Characterization of FUS Mutations in Amyotrophic Lateral Sclerosis Using RNA-Seq

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  van Blitterswijk, Marka ^a,b   Wang, Eric T ^c,d   Friedman, Brad A ^c,e   Keagle, Pamela J ^b   Lowe, Patrick ^b   Leclerc, Ashley Lyn ^b   van den Berg, Leonard H ^a   Housman, David E ^c   Veldink, Jan H ^a   Landers, John E ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUSED IN SARCOMA PROTEIN; MUTANT PROTEIN; RNA;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; FUS GENE; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RIBOSOMAL GENE; RNA SEQUENCE; RNA SPLICING; SPLICEOSOME RELATED GENE; WILD TYPE;

AMYOTROPHIC LATERAL SCLEROSIS; EXONS; HEK293 CELLS; HUMANS; INTRONS; MUTATION; RNA, SMALL INTERFERING; RNA-BINDING PROTEIN FUS; SEQUENCE ANALYSIS, RNA;

EID: 84875995777     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060788     Document Type: Article

References (51)

1. Rowland LP, Shneider NA, (2001) Amyotrophic lateral sclerosis. N Engl J Med 344: 1688-1700.
2. Andersen PM, Al-Chalabi A, (2011) Clinical genetics of amyotrophic lateral sclerosis: what do we really know? Nat Rev Neurol 7: 603-615.
3. van Blitterswijk M, van Es MA, Hennekam EA, Dooijes D, van Rheenen W, et al. (2012) Evidence for an oligogenic basis of amyotrophic lateral sclerosis. Hum Mol Genet 21: 3776-3784.
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: 245-256.
5. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, et al. (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72: 257-268.
6. Wu CH, Fallini C, Ticozzi N, Keagle PJ, Sapp PC, et al. (2012) Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488: 499-503.
7. Mackenzie IR, Rademakers R, Neumann M, (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9: 995-1007.
8. van Blitterswijk M, Landers JE, (2010) RNA processing pathways in amyotrophic lateral sclerosis. Neurogenetics 11: 275-290.
9. Calvio C, Neubauer G, Mann M, Lamond AI, (1995) Identification of hnRNP P2 as TLS/FUS using electrospray mass spectrometry. RNA 1: 724-733.
10. 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. Neurobiol Aging 32: 2323 e2327-2340.
11. 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: 1205-1208.
12. Vance C, Rogelj B, Hortobagyi 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: 1208-1211.
13. Deng HX, Zhai H, Bigio EH, Yan J, Fecto F, et al. (2010) FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Ann Neurol 67: 739-748.
14. Pokrishevsky E, Grad LI, Yousefi M, Wang J, Mackenzie IR, et al. (2012) Aberrant localization of FUS and TDP43 is associated with misfolding of SOD1 in amyotrophic lateral sclerosis. PLoS One 7: e35050.
15. Lagier-Tourenne C, Polymenidou M, Hutt KR, Vu AQ, Baughn M, et al. (2012) Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat Neurosci.
16. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
17. Friedman BA, Maniatis T, (2011) ExpressionPlot: a web-based framework for analysis of RNA-Seq and microarray gene expression data. Genome Biol 12: R69.
18. Oshlack A, Wakefield MJ, (2009) Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 4: 14.
19. Zinszner H, Albalat R, Ron D, (1994) A novel effector domain from the RNA-binding protein TLS or EWS is required for oncogenic transformation by CHOP. Genes Dev 8: 2513-2526.
20. Bertolotti A, Lutz Y, Heard DJ, Chambon P, Tora L, (1996) hTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J 15: 5022-5031.
21. Tan AY, Manley JL, (2010) TLS inhibits RNA polymerase III transcription. Mol Cell Biol 30: 186-196.
22. Wang X, Arai S, Song X, Reichart D, Du K, et al. (2008) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454: 126-130.
23. Goransson M, Andersson MK, Forni C, Stahlberg A, Andersson C, et al. (2009) The myxoid liposarcoma FUS-DDIT3 fusion oncoprotein deregulates NF-kappaB target genes by interaction with NFKBIZ. Oncogene 28: 270-278.
24. Uranishi H, Tetsuka T, Yamashita M, Asamitsu K, Shimizu M, et al. (2001) Involvement of the pro-oncoprotein TLS (translocated in liposarcoma) in nuclear factor-kappa B p65-mediated transcription as a coactivator. J Biol Chem 276: 13395-13401.
25. Zinszner H, Sok J, Immanuel D, Yin Y, Ron D, (1997) TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling. J Cell Sci 110 (Pt 15): 1741-1750.
26. Selamat W, Jamari I, Wang Y, Takumi T, Wong F, et al. (2009) TLS interaction with NMDA R1 splice variant in retinal ganglion cell line RGC-5. Neurosci Lett 450: 163-166.
27. Yoshimura A, Fujii R, Watanabe Y, Okabe S, Fukui K, et al. (2006) Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr Biol 16: 2345-2351.
28. Belly A, Moreau-Gachelin F, Sadoul R, Goldberg Y, (2005) Delocalization of the multifunctional RNA splicing factor TLS/FUS in hippocampal neurones: exclusion from the nucleus and accumulation in dendritic granules and spine heads. Neurosci Lett 379: 152-157.
29. Meissner M, Lopato S, Gotzmann J, Sauermann G, Barta A, (2003) Proto-oncoprotein TLS/FUS is associated to the nuclear matrix and complexed with splicing factors PTB, SRm160, and SR proteins. Exp Cell Res 283: 184-195.
30. Hoell JI, Larsson E, Runge S, Nusbaum JD, Duggimpudi S, et al. (2011) RNA targets of wild-type and mutant FET family proteins. Nat Struct Mol Biol 18: 1428-1431.
31. Lagier-Tourenne C, Polymenidou M, Cleveland DW, (2010) TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 19: R46-64.
32. Da Cruz S, Cleveland DW, (2011) Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol 21: 904-919.
33. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14: 452-458.
34. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14: 459-468.
35. Sephton CF, Cenik C, Kucukural A, Dammer EB, Cenik B, et al. (2011) Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J Biol Chem 286: 1204-1215.
36. Vaccaro A, Tauffenberger A, Aggad D, Rouleau G, Drapeau P, et al. (2012) Mutant TDP-43 and FUS cause age-dependent paralysis and neurodegeneration in C. elegans. PLoS One 7: e31321.
37. Vaccaro A, Patten SA, Ciura S, Maios C, Therrien M, et al. (2012) Methylene Blue Protects against TDP-43 and FUS Neuronal Toxicity in C. elegans and D. rerio. PLoS One 7: e42117.
38. Murakami T, Yang SP, Xie L, Kawano T, Fu D, 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.
39. Mitchell JC, McGoldrick P, Vance C, Hortobagyi T, Sreedharan J, et al. (2012) Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathol.
40. Lanson NA Jr, Maltare A, King H, Smith R, Kim JH, et al. (2011) A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum Mol Genet 20: 2510-2523.
41. Sasayama H, Shimamura M, Tokuda T, Azuma Y, Yoshida T, et al. (2012) Knockdown of the Drosophila fused in sarcoma (FUS) homologue causes deficient locomotive behavior and shortening of motoneuron terminal branches. PLoS One 7: e39483.
42. Wang JW, Brent JR, Tomlinson A, Shneider NA, McCabe BD, (2011) The ALS-associated proteins FUS and TDP-43 function together to affect Drosophila locomotion and life span. J Clin Invest 121: 4118-4126.
43. Halliday G, Bigio EH, Cairns NJ, Neumann M, Mackenzie IR, et al. (2012) Mechanisms of disease in frontotemporal lobar degeneration: gain of function versus loss of function effects. Acta Neuropathol 124: 373-382.
44. Ju S, Tardiff DF, Han H, Divya K, Zhong Q, et al. (2011) A yeast model of FUS/TLS-dependent cytotoxicity. PLoS Biol 9: e1001052.
45. 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 Biol 9: e1000614.
46. Kryndushkin D, Wickner RB, Shewmaker F, (2011) FUS/TLS forms cytoplasmic aggregates, inhibits cell growth and interacts with TDP-43 in a yeast model of amyotrophic lateral sclerosis. Protein Cell 2: 223-236.
47. Fushimi K, Long C, Jayaram N, Chen X, Li L, et al. (2011) Expression of human FUS/TLS in yeast leads to protein aggregation and cytotoxicity, recapitulating key features of FUS proteinopathy. Protein Cell 2: 141-149.
48. 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. EMBO J 29: 2841-2857.
49. Shelkovnikova TA, Ustyugov AA, Smirnov AP, Skvortsova VI, Buchman VL, et al. (2011) FUS gene mutations associated with familiar forms of amyotrophic lateral sclerosis affect cellular localization and aggregation properties of the encoded protein. Dokl Biochem Biophys 438: 123-126.
50. Elbers CC, van Eijk KR, Franke L, Mulder F, van der Schouw YT, et al. (2009) Using genome-wide pathway analysis to unravel the etiology of complex diseases. Genet Epidemiol 33: 419-431.
51. 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. Hum Mol Genet 19: 4160-4175.