Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo

Human Molecular Genetics

Volumn 19, Issue 4, 2009, Pages 671-683

  Kabashi, Edor ^a,b   Lin, Li ^b   Tradewell, Miranda L ^c   Dion, Patrick A ^a   Bercier, Valérie ^a,b   Bourgouin, Patrick ^a   Rochefort, Daniel ^a   Bel Hadj, Samar ^a   Durham, Heather D ^c   Velde, Christine Vande ^a   Rouleau, Guy A ^a   Drapeau, Pierre ^b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TAR DNA BINDING PROTEIN; DNA BINDING PROTEIN; PROTEIN TDP-43;

ALLELE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL AGGREGATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC RISK; GENETIC TRANSFECTION; IN VIVO STUDY; MOTONEURON; MOTOR DYSFUNCTION; MOUSE; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SPINAL CORD; SWIMMING; ZEBRA FISH; ANIMAL; CELL CULTURE; CELL LINE; GENETICS; HUMAN; METABOLISM; MOTOR ACTIVITY; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

DANIO RERIO;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; CELLS, CULTURED; DNA-BINDING PROTEINS; HUMANS; MICE; MOTOR ACTIVITY; MOTOR NEURONS; MUTATION; ZEBRAFISH;

EID: 77950360176     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp534     Document Type: Article

References (69)

1. Nelson, L.M. (1995) Epidemiology of ALS. Clin. Neurosci., 3, 327-331.
2. Boillee, S., Vande Velde, C. and Cleveland, D.W. (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron, 52, 39-59.
3. Gros-Louis, F., Gaspar, C. and Rouleau, G.A. (2006) Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochim. Biophys. Acta, 1762, 956-972.
4. Rosen, D.R., Siddique, T., Patterson, D., Figlewicz, D.A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J.P., Deng, H.X. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 362, 59-62.
5. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X. et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264, 1772-1775.
6. Howland, D.S., Liu, J., She, Y., Goad, B., Maragakis, N.J., Kim, B., Erickson, J., Kulik, J., DeVito, L., Psaltis, G. et al. (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl Acad. Sci. USA, 99, 1604-1609.
7. Lemmens, R., Van Hoecke, A., Hersmus, N., Geelen, V., D'Hollander, I., Thijs, V., Van Den Bosch, L., Carmeliet, P. and Robberecht, W. (2007) Overexpression of mutant superoxide dismutase 1 causes a motor axonopathy in the zebrafish. Hum. Mol. Genet., 16, 2359-2365.
8. Julien, J.P. and Kriz, J. (2006) Transgenic mouse models of amyotrophic lateral sclerosis. Biochim. Biophys. Acta, 1762, 1013-1024.
9. Hadano, S., Hand, C.K., Osuga, H., Yanagisawa, Y., Otomo, A., Devon, R.S., Miyamoto, N., Showguchi-Miyata, J., Okada, Y., Singaraja, R. et al. (2001) A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat. Genet., 29, 166-173.
10. Nishimura, A.L., Mitne-Neto, M., Silva, H.C., Richieri-Costa, A., Middleton, S., Cascio, D., Kok, F., Oliveira, J.R., Gillingwater, T., Webb, J. et al. (2004) A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet., 75, 822-831.
11. Chen, Y.Z., Bennett, C.L., Huynh, H.M., Blair, I.P., Puls, I., Irobi, J., Dierick, I., Abel, A., Kennerson, M.L., Rabin, B.A. et al. (2004) DNA/ RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet., 74, 1128-1135.
12. Lambrechts, D., Storkebaum, E., Morimoto, M., Del-Favero, J., Desmet, F., Marklund, S.L., Wyns, S., Thijs, V., Andersson, J., van Marion, I. et al. (2003) VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet., 34, 383-394.
13. Greenway, M.J., Andersen, P.M., Russ, C., Ennis, S., Cashman, S., Donaghy, C., Patterson, V., Swingler, R., Kieran, D., Prehn, J. et al. (2006) ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet., 38, 411-413.
14. Ou, S.H., Wu, F., Harrich, D., Garcia-Martinez, L.F. and Gaynor, R.B. (1995) Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol., 69, 3584-3596.
15. Buratti, E., Brindisi, A., Giombi, M., Tisminetzky, S., Ayala, Y.M. and Baralle, F.E. (2005) TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J. Biol. Chem., 280, 37572-37584.
16. Bose, J.K., Wang, I.F., Hung, L., Tarn, W.Y. and Shen, C.K. (2008) TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron pre-mRNA splicing. J. Biol. Chem., 283, 28852-28859.
17. Buratti, E., Dork, T., Zuccato, E., Pagani, F., Romano, M. and Baralle, F.E. (2001) Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J., 20, 1774-1784.
18. Mercado, P.A., Ayala, Y.M., Romano, M., Buratti, E. and Baralle, F.E. (2005) Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res., 33, 6000-6010.
19. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., Bruce, J., Schuck, T., Grossman, M., Clark, C.M. et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314, 130-133.
20. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y. et al. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun., 351, 602-611.
21. Amador-Ortiz, C., Lin, W.L., Ahmed, Z., Personett, D., Davies, P., Duara, R., Graff-Radford, N.R., Hutton, M.L. and Dickson, D.W. (2007) TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease. Ann. Neurol., 61, 435-445.
22. Nakashima-Yasuda, H., Uryu, K., Robinson, J., Xie, S.X., Hurtig, H., Duda, J.E., Arnold, S.E., Siderowf, A., Grossman, M., Leverenz, J.B. et al. (2007) Co-morbidity of TDP-43 proteinopathy in Lewy body related diseases. Acta Neuropathol., 114, 221-229.
23. Rothstein, J.D. (2007) TDP-43 in amyotrophic lateral sclerosis: pathophysiology or patho-babel? Ann. Neurol., 61, 382-384.
24. Gitcho, M.A., Baloh, R.H., Chakraverty, S., Mayo, K., Norton, J.B., Levitch, D., Hatanpaa, K.J., White, C.L. III, Bigio, E.H., Caselli, R. et al. (2008) TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol., 63, 535-538.
25. Kabashi, E., Valdmanis, P.N., Dion, P., Spiegelman, D., McConkey, B.J., Vande Velde, C., Bouchard, J.P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574.
26. Sreedharan, J., Blair, I.P., Tripathi, V.B., Hu, X., Vance, C., Rogelj, B., Ackerley, S., Durnall, J.C., Williams, K.L., Buratti, E. et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science, 319, 1668-1672.
27. Rutherford, N.J., Zhang, Y.J., Baker, M., Gass, J.M., Finch, N.A., Xu, Y.F., Stewart, H., Kelley, B.J., Kuntz, K., Crook, R.J. et al. (2008) Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet., 4, e1000193.
28. Daoud, H., Valdmanis, P.N., Kabashi, E., Dion, P., Dupre, N., Camu, W.,Meininger, V. and Rouleau, G.A. (2009) Contribution of TARDBP mutations to sporadic amyotrophic lateral sclerosis. J. Med. Genet., 46, 112-114.
29. Corrado, L., Ratti, A., Gellera, C., Buratti, E., Castellotti, B., Carlomagno, Y., Ticozzi, N., Mazzini, L., Testa, L., Taroni, F. et al. (2009) High frequency of TARDBP gene mutations in Italian patients with amyotrophic lateral sclerosis. Hum. Mutat., 30, 688-694.
30. Van Deerlin, V.M., Leverenz, J.B., Bekris, L.M., Bird, T.D., Yuan, W., Elman, L.B., Clay, D., Wood, E.M., Chen-Plotkin, A.S., Martinez-Lage, M. et al. (2008) TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol., 7, 409-416.
31. Del Bo, R., Ghezzi, S., Corti, S., Pandolfo, M., Ranieri, M., Santoro, D., Ghione, I., Prelle, A., Orsetti, V., Mancuso, M. et al. (2009) TARDBP (TDP-43) sequence analysis in patients with familial and sporadic ALS: identification of two novel mutations. Eur. J. Neurol., 16, 727-732.
32. Yokoseki, A., Shiga, A., Tan, C.F., Tagawa, A., Kaneko, H., Koyama, A., Eguchi, H., Tsujino, A., Ikeuchi, T., Kakita, A. et al. (2008) TDP-43 mutation in familial amyotrophic lateral sclerosis. Ann. Neurol., 63, 538-542.
33. Lemmens, R., Race, V., Hersmus, N., Matthijs, G., Van Den Bosch, L., Van Damme, P., Dubois, B., Boonen, S., Goris, A. and Robberecht, W. (2009) TDP-43 M311V mutation in familial amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry, 80, 354-355.
34. Kuhnlein, P., Sperfeld, A.D., Vanmassenhove, B., Van Deerlin, V., Lee, V.M., Trojanowski, J.Q., Kretzschmar, H.A., Ludolph, A.C. and Neumann, M. (2008) Two German kindreds with familial amyotrophic lateral sclerosis due to TARDBP mutations. Arch. Neurol., 65, 1185-1189.
35. Zhang, Y.J., Xu, Y.F., Dickey, C.A., Buratti, E., Baralle, F., Bailey, R., Pickering-Brown, S., Dickson, D. and Petrucelli, L. (2007) Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J. Neurosci., 27, 10530-10534.
36. Moisse, K., Volkening, K., Leystra-Lantz, C., Welch, I., Hill, T. and Strong, M.J. (2009) Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Brain Res., 1249, 202-211.
37. Roy, J., Minotti, S., Dong, L., Figlewicz, D.A. and Durham, H.D. (1998) Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci., 18, 9673-9684.
38. Durham, H.D., Roy, J., Dong, L. and Figlewicz, D.A. (1997) Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS. J. Neuropathol. Exp. Neurol., 56, 523-530.
39. Grunwald, D.J. and Eisen, J.S. (2002) Headwaters of the zebrafish-emergence of a new model vertebrate. Nat. Rev. Genet., 3, 717-724.
40. Lieschke, G.J. and Currie, P.D. (2007) Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet., 8, 353-367.
41. Beattie, C.E., Carrel, T.L. and McWhorter, M.L. (2007) Fishing for a mechanism: using zebrafish to understand spinal muscular atrophy. J. Child Neurol., 22, 995-1003.
42. Shankaran, S.S., Capell, A., Hruscha, A.T., Fellerer, K., Neumann, M., Schmid, B. and Haass, C. (2008) Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J. Biol. Chem., 283, 1744-1753.
43. Gros-Louis, F., Kriz, J., Kabashi, E., McDearmid, J., Millecamps, S., Urushitani, M., Lin, L., Dion, P., Zhu, Q., Drapeau, P. et al. (2008) Als2 mRNA splicing variants detected in KO mice rescue severe motor dysfunction phenotype in Als2 knock-down zebrafish. Hum. Mol. Genet., 17, 2691-2702.
44. Messaed, C., Dion, P.A., Abu-Baker, A., Rochefort, D., Laganiere, J., Brais, B. and Rouleau, G.A. (2007) Soluble expanded PABPN1 promotes cell death in oculopharyngeal muscular dystrophy. Neurobiol. Dis., 26, 546-557.
45. Valdmanis, P.N., Meijer, I.A., Reynolds, A., Lei, A., MacLeod, P., Schlesinger, D., Zatz, M., Reid, E., Dion, P.A., Drapeau, P. et al. (2007) Mutations in the KIAA0196 gene at the SPG8 locus cause hereditary spastic paraplegia. Am. J. Hum. Genet., 80, 152-161.
46. Mao, A.J., Bechberger, J., Lidington, D., Galipeau, J., Laird, D.W. and Naus, C.C. (2000) Neuronal differentiation and growth control of neuro-2a cells after retroviral gene delivery of connexin43. J. Biol. Chem., 275, 34407-34414.
47. Igaz, L.M., Kwong, L.K., Chen-Plotkin, A., Winton, M.J., Unger, T.L., Xu, Y., Neumann, M., Trojanowski, J.Q. and Lee, V.M. (2009) Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J. Biol. Chem., 284, 8516-8524.
48. Igaz, L.M., Kwong, L.K., Xu, Y., Truax, A.C., Uryu, K., Neumann, M., Clark, C.M., Elman, L.B., Miller, B.L., Grossman, M. et al. (2008) Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Am. J. Pathol., 173, 182-194.
49. Zhang, Y.J., Xu, Y.F., Cook, C., Gendron, T.F., Roettges, P., Link, C.D., Lin, W.L., Tong, J., Castanedes-Casey, M., Ash, P. et al. (2009) Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc. Natl Acad. Sci. USA, 106, 7607-7612.
50. Wang, I.F., Wu, L.S., Chang, H.Y. and Shen, C.K. (2008) TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem., 105, 797-806.
51. Feiguin, F., Godena, V.K., Romano, G., D'Ambrogio, A., Klima, R. and Baralle, F.E. (2009) Depletion of TDP-43 affects Drosophila motoneurons terminal synapsis and locomotive behavior. FEBS Lett., 583, 1586-1592.
52. Strong, M.J., Volkening, K., Hammond, R., Yang, W., Strong, W., Leystra-Lantz, C. and Shoesmith, C. (2007) TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol. Cell. Neurosci., 35, 320-327.
53. Kwiatkowski, T.J. Jr, Bosco, D.A., Leclerc, A.L., Tamrazian, E., Vanderburg, C.R., Russ, C., Davis, A., Gilchrist, J., Kasarskis, E.J., Munsat, T. et al. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science, 323, 1205-1208.
54. Vance, C., Rogelj, B., Hortobagyi, T., De Vos, K.J., Nishimura, A.L., Sreedharan, J., Hu, X., Smith, B., Ruddy, D., Wright, P. et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science, 323, 1208-1211.
55. Lagier-Tourenne, C. and Cleveland, D.W. (2009) Rethinking ALS: the FUS about TDP-43. Cell, 136, 1001-1004.
56. Kabashi, E., Valdmanis, P.N., Dion, P. and Rouleau, G.A. (2007) Oxidized/misfolded superoxide dismutase-1: the cause of all amyotrophic lateral sclerosis? Ann. Neurol., 62, 553-559.
57. Kabashi, E. and Durham, H.D. (2006) Failure of protein quality control in amyotrophic lateral sclerosis. Biochim. Biophys. Acta., 1762, 1038-1050.
58. Wang, Q., Johnson, J.L., Agar, N.Y. and Agar, J.N. (2008) Protein aggregation and protein instability govern familial amyotrophic lateral sclerosis patient survival. PLoS Biol., 6, e170.
59. Cleveland, D.W. and Rothstein, J.D. (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci., 2, 806-819.
60. De Vos, K.J., Grierson, A.J., Ackerley, S. and Miller, C.C. (2008) Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci., 31, 151-173.
61. Reaume, A.G., Elliott, J.L., Hoffman, E.K., Kowall, N.W., Ferrante, R.J., Siwek, D.F., Wilcox, H.M., Flood, D.G., Beal, M.F., Brown, R.H. Jr et al. (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet., 13, 43-47.
62. Di Prospero, N.A. and Fischbeck, K.H. (2005) Therapeutics development for triplet repeat expansion diseases. Nat. Rev. Genet., 6, 756-765.
63. Diekmann, H., Anichtchik, O., Fleming, A., Futter, M., Goldsmith, P., Roach, A. and Rubinsztein, D.C. (2009) Decreased BDNF levels are a major contributor to the embryonic phenotype of huntingtin knockdown zebrafish. J. Neurosci., 29, 1343-1349.
64. Schiffer, N.W., Broadley, S.A., Hirschberger, T., Tavan, P., Kretzschmar, H.A., Giese, A., Haass, C., Hartl, F.U. and Schmid, B. (2007) Identification of anti-prion compounds as efficient inhibitors of polyglutamine protein aggregation in a zebrafish model. J. Biol. Chem., 282, 9195-9203.
65. Lim, J., Crespo-Barreto, J., Jafar-Nejad, P., Bowman, A.B., Richman, R., Hill, D.E., Orr, H.T. and Zoghbi, H.Y. (2008) Opposing effects of polyglutamine expansion on native protein complexes contribute to SCA. Nature, 452, 713-718.
66. Zoghbi, H.Y. and Orr, H.T. (2009) Pathogenic mechanisms of a polyglutamine mediated neurodegenerative disease, spinocerebellar ataxia type. J. Biol. Chem., 284, 7425-7429.
67. Thomas, P.S. Jr, Fraley, G.S., Damian, V., Woodke, L.B., Zapata, F., Sopher, B.L., Plymate, S.R. and La Spada, A.R. (2006) Loss of endogenous androgen receptor protein accelerates motor neuron degeneration and accentuates androgen insensitivity in a mouse model of X linked spinal and bulbar muscular atrophy. Hum. Mol. Genet., 15, 2225-2238.
68. McWhorter, M.L., Monani, U.R., Burghes, A.H. and Beattie, C.E. (2003) Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J. Cell. Biol., 162, 919-931.
69. Paquet, D., Bhat, R., Sydow, A., Mandelkow, E.M., Berg, S., Hellberg, S., Falting, J., Distel, M., Koster, R.W., Schmid, B. et al. (2009) A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J. Clin. Invest., 119, 1382-1395.