Modelling FUSopathies: Focus on protein aggregation

Biochemical Society Transactions

Volumn 41, Issue 6, 2013, Pages 1613-1617

  Shelkovnikova, Tatyana A ^a,b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b INSTITUTE OF PHYSIOLOGICALLY ACTIVE COMPOUNDS   (Russian Federation)

Author keywords

Amyotrophic lateral sclerosis (ALS); Fused in sarcoma (FUS); Protein aggregation; Proteinopathy; Transgenic model

Indexed keywords

FUSED IN SARCOMA PROTEIN; PRION PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; CONFERENCE PAPER; DEGENERATIVE DISEASE; DISEASE MODEL; DROSOPHILA; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HISTOPATHOLOGY; HUMAN; IN VIVO STUDY; MAMMAL; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA METABOLISM; SOLUBILITY;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; RNA-BINDING PROTEIN FUS;

EID: 84887903154     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130212     Document Type: Conference Paper

References (37)

1. Hicks, G.G., Singh, N., Nashabi, A., Mai, S., Bozek, G., Klewes, L., Arapovic, D., White, E.K., Koury, M.J., Oltz, E.M. et al. (2000) Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 24, 175-179
2. Kuroda, M., Sok, J., Webb, L., Baechtold, H., Urano, F., Yin, Y., Chung, P., de Rooij, D.G., Akhmedov, A., Ashley, T. and Ron, D. (2000) Male sterility and enhanced radiation sensitivity in TLS/ mice. EMBO J. 19, 453-462
3. Kwiatkowski, Jr, 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
4. Neumann, M., Rademakers, R., Roeber, S., Baker, M., Kretzschmar, H.A. and Mackenzie, I.R. (2009) A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 132, 2922-2931
5. 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
6. Neumann, M., Roeber, S., Kretzschmar, H.A., Rademakers, R., Baker, M. and Mackenzie, I.R. (2009) Abundant FUS-immunoreactive pathology in neuronal intermediate filament inclusion disease. Acta Neuropathol. 118, 605-616
7. Lattante, S., Rouleau, G.A. and Kabashi, E. (2013) TARDBP and FUS mutations associated with amyotrophic lateral sclerosis: summary and update. Hum. Mutat. 34, 812-826
8. Bigio, E.H., Wu, J.Y., Deng, H.X., Bit-Ivan, E.N., Mao, Q., Ganti, R., Peterson, M., Siddique, N., Geula, C., Siddique, T. and Mesulam, M. (2013) Inclusions in frontotemporal lobar degeneration with TDP-43 proteinopathy (FTLD-TDP) and amyotrophic lateral sclerosis (ALS), but not FTLD with FUS proteinopathy (FTLD-FUS), have properties of amyloid. Acta Neuropathol. 125, 463-465
9. Lashley, T., Rohrer, J.D., Bandopadhyay, R., Fry, C., Ahmed, Z., Isaacs, A.M., Brelstaff, J.H., Borroni, B., Warren, J.D., Troakes, C. et al. (2011) A comparative clinical, pathological, biochemical and genetic study of fused in sarcoma proteinopathies. Brain 134, 2548-2564
10. Neumann, M., Kwong, L.K., Sampathu, D.M., Trojanowski, J.Q. and Lee, V.M. (2007) TDP-43 proteinopathy in frontotemporal lobar degeneration and amyotrophic lateral sclerosis: protein misfolding diseases without amyloidosis. Arch. Neurol. 64, 1388-1394
11. Cushman, M., Johnson, B.S., King, O.D., Gitler, A.D. and Shorter, J. (2010) Prion-like disorders: blurring the divide between transmissibility and infectivity. J. Cell Sci. 123, 1191-1201
12. Gitler, A.D. and Shorter, J. (2011) RNA-binding proteins with prion-like domains in ALS and FTLD-U. Prion 5, 179-187
13. Udan, M. and Baloh, R.H. (2011) Implications of the prion-related Q/N domains in TDP-43 and FUS. Prion 5, 1-5
14. Sun, Z., Diaz, Z., Fang, X., Hart, M.P., Chesi, A., Shorter, J. and Gitler, A.D. (2011) Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol. 9, e1000614
15. Kato, M., Han, T.W., Xie, S., Shi, K., Du, X., Wu, L.C., Mirzaei, H., Goldsmith, E.J., Longgood, J., Pei, J. et al. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753-767
16. Han, T.W., Kato, M., Xie, S., Wu, L.C., Mirzaei, H., Pei, J., Chen, M., Xie, Y., Allen, J., Xiao, G. and McKnight, S.L. (2012) Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149, 768-779
17. Andersson, M.K., Stahlberg, A., Arvidsson, Y., Olofsson, A., Semb, H., Stenman, G., Nilsson, O. and Aman, P. (2008) The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response. BMC Cell Biol. 9, 37
18. Fujii, R. and Takumi, T. (2005) TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines. J. Cell Sci. 118, 5755-5765
19. Kanai, Y., Dohmae, N. and Hirokawa, N. (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525
20. Dormann, D., Rodde, R., Edbauer, D., Bentmann, E., Fischer, I., Hruscha, A., Than, M.E., Mackenzie, I.R., Capell, A., Schmid, B. et al. (2010) ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J. 29, 2841-2857
21. Wolozin, B. (2012) Regulated protein aggregation: stress granules and neurodegeneration. Mol. Neurodegener. 7, 56
22. Kedersha, N. and Anderson, P. (2002) Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963-969
23. Ito, D., Seki, M., Tsunoda, Y., Uchiyama, H. and Suzuki, N. (2011) Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Ann. Neurol. 69, 152-162
24. Shelkovnikova, T.A., Robinson, H., Connor-Robson, N. and Buchman, V.L. (2013) Recruitment into stress granules prevents irreversible aggregation of FUS protein mislocalized to the cytoplasm. Cell Cycle 12, article 26241
25. Xia, R., Liu, Y., Yang, L., Gal, J., Zhu, H. and Jia, J. (2012) Motor neuron apoptosis and neuromuscular junction perturbation are prominent features in a Drosophila model of Fus-mediated ALS. Mol. Neurodegener. 7, 10
26. Miguel, L., Avequin, T., Delarue, M., Feuillette, S., Frebourg, T., Campion, D. and Lecourtois, M. (2012) Accumulation of insoluble forms of FUS protein correlates with toxicity in Drosophila. Neurobiol. Aging 33, e1001-e1015
27. Daigle, J.G., Lanson, Jr, N.A., Smith, R.B., Casci, I., Maltare, A., Monaghan, J., Nichols, C.D., Kryndushkin, D., Shewmaker, F. and Pandey, U.B. (2013) 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
28. Lanson, Jr, N.A., Maltare, A., King, H., Smith, R., Kim, J.H., Taylor, J.P., Lloyd, T.E. and Pandey, U.B. (2011) A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum. Mol. Genet. 20, 2510-2523
29. 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
30. Vaccaro, A., Tauffenberger, A., Aggad, D., Rouleau, G., Drapeau, P. and Parker, J.A. (2012) Mutant TDP-43 and FUS cause age-dependent paralysis and neurodegeneration in C. elegans. PLoS ONE 7, e31321
31. Belzil, V.V., Valdmanis, P.N., Dion, P.A., Daoud, H., Kabashi, E., Noreau, A., Gauthier, J., S2D team, Hince, P., Desjarlais, A. et al. (2009) Mutations in FUS cause FALS and SALS in French and French Canadian populations. Neurology 73, 1176-1179
32. Huang, C., Zhou, H., Tong, J., Chen, H., Liu, Y.J., Wang, D., Wei, X. and Xia, X.G. (2011) FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet. 7, e1002011
33. Verbeeck, C., Deng, Q., Dejesus-Hernandez, M., Taylor, G., Ceballos-Diaz, C., Kocerha, J., Golde, T., Das, P., Rademakers, R., Dickson, D.W. and Kukar, T. (2012) Expression of Fused in sarcoma mutations in mice recapitulates the neuropathology of FUS proteinopathies and provides insight into disease pathogenesis. Mol. Neurodegener. 7, 53
34. DeJesus-Hernandez, M., Kocerha, J., Finch, N., Crook, R., Baker, M., Desaro, P., Johnston, A., Rutherford, N., Wojtas, A., Kennelly, K. et al. (2010) De novo truncating FUS gene mutation as a cause of sporadic amyotrophic lateral sclerosis. Hum. Mutat. 31, E1377-E1389
35. Bosco, D.A., Lemay, N., Ko, H.K., Zhou, H., Burke, C., Kwiatkowski, Jr, T.J., Sapp, P., McKenna-Yasek, D., Brown, Jr, 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
36. Mitchell, J.C., McGoldrick, P., Vance, C., Hortobagyi, T., Sreedharan, J., Rogelj, B., Tudor, E.L., Smith, B.N., Klasen, C., Miller, C.C. 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
37. Shelkovnikova, T.A., Peters, O.M., Deykin, A.V., Connor-Robson, N., Robinson, H., Ustyugov, A.A., Bachurin, S.O., Ermolkevich, T.G., Goldman, I.L., Sadchikova, E.R. et al. (2013) Fused in sarcoma (FUS) protein lacking nuclear localization signal (NLS) and major RNA binding motifs triggers proteinopathy and severe motor phenotype in transgenic mice. J. Biol. Chem. 288, 25266-25274