Beta tubulin isoforms are not interchangeable for rescuing impaired radial migration due to Tubb3 knockdown

Human Molecular Genetics

Volumn 23, Issue 6, 2014, Pages 1516-1526

  Saillour, Yoann ^a   Broix, Loïc ^a   Bruel Jungerman, Elodie ^b,c,d   Lebrun, Nicolas ^a   Muraca, Giuseppe ^a   Rucci, Julien ^a   Poirier, Karine ^a   Belvindrah, Richard ^b,c,d   Francis, Fiona ^b,c,d   Chelly, Jamel ^a  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d INSTITUT DU FER À MOULIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; ELECTROPORATION; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; MICE; MUTATION, MISSENSE; PREGNANCY; PROTEIN ISOFORMS; TUBULIN;

EID: 84894383692     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt538     Document Type: Article

References (31)

1. Gupta, A., Tsai, L.H. and Wynshaw-Boris, A. (2002) Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet., 3, 342-355.
2. Tabata, H. and Nakajima, K. (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci., 23, 9996-10001.
3. Kriegstein, A.R. and Noctor, S.C. (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci., 27, 392-399.
4. Saillour, Y., Carion, N., Quelin, C., Leger, P.L., Boddaert, N., Elie, C., Toutain, A., Mercier, S., Barthez, M.A., Milh, M. et al. (2009) LIS1-related isolated lissencephaly: spectrum of mutations and relationships with malformation severity. Arch. Neurol., 66, 1007-1015.
5. 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. et al. (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell, 92, 63-72.
6. Reiner, O., Carrozzo, R., Shen, Y., Wehnert, M., Faustinella, F., Dobyns, W.B., Caskey, C.T. and Ledbetter, D.H. (1993) Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature, 364, 717-721.
7. Bahi-Buisson, N., Souville, I., Fourniol, F.J., Toussaint, A., Moores, C.A., Houdusse, A., Lemaitre, J.Y., Poirier, K., Khalaf-Nazzal, R., Hully, M. et al. (2013) New insights into genotype-phenotype correlations for the doublecortin-related lissencephaly spectrum. Brain, 136, 223-244.
8. des Portes, V., Francis, F., Pinard, J.M., Desguerre, I., Moutard, M.L., Snoeck, I., Meiners, L.C., Capron, F., Cusmai, R., Ricci, S. et al. (1998) Doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum. Mol. Genet., 7, 1063-1070.
9. Poirier, K., Lebrun, N., Broix, L., Tian, G., Saillour, Y., Boscheron, C., Parrini, E., Valence, S., Pierre, B.S., Oger, M. et al. (2013) Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat. Genet., 45, 639-647.
10. Jaglin, X.H. and Chelly, J. (2009) Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects. Trends Genet., 25, 555-566.
11. Keays, D.A., Tian, G., Poirier, K., Huang, G.J., Siebold, C., Cleak, J., Oliver, P.L., Fray, M., Harvey, R.J., Molnar, Z. et al. (2007) Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell, 128, 45-57.
12. Poirier, K., Keays, D.A., Francis, F., Saillour, Y., Bahi, N., Manouvrier, S., Fallet-Bianco, C., Pasquier, L., Toutain, A., Tuy, F.P. et al. (2007) Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Hum. Mutat., 28, 1055-1064.
13. Jaglin, X.H., Poirier, K., Saillour, Y., Buhler, E., Tian, G., Bahi-Buisson, N., Fallet-Bianco, C., Phan-Dinh-Tuy, F., Kong, X.P., Bomont, P. et al. (2009) Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat. Genet., 41, 746-752.
14. Abdollahi, M.R., Morrison, E., Sirey, T., Molnar, Z., Hayward, B.E., Carr, I.M., Springell, K., Woods, C.G., Ahmed, M., Hattingh, L. et al. (2009) Mutation of the variant alpha-tubulinTUBA8results in polymicrogyria with optic nerve hypoplasia. Am. J. Hum. Genet., 85, 737-744.
15. Breuss, M., Heng, J.I., Poirier, K., Tian, G., Jaglin, X.H., Qu, Z., Braun, A., Gstrein, T., Ngo, L., Haas, M. et al. (2012) Mutations in the beta-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell. Rep., 2, 1554-1562.
16. Poirier, K., Saillour, Y., Bahi-Buisson, N., Jaglin, X.H., Fallet-Bianco, C., Nabbout, R., Castelnau-Ptakhine, L., Roubertie, A., Attie-Bitach, T., Desguerre, I. et al. (2010) Mutations in the neuronal ss-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects. Hum. Mol. Genet., 19, 4462-4473.
17. Cederquist, G.Y., Luchniak, A., Tischfield, M.A., Peeva, M., Song, Y., Menezes, M.P., Chan, W.M., Andrews, C., Chew, S., Jamieson, R.V. et al. (2012) An inherited TUBB2B mutation alters a kinesin-binding site and causes polymicrogyria, CFEOM and axon dysinnervation. Hum. Mol. Genet., 21, 5484-5499.
18. Tischfield, M.A., Baris, H.N., Wu, C., Rudolph, G., Van Maldergem, L., He, W., Chan, W.M., Andrews, C., Demer, J.L., Robertson, R.L. et al. (2010) Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell, 140, 74-87.
19. Lohmann, K., Wilcox, R.A., Winkler, S., Ramirez, A., Rakovic, A., Park, J.S., Arns, B., Lohnau, T., Groen, J., Kasten, M. et al. (2012) Whispering dysphonia (DYT4 dystonia) is caused by a mutation in the TUBB4 gene. Ann. Neurol., 73, 537-545.
20. Hersheson, J., Mencacci, N.E., Davis, M., Macdonald, N., Trabzuni, D., Ryten, M., Pittman, A., Paudel, R., Kara, E., Fawcett, K. et al. (2013) Mutations in the autoregulatory domain of beta-tubulin 4a cause hereditary dystonia. Ann. Neurol., 73, 546-553.
21. Simons, C., Wolf, N.I., McNeil, N., Caldovic, L., Devaney, J.M., Takanohashi, A., Crawford, J., Ru, K., Grimmond, S.M., Miller, D. et al. (2013) A de novo mutation in the beta-tubulin gene TUBB4A results in the leukoencephalopathy hypomyelination with atrophy of the basal ganglia and cerebellum. Am. J. Hum. Genet., 92, 767-773.
22. Khodiyar, V.K., Maltais, L.J., Ruef, B.J., Sneddon, K.M., Smith, J.R., Shimoyama, M., Cabral, F., Dumontet, C., Dutcher, S.K., Harvey, R.J. et al. (2007)Arevised nomenclature for the human and rodent alpha-tubulin gene family. Genomics, 90, 285-289.
23. Hallworth, R. and Luduena, R.F. (2000) Differential expression of beta tubulin isotypes in the adult gerbil cochlea. Hear. Res., 148, 161-172.
24. Lewis, S.A. and Cowan, N.J. (1988) Complex regulation and functional versatility of mammalian alpha- and beta-tubulin isotypes during the differentiation of testis and muscle cells. J. Cell. Biol., 106, 2023-2033.
25. Guo, J., Walss-Bass, C. and Luduena, R.F. (2010) The beta isotypes of tubulin in neuronal differentiation. Cytoskeleton (Hoboken), 67, 431-441.
26. Cleveland, D.W. (1987) The multitubulin hypothesis revisited: what have we learned? J. Cell. Biol., 104, 381-383.
27. Manent, J.B., Wang, Y., Chang, Y., Paramasivam, M.andLoTurco, J.J. (2009) Dcx reexpression reduces subcortical band heterotopia and seizure threshold in an animal model of neuronal migration disorder. Nat. Med., 15, 84-90.
28. LoTurco, J.J. and Bai, J. (2006) The multipolar stage and disruptions in neuronal migration. Trends Neurosci., 29, 407-413.
29. Tischfield, M.A., Cederquist, G.Y., Gupta, M.L. Jr and Engle, E.C. (2011) Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr. Opin. Genet. Dev., 21, 286-294.
30. Tabata, H. and Nakajima, K. (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience, 103, 865-872.
31. Niwa, S., Takahashi, H. and Hirokawa, N. (2013) Beta-tubulin mutations that cause severe neuropathies disrupt axonal transport. EMBO J., 32, 1352-1364.