Loss and gain of FUS function impair neuromuscular synaptic transmission in a genetic model of ALS

Human Molecular Genetics

Volumn 22, Issue 21, 2013, Pages 4282-4292

  Armstrong, Gary A B ^a   Drapeau, Pierre ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FUSED IN SARCOMA PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL TISSUE; ARTICLE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; GENETIC MODEL; LOSS OF FUNCTION MUTATION; MOTONEURON; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SWIMMING; SYNAPTIC TRANSMISSION; ZEBRA FISH;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MOTOR ACTIVITY; MOTOR NEURONS; NEUROMUSCULAR JUNCTION; RNA-BINDING PROTEIN FUS; SWIMMING; SYNAPTIC TRANSMISSION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84885763677     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt278     Document Type: Article

References (40)

1. Kwiatkowski, T.J., 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.
2. Vance, C., Rogelj, B., Hortobágyi, 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.
3. Rademakers, R., Stewart, H., Dejesus-Hernandez, M., Krieger, C., Graff-Radford, N., Fabros, M., Briemberg, H., Cashman, N., Eisen, A. and Mackenzie, I.R.A. (2010) Fus gene mutations in familial and sporadic amyotrophic lateral sclerosis. Muscle Nerve, 42, 170-176.
4. 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)TARDBPmutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574.
5. 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.
6. Murray, L.M., Talbot, K. and Gillingwater, T.H. (2010) Review: neuromuscular synaptic vulnerability in motor neurone disease: amyotrophic lateral sclerosis and spinal muscular atrophy. Neuropathol. Appl. Neurobiol., 36, 133-156.
7. Dadon-Nachum, M., Melamed, E. and Offen, D. (2011) The 'dying-back' phenomenon of motor neurons in ALS. J. Mol. Neurosci., 43, 470-477.
8. Armstrong, G.A.B. and Drapeau, P. (2013) Calcium channel agonists protect against neuromuscular dysfunction in a genetic model of TDP-43 mutation in ALS. J. Neurosci., 33, 1741-1752.
9. Diaper, D.C., Adachi, Y., Sutcliffe, B., Humphrey, D.M., Elliott, C.J.H., Stepto, A., Ludlow, Z.N., Broeck, L.V., Callaerts, P., Dermaut, B. et al. (2013) Loss and gain of Drosophila TDP-43 impair synaptic efficacy and motor control leading to age-related neurodegeneration by loss-of-function phenotypes. Hum. Mol. Genet., 22, 1539-1557.
10. Mitchell, J., McGoldrick, P., Vance, C., Hortobagyi, T., Sreedharan, J., Rogelj, B., Tudor, E., Smith, B., Klasen, C., Miller, C.J. et al. (2013) Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathol., 125, 273-288.
11. Murakami, T., Yang, S.-P., Xie, L., Kawano, T., Fu, D., Mukai, A., Bohm, C., Chen, F., Robertson, J., Suzuki, H. et al. (2012)ALS mutations in FUS cause neuronal dysfunction and death in Caenorhabditis elegans by a dominant gain-of-function mechanism. Hum. Mol. Genet., 21, 1-9.
12. Kabashi, E., Bercier, V., Lissouba, A., Liao, M., Brustein, E., Rouleau, G.A. and Drapeau, P. (2011) FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS Genet., 7, e1002214.
13. Bosco, D.A., Lemay, N., Ko, H.K., Zhou, H., Burke, C., Kwiatkowski, T.J., Sapp, P., McKenna-Yasek, D., Brown, R.H. and Hayward, L.J. (2010) Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet., 19, 4160-4175.
14. Westerfield, M., McMurray, J. and Eisen, J. (1986) Identified motoneurons and their innervation of axial muscles in the zebrafish. J. Neurosci., 6, 2267-2277.
15. Wen, H. and Brehm, P. (2005) Paired motor neuron-muscle recordings in zebrafish test the receptor blockade model for shaping synaptic current. J. Neurosci., 25, 8104-8111.
16. Boon, K.-L., Xiao, S., McWhorter, M.L., Donn, T., Wolf-Saxon, E., Bohnsack, M.T., Moens, C.B. and Beattie, C.E. (2009) Zebrafish survival motor neuron mutants exhibit presynaptic neuromuscular junction defects. Hum. Mol. Genet., 18, 3615-3625.
17. Daigle, J.G., Lanson, N.A., Smith, R.B., Casci, I., Maltare, A., Monaghan, J., Nichols, C.D., Kryndushkin, D., Shewmaker, F. and Pandey, U.B. (2012) RNA-binding ability of FUS regulates neurodegeneration, cytoplasmic mislocalization and incorporation into stress granules associated with FUS carrying ALS-linked mutations. Hum. Mol. Genet., 22, 1193-1205.
18. Souayah, N., Coakley, K., Chen, R., Ende, N. and McArdle, J. (2012) Defective neuromuscular transmission in the SOD1G93A transgenic mouse improves after administration ofhumanumbilical cord blood cells. Stem Cell Rev., 8, 224-228.
19. Maselli, R.A., Wollman, R.L., Leung, C., Distad, B., Palombi, S., Richman, D.P., Salazar-Grueso, E.F. and Roos, R.P. (1993) Neuromuscular transmission in amyotrophic lateral sclerosis. Muscle Nerve, 16, 1193-1203.
20. Naumenko, N., Pollari, E., Kurronen, A., Giniatullina, R., Shakirzyanova, A., Magga, J., Koistinaho, J. and Giniatullin, R. (2011) Gender specific mechanism of synaptic impairment and its prevention by GCSF in a mouse model of ALS. Front. Cell. Neurosci., 5, 1-8.
21. Lagier-Tourenne, C., Polymenidou, M., Hutt, K.R., Vu, A.Q., Baughn, M., Huelga, S.C., Clutario, K.M., Ling, S.-C., Liang, T.Y., Mazur, C. et al. (2012) Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci., 14, 459-469.
22. + current and its effect on excitability in motoneurones cultured from mutant SOD1 mice. J. Physiol., 563, 843-854.
23. Bories, C., Amendola, J., Lamotte d'Incamps, B. and Durand, J. (2007) Early electrophysiological abnormalities in lumbar motoneurons in a transgenic mouse model of amyotrophic lateral sclerosis. Eur. J. Neurosci., 25, 451-459.
24. Quinlan, K.A., Schuster, J.E., Fu, R., Siddique, T. and Heckman, C.J. (2011) Altered postnatal maturation of electrical properties in spinal motoneurons in a mouse model of amyotrophic lateral sclerosis. J. Physiol., 589, 2245-2260.
25. McGown, A., McDearmid, J.R., Panagiotaki, N., Tong, H., Al Mashhadi, S., Redhead, N., Lyon, A.N., Beattie, C.E., Shaw, P.J. and Ramesh, T.M. (2012) Early interneuron dysfunction in ALS: insights from a mutant sod1 zebrafish model. Ann. Neurol., 73, 246-258.
26. Shaw, P. and Ince, P. (1997) Glutamate, excitotoxicity and amyotrophic lateral sclerosis. J. Neurol., 244, S3-S14.
27. Ferraiuolo, L., Kirby, J., Grierson, A.J., Sendtner, M. and Shaw, P.J. (2011) Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat. Rev. Neurol., 7, 616-630.
28. Rothstein, J.D. (1995) Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. J. Clin. Neurosci., 3, 348-359.
29. Quinlan, K.A. (2011) Links between electrophysiological and molecular pathology of amyotrophic lateral sclerosis. Integr. Comp. Biol., 51, 913-925.
30. McDearmid, J.R. and Drapeau, P. (2006) Rhythmic motor activity evokedby NMDA in the spinal zebrafish larva. J. Neurophysiol., 95, 401-417.
31. Menelaou, E. and McLean, D.L. (2012) A gradient in endogenous rhythmicity and oscillatory drive matches recruitment order in an axial motor pool. J. Neurosci., 32, 10925-10939.
32. Ramesh, T., Lyon, A.N., Pineda, R.H., Wang, C., Janssen, P.M.L., Canan, B.D., Burghes, A.H.M. and Beattie, C.E. (2010) A genetic model of amyotrophic lateral sclerosis in zebrafish displays phenotypic hallmarks of motoneuron disease. Dis. Model. Mech., 3, 652-662.
33. 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.
34. Sakowski, S., Lunn, J., Busta, A., Oh, S., Zamora-Berridi, G., Palmer, M., Rosenberg, A., Philip, S., Dowling, J. and Feldman, E. (2012) Neuromuscular effects of G93A-SOD1 expression in zebrafish. Mol. Neurodegener., 7, 1-15.
35. Frey, D., Schneider, C., Xu, L., Borg, J., Spooren, W. and Caroni, P. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci., 20, 2534-2542.
36. Fischer, L.R., Culver, D.G., Tennant, P., Davis, A.A., Wang, M., Castellano-Sanchez, A., Khan, J., Polak, M.A. and Glass, J.D. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol., 185, 232-240.
37. Westerfield, M. (1995) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4th edn. University of Oregon Press, OR, Eugene.
38. Kabashi, E., Lin, L., Tradewell, M.L., Dion, P.A., Bercier, V., Bourgouin, P., Rochefort, D., Bel Hadj, S., Durham, H.D., Vande Velde, C. et al. (2010) Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum. Mol. Genet., 19, 671-683.
39. Buss, R.R. and Drapeau, P. (2002) Activation of embryonic red and white muscle fibers during fictive swimming in the developing zebrafish. J. Neurophysiol., 87, 1244-1251.
40. Buss, R.R. and Drapeau, P. (2000) Physiological properties of zebrafish embryonic red and white muscle fibers during early development. J. Neurophysiol., 84, 1545-1557.