The cerebral cortex malformation in thanatophoric dysplasia: Neuropathology and pathogenesis

Acta Neuropathologica

Volumn 110, Issue 3, 2005, Pages 208-221

  Hevner, Robert F ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Fibroblast growth factor 8 (FGF8); Fibroblast growth factor receptor 3 (FGFR3); Megalencephaly; Polymicrogyria

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3;

APOPTOSIS; BRAIN CORTEX LESION; BRAIN MALFORMATION; CELL PROLIFERATION; CHONDRODYSPLASIA; CLINICAL FEATURE; CLINICAL OBSERVATION; DISEASE ASSOCIATION; DISEASE MODEL; DISEASE SEVERITY; ENZYME ACTIVATION; GENETIC ANALYSIS; GESTATIONAL AGE; HIPPOCAMPUS; HUMAN; HYPERPLASIA; MOUSE; NEUROPATHOLOGY; NONHUMAN; ONTOGENY; PHENOTYPE; PREMATURITY; PRIORITY JOURNAL; PUBLISHING; REVIEW; STEM CELL; TEMPORAL LOBE; THANATOPHORIC DWARFISM;

ANIMALS; APOPTOSIS; BODY PATTERNING; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBRAL CORTEX; HUMANS; MUTATION; NERVOUS SYSTEM MALFORMATIONS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; THANATOPHORIC DYSPLASIA;

EID: 26444491115     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-005-1059-8     Document Type: Review

References (78)

1. Assimacopoulos S, Grove EA, Ragsdale CW (2003) Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci 23:6399-6403 12878679
2. Baker KM, Olson DS, Harding CO, Pauli RM (1997) Long-term survival in typical thanatophoric dysplasia type 1. Am J Med Genet 70:427-436 10.1002/(SICI)1096-8628(19970627)70:4<427::AID-AJMG18>3.0.CO;2-J
3. Bansal R, Lakhina V, Remedios R, Tole S (2003) Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with Pdgfrα, Olig2 and Plp/dm20: Implications for oligodendrocyte development. Dev Neurosci 25:83-95 10.1159/000072258
4. Bishop KM, Garel S, Nakagawa Y, Rubenstein JLR, O'Leary DDM (2003) Emx1 and Emx2 cooperate to regulate cortical size, lamination, neuronal differentiation, development of cortical efferents, and thalamocortical pathfinding. J Comp Neurol 457:345-360 10.1002/cne.10550
5. Bloomfield JA (1970) Cloverleaf skull and thanatophoric dwarfism. Australas Radiol 14:429-437 5498302
6. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369 10.1126/ science.1074192
7. Cohen MM Jr (2002) Some chondrodysplasias with short limbs: Molecular perspectives. Am J Med Genet 112:304-313 10.1002/ajmg.10780
8. Cohen MM Jr, Kreiborg S (1990) The central nervous system in the Apert syndrome. Am J Med Genet 35:36-45 10.1002/ajmg.1320350108
9. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet 12:390-397 10.1038/ng0496-390
10. Coulter CL, Leech RW, Brumback RA, Schaefer GB (1991) Cerebral abnormalities in thanatophoric dysplasia. Child's Nerv Syst 7:21-26
11. Crossley PH, Martin GR (1995) The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121:439-451 7768185
12. De Basio P, Prefumo F, Baffico M, Baldi M, Priolo M, Lerone M, Toma P, Venturini PL (2000) Sonographic and molecular diagnosis of thanatophoric dysplasia type I at 18 weeks of gestation. Prenat Diagn 20:835-837 10.1002/1097-0223(200010)20:10<835::AID-PD903>3.0.CO;2-N
13. Dennis JP, Rosenberg HS, Alvord EC Jr (1961) Megalencephaly, internal hydrocephalus and other neurological aspects of achondroplasia. Brain 84:427-445 13885465
14. Dono R, Texido G, Dussel R, Ehmke H, Zeller R (1998) Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213-4225 10.1093/emboj/17.15.4213
15. Faye-Peterson OM, Knisely AS (1991) Neural arch stenosis and spinal cord injury in thanatophoric dysplasia. Am J Dis Child 145:87-89 1985437
16. Ford-Perriss M, Abud H, Murphy M (2001) Fibroblast growth factors in the developing central nervous system. Clin Exp Pharmacol Physiol 28:493-503 10.1046/j.1440-1681.2001.03477.x
17. Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071-1074 10.1126/ science.1064252
18. Galatioto S, Gemelli M, Granese D, Longo M (1984) Thanatophoric dwarfism and "cloverleaf skull" syndrome: A neuropathological report. Pathologica 76:255-261 6472902
19. Garel S, Huffman KJ, Rubenstein JLR (2003) Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 130:1903-1914 10.1242/dev.00416
20. Gemelli M, Galatioto S, Longo M, Granese D (1982) Nanismo tanatoforo con cranio a trifoglio [Thanatophoric dwarfism with cloverleaf skull]. Minerva Pediatr 34:977-982 7155102
21. Golden JA (2001) Periventricular heterotopia may result from radial glial fiber disruption. J Neuropathol Exp Neurol 60:856-862
22. Gouti F, Aicardi J, Farkas-Bargeton E (1971) Une malformation cérébrale particulière associé au nanisme thanatophore. Presse Med 79:960
23. Goutieres F, Aicardi J. Farkas-Bargeton E (1971) Une malformation cérébrale particuliere associée au nanisme thanatophore. Rev Neurol 125:435-440 5154079
24. Grove EA, Fukuchi-Shimogori T (2003) Generating the cerebral cortical area map. Annu Rev Neurosci 26:355-380 10.1146/ annurev.neuro.26.041002.131137
25. Gruenwald P, Minh HN (1960) Evaluation of body and organ weights in perinatal pathology. I. Normal standards derived from autopsies. Am J Clin Pathol 34:247-253
26. Hamasaki T, Leingartner A, Ringstedt T, O'Leary D (2004) EMX2 regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron 43:359-372 10.1016/j.neuron.2004.07.016
27. Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, Kageyama R (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131:5539-5550 10.1242/dev.01436
28. Haydar TF, Kuan C-Y, Flavell RA, Rakic P (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb Cortex 9:621-626 10.1093/cercor/9.6.621
29. Hevner RF (2005) From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol, in press
30. Ho K-L, Chang C-H, Yang SS, Chason JL (1984) Neuropathologic findings in thanatophoric dysplasia. Acta Neuropathol (Berl) 63:218-228
31. Hodge RD, D'Ercole AJ, O'Kusky JR (2004) Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J Neurosci 10:10201-10210 10.1523/JNEUROSCI.3246-04.2004
32. Hodge RD, D'Ercole AJ, O'Kusky JR (2005) Increased expression of insulin-like growth factor-I (IGF-I) during embryonic development produces neocortical overgrowth with differentially greater effects on specific architectonic areas and cortical layers. Brain Res Dev Brain Res 154:227-237 10.1016/j.devbrainres.2004.10.016
33. Hori A, Friede RL, Fischer G (1983) Ventricular diverticles with localized dysgenesis of the temporal lobe in cloverleaf skull anomaly. Acta Neuropathol (Berl) 60:132-136
34. Huguenin M, Godard C, Ferrier PE, Bamatter F (1969) Two different mutations within the same sibship: Thanatophoric dwarfism and Ullrich-Feichtiger syndrome. Helv Paediatr Acta 24:239-245 5800158
35. Inglis-Broadgate SL, Thomson RE, Pellicano F, Tartaglia MA, Pontikis CC, Cooper JD, Iwata T (2005) FGFR3 regulates brain size by controlling progenitor cell proliferation and apoptosis during embryonic development. Dev Biol 279:73-85 10.1016/j.ydbio.2004.11.035
36. International nomenclature of constitutional diseases of bone (1978) Revision - May, 1977. J Pediatr 93:614-616 702238
37. Iwata T, Chen L, Li C, Ovchinnikov DA, Behringer RR, Francomano CA, Deng CX (2000) A neonatal lethal mutation in FGFR3 uncouples proliferation and differentiation of growth plate chondrocytes in embryos. Hum Mol Genet 9:1603-1613 10.1093/hmg/9.11.1603
38. Joyner AL, Liu A, Millet S (2000) Otx2, Gbx2 and Fgf8 interact to position and maintain a mid - hindbrain organizer. Curr Opin Cell Biol 12:736-741 10.1016/S0955-0674(00)00161-7
39. Kalache KD, Lehmann K, Chaoui R, Kivelitz DE, Mundlos S, Bollmann R (2002) Prenatal diagnosis of partial agenesis of the corpus callosum in a fetus with thanatophoric dysplasia type 2. Prenat Diagn 22:404-407 10.1002/pd.327
40. Knisely AS, Ambler MW (1988) Temporal-lobe abnormalities in thanatophoric dysplasia. Pediatr Neurosci 14:169-176 3269536
41. Kozlowski K, Warren PS, Fisher CC (1985) Cloverleaf skull with generalized bone dysplasia: Report of a case with short review of the literature. Pediatr Radiol 15:412-414 4058967
42. Kuida K, Haydar TF, Kuan C-Y, Gu Y, Taya C, Karasuyama H, Su MS-S, Rakic P, Flavell RA (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94:325-337 10.1016/ S0092-8674(00)81476-2
43. Langer LO Jr, Yang SS, Hall JG, Sommer A, Kottamasu SR, Golabi M, Krassikoff N (1987) Thanatophoric dysplasia and cloverleaf skull. Am J Med Genet (Suppl) 3:167-179
44. Leroy JG, Timmermans J, Elsen AF van (1974) Fatal neonatal dwarfism: examples of thanatophoric dwarfism and of hypophosphatasia. Birth Defects Orig Artic Ser 10:21-30 4618133
45. Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA (2003) Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302:1560-1563 10.1126/science.1087621
46. Lievens PM-J, Liboi E (2003) The thanatophoric dysplasia type II mutation hampers complete maturation of fibroblast growth factor receptor 3 (FGFR3), which activates signal transducer and activator of transcription 1 (STAT1) from the endoplasmic reticulum. J Biol Chem 278:17344-17349 10.1074/jbc.M212710200
47. Lin T, Sandusky SB, Xue H, Fishbein KW, Spencer RG, Rao MS, Francomano CA (2003) A central nervous system specific mouse model for thanatophoric dysplasia type II. Hum Mol Genet 12:2863-2871 10.1093/hmg/ ddg309
48. Maksem JA, Roessmann U (1979) Apert's syndrome with central nervous system anomalies. Acta Neuropathol (Berl) 48:59-61
49. Maroteaux P, Lamy M, Robert J-M (1967) Le nanisme thanatophore [Thanatophoric dwarfism]. Presse Med 75:2519-2524 6073727
50. Martinelli B, Campailla E, Ferrari G (1975) Malformation cerebrale particuliere et nanisme thanatophore. Arch Fr Pediatr 32:455-459 1181996
51. Maruoka Y, Ohbayashi N, Hoshikawa M, Itoh N, Hogan BLM, Furuta Y (1998) Comparison of the expression of three highly related genes, Fgf8, Fgf17 and Fgf18, in the mouse embryo. Mech Dev 74:175-177
52. Mueller SM (1980) Enlarged cerebral ventricular system in infant achondroplastic dwarf. Neurology 30:767-769
53. Muzio L, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P, Mallamaci A (2002) Emx2 and Pax6 control regionalization of the pre-neuronogenic cortical primordium. Cereb Cortex 12:129-139
54. Naski MC, Wang Q, Xu J, Ornitz DM (1996) Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat Genet 13:233-237 10.1038/ng0696-233
55. Norman A, Rimmer S, Landy S, Donnai D (1992) Thanatophoric dysplasia of the straight - bone type (type 2). Clin Dysmorphol 1:115-120 1345514
56. Noronha L, Prevedello LMS, Maggio EM, Serapião MJ, Torres LFB (2002) Displasia tanatofórica: Relato de dois casos com estudo neuropatológico. Arq Neuropsiquiatr 60:133-137 11965423
57. Orioli I, Castilla E, Barbosa-Neto J (1986) The birth prevalence rates for the skeletal dysplasias. J Med Genet 23:328-332
58. Partington MW, Gonzales-Crussi F, Khakee SG, Wollin DG (1971) Cloverleaf skull and thanatophoric dwarfism: Report of four cases, two in the same sibship. Arch Dis Child 46:656-664 5315768
59. Peters K, Ornitz D, Werner S, Williams L (1993) Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev Biol 155:423-430 10.1006/dbio.1993.1040
60. Plomp AS, Hamel BCJ, Cobben JM, Verloes A, Offermans JPM, Lajeunie E, Fryns JP, Die-Smulders CEM de (1998) Pfeiffer syndrome type 2: Further delineation and review of the literature. Am J Med Genet 75:245-251 10.1002/(SICI)1096-8628(19980123)75:3<245::AID-AJMG3>3.0.CO;2-P
61. Potter EL, Craig J (1972) Pathology of the fetus and infant. Year Book Medical Publishers, Chicago
62. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000) Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20:5012-5023 10864959
63. Ragsdale CW, Grove EA (2001) Patterning the mammalian cerebral cortex. Curr Opin Neurobiol 11:50-58 10.1016/S0959-4388(00)00173-2
64. Rakic P (1988) Specification of cerebral cortical areas. Science 241:170-176 3291116
65. Ronconi GF, Pesenti P, Mercurella A, Sassolino S (1986) Descrizione di un caso di displasia tanatofora con cranio a trifoglio [A case of thanatophoric dysplasia with cloverleaf skull]. Pediatr Med Chir 8:423-426
66. Rubenstein JLR, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R (1999) Genetic control of cortical regionalization and connectivity. Cereb Cortex 9:524-532 10.1093/cercor/9.6.524
67. Sahinoglu Z, Uludogan M, Gurbuz A, Karateke A (2003) Prenatal diagnosis of thanatophoric dysplasia in the second trimester: Ultrasonography and other diagnostic modalities. Arch Gynecol Obstet 269:57-61 10.1007/ s00404-002-0417-1
68. Shah K, Astley R, Cameron AH (1973) Thanatophoric dwarfism. J Med Genet 10:243-252 4204337
69. Shigematsu H, Takashima S, Otani K, Ieshima A (1985) Neuropathological and Golgi study on a case of thanatophoric dysplasia. Brain Dev 7:628-632 3832954
70. Shimogori T, Banuchi V, Ng HY, Strauss JB, Grove EA (2004) Embryonic signaling centers expressing BMP, WNT, and FGF proteins interact to pattern the cerebral cortex. Development 131:5639-5647 10.1242/dev.01428
71. Tavormina PL, Shiang R, Thompson LM, Zhu Y-Z, Wilkin DJ, Lachman RS, Wilcox WR, Rimoin DL, Cohn DH, Wasmuth JJ (1995) Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat Genet 9:321-328. 10.1038/ng0395-321
72. Ueno H, Gunn M, Dell K, Tseng A Jr, Williams L (1992) A truncated form of fibroblast growth factor receptor 1 inhibits signal transduction by multiple types of fibroblast growth factor receptor. J Biol Chem 267:1470-1476 1309784
73. Van der Harten HJ, Brons JTJ, Dijkstra PF, Barth PG, Niermeyer MF, Meijer CJLM, van Geijn HP, Arts NFT (1993) Some variants of lethal neonatal short-limbed platyspondylic dysplasia: A radiological ultrasonographic, neuropathological and histopathological study of 22 cases. Clin Dysmorphol 2:1-19 8298733
74. Webster MK, D'Avis PY, Robertson SC, Donoghue DJ (1996) Profound ligand - independent kinase activation of fibroblast growth factor receptor 3 by the activation loop mutation responsible for a lethal skeletal dysplasia, thanatophoric dysplasia type II. Mol Cell Biol 16:4081-4087 8754806
75. Wilcox WR, Tavormina PL, Krakow D, Kitoh H, Lachman RS, Wasmuth JJ, Thompson LM, Rimoin DL (1998) Molecular, radiologic, and histopathologic correlations in thanatophoric dysplasia. Am J Med Genet 78:274-281 10.1002/(SICI)1096-8628(19980707)78:3<274::AID-AJMG14>3.0.CO;2-C
76. Wongmongkolrit T, Bush M, Roessmann U (1983) Neuropathological findings in thanatophoric dysplasia. Arch Pathol Lab Med 107:132-135
77. Yamaguchi K, Honma K (2001) Autopsy case of thanatophoric dysplasia: observations on the serial sections of the brain. Neuropathology 21:222-228 10.1046/j.1440-1789.2001.00386.x
78. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA (2004) Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131:5441-5448 10.1242/dev.0143