993; 34: 79-83.
42. Ledbetter SA, Kuwano A, Dobyns WB, Ledbetter DH. Microdeletions of chromosome 17p13 as a cause of isolated lissencephaly. Am J Hum Genet 1992; 50: 182-9.
43. Lo Nigro C, Chong CS, Smith AC, Dobyns WB, Carrozzo R, Ledbetter DH. Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum Mol Genet 1997; 6: 157-64.
44. Luria AR. The Working Brain: An Introduction to Neuropsychology. New York: Basic Books; 1973.
45. Matell M. Ein fall von heterotopie der grauen substanz in den beiden hemisphären des grosshirns. Arch Psychiat Nervkrankh 1893; 25: 124-36.
46. Matsumoto N, Leventer RJ, Kuc JA, Mewborn SK, Dudlicek LL, Ramocki MB, et al. Mutation analysis of the DCX gene and genotype/phenotype correlation in subcortical band heterotopia. Eur J Hum Genet 2001; 9: 5-12.
47. Miura K, Watanabe K, Maeda N, Matsumoto A, Kumagai T, Ito K, et al. Magnetic resonance imaging and positron emission tomography of band heterotopia. Brain Dev 1993; 15: 288-90.
48. Ogawa M, Miyata T, Nakajima K Yagyu K, Seike M, Ikenaka K, et al. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 1995; 14: 899-912.
49. Ono J, Mano T, Andermann E, Harada K, Sakurai K, Ikeda T, et al. Band heterotopia or double cortex in a male: Bridging structures suggest abnormality of the radial glial guide system. Neurology 1997; 48: 1701-3.
50. Palmini A, Andermann F, Aicardi J, Dulac O, Chaves F, Ponsot G, et al. Diffuse cortical dysplasia, or the 'double cortex' syndrome: The clinical and epileptic spectrum in 10 patients. Neurology 1991; 41: 1656-62.
51. Palmini A, Andermann F, de Grissac H, Tampieri D, Robitaille Y, Langevin P, et al. Stages and patterns of centrifugal arrest of diffuse neuronal migration disorders. Dev Med Child Neurol 1993; 35: 331-9.
52. Parmeggiani A, Santucci M, Ambrosetto P, Amadi A, Baioni E, Rossi PG. Interictal EEG findings in two cases with 'double cortex' syndrome. Brain Dev 1994; 16: 320-4.
53. Pilz DT, Matsumoto N, Minnerath S, Mills P, Gleeson JG, Allen KM, et al. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum Mol Genet 1998; 7: 2029-37.
54. Pilz DT, Kuc J, Matsumoto N, Bodurtha J, Bernadi B, Tassinari CA, et al. Subcortical band heterotopia in rare affected males can be caused by missense mutations in DCX (XLIS) or LIS1. Hum Mol Genet 1999; 8: 1757-60.
55. Pilz D, Stoodley N, Golden JA. Neuronal migration, cerebral cortical development and cerebral cortical anomalies. [Review]. J Neuropathol Exp Neurol 2002; 61: 1-11.
56. Pinard JM, Motte J, Chiron C, Brian R, Andermann E, Dulac O. Subcortical laminar heterotopia and lissencephaly in two families: A single X linked dominant gene. J Neurol Neurosurg Psychiatry 1994; 57: 914-20.
57. Pinard JM, Feydy A, Carlier R, Perez N, Pierot L, Burnod Y. Functional MRI in double cortex: Functionality of heterotopia. Neurology 2000; 54: 1531-3.
58. Poolos NP, Das S, Clark GD, Lardizabal D, Noebels JL, Wyllie E, et al. Males with epilepsy, complete subcortical band heterotopia, and somatic mosaicism for DCX. Neurology 2002; 58: 1559-62.
59. Rakic P, Caviness VS Jr. Cortical development: View from neurological mutants two decades later. [Review]. Neuron 1995; 14: 1101-4.
60. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, et al. Isolation of a Miller-Dieker lissencephaly gene containing G protein β-subunit-like repeats. Nature 1993; 364: 717-21.
61. Ricci S, Cusmai R, Fariello G, Fusco L, Vigevano F. Double cortex. A neuronal migration anomaly as possible cause of Lennox-Gastaut syndrome. Arch Neurol 1992; 49: 61-4.
62. Rice DS, Sheldon M, D'Arcangelo G Nakajima K, Goldowitz D, Curran T. Disabled-1 acts downstream of reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development 1998; 125: 3719-29.
63. Rio C, Rieff HI, Qi P, Khurana TS, Corfas G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 1997; 19: 39-50.
64. Ross ME, Allen KM, Srivastava AK, Featherstone T, Gleeson JG, Hirsch B, et al. Linkage and physical mapping of X-linked lissencephaly/SBH (XLIS): A gene causing neuronal migration defects in human brain. Hum Mol Genet 1997; 6: 555-62.
65. Saneto RP, Applegate KE, Frankel DG. Atypical manifestations of two cases of trisomy 9 syndrome: Rethinking development delay. Am J Med Genet 1998; 80: 42-5.
66. Sapir T, Elbaum M, Reiner O. Reduction in microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J 1997; 16: 6977-84.
67. Scheffer IE, Mitchell LA, Howell RA, Fitt G, Syngeniotis A, Saling M, et al. Familial band heterotopias: An X linked dominant disorder with variable severity [abstract]. Ann Neurol 1994; 36: 511.
68. 2+-dependent signaling protein which is mutated in human X-linked neuronal migration defects. Hum Mol Genet 1998; 7: 1372-32.
69. Soucek D, Birbamer G, Luef G, Felber S, Kristmann E, Bauer G. Laminar heterotopic grey matter (double cortex) in a patient with late onset Lennox-Gastaut syndrome. Wien Klin Wochenschr 1992; 104: 607-8.
70. Stem JM. The epilepsy of trisomy 9p. Neurology 1996; 47: 821-4.
71. Tohyama J, Kato M, Koeda T, Inagaki M, Ohno K. The double cortex syndrome. Brain Dev 1993; 15: 83-4.
72. Vossler GD, Lee JK, Ko TS. Treatment of seizures in subcortical laminar heterotopia with corpus callosotomy and lamotrigine. J Child Neurol 1999; 14: 282-8.
73. Wiest WD, Hallervorden J. Migrationshemmung in groß- und kleinhim. Dt Z Nervheilk 1958; 178: 224-38.
74. Wilson GN, Raj A, Baker D. The phenotypic and cytogenetic spectrum of partial trisomy 9. Am J Med Genet 1985; 20: 277-82.
75. Yoneshima H, Nagata E, Matsumoto M, Yamada M, Nakajima K, Miyata T, et al. A novel neurological mutation of mouse, yotari, which exhibits a reeler-like phenotype but expresses CR-50 antigen/reelin. Neurosci Res 1997; 29: 217-23.