Exome-wide rare variant analysis identifies TUBA4A mutations associated with familial ALS

Neuron

Volumn 84, Issue 2, 2014, Pages 324-331

  Smith, Bradley N ^a   Ticozzi, Nicola ^b,c   Fallini, Claudia ^d   Gkazi, Athina Soragia ^a   Topp, Simon ^a   Kenna, Kevin P ^d,e   Scotter, Emma L ^a   Kost, Jason ^d,f   Keagle, Pamela ^d   Miller, Jack W ^a   Calini, Daniela ^b,c   Vance, Caroline ^a   Danielson, Eric W ^d   Troakes, Claire ^a   Tiloca, Cinzia ^b   Al Sarraj, Safa ^a   Lewis, Elizabeth A ^d   King, Andrew ^a   Colombrita, Claudia ^b,c   Pensato, Viviana ^g   Castellotti, Barbara ^g   de Belleroche, Jacqueline ^h   Baas, Frank ⁱ   ten Asbroek, Anneloor L M A ⁱ   Sapp, Peter C ^d   McKenna Yasek, Diane ^d   McLaughlin, Russell L ^e   Polak, Meraida ^j   Asress, Seneshaw ^j   Esteban Pérez, Jesús ^k,z   Muñoz Blanco, JoséLuis ^l   Simpson, Michael ^m   van Rheenen, Wouter ⁿ   Diekstra, Frank P ⁿ   Lauria, Giuseppe ^g   Duga, Stefano ^c   Corti, Stefania ^c,o   Cereda, Cristina ^p   Corrado, Lucia ^q   Sorarù, Gianni ^r   Morrison, Karen E ^s,t   Williams, Kelly L ^u   Nicholson, Garth A ^u,v   Blair, Ian P ^u   Dion, Patrick A ^w   Leblond, Claire S ^w   Rouleau, Guy A ^w   Hardiman, Orla ^e   Veldink, Jan H ⁿ   Van Den Berg, Leonard H ⁿ   Al Chalabi, Ammar ^a   Pall, Hardev ^s   Shaw, Pamela J ^x   Turner, Martin R ^y   Talbot, Kevin ^y   Taroni, Franco ^g   García Redondo, Alberto ^k,z   Wu, Zheyang ^f   Glass, Jonathan D ^j   Gellera, Cinzia ^g   Ratti, Antonia ^b,c   Brown, Robert H ^d   Silani, Vincenzo ^b,c   Shaw, Christopher E ^a   Landers, John E ^d   D’Alfonso, Sandra ^aa   Mazzini, Letizia ^aa   Comi, Giacomo P ^aa   Del Bo, Roberto ^aa   Ceroni, Mauro ^aa   Gagliardi, Stella ^aa   Querin, Giorgia ^aa   Bertolin, Cinzia ^aa   more..

^a KING'S COLLEGE LONDON   (United Kingdom)

^b ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f WORCESTER POLYTECHNIC INSTITUTE   (United States)

^g DEPARTMENT OF NEUROSURGERY   (Italy)

^h IMPERIAL COLLEGE LONDON   (United Kingdom)

ⁱ ACADEMIC MEDICAL CENTER   (Netherlands)

^j EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^l HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^m GUY S HOSPITAL   (United Kingdom)

ⁿ UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^o FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^p C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^q UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^r UNIVERSITY OF PADOVA   (Italy)

^s UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^t QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^u MACQUARIE UNIVERSITY   (Australia)

^v UNIVERSITY OF SYDNEY   (Australia)

^w MCGILL UNIVERSITY   (Canada)

^x UNIVERSITY OF SHEFFIELD   (United Kingdom)

^y UNIVERSITY OF OXFORD   (United Kingdom)

^z CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^aa Centro de Investigació n Biomé dica en Red de Enfermedades Raras ^*

more..

Author keywords

[No Author keywords available]

Indexed keywords

TUBA1A PROTEIN, HUMAN; TUBULIN;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; DNA SEQUENCE; EXOME; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; EXOME; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUTATION; NEURONS; SEQUENCE ANALYSIS, DNA; TUBULIN;

EID: 84908224269     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.09.027     Document Type: Article

References (34)

1. Abdollahi, M.R., Morrison, E., Sirey, T., Molná r, Z., Hayward, B.E., Carr, I.M., Springell, K., Woods, C.G., Ahmed, M., Hattingh, L., et al. (2009). Mutation of the variant α-tubulin TUBA8 results in polymicrogyria with optic nerve hypoplasia Am. J. Hum. Genet. 85, 737-744
2. Al-Chalabi, A., Andersen, P.M., Nilsson, P., Chioza, B., Andersson, J.L., Russ, C., Shaw, C.E., Powell, J.F., and Leigh, P.N. (1999). Deletions of the heavy neurofilament subunit tail in amyotrophic lateral sclerosis. Hum. Mol. Genet. 8, 157-164
3. Bömmel, H., Xie, G., Rossoll, W., Wiese, S., Jablonka, S., Boehm, T., and Sendtner, M. (2002). Missense mutation in the tubulin-specific chaperone E (Tbce) gene in the mouse mutant progressive motor neuronopathy, a model of human motoneuron disease. J. Cell Biol. 159, 563-569
4. Breuss, M., Heng, J.I.-T., Poirier, K., Tian, G., Jaglin, X.H., Qu, Z., Braun, A., Gstrein, T., Ngo, L., Haas, M., et al. (2012). Mutations in the β-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rep. 2, 1554-1562
5. Chiò, A., Calvo, A., Mazzini, L., Cantello, R., Mora, G., Moglia, C., Corrado, L., D'Alfonso, S., Majounie, E., Renton, A., et al.; PARALS (2012). Extensive genetics of ALS: a population-based study in Italy. Neurology 79, 1983-1989
6. Cleveland, D.W., Kirschner, M.W., and Cowan, N.J. (1978). Isolation of separate mRNAs for alpha- and beta-tubulin and characterization of the corresponding in vitro translation products. Cell 15, 1021-1031
7. Fallini, C., Bassell, G.J., and Rossoll, W. (2010). High-efficiency transfection of cultured primary motor neurons to study protein localization, trafficking, and function. Mol. Neurodegener. 5, 17
8. Gilissen, C., Hoischen, A., Brunner, H.G., and Veltman, J.A. (2011). Unlocking Mendelian disease using exome sequencing. Genome Biol. 12, 228
9. Gros-Louis, F., Larivière, R., Gowing, G., Laurent, S., Camu, W., Bouchard, J.P., Meininger, V., Rouleau, G.A., and Julien, J.P. (2004). A frameshift deletion in peripherin gene associated with amyotrophic lateral sclerosis. J. Biol. Chem 279, 45951-45956
10. 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 β-tubulin 4a cause hereditary dystonia. Ann. Neurol 73, 546-553
11. Howes, S.C., Alushin, G.M., Shida, T., Nachury, M.V., and Nogales, E. (2014) Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol. Biol. Cell 25, 257-266
12. 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 β-tubulin gene TUBB2B result in asymmetrical polymicrogyria Nat. Genet. 41, 746-752
13. Jiang, Y.-M., Yamamoto, M., Kobayashi, Y., Yoshihara, T., Liang, Y., Terao, S., Takeuchi, H., Ishigaki, S., Katsuno, M., Adachi, H., et al. (2005). Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis Ann. Neurol. 57, 236-251
14. Johnson, J.O., Pioro, E.P., Boehringer, A., Chia, R., Feit, H., Renton, A.E., Pliner, H.A., Abramzon, Y., Marangi, G., Winborn, B.J., et al.; ITALSGEN Consortium (2014). Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat. Neurosci. 17, 664-666
15. Keays, D.A., Tian, G., Poirier, K., Huang, G.-J., Siebold, C., Cleak, J., Oliver, P.L., Fray, M., Harvey, R.J., Molná r, Z., et al. (2007). Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128, 45-57
16. Kenna, K.P., McLaughlin, R.L., Byrne, S., Elamin, M., Heverin, M., Kenny, E.M., Cormican, P., Morris, D.W., Donaghy, C.G., Bradley, D.G., and Hardiman, O (2013). Delineating the genetic heterogeneity of ALS using targeted highthroughput sequencing. J. Med. Genet. 50, 776-783
17. Kiezun, A., Garimella, K., Do, R., Stitziel, N.O., Neale, B.M., McLaren, P.J., Gupta, N., Sklar, P., Sullivan, P.F., Moran, J.L., et al. (2012). Exome sequencing and the genetic basis of complex traits. Nat. Genet. 44, 623-630
18. Kumar, R.A., Pilz, D.T., Babatz, T.D., Cushion, T.D., Harvey, K., Topf, M., Yates, L., Robb, S., Uyanik, G., Mancini, G.M.S., et al. (2010). TUBA1A mutations cause wide spectrum lissencephaly (smooth brain) and suggest that multiple neuronal migration pathways converge on alpha tubulins. Hum Mol. Genet. 19, 2817-2827
19. Liu, J.S., Schubert, C.R., Fu, X., Fourniol, F.J., Jaiswal, J.K., Houdusse, A., Stultz, C.M., Moores, C.A., and Walsh, C.A. (2012). Molecular basis for specific regulation of neuronal kinesin-3 motors by doublecortin family proteins. Mol Cell 47, 707-721
20. Martin, N., Jaubert, J., Gounon, P., Salido, E., Haase, G., Szatanik, M., and Guénet, J.-L. (2002). A missense mutation in Tbce causes progressive motor neuronopathy in mice. Nat. Genet. 32, 443-447
21. Matsuyama, A., Shimazu, T., Sumida, Y., Saito, A., Yoshimatsu, Y., Seigneurin-Berny, D., Osada, H., Komatsu, Y., Nishino, N., Khochbin, S., et al. (2002). In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831
22. Panoutsopoulou, K., Tachmazidou, I., and Zeggini, E. (2013). In search of lowfrequency and rare variants affecting complex traits. Hum. Mol. Genet. 22 (R1), R16-R21
23. Piperno, G., LeDizet, M., and Chang, X.J. (1987). Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 104, 289-302
24. Poirier, K., Keays, D.A., Francis, F., Saillour, Y., Bahi, N., Manouvrier, S., Fallet-Bianco, C., Pasquier, L., Toutain, A., Tuy, F.P.D., 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
25. 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
26. 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
27. Puls, I., Jonnakuty, C., LaMonte, B.H., Holzbaur, E.L.F., Tokito, M., Mann, E., Floeter, M.K., Bidus, K., Drayna, D., Oh, S.J., et al. (2003). Mutant dynactin in motor neuron disease. Nat. Genet. 33, 455-456
28. Rustici, G., Kolesnikov, N., Brandizi, M., Burdett, T., Dylag, M., Emam, I., Farne, A., Hastings, E., Ison, J., Keays, M., et al. (2013). ArrayExpress update- trends in database growth and links to data analysis tools. Nucleic Acids Res. 41 (Database issue), D987-D990
29. Stitziel, N.O., Kiezun, A., and Sunyaev, S. (2011). Computational and statistical approaches to analyzing variants identified by exome sequencing. Genome Biol. 12, 227
30. Tennessen, J.A., Bigham, A.W., O'Connor, T.D., Fu, W., Kenny, E.E., Gravel, S., McGee, S., Do, R., Liu, X., Jun, G., et al.; Broad GO; Seattle GO; NHLBI Exome Sequencing Project (2012). Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337, 64-69
31. Tian, G., Kong, X.P., Jaglin, X.H., Chelly, J., Keays, D., and Cowan, N.J. (2008) A pachygyria-causing alpha-tubulin mutation results in inefficient cycling with CCT and a deficient interaction with TBCB. Mol. Biol. Cell 19, 1152-1161
32. Tian, G., Jaglin, X.H., Keays, D.A., Francis, F., Chelly, J., and Cowan, N.J (2010). Disease-associated mutations in TUBA1A result in a spectrum of defects in the tubulin folding and heterodimer assembly pathway. Hum. Mol Genet. 19, 3599-3613
33. 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
34. Wu, C.-H., Fallini, C., Ticozzi, N., Keagle, P.J., Sapp, P.C., Piotrowska, K., Lowe, P., Koppers, M., McKenna-Yasek, D., Baron, D.M., et al. (2012) Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis Nature 488, 499-503