Mutant human FUS is ubiquitously mislocalized and generates persistent stress granules in primary cultured transgenic zebrafish cells

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Acosta, Jamie Rae ^a   Goldsbury, Claire ^a   Winnick, Claire ^a,b   Badrock, Andrew P ^a,b   Fraser, Stuart T ^a   Laird, Angela S ^a   Hall, Thomas E ^c   Don, Emily K ^a,b   Fifita, Jennifer A ^a,b   Blair, Ian P ^a,b   Nicholson, Garth A ^a,b   Cole, Nicholas J ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; FUSED IN SARCOMA PROTEIN; RNA BINDING PROTEIN; TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL INCLUSION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DEGENERATIVE DISEASE; EMBRYO; GENE MUTATION; MOTONEURON; NONHUMAN; PROTEIN LOCALIZATION; TRANSGENIC ZEBRAFISH; WILD TYPE; ANIMAL; CELL GRANULE; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MUTATION; PROTEIN TRANSPORT; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; CYTOPLASMIC GRANULES; CYTOSOL; HUMANS; MOTOR NEURONS; MUTATION; PROTEIN TRANSPORT; RNA-BINDING PROTEIN FUS; ZEBRAFISH;

EID: 84902668919     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090572     Document Type: Article

References (32)

1. Robberecht W, Philips T (2013) The changing scene of amyotrophic lateral sclerosis. Nature Reviews Neuroscience 14(4): 248-64.
2. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, et al. (2008) TDP-43 Mutations in Familial and Sporadic Amyotrophic Lateral Sclerosis. Science 319(5870): 1668-1672. (Pubitemid 351432505)
3. Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, et al. (2009) Mutations in the FUS/TLS Gene on Chromosome 16 Cause Familial Amyotrophic Lateral Sclerosis. Science 323(5918): 1205-1208.
4. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, et al. (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72(2): 245-256.
5. Vance C, Rogelj B, Hortobágyi T, De Vos KJ, Nishimura AL, et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323(5918): 1208-1211.
6. Corrado L, Del Bo R, Castellotti B, Ratti A, Cereda C, et al. (2010) Mutations of FUS gene in sporadic amyotrophic lateral sclerosis. Journal of Medical Genetics 47(3): 190-194.
7. Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, et al. (2010) Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Human molecular genetics 19(21): 4160-4175.
8. Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, et al. (2010) ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. The EMBO journal 29(16): 2841-2857.
9. Gal J, Zhang J, Kwinter DM, Zhai J, Jia H, et al. (2011) Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Neurobiology of aging 32(12): 2323. e27-40.
10. Armstrong GA, Drapeau P (2013) Loss and gain of FUS function impair neuromuscular synaptic transmission in a genetic model of ALS. Human Molecular Genetics 22(21): 4282-92.
11. Ito D, Seki M, Tsunoda Y, Uchiyama H, Suzuki N (2011) Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Annals of neurology 69(1): 152-162.
12. Kino Y, Washizu C, Aquilanti E, Okuno M, Kurosawa M, et al. (2011) Intracellular localization and splicing regulation of FUS/TLS are variably affected by amyotrophic lateral sclerosis-linked mutations. Nucleic acids research 39(7): 2781-2798.
13. Li YR, King OD, Shorter J, Gitler AD (2013) Stress granules as crucibles of ALS pathogenesis. Journal of cell biology 201(3): 361-72.
14. Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage. Trends in Biochemical Sciences 33(3): 141-150.
15. Fujita K, Ito H, Nakano S, Kinoshita Y, Wate R, et al. (2008) Immunohistochemical identification of messenger RNA-related proteins in basophilic inclusions of adult-onset atypical motor neuron disease. Acta Neuropathologica 116(4): 439-445.
16. Bentmann E, Neumann M, Tahirovic S, Rodde R, Dormann D, et al. (2012). Requirements for stress granule recruitment of fused in sarcoma (FUS) and TAR DNA-binding protein of 43 kDa (TDP-43). The Journal of biological chemistry 287(27): 23079.
17. Vanderweyde T, Yu H, Varnum M, Liu-Yesucevitz L, Citro A, et al. (2012) Contrasting pathology of the stress granule proteins TIA-1 and G3BP in tauopathies. J Neurosci 32(24): 8270-8283.
18. Lee EB, Lee VM, Trojanowski JQ (2011) Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nature Reviews Neuroscience 13(1): 38-50.
19. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236(11): 3088-99. (Pubitemid 350175006)
20. Higashijima S, Okamoto H, Ueno N, Hotta Y, Eguchi G, et al. (1997) High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev Biol 192(2): 289-99. (Pubitemid 28066934)
21. Higashijima S, Hotta Y, Okamoto H (2000) Visualization of Cranial Motor Neurons in Live Transgenic Zebrafish Expressing Green Fluorescent Protein Under the Control of the Islet-1 Promoter/Enhancer. Journal of Neuroscience 20(1): 206-218. (Pubitemid 30220508)
22. Imlach WL, Beck ES, Choi BJ, Lotti F, Pellizzoni L, et al. (2012) SMN is required for sensory-motor circuit function in Drosophila. Cell 151(2): 427-39.
23. Lobsiger CS, Cleveland DW (2007) Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nature Neuroscience 10(11): 1355-1360. (Pubitemid 350014678)
24. Belzil VV, Valdmanis PN, Dion PA, Daoud H, Kabashi E, et al. (2009) Mutations in FUS cause FALS and SALS in French and French Canadian populations. Neurology 73(15): 1176.
25. Ticozzi N, Silani V, LeClerc AL, Keagle P, Gellera C, et al. (2009) Analysis of FUS gene mutation in familial amyotrophic lateral sclerosis within an Italian cohort. Neurology 73(15): 1180-5.
26. Drepper C, Herrmann T, Wessig C, Beck M, Sendtner M (2011) C-terminal FUS/TLS mutations in familial and sporadic ALS in Germany. Neurobiology of Aging 32(3): 548. e541-548. e544.
27. Anthony HH, Kai S (2011) Beyond HeLa cells. Nature 480(7375): 34.
28. Sun Z, Diaz Z, Fang X, Hart MP, Chesi A, et al. (2011) Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS biology 9(4): e1000614.
29. Huang C, Zhou H, Tong J, Chen H, Liu YJ, et al. (2011) FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS genetics 7(3): e1002011.
30. Laird AS, Van Hoecke A, De Muynck L, Timmers M, Van den Bosch L, et al. (2010) Progranulin is neurotrophic in vivo and protects against a mutant TDP-43 induced axonopathy. PLOS ONE 5(10): e13368.
31. Lemmens R, Van Hoecke A, Hersmus N, Geelen V, D'Hollander I, et al. (2007) Overexpression of mutant superoxide dismutase 1 causes a motor axonopathy in the zebrafish. Human molecular genetics 16(19): 2359-2365. (Pubitemid 47423902)
32. Manfredi G, Kawamata H (2011) Neurodegeneration: Methods and Protocols, Humana Press.