Mutations in α-Tubulin Cause Abnormal Neuronal Migration in Mice and Lissencephaly in Humans

Cell

Volumn 128, Issue 1, 2007, Pages 45-57

  Keays, David A ^a   Tian, Guoling ^b   Poirier, Karine ^g   Huang, Guo Jen ^a   Siebold, Christian ^a   Cleak, James ^a   Oliver, Peter L ^c   Fray, Martin ^d   Harvey, Robert J ^e   Molnár, Zoltán ^f   Piñon, Maria C ^f   Dear, Neil ^d   Valdar, William ^a   Brown, Steve D M ^d   Davies, Kay E ^c   Rawlins, J Nicholas P ^f   Cowan, Nicholas J ^b   Nolan, Patrick ^d   Chelly, Jamel ^g   Flint, Jonathan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c MRC Functional Genetics Unit   (United Kingdom)

^d MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^e UNIVERSITY OF LONDON   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; ETHYLNITROSOUREA; GUANINE NUCLEOTIDE BINDING PROTEIN;

AGYRIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MALFORMATION; BRAIN NERVE CELL; CASE REPORT; CAUSAL ATTRIBUTION; CELL MIGRATION; CHEMICAL MUTAGENESIS; CONTROLLED STUDY; CYTOARCHITECTURE; DNA BINDING MOTIF; EMBRYO; FEMALE; GENE; GENE IDENTIFICATION; GENE MUTATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC SCREENING; GENOTYPE PHENOTYPE CORRELATION; HIPPOCAMPUS; HUMAN; INDUCED MUTATION; MALE; MAMMALIAN GENETICS; MICROTUBULE ASSEMBLY; MOUSE; MOUSE MUTANT; MUTATIONAL ANALYSIS; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; TUBA1 GENE; TUBA3 GENE;

MAMMALIA; MUS;

EID: 33846037932     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.12.017     Document Type: Article

References (46)

1. Angevine Jr. J.B. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl 2 (1965) 1-70
2. Bannerman D.M., Deacon R.M., Brady S., Bruce A., Sprengel R., Seeburg P.H., and Rawlins J.N. A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav. Neurosci. 118 (2004) 643-647
3. Bartolini F., Bhamidipati A., Thomas S., Schwahn U., Lewis S.A., and Cowan N.J. Functional overlap between retinitis pigmentosa 2 protein and the tubulin-specific chaperone cofactor C. J. Biol. Chem. 277 (2002) 14629-14634
4. Basten C.J., Zeng Z.B., and Weir B.S. QTLCartographer: a suite of programs for mapping quantitative trait loci. Abstracts to Plant Genome, IV (1996), Academic Press, San Diego
5. 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., and 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. 77 (2005) 477-483
6. Buhot M.C., Dubayle D., Malleret G., Javerzat S., and Segu L. Exploration, anxiety, and spatial memory in transgenic anophthalmic mice. Behav. Neurosci. 115 (2001) 455-467
7. Churchill G.A., and Doerge R.W. Empirical threshold values for quantitative trait mapping. Genetics 138 (1994) 963-971
8. Corbo J.C., Deuel T.A., Long J.M., LaPorte P., Tsai E., Wynshaw-Boris A., and Walsh C.A. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22 (2002) 7548-7557
9. Deacon R.M., Croucher A., and Rawlins J.N. Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behav. Brain Res. 132 (2002) 203-213
10. Demyanenko G.P., Schachner M., Anton E., Schmid R., Feng G., Sanes J., and Maness P.F. Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron 44 (2004) 423-437
11. des Portes V., Pinard J.M., Billuart P., Vinet M.C., Koulakoff A., Carrie A., Gelot A., Dupuis E., Motte J., Berwald-Netter Y., et al. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92 (1998) 51-61
12. Dobyns W.B., and Truwit C.L. Lissencephaly and other malformations of cortical development: 1995 update. Neuropediatrics 26 (1995) 132-147
13. Farr S.A., Banks W.A., La Scola M.E., and Morley J.E. Blind mice are not impaired in T-maze footshock avoidance acquisition and retention. Physiol. Behav. 76 (2002) 531-538
14. Francis F., Meyer G., Fallet-Bianco C., Moreno S., Kappeler C., Socorro A.C., Tuy F.P., Beldjord C., and Chelly J. Human disorders of cortical development: from past to present. Eur. J. Neurosci. 23 (2006) 877-893
15. Gao Y., Thomas J.O., Chow R.L., Lee G.H., and Cowan N.J. A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell 69 (1992) 1043-1050
16. 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., and Walsh C.A. 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
17. Gloster A., El-Bizri H., Bamji S.X., Rogers D., and Miller F.D. Early induction of Talpha1 alpha-tubulin transcription in neurons of the developing nervous system. J. Comp. Neurol. 405 (1999) 45-60
18. Gu W., and Cowan N.J. Assembly properties of altered beta-tubulin polypeptides containing disrupted autoregulatory domains. Mol. Cell. Biol. 9 (1989) 3418-3428
19. Gupta A., Tsai L.H., and Wynshaw-Boris A. Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3 (2002) 342-355
20. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., and Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 26 (2000) 93-96
21. Huang G.J., and Herbert J. Serotonin modulates the suppressive effects of corticosterone on proliferating progenitor cells in the dentate gyrus of the hippocampus in the adult rat. Neuropsychopharmacology 30 (2005) 231-241
22. Kappeler C., Saillour Y., Baudoin J.P., Tuy F.P., Alvarez C., Houbron C., Gaspar P., Hamard G., Chelly J., Metin C., and Francis F. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum. Mol. Genet. 15 (2006) 1387-1400
23. Kikkawa M., and Hirokawa N. High-resolution cryo-EM maps show the nucleotide binding pocket of KIF1A in open and closed conformations. EMBO J. 25 (2006) 4187-4194
24. Leventer R.J. Genotype-phenotype correlation in lissencephaly and subcortical band heterotopia: the key questions answered. J. Child Neurol. 20 (2005) 307-312
25. Lewis S.A., Tian G., Vainberg I.E., and Cowan N.J. Chaperonin-mediated folding of actin and tubulin. J. Cell Biol. 132 (1996) 1-4
26. Lowe J., Li H., Downing K.H., and Nogales E. Refined structure of alpha beta-tubulin at 3.5 A resolution. J. Mol. Biol. 313 (2001) 1045-1057
27. Moores C.A., Perderiset M., Francis F., Chelly J., Houdusse A., and Milligan R.A. Mechanism of microtubule stabilization by doublecortin. Mol. Cell 14 (2004) 833-839
28. Nolan P.M., Peters J., Strivens M., Rogers D., Hagan J., Spurr N., Gray I.C., Vizor L., Brooker D., Whitehill E., et al. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat. Genet. 25 (2000) 440-443
29. Paylor R., Hirotsune S., Gambello M.J., Yuva-Paylor L., Crawley J.N., and Wynshaw-Boris A. Impaired learning and motor behavior in heterozygous Pafah1b1 (Lis1) mutant mice. Learn. Mem. 6 (1999) 521-537
30. Phillips J.B., Lyczak R., Ellis G.C., and Bowerman B. Roles for two partially redundant alpha-tubulins during mitosis in early Caenorhabditis elegans embryos. Cell Motil. Cytoskeleton 58 (2004) 112-126
31. Pinheiro J.C., and Bates D.M. Mixed effects models in S and S-PLUS (2000), Springer-Verlag, New York
32. Qiu S., Korwek K.M., Pratt-Davis A.R., Peters M., Bergman M.Y., and Weeber E.J. Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiol. Learn. Mem. 85 (2005) 228-242
33. R-Development-Core-Team. A language and environment for statistical computing (2004), R Foundation for Statistical Computing, Vienna
34. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., and Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364 (1993) 717-721
35. Solberg L.C., Valdar W., Gauguier D., Nunez G., Taylor A., Burnett S., Arboledas-Hita C., Hernandez-Pliego P., Davidson S., Burns P., et al. A protocol for high-throughput phenotyping, suitable for quantitative trait analysis in mice. Mamm. Genome 17 (2006) 129-146
36. Spiegelman B.M., Penningroth S.M., and Kirschner M.W. Turnover of tubulin and the N site GTP in Chinese hamster ovary cells. Cell 12 (1977) 587-600
37. Studier F.W., Rosenberg A.H., Dunn J.J., and Dubendorff J.W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185 (1990) 60-89
38. Takahashi T., Goto T., Miyama S., Nowakowski R.S., and Caviness Jr. V.S. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19 (1999) 10357-10371
39. Thornton C.E., Brown S.D., and Glenister P.H. Large numbers of mice established by in vitro fertilization with cryopreserved spermatozoa: implications and applications for genetic resource banks, mutagenesis screens, and mouse backcrosses. Mamm. Genome 10 (1999) 987-992
40. Tian G., Vainberg I.E., Tap W.D., Lewis S.A., and Cowan N.J. Quasi-native chaperonin-bound intermediates in facilitated protein folding. J. Biol. Chem. 270 (1995) 23910-23913
41. Tian G., Bhamidipati A., Cowan N.J., and Lewis S.A. Tubulin folding cofactors as GTPase-activating proteins. GTP hydrolysis and the assembly of the alpha/beta-tubulin heterodimer. J. Biol. Chem. 274 (1999) 24054-24058
42. Tian G., Huang M.C., Parvari R., Diaz G.A., and Cowan N.J. Cryptic out-of-frame translational initiation of TBCE rescues tubulin formation in compound heterozygous HRD. Proc. Natl. Acad. Sci. USA 103 (2006) 13491-13496
43. Vega L.R., Fleming J., and Solomon F. An alpha-tubulin mutant destabilizes the heterodimer: phenotypic consequences and interactions with tubulin-binding proteins. Mol. Biol. Cell 9 (1998) 2349-2360
44. Villasante A., Wang D., Dobner P., Dolph P., Lewis S.A., and Cowan N.J. Six mouse alpha-tubulin mRNAs encode five distinct isotypes: testis-specific expression of two sister genes. Mol. Cell. Biol. 6 (1986) 2409-2419
45. Willins D.A., Xiang X., and Morris N.R. An alpha tubulin mutation suppresses nuclear migration mutations in Aspergillus nidulans. Genetics 141 (1995) 1287-1298
46. Zeng Z.B. Precision mapping of quantitative trait loci. Genetics 136 (1994) 1457-1468