Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects

Trends in Genetics

Volumn 25, Issue 12, 2009, Pages 555-566

  Jaglin, Xavier H ^a,b   Chelly, Jamel ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN 1A; BETA TUBULIN 2B; DOUBLECORTIN; MICROTUBULE ASSOCIATED PROTEIN; PLATELET ACTIVATING FACTOR ACETYLHYDROLASE 1B1; REELIN; TUBULIN; UNCLASSIFIED DRUG;

AGYRIA; BRAIN DEVELOPMENT; CORPUS CALLOSUM AGENESIS; CORTICAL DYSPLASIA; EPILEPSY; FACE DYSMORPHIA; GENE MUTATION; HUMAN; MENTAL DEFICIENCY; MICROGYRIA; MICROTUBULE ASSEMBLY; NERVE CELL PLASTICITY; NEURONAL MIGRATION DISORDER; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SUBVENTRICULAR ZONE;

ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; HUMANS; MICROTUBULES; NEURONS; TUBULIN;

EID: 70449720657     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2009.10.003     Document Type: Review

References (109)

1. Francis F., et al. Human disorders of cortical development: from past to present. Eur. J. Neurosci. 23 (2006) 877-893
2. Ayala R., et al. Trekking across the brain: the journey of neuronal migration. Cell 128 (2007) 29-43
3. Guerrini R., et al. Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci. 31 (2008) 154-162
4. Reiner O., et al. Isolation of a Miller-Dieker lissencephaly gene containing G-protein beta-subunit-like repeats. Nature 364 (1993) 717-721
5. des Portes V., et al. Doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum. Mol. Genet. 7 (1998) 1063-1070
6. Gleeson J.G., et al. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92 (1998) 63-72
7. Kato M., et al. Mutations of ARX are associated with striking pleiotropy and consistent genotype-phenotype correlation. Hum. Mutat. 23 (2004) 147-159
8. Hong S.E., et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 26 (2000) 93-96
9. Ross M.E., et al. Lissencephaly with cerebellar hypoplasia (LCH): a heterogeneous group of cortical malformations. Neuropediatrics 32 (2001) 256-263
10. Zaki M., et al. Identification of a novel recessive RELN mutation using a homozygous balanced reciprocal translocation. Am. J. Med. Genet. 143A (2007) 939-944
11. Francis F., et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23 (1999) 247-256
12. Gleeson J.G., et al. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
13. Moores C.A., et al. Mechanism of microtubule stabilization by Doublecortin. Mol. Cell 14 (2004) 833-839
14. Moores C.A., et al. Distinct roles of Doublecortin modulating the microtubule cytoskeleton. EMBO J. 25 (2006) 4448-4457
15. Corbo J.C., et al. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 22 (2002) 7548-7557
16. Kappeler C., et al. Branching and nucleokinesis defects in migrating interneurons derived from Doublecortin knockout mice. Hum. Mol. Genet. 15 (2006) 1387-1400
17. Kappeler C., et al. Magnetic resonance imaging and histological studies of corpus callosal and hippocampal abnormalities linked to Doublecortin deficiency. J. Comp. Neurol. 500 (2007) 239-254
18. Hirotsune S., et al. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet. 19 (1998) 333-339
19. Cahana A., et al. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6429-6434
20. Gambello M.J., et al. Multiple dose-dependent effects of Lis1 on cerebral cortical development. J. Neurosci. 23 (2003) 1719-1729
21. Keays D.A., et al. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128 (2007) 45-57
22. Poirier K., et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin-alpha-1A (TUBA1A). Hum. Mutat. 28 (2007) 1055-1064
23. Bahi-Buisson N., et al. Refinement of cortical dysgeneses spectrum associated with TUBA1A mutations. J. Med. Genet. 45 (2008) 647-653
24. Morris-Rosendahl D.J., et al. Refining the phenotype of alpha-1a-tubulin (TUBA1A) mutation in patients with classical lissencephaly. Clin. Genet. 74 (2008) 425-433
25. Fallet-Bianco C., et al. Neuropathological phenotype of a distinct form of lissencephaly associated with mutations in TUBA1A. Brain 131 (2008) 2304-2320
26. Jansen A., and Andermann E. Genetics of the polymicrogyria syndromes. J. Med. Genet. 42 (2005) 369-378
27. Barkovich A.J., et al. A developmental and genetic classification for malformations of cortical development. Neurology 65 (2005) 1873-1887
28. Piao X., et al. G-protein-coupled receptor-dependent development of human frontal cortex. Science (New York, N.Y.) 303 (2004) 2033-2036
29. Roll P., et al. SRPX2 mutations in disorders of language cortex and cognition. Hum. Mol. Genet. 15 (2006) 1195-1207
30. Glaser T., et al. PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat. Genet. 7 (1994) 463-471
31. Baala L., et al. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat. Genet. 39 (2007) 454-456
32. Brooks A.S., et al. Homozygous nonsense mutations in KIAA1279 are associated with malformations of the central and enteric nervous systems. Am. J. Hum. Genet. 77 (2005) 120-126
33. Cantagrel V., et al. Truncation of NHEJ1 in a patient with polymicrogyria. Hum. Mutat. 28 (2007) 356-364
34. Aligianis I.A., et al. Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome. Nat. Genet. 37 (2005) 221-223
35. Jaglin X.H., et al. Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat. Genet. 41 (2009) 746-752
36. Li S., et al. GPR56 regulates pial basement membrane integrity and cortical lamination. J. Neurosci. 28 (2008) 5817-5826
37. Nasrallah I.M., et al. Analysis of non-radial interneuron migration dynamics and its disruption in Lis1+/- mice. J. Comp. Neurol. 496 (2006) 847-858
38. Pancoast M., et al. Interneuron deficits in patients with the Miller-Dieker syndrome. Acta Neuropathol. 109 (2005) 400-404
39. Coksaygan T., et al. Neurogenesis in alpha-1-tubulin transgenic mice during development and after injury. Exp. Neurol. 197 (2006) 475-485
40. Bai J., et al. RNAi reveals Doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 6 (2003) 1277-1283
41. LoTurco J.J., and Bai J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 29 (2006) 407-413
42. Witte H., et al. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180 (2008) 619-632
43. Sapir T., et al. Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J. Neurosci. 28 (2008) 5710-5720
44. Sapir T., et al. Antagonistic effects of Doublecortin and MARK2/Par-1 in the developing cerebral cortex. J. Neurosci. 28 (2008) 13008-13013
45. Tian G., et al. A pachygyria-causing alpha-tubulin mutation results in inefficient cycling with CCT and a deficient interaction with TBCB. Mol. Biol. Cell 19 (2008) 1152-1161
46. Lewis S.A., et al. Five mouse tubulin isotypes and their regulated expression during development. J. Cell Biol. 101 (1985) 852-861
47. Hoyle H.D., and Raff E.C. Two Drosophila beta-tubulin isoforms are not functionally equivalent. J. Cell Biol. 111 (1990) 1009-1026
48. Luduena R.F., et al. Interaction of halichondrin B and homohalichondrin B with bovine brain tubulin. Biochem. Pharmacol. 45 (1993) 421-427
49. Lu Q., and Luduena R.F. In vitro analysis of microtubule assembly of isotypically pure tubulin dimers. Intrinsic differences in the assembly properties of alpha beta II, alpha beta III and alpha beta IV tubulin dimers in the absence of microtubule-associated proteins. J. Biol. Chem. 269 (1994) 2041-2047
50. Schwer H.D., et al. A lineage-restricted and divergent beta-tubulin isoform is essential for the biogenesis, structure and function of blood platelets. Curr. Biol. 11 (2001) 579-586
51. McKean P.G., et al. The extended tubulin superfamily. J. Cell Sci. 114 (2001) 2723-2733
52. Bode C.J., et al. The two alpha-tubulin isotypes in budding yeast have opposing effects on microtubule dynamics in vitro. EMBO Reports 4 (2003) 94-99
53. Barnes A.P., et al. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129 (2007) 549-563
54. Shi S.H., et al. APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14 (2004) 2025-2032
55. Yokota Y., et al. The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 61 (2009) 42-56
56. Deuel T.A., et al. Genetic interactions between Doublecortin and Doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49 (2006) 41-53
57. Koizumi H., et al. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat. Neurosci. 9 (2006) 779-786
58. Poulain F.E., and Sobel A. The microtubule network and neuronal morphogenesis: dynamic and coordinated orchestration through multiple players. Molecular and Cellular Neurosciences (2009)
59. Lopez-Bendito G., et al. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125 (2006) 127-142
60. Westermann S., and Weber K. Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4 (2003) 938-947
61. Creppe C., et al. Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136 (2009) 551-564
62. Li H., et al. Microtubules are critical for radial glial morphology: possible regulation by MAPs and MARKs. Glia 44 (2003) 37-46
63. Jin Z., et al. Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum. Mol. Genet. 16 (2007) 1972-1985
64. Chang B.S., et al. A familial syndrome of unilateral polymicrogyria affecting the right hemisphere. Neurology 66 (2006) 133-135
65. Sun T., and Walsh C.A. Molecular approaches to brain asymmetry and handedness. Nature Reviews 7 (2006) 655-662
66. Bommel H., et al. Missense mutation in the tubulin-specific chaperone E (TBCE) gene in the mouse mutant progressive motor neuronopathy, a model of human motoneuron disease. Journal Cell Biol. 159 (2002) 563-569
67. Martin N., et al. A missense mutation in TBCE causes progressive motor neuronopathy in mice. Nat. Genet. 32 (2002) 443-447
68. Padidela R., et al. Mutation in the TBCE gene is associated with hypoparathyroidism-retardation-dysmorphism syndrome featuring pituitary hormone deficiencies and hypoplasia of the anterior pituitary and the corpus callosum. J. Clin. Endocr. Metab. 94 (2009) 2686-2691
69. Bond J., et al. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32 (2002) 316-320
70. Bond J., and Woods C.G. Cytoskeletal genes regulating brain size. Curr. Opin. Cell Biol. 18 (2006) 95-101
71. Heng J.I., et al. Neurotransmitters regulate cell migration in the telencephalon. Eur. J. Neurosci. 26 (2007) 537-546
72. Métin C., et al. Modes and mishaps of neuronal migration in the mammalian brain. J. Neurosci. 28 (2008) 11746-11752
73. Bortone D., and Polleux F. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62 (2009) 53-71
74. Gascon E., et al. GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 26 (2006) 12956-12966
75. Kriegstein A., et al. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nature Reviews 7 (2006) 883-890
76. Molnar Z., et al. Comparative aspects of cerebral cortical development. Eur. J. Neurosci. 23 (2006) 921-934
77. Bystron I., et al. Development of the human cerebral cortex: boulder committee revisited. Nature Reviews 9 (2008) 110-122
78. Ramòn y Cajal S., et al. Histology of the nervous system of man and vertebrates (1995), Oxford University Press
79. Bystron I., et al. The first neurons of the human cerebral cortex. Nat. Neurosci. 9 (2006) 880-886
80. Garcia-Moreno F., et al. Origins and migratory routes of murine Cajal-Retzius cells. J. Comp. Neurol. 500 (2007) 419-432
81. Noctor S.C., et al. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409 (2001) 714-720
82. Malatesta P., et al. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development (Cambridge, England) 127 (2000) 5253-5263
83. Hartfuss E., et al. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229 (2001) 15-30
84. Heins N., et al. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5 (2002) 308-315
85. Malatesta P., et al. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37 (2003) 751-764
86. Anthony T.E., et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41 (2004) 881-890
87. Noctor S.C., et al. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7 (2004) 136-144
88. Mo Z., et al. Human cortical neurons originate from radial glia and neuron-restricted progenitors. J Neurosci 27 (2007) 4132-4145
89. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145 (1972) 61-83
90. Kriegstein A.R., and Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27 (2004) 392-399
91. Wonders C.P., and Anderson S.A. The origin and specification of cortical interneurons. Nature Reviews 7 (2006) 687-696
92. Marin O., and Rubenstein J.L. A long, remarkable journey: tangential migration in the telencephalon. Nature Reviews 2 (2001) 780-790
93. Letinic K., et al. Origin of GABAergic neurons in the human neocortex. Nature 417 (2002) 645-649
94. Petanjek Z., et al. Distinct origin of GABAergic neurons in forebrain of man, nonhuman primates and lower mammals. Collegium Antropol. 32 Suppl 1 (2008) 9-17
95. Petanjek Z., et al. Origins of cortical GABAergic neurons in the cynomolgus monkey. Cereb. Cortex 19 (2009) 249-262
96. Price D.J., et al. The development of cortical connections. Eur. J. Neurosci. 23 (2006) 910-920
97. Dutcher S.K. The tubulin fraternity: alpha to eta. Curr. Opin. Cell Biol. 13 (2001) 49-54
98. Miller F.D., et al. Isotypes of alpha-tubulin are differentially regulated during neuronal maturation. J. Cell Biol. 105 (1987) 3065-3073
99. Cowan N.J., and Lewis S.A. Type II chaperonins, prefoldin and the tubulin-specific chaperones. Adv. in Prot. Chem. 59 (2001) 73-104
100. Desai A., and Mitchison T.J. Microtubule polymerization dynamics. Ann. Rev. Cell Dev. Bi. 13 (1997) 83-117
101. Mitchison T., and Kirschner M. Dynamic instability of microtubule growth. Nature 312 (1984) 237-242
102. Nogales E., et al. High-resolution model of the microtubule. Cell 96 (1999) 79-88
103. Palazzo A., et al. Cell biology: tubulin acetylation and cell motility. Nature 421 (2003) 230
104. Barnes A.P., and Polleux F. Establishment of axon-dendrite polarity in developing neurons. Ann. Rev. Neurosci. 32 (2009) 347-381
105. Conde C., and Caceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nature Reviews 10 (2009) 319-332
106. Metin C., et al. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur. J. Neurosci. 23 (2006) 894-900
107. Tian G., et al. Pathway leading to correctly folded beta-tubulin. Cell 86 (1996) 287-296
108. Lewis S.A., et al. The alpha- and beta-tubulin folding pathways. Trends in Cell Biology 7 (1997) 479-484
109. Graus-Porta D., et al. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31 (2001) 367-379