Interaction of amyotrophic lateral sclerosis/frontotemporal lobar degeneration-associated fused-in-sarcoma with proteins involved in metabolic and protein degradation pathways

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 527-535

  Wang, Tao ^a   Jiang, Xin ^a   Chen, Gang ^a   Xu, Jin ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Amyotrophic lateral sclerosis (ALS); Frontotemporal dementia (FTD); Fused in sarcoma (FUS); Metabolic; Protein degradation; Valocin containing protein (VCP)

Indexed keywords

26S PROTEASOME NON ATPASE REGULATORY SUBUNIT 12; ADENOSINE TRIPHOSPHATE; FUSED IN SARCOMA PROTEIN; MESSENGER RNA; POLYPYRIMIDINE TRACT BINDING PROTEIN ASSOCIATED SPLICING; POLYUBIQUITIN; PROTEASOME; PROTEIN; UBIQUITIN; UBIQUITIN LIKE MODIFIER ACTIVATING ENZYME 1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VALOCIN CONTAINING PROTEIN; ADENOSINE TRIPHOSPHATASE; CDC48 PROTEIN; CELL CYCLE PROTEIN; MUTANT PROTEIN; PROTEIN BINDING; RNA BINDING PROTEIN;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BIOACCUMULATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENERGY METABOLISM; FRONTOTEMPORAL DEMENTIA; MASS SPECTROMETRY; METABOLIC DISORDER; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEOMICS; RNA METABOLISM; UBIQUITINATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMYOTROPHIC LATERAL SCLEROSIS; CELL CYCLE PROTEINS; ENERGY METABOLISM; FRONTOTEMPORAL LOBAR DEGENERATION; HEK293 CELLS; HUMANS; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEOLYSIS; RNA, MESSENGER; RNA-BINDING PROTEIN FUS;

EID: 84920379368     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.07.044     Document Type: Article

References (55)

1. Allen S.P., Rajan S., Duffy L., Mortiboys H., Higginbottom A., Grierson A.J., Shaw P.J. Superoxide dismutase 1 mutation in a cellular model of amyotrophic lateral sclerosis shifts energy generation from oxidative phosphorylation to glycolysis. Neurobiol. Aging 2014, 35:1499-1509.
2. Anderson P., Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 2009, 10:430-436.
3. Azuma Y., Tokuda T., Shimamura M., Kyotani A., Sasayama H., Yoshida T., Mizuta I., Mizuno T., Nakagawa M., Fujikake N., Ueyama M., Nagai Y., Yamaguchi M. Identification of ter94, Drosophila VCP, as a strong modulator of motor neuron degeneration induced by knockdown of Caz, Drosophila FUS. Hum. Mol. Genet. 2014, 23:3467-3480.
4. Balagopal V., Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 2009, 21:403-408.
5. Blokhuis A.M., Groen E.J., Koppers M., van den Berg L.H., Pasterkamp R.J. Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 2013, 125:777-794.
6. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
7. Chen Y., Yang M., Deng J., Chen X., Ye Y., Zhu L., Liu J., Ye H., Shen Y., Li Y., Rao E.J., Fushimi K., Zhou X., Bigio E.H., Mesulam M., Xu Q., Wu J.Y. Expression of human FUS protein in Drosophila leads to progressive neurodegeneration. Protein Cell 2011, 2:477-486.
8. Couthouis J., Hart M.P., Erion R., King O.D., Diaz Z., Nakaya T., Ibrahim F., Kim H.J., Mojsilovic-Petrovic J., Panossian S., Kim C.E., Frackelton E.C., Solski J.A., Williams K.L., Clay-Falcone D., Elman L., McCluskey L., Greene R., Hakonarson H., Kalb R.G., Lee V.M., Trojanowski J.Q., Nicholson G.A., Blair I.P., Bonini N.M., Van Deerlin V.M., Mourelatos Z., Shorter J., Gitler A.D. Evaluating the role of the FUS/TLS-related gene EWSR1 in amyotrophic lateral sclerosis. Hum. Mol. Genet. 2012, 21:2899-2911.
9. Couthouis J., Hart M.P., Shorter J., DeJesus-Hernandez M., Erion R., Oristano R., Liu A.X., Ramos D., Jethava N., Hosangadi D., Epstein J., Chiang A., Diaz Z., Nakaya T., Ibrahim F., Kim H.J., Solski J.A., Williams K.L., Mojsilovic-Petrovic J., Ingre C., Boylan K., Graff-Radford N.R., Dickson D.W., Clay-Falcone D., Elman L., McCluskey L., Greene R., Kalb R.G., Lee V.M., Trojanowski J.Q., Ludolph A., Robberecht W., Andersen P.M., Nicholson G.A., Blair I.P., King O.D., Bonini N.M., Van Deerlin V., Rademakers R., Mourelatos Z., Gitler A.D. Ayeast functional screen predicts new candidate ALS disease genes. Proc. Natl. Acad. Sci. U.S.A 2011, 108:20881-20890.
10. Crozat A., Aman P., Mandahl N., Ron D. Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature 1993, 363:640-644.
11. Dichmann D.S., Harland R.M. fus/TLS orchestrates splicing of developmental regulators during gastrulation. Genes Dev. 2012, 26:1351-1363.
12. Dormann D., Rodde R., Edbauer D., Bentmann E., Fischer I., Hruscha A., Than M.E., Mackenzie I.R., Capell A., Schmid B., Neumann M., Haass C. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J. 2010, 29:2841-2857.
13. Elden A.C., Kim H.J., Hart M.P., Chen-Plotkin A.S., Johnson B.S., Fang X., Armakola M., Geser F., Greene R., Lu M.M., Padmanabhan A., Clay-Falcone D., McCluskey L., Elman L., Juhr D., Gruber P.J., Rub U., Auburger G., Trojanowski J.Q., Lee V.M., Van Deerlin V.M., Bonini N.M., Gitler A.D. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010, 466:1069-1075.
14. Gitcho M.A., Strider J., Carter D., Taylor-Reinwald L., Forman M.S., Goate A.M., Cairns N.J. VCP mutations causing frontotemporal lobar degeneration disrupt localization of TDP-43 and induce cell death. J.Biol. Chem. 2009, 284:12384-12398.
15. Gitler A.D., Shorter J. RNA-binding proteins with prion-like domains in ALS and FTLD-U. Prion 2011, 5:179-187.
16. Gwinn-Hardy K., Chen J.Y., Liu H.C., Liu T.Y., Boss M., Seltzer W., Adam A., Singleton A., Koroshetz W., Waters C., Hardy J., Farrer M. Spinocerebellar ataxia type 2 with parkinsonism in ethnic Chinese. Neurology 2000, 55:800-805.
17. Han T.W., Kato M., Xie S., Wu L.C., Mirzaei H., Pei J., Chen M., Xie Y., Allen J., Xiao G., McKnight S.L. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 2012, 149:768-779.
18. Hoell J.I., Larsson E., Runge S., Nusbaum J.D., Duggimpudi S., Farazi T.A., Hafner M., Borkhardt A., Sander C., Tuschl T. RNA targets of wild-type and mutant FET family proteins. Nat. Struct. Mol. Biol. 2011, 18:1428-1431.
19. Huang C., Zhou H., Tong J., Chen H., Liu Y.J., Wang D., Wei X., Xia X.G. FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet. 2011, 7:e1002011.
20. Hubbard R.W., Will A.D., Peterson G.W., Sanchez A., Gillan W.W., Tan S.A. Elevated plasma glucagon in amyotrophic lateral sclerosis. Neurology 1992, 42:1532-1534.
21. Johnson J.O., Mandrioli J., Benatar M., Abramzon Y., Van Deerlin V.M., Trojanowski J.Q., Gibbs J.R., Brunetti M., Gronka S., Wuu J., Ding J., McCluskey L., Martinez-Lage M., Falcone D., Hernandez D.G., Arepalli S., Chong S., Schymick J.C., Rothstein J., Landi F., Wang Y.D., Calvo A., Mora G., Sabatelli M., Monsurro M.R., Battistini S., Salvi F., Spataro R., Sola P., Borghero G., Galassi G., Scholz S.W., Taylor J.P., Restagno G., Chio A., Traynor B.J. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010, 68:857-864. ITALSGEN Consortium.
22. Kaehler C., Isensee J., Nonhoff U., Terrey M., Hucho T., Lehrach H., Krobitsch S. Ataxin-2-like is a regulator of stress granules and processing bodies. PLoS One 2012, 7:e50134.
23. Ke Y.D., Dramiga J., Schutz U., Kril J.J., Ittner L.M., Schroder H., Gotz J. Tau-mediated nuclear depletion and cytoplasmic accumulation of SFPQ in Alzheimer's and Pick's disease. PLoS One 2012, 7:e35678.
24. King O.D., Gitler A.D., Shorter J. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 2012, 1462:61-80.
25. 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., Valdmanis P., Rouleau G.A., Hosler B.A., Cortelli P., de Jong P.J., Yoshinaga Y., Haines J.L., Pericak-Vance M.A., Yan J., Ticozzi N., Siddique T., McKenna-Yasek D., Sapp P.C., Horvitz H.R., Landers J.E., Brown R.H. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
26. Kwon I., Kato M., Xiang S., Wu L., Theodoropoulos P., Mirzaei H., Han T., Xie S., Corden J.L., McKnight S.L. Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 2013, 155:1049-1060.
27. 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., Wancewicz E., Kim A.S., Watt A., Freier S., Hicks G.G., Donohue J.P., Shiue L., Bennett C.F., Ravits J., Cleveland D.W., Yeo G.W. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci. 2012, 15:1488-1497.
28. Lee Y.J., Wei H.M., Chen L.Y., Li C. Localization of SERBP1 in stress granules and nucleoli. FEBS J. 2014, 281:352-364.
29. Ling S.C., Albuquerque C.P., Han J.S., Lagier-Tourenne C., Tokunaga S., Zhou H., Cleveland D.W. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc. Natl. Acad. Sci. U.S.A 2010, 107:13318-13323.
30. Ling S.C., Polymenidou M., Cleveland D.W. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 2013, 79:416-438.
31. Mackenzie I.R., Neumann M. FET proteins in frontotemporal dementia and amyotrophic lateral sclerosis. Brain Res. 2012, 1462:40-43.
32. Mackenzie I.R., Rademakers R., Neumann M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 2010, 9:995-1007.
33. Malaspina A., Kaushik N., de Belleroche J. A14-3-3 mRNA is up-regulated in amyotrophic lateral sclerosis spinal cord. J.Neurochem. 2000, 75:2511-2520.
34. Meerang M., Ritz D., Paliwal S., Garajova Z., Bosshard M., Mailand N., Janscak P., Hubscher U., Meyer H., Ramadan K. The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat. Cell Biol. 2011, 13:1376-1382.
35. Meyer H., Bug M., Bremer S. Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 2012, 14:117-123.
36. Oh S.M., Liu Z., Okada M., Jang S.W., Liu X., Chan C.B., Luo H., Ye K. Ebp1 sumoylation, regulated by TLS/FUS E3 ligase, is required for its anti-proliferative activity. Oncogene 2010, 29:1017-1030.
37. Pradat P.F., Bruneteau G., Gordon P.H., Dupuis L., Bonnefont-Rousselot D., Simon D., Salachas F., Corcia P., Frochot V., Lacorte J.M., Jardel C., Coussieu C., Le Forestier N., Lacomblez L., Loeffler J.P., Meininger V. Impaired glucose tolerance in patients with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:166-171.
38. Pulst S.M., Nechiporuk A., Nechiporuk T., Gispert S., Chen X.N., Lopes-Cendes I., Pearlman S., Starkman S., Orozco-Diaz G., Lunkes A., DeJong P., Rouleau G.A., Auburger G., Korenberg J.R., Figueroa C., Sahba S. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat. Genet. 1996, 14:269-276.
39. Qiu H., Lee S., Shang Y., Wang W.Y., Au K.F., Kamiya S., Barmada S.J., Finkbeiner S., Lui H., Carlton C.E., Tang A.A., Oldham M.C., Wang H., Shorter J., Filiano A.J., Roberson E.D., Tourtellotte W.G., Chen B., Tsai L.H., Huang E.J. ALS-associated mutation FUS-R521C causes DNA damage and RNA splicing defects. J.Clin. Invest. 2014, 124:981-999.
40. Seyfried N.T., Gozal Y.M., Donovan L.E., Herskowitz J.H., Dammer E.B., Xia Q., Ku L., Chang J., Duong D.M., Rees H.D., Cooper D.S., Glass J.D., Gearing M., Tansey M.G., Lah J.J., Feng Y., Levey A.I., Peng J. Quantitative analysis of the detergent-insoluble brain proteome in frontotemporal lobar degeneration using SILAC internal standards. J.Proteome Res. 2012, 11:2721-2738.
41. Shav-Tal Y., Zipori D. PSF and p54(nrb)/NonO-multi-functional nuclear proteins. FEBS Lett. 2002, 531:109-114.
42. Shelkovnikova T.A., Robinson H.K., Troakes C., Ninkina N., Buchman V.L. Compromised paraspeckle formation as a pathogenic factor in FUSopathies. Hum. Mol. Genet. 2014, 23:2298-2312.
43. Stallings N.R., Puttaparthi K., Dowling K.J., Luther C.M., Burns D.K., Davis K., Elliott J.L. TDP-43, an ALS linked protein, regulates fat deposition and glucose homeostasis. PLoS One 2013, 8:e71793.
44. Swisher K.D., Parker R. Localization to, and effects of Pbp1, Pbp4, Lsm12, Dhh1, and Pab1 on stress granules in Saccharomyces cerevisiae. PLoS One 2010, 5:e10006.
45. Tan A.Y., Riley T.R., Coady T., Bussemaker H.J., Manley J.L. TLS/FUS (translocated in liposarcoma/fused in sarcoma) regulates target gene transcription via single-stranded DNA response elements. Proc. Natl. Acad. Sci. U.S.A 2012, 109:6030-6035.
46. Taylor R.C., Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 2011, 3. pii:a004440.
47. Tradewell M.L., Yu Z., Tibshirani M., Boulanger M.C., Durham H.D., Richard S. Arginine methylation by PRMT1 regulates nuclear-cytoplasmic localization and toxicity of FUS/TLS harbouring ALS-linked mutations. Hum. Mol. Genet. 2012, 21:136-149.
48. Vance C., Rogelj B., Hortobagyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., Ganesalingam J., Williams K.L., Tripathi V., Al-Saraj S., Al-Chalabi A., Leigh P.N., Blair I.P., Nicholson G., de Belleroche J., Gallo J.M., Miller C.C., Shaw C.E. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
49. Wang W.Y., Pan L., Su S.C., Quinn E.J., Sasaki M., Jimenez J.C., Mackenzie I.R., Huang E.J., Tsai L.H. Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons. Nat. Neurosci. 2013, 16:1383-1391.
50. Wang X., Arai S., Song X., Reichart D., Du K., Pascual G., Tempst P., Rosenfeld M.G., Glass C.K., Kurokawa R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 2008, 454:126-130.
51. Wu C.H., Fallini C., Ticozzi N., Keagle P.J., Sapp P.C., Piotrowska K., Lowe P., Koppers M., McKenna-Yasek D., Baron D.M., Kost J.E., Gonzalez-Perez P., Fox A.D., Adams J., Taroni F., Tiloca C., Leclerc A.L., Chafe S.C., Mangroo D., Moore M.J., Zitzewitz J.A., Xu Z.S., van den Berg L.H., Glass J.D., Siciliano G., Cirulli E.T., Goldstein D.B., Salachas F., Meininger V., Rossoll W., Ratti A., Gellera C., Bosco D.A., Bassell G.J., Silani V., Drory V.E., Brown R.H., Landers J.E. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012, 488:499-503.
52. Xu J., Zhong N., Wang H., Elias J.E., Kim C.K., Woldman I., Pifl C., Gygi S.P., Geula C., Yankner B.A. The Parkinson's disease-associated DJ-1 protein is a transcriptional co-activator that protects against neuronal apoptosis. Hum. Mol. Genet. 2005, 14:1231-1241.
53. Yamazaki T., Chen S., Yu Y., Yan B., Haertlein T.C., Carrasco M.A., Tapia J.C., Zhai B., Das R., Lalancette-Hebert M., Sharma A., Chandran S., Sullivan G., Nishimura A.L., Shaw C.E., Gygi S.P., Shneider N.A., Maniatis T., Reed R. FUS-SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Rep. 2012, 2:799-806.
54. Yasuda K., Zhang H., Loiselle D., Haystead T., Macara I.G., Mili S. The RNA-binding protein Fus directs translation of localized mRNAs in APC-RNP granules. J.Cell Biol. 2013, 203:737-746.
55. Zhong N., Kim C., Rizu P., Geula C., Porter D., Pothos E., Squitieri F., Heutink P., Xu J. DJ-1 transcriptionally up-regulates the human tyrosine hydroxylase by inhibiting the sumoylation of PSF. J.Biol. Chem. 2006, 281:20940-20948.