Cobblestone lissencephaly: Neuropathological subtypes and correlations with genes of dystroglycanopathies

Brain

Volumn 135, Issue 2, 2012, Pages 469-482

  Devisme, Louise ^a   Bouchet, Céline ^b   Gonzals, Marie ^c   Alanio, Elisabeth ^d   Bazin, Anne ^e   Bessires, Bettina ^f   Bigi, Nicole ^g   Blanchet, Patricia ^g   Bonneau, Dominique ^h   Bonnires, Maryse ^f   Bucourt, Martine ⁱ   Carles, Dominique ^j   Clarisse, Bénedicte ^k   Delahaye, Sophie ^l   Fallet Bianco, Catherine ^m   Figarella Branger, Dominique ⁿ   Gaillard, Dominique ^d   Gasser, Bernard ^o   Delezoide, Anne Lise ^p   Guimiot, Fabien ^p   Joubert, Madeleine ^q   Laurent, Nicole ^r   Laquerrire, Annie ^s   Liprandi, Agns ⁿ   Loget, Philippe ^t   Marcorelles, Pascale ^u   Martinovic, Jelena ^e,f   Menez, Francoise ^p   Patrier, Sophie ^c   Pelluard, Fanny ^j   Perez, Marie José ^g   Rouleau, Caroline ^v   Triau, Stéphane ^w   Attié Bitach, Tania ^f   Vuillaumier Barrot, Sandrine ^b   Seta, Nathalie ^b   Encha Razavi, Férechté ^f   more..

^a LILLE UNIVERSITY HOSPITAL   (France)

^b BICHAT HOSPITAL   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d REIMS UNIVERSITY HOSPITAL   (France)

^e LABORATOIRE CERBA   (France)

^f HÔPITAL NECKER ENFANTS MALADES   (France)

^g HÔPITAL ARNAUD DE VILLENEUVE   (France)

^h UNIVERSITÉ D'ANGERS   (France)

ⁱ HÔPITAL JEAN VERDIER   (France)

^j HÔPITAL PELLEGRIN   (France)

^k UNIVERSITÉ PARIS DESCARTES   (France)

^l ARMAND TROUSSEAU HOSPITAL   (France)

^m CENTRE HOSPITALIER SAINTE ANNE   (France)

ⁿ TIMONE HOSPITAL   (France)

^o Hôpitaux Universitaires de Strasbourg   (France)

^p HÔPITAL ROBERT DEBRÉ   (France)

^q HÔTEL DIEU   (France)

^r DIJON UNIVERSITY HOSPITAL   (France)

^s UNIVERSITÉ DE ROUEN   (France)

^t PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

^u BREST UNIVERSITY HOSPITAL   (France)

^v MONTPELLIER UNIVERSITY HOSPITAL   (France)

^w ANGERS UNIVERSITY HOSPITAL   (France)

more..

Author keywords

cobblestone lissencephaly; lissencephaly type II; muscle eye brain disease; Walker Warburg syndrome; dystroglycanopathies

Indexed keywords

DOLICHOL PHOSPHATE MANNOSE; FUKUTIN; FUKUTIN RELATED PROTEIN; MEMBRANE PROTEIN; N ACETYLGLUCOSAMINYLTRANSFERASE; PROTEIN LARGE; PROTEIN POMGNT1; PROTEIN POMT1; PROTEIN POMT2; UNCLASSIFIED DRUG;

ARTICLE; COBBLESTONE LISSENCEPHALY; COBBLESTONE LISSENCEPHALY A; COBBLESTONE LISSENCEPHALY B; COBBLESTONE LISSENCEPHALY C; DISEASE CLASSIFICATION; DISEASE SEVERITY; FEMALE; FETUS; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; GENOTYPE PHENOTYPE CORRELATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; NEWBORN; PRIORITY JOURNAL;

EID: 84857207651     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr357     Document Type: Article

References (71)

1. Akasaka-Manya K, Manya H, Nakajima A, Kawakita M, Endo T. Physical and functional association of human protein o-mannosyltransferases 1 and 2. J Biol Chem 2006; 281: 19339-45. (Pubitemid 44035439)
2. Bahi-Buisson N, Poirier K, Boddaert N, Fallet-Bianco C, Specchio N, Bertini E, et al. GPR56-related bilateral frontoparietal polymicrogyria: further evidence for an overlap with the cobblestone complex. Brain 2010; 133: 3194-209.
3. Barkovich AJ. Neuroimaging manifestations and classification of congenital muscular dystrophies. AJNR Am J Neuroradiol 1998; 19: 1389-96. (Pubitemid 30431026)
4. Barkovich AJ, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns WB. Classification system for malformations of cortical development: update 2001. Neurology 2001; 57: 2168-78. (Pubitemid 34016447)
5. Barkovich AJ, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns WB. A developmental and genetic classification for malformations of cortical development. Neurology 2005; 65: 1873-87. (Pubitemid 43970104)
6. Barresi R, Campbell KP. Dystroglycan: from biosynthesis to pathogenesis of human disease. J Cell Sci 2006; 119 (Pt 2): 199-207. (Pubitemid 43210689)
7. Barresi R, Michele DE, Kanagawa M, Harper HA, Dovico SA, Satz JS, et al. LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med 2004; 10: 696-703. (Pubitemid 38937634)
8. Beltran-Valero de Bernabe D, Currier S, Steinbrecher A, Celli J, van Beusekom E, van der Zwaag B, et al. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 2002; 71: 1033-43. (Pubitemid 35305223)
9. Beltran-Valero de Bernabe D, Voit T, Longman C, Steinbrecher A, Straub V, Yuva Y, et al. Mutations in the FKRP gene can cause muscle-eye-brain disease and Walker-Warburg syndrome. J Med Genet 2004; 41: e61.
10. Bornemann A, Pfeiffer R, Beinder E, Wenkel H, Schlicker U, Meyermann R, et al. Three siblings with Walker-Warburg Syndrome. Gen Diagn Pathol 1996; 141: 371-5. (Pubitemid 26167131)
11. Bouchet C, Gonzales M, Vuillaumier-Barrot S, Devisme L, Lebizec C, Alanio E, et al. Molecular heterogeneity in fetal forms of type II lissencephaly. Hum Mutat 2007; 28: 1020-7. (Pubitemid 47519395)
12. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, et al. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha2 deficiency and abnormal glycosylation of alpha-dystroglycan. Am J Hum Genet 2001a; 69: 1198-209. (Pubitemid 33124201)
13. Brockington M, Yuva Y, Prandini P, Brown SC, Torelli S, Benson MA, et al. Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C. Hum Mol Genet 2001b; 10: 2851-9. (Pubitemid 34030916)
14. Chan YM, Keramaris-Vrantsis E, Lidov HG, Norton JH, Zinchenko N, Gruber HE, et al. Fukutin-related protein is essential for mouse muscle, brain and eye development and mutation recapitulates the wide clinical spectrums of dystroglycanopathies. Hum Mol Genet 2010; 19: 3995-4006.
15. Chiyonobu T, Sasaki J, Nagai Y, Takeda S, Funakoshi H, Nakamura T, et al. Effects of fukutin deficiency in the developing mouse brain. Neuromuscul Disord 2005; 15: 416-26. (Pubitemid 40720020)
16. Clement EM, Godfrey C, Tan J, Brockington M, Torelli S, Feng L, et al. Mild POMGnT1 mutations underlie a novel limb-girdle muscular dystrophy variant. Arch Neurol 2008; 65: 137-41.
17. Cotarelo RP, Valero MC, Prados B, Pena A, Rodriguez L, Fano O, et al. Two new patients bearing mutations in the fukutin gene confirm the relevance of this gene in Walker-Warburg syndrome. Clin Genet 2008; 73: 139-45.
18. Currier SC, Lee CK, Chang BS, Bodell AL, Pai GS, Job L, et al. Mutations in POMT1 are found in a minority of patients with Walker-Warburg syndrome. Am J Med Genet A 2005; 133A: 53-7. (Pubitemid 40175565)
19. D'Amico A, Tessa A, Bruno C, Petrini S, Biancheri R, Pane M, et al. Expanding the clinical spectrum of POMT1 phenotype. Neurology 2006; 66: 1564-7, discussion 461. (Pubitemid 43958556)
20. Dambska M, Wisniewski K, Sher JH. Lissencephaly: two distinct clinico-pathological types. Brain Dev 1983; 5: 302-10. (Pubitemid 13028342)
21. Dobyns WB, Pagon RA, Armstrong D, Curry CJ, Greenberg F, Grix A, et al. Diagnostic criteria for Walker-Warburg syndrome. Am J Med Genet 1989; 32: 195-210. (Pubitemid 19079374)
22. Encha-Razavi F, Chelly J. Pitfalls of the morphologic approach. J Neuropathol Exp Neurol 2006; 65: 302, author reply 303.
23. Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, et al. Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 2006; 26: 9184-95. (Pubitemid 44359845)
24. Esapa CT, Benson MA, Schroder JE, Martin-Rendon E, Brockington M, Brown SC, et al. Functional requirements for fukutin-related protein in the Golgi apparatus. Hum Mol Genet 2002; 11: 3319-31. (Pubitemid 36054660)
25. Esapa CT, McIlhinney RA, Blake DJ. Fukutin-related protein mutations that cause congenital muscular dystrophy result in ER-retention of the mutant protein in cultured cells. Hum Mol Genet 2005; 14: 295-305.
26. Ever L, Gaiano N. Radial 'glial' progenitors: neurogenesis and signaling. Curr Opin Neurobiol 2005; 15: 29-33. (Pubitemid 40249958)
27. Fink AJ, Englund C, Daza RA, Pham D, Lau C, Nivison M, et al. Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci 2006; 26: 3066-76.
28. Frost AR, Bohm SV, Sewduth RN, Josifova D, Ogilvie CM, Izatt L, et al. Heterozygous deletion of a 2-Mb region including the dystroglycan gene in a patient with mild myopathy, facial hypotonia, oral-motor dyspraxia and white matter abnormalities. Eur J Hum Genet 2010; 18: 852-5.
29. Fukuyama Y, Osawa M, Suzuki H. Congenital progressive muscular dystrophy of the Fukuyama type-clinical, genetic and pathological considerations. Brain Dev 1981; 3: 1-29. (Pubitemid 11125887)
30. Godfrey C, Clement E, Mein R, Brockington M, Smith J, Talim B, et al. Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain 2007; 130 (Pt 10): 2725-35. (Pubitemid 47511718)
31. Haltia M, Leivo I, Somer H, Pihko H, Paetau A, Kivela T, et al. Muscle-eye-brain disease: a neuropathological study. Ann Neurol 1997; 41: 173-80. (Pubitemid 27082098)
32. Hausmann B, Sievers J. Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity. J Comp Neurol 1985; 241: 50-62. (Pubitemid 16248801)
33. Hecht JH, Siegenthaler JA, Patterson KP, Pleasure SJ. Primary cellular meningeal defects cause neocortical dysplasia and dyslamination. Ann Neurol 2010; 68: 454-64.
34. Jayasinha V, Nguyen HH, Xia B, Kammesheidt A, Hoyte K, Martin PT. Inhibition of dystroglycan cleavage causes muscular dystrophy in transgenic mice. Neuromuscul Disord 2003; 13: 365-75. (Pubitemid 36687812)
35. Jellinger K, Rett A. Agyria-pachygyria (lissencephaly syndrome). Neuropadiatrie 1976; 7: 66-91.
36. Jissendi-Tchofo P, Kara S, Barkovich AJ. Midbrain-hindbrain involvement in lissencephalies. Neurology 2009; 72: 410-8.
37. Koirala S, Jin Z, Piao X, Corfas G. GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 2009; 29: 7439-49.
38. Labelle-Dumais C, Dilworth DJ, Harrington EP, de Leau M, Lyons D, Kabaeva Z, et al. COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker-Warburg syndrome in humans. PLoS Genet 2011; 7: e1002062.
39. Leyten QH, Renkawek K, Renier WO, Gabreels FJ, Mooy CM, ter Laak HJ, et al. Neuropathological findings in muscle-eye-brain disease (MEB-D). Neuropathological delineation of MEB-D from congenital muscular dystrophy of the Fukuyama type. Acta Neuropathol 1991; 83: 55-60.
40. Li S, Jin Z, Koirala S, Bu L, Xu L, Hynes RO, et al. GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 2008; 28: 5817-26.
41. Manya H, Chiba A, Yoshida A, Wang X, Chiba Y, Jigami Y, et al. Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci USA 2004; 101: 500-5. (Pubitemid 38084665)
42. Manzini MC, Gleason D, Chang BS, Hill RS, Barry BJ, Partlow JN, et al. Ethnically diverse causes of Walker-Warburg syndrome (WWS): FCMD mutations are a more common cause of WWS outside of the Middle East. Hum Mutat 2008; 29: E231-41.
43. Mercuri E, Messina S, Bruno C, Mora M, Pegoraro E, Comi GP, et al. Congenital muscular dystrophies with defective glycosylation of dystroglycan: a population study. Neurology 2009; 72: 1802-9.
44. Messina S, Mora M, Pegoraro E, Pini A, Mongini T, D'Amico A, et al. POMT1 and POMT2 mutations in CMD patients: a multicentric Italian study. Neuromuscul Disord 2008; 18: 565-71.
45. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, et al. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 2002; 418: 417-22. (Pubitemid 34826841)
46. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, et al. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 2002; 418: 422-5. (Pubitemid 34826842)
47. Morava E, Kuhnisch J, Drijvers JM, Robben JH, Cremers C, van Setten P, et al. Autosomal recessive mental retardation, deafness, ankylosis, and mild hypophosphatemia associated with a novel ANKH mutation in a consanguineous family. J Clin Endocrinol Metab 2010; 96: E189-98.
48. Muntoni F, Brockington M, Godfrey C, Ackroyd M, Robb S, Manzur A, et al. Muscular dystrophies due to defective glycosylation of dystroglycan. Acta Myol 2007; 26: 129-35. (Pubitemid 351668920)
49. Nadarajah B, Parnavelas JG. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 2002; 3: 423-32. (Pubitemid 135711798)
50. Nakano I, Funahashi M, Takada K, Toda T. Are breaches in the glia limitans the primary cause of the micropolygyria in Fukuyama-type congenital muscular dystrophy (FCMD)? Pathological study of the cerebral cortex of an FCMD fetus. Acta Neuropathol 1996; 91: 313-21. (Pubitemid 26042225)
51. Pagon RA, Chandler JW, Collie WR, Clarren SK, Moon J, Minkin SA, et al. Hydrocephalus, agyria, retinal dysplasia, encephalocele (HARD + -E) syndrome: an autosomal recessive condition. Birth Defects Orig Artic Ser 1978; 14: 233-41. (Pubitemid 9069999)
52. Peters A, Palay SL, Webster H. The fine structure of the nervous system: neurons and their supporting cells. New York: Oxford University Press; 1991.
53. Raitta C, Lamminen M, Santavuori P, Leisti J. Ophthalmological findings in a new syndrome with muscle, eye and brain involvement. Acta Ophthalmol (Copenh) 1978; 56: 465-72. (Pubitemid 8355406)
54. Ross ME. Full circle to cobbled brain. Nature 2002; 418: 376-7. (Pubitemid 34826826)
55. Santavuori P, Somer H, Sainio K, Rapola J, Kruus S, Nikitin T, et al. Muscle-eye-brain disease (MEB). Brain Dev 1989; 11: 147-53. (Pubitemid 19149730)
56. Satz JS, Barresi R, Durbeej M, Willer T, Turner A, Moore SA, et al. Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J Neurosci 2008; 28: 10567-75.
57. Silan F, Yoshioka M, Kobayashi K, Simsek E, Tunc M, Alper M, et al. A new mutation of the fukutin gene in a non-Japanese patient. Ann Neurol 2003; 53: 392-6. (Pubitemid 36258644)
58. Takada K, Nakamura H, Tanaka J. Cortical dysplasia in congenital muscular dystrophy with central nervous system involvement (Fukuyama type). J Neuropathol Exp Neurol 1984; 43: 395-407. (Pubitemid 14089420)
59. Takahashi S, Sasaki T, Manya H, Chiba Y, Yoshida A, Mizuno M, et al. A new beta-1,2-N-acetylglucosaminyltransferase that may play a role in the biosynthesis of mammalian O-mannosyl glycans. Glycobiology 2001; 11: 37-45. (Pubitemid 32201335)
60. Taniguchi K, Kobayashi K, Saito K, Yamanouchi H, Ohnuma A, Hayashi YK, et al. Worldwide distribution and broader clinical spectrum of muscle-eye-brain disease. Hum Mol Genet 2003; 12: 527-34. (Pubitemid 36305591)
61. Van der Knaap MS, Smit LM, Barth PG, Catsman-Berrevoets CE, Brouwer OF, Begeer JH, et al. Magnetic resonance imaging in classification of congenital muscular dystrophies with brain abnormalities. Ann Neurol 1997; 42: 50-9. (Pubitemid 27304780)
62. Van Reeuwijk J, Brunner HG, van Bokhoven H. Glyc-O-genetics of Walker-Warburg syndrome. Clin Genet 2005; 67: 281-9. (Pubitemid 40424824)
63. Van Reeuwijk J, Maugenre S, van den Elzen C, Verrips A, Bertini E, Muntoni F, et al. The expanding phenotype of POMT1 mutations: from Walker-Warburg syndrome to congenital muscular dystrophy, microcephaly, and mental retardation. Hum Mutat 2006; 27: 453-9. (Pubitemid 43673332)
64. Van Reeuwijk J, Grewal PK, Salih MA, Beltran-Valero de Bernabe D, McLaughlan JM, Michielse CB, et al. Intragenic deletion in the LARGE gene causes Walker-Warburg syndrome. Hum Genet 2007; 121: 685-90. (Pubitemid 46916967)
65. Viot G, Sonigo P, Simon I, Simon-Bouy B, Chadeyron F, Beldjord C, et al. Neocortical neuronal arrangement in LIS1 and DCX lissencephaly may be different. Am J Med Genet A 2004; 126A: 123-8. (Pubitemid 38445467)
66. Voss AK, Britto JM, Dixon MP, Sheikh BN, Collin C, Tan SS, et al. C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 2008; 135: 2139-49. (Pubitemid 352015148)
67. Wang VY, Rose MF, Zoghbi HY. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 2005; 48: 31-43. (Pubitemid 41384164)
68. Wang VY, Zoghbi HY. Genetic regulation of cerebellar development. Nat Rev Neurosci 2001; 2: 484-91. (Pubitemid 33676583)
69. Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, et al. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet 1997; 6: 831-41. (Pubitemid 27239066)
70. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M, et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 2001; 1: 717-24. (Pubitemid 33586123)
71. Zarbalis K, Siegenthaler JA, Choe Y, May SR, Peterson AS, Pleasure SJ. Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 2007; 104: 14002-7. (Pubitemid 350003326)