Endogenous TDP-43, but not FUS, contributes to stress granule assembly via G3BP

Molecular Neurodegeneration

Volumn 7, Issue 1, 2012, Pages

  Aulas, Anaïs ^a   Stabile, Stéphanie ^a   Vande Velde, Christine ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

ALS; Cell death; FUS TLS; G3BP; Oxidative stress; Stress granules; TDP 43; TIA 1

Indexed keywords

CELL PROTEIN; G3BP PROTEIN; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL AGGREGATION; CELL GRANULE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; STRESS GRANULE;

AMYOTROPHIC LATERAL SCLEROSIS; CARRIER PROTEINS; CYTOPLASMIC GRANULES; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IMMUNOBLOTTING; OXIDATIVE STRESS; RNA-BINDING PROTEIN FUS; TRANSFECTION;

EID: 84867686875     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-7-54     Document Type: Article

References (49)

1. Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Dion PA, Daoud H, Rouleau GA, Nat Rev Genet 2009 10 769 782 19823194
2. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, et al. Nat Genet 2008 40 572 574 10.1038/ng.132 18372902 (Pubitemid 351601218)
3. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, et al. Science 2008 319 1668 1672 10.1126/science.1154584 18309045 (Pubitemid 351432505)
4. Rethinking ALS: the FUS about TDP-43. Lagier-Tourenne C, Cleveland DW, Cell 2009 136 1001 1004 10.1016/j.cell.2009.03.006 19303844
5. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, et al. Science 2009 323 1205 1208 10.1126/science.1166066 19251627
6. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, et al. Science 2009 323 1208 1211 10.1126/science.1165942 19251628
7. Stress granules. Anderson P, Kedersha N, Curr Biol 2009 19 397 R398 10.1016/j.cub.2009.03.013 19467203
8. Stress granules: the Tao of RNA triage. Anderson P, Kedersha N, Trends Biochem Sci 2008 33 141 150 10.1016/j.tibs.2007.12.003 18291657
9. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, et al. Mol Biol Cell 2004 15 5383 5398 10.1091/mbc.E04-08-0715 15371533 (Pubitemid 39564732)
10. The RasGAP-associated endoribonuclease G3BP assembles stress granules. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, et al. J Cell Biol 2003 160 823 831 10.1083/jcb.200212128 12642610 (Pubitemid 36350838)
11. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Kedersha N, Anderson P, Biochem Soc Trans 2002 30 963 969 12440955 (Pubitemid 36002389)
12. TAR DNA-binding protein 43 (TDP-43) regulates stress granule dynamics via differential regulation of G3BP and TIA-1. McDonald KK, Aulas A, Destroismaisons L, Pickles S, Beleac E, Camu W, et al. Hum Mol Genet 2011 20 1400 1410 10.1093/hmg/ddr021 21257637
13. hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Guil S, Long JC, Caceres JF, Mol Cell Biol 2006 26 5744 5758 10.1128/MCB.00224-06 16847328 (Pubitemid 44134331)
14. SMN deficiency reduces cellular ability to form stress granules, sensitizing cells to stress. Zou T, Yang X, Pan D, Huang J, Sahin M, Zhou J, Cell Mol Neurobiol 2011 31 541 550 10.1007/s10571-011-9647-8 21234798
15. Monocyte chemotactic protein-induced protein 1 (MCPIP1) suppresses stress granule formation and determines apoptosis under stress. Qi D, Huang S, Miao R, She ZG, Quinn T, Chang Y, et al. J Biol Chem 2011 286 41692 41700 10.1074/jbc.M111.276006 21971051
16. Cells lacking the fragile X mental retardation protein (FMRP) have normal RISC activity but exhibit altered stress granule assembly. Didiot MC, Subramanian M, Flatter E, Mandel JL, Moine H, Mol Biol Cell 2009 20 428 437 10.1091/mbc.E08-07-0737 19005212
17. Survival motor neuron protein facilitates assembly of stress granules. Hua Y, Zhou J, FEBS Lett 2004 572 69 74 10.1016/j.febslet.2004.07.010 15304326 (Pubitemid 39092515)
18. Ataxin-2 interacts with the DEAD/H-box RNA helicase DDX6 and interferes with P-bodies and stress granules. Nonhoff U, Ralser M, Welzel F, Piccini I, Balzereit D, Yaspo ML, et al. Mol Biol Cell 2007 18 1385 1396 10.1091/mbc.E06-12-1120 17392519 (Pubitemid 46626633)
19. PolyQ Repeat Expansions in ATXN2 Associated with ALS Are CAA Interrupted Repeats. Yu Z, Zhu Y, Chen-Plotkin AS, Clay-Falcone D, McCluskey L, Elman L, et al. PLoS One 2011 6 17951 10.1371/journal.pone.0017951 21479228
20. Ataxin-2 intermediate-length polyglutamine expansions in European ALS patients. Lee T, Li YR, Ingre C, Weber M, Grehl T, Gredal O, et al. Hum Mol Genet 2011 20 1697 1700 10.1093/hmg/ddr045 21292779
21. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Elden AC, Kim HJ, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, et al. Nature 2010 466 1069 1075 10.1038/nature09320 20740007
22. Association of Long ATXN2 CAG Repeat Sizes With Increased Risk of Amyotrophic Lateral Sclerosis. Daoud H, Belzil V, Martins S, Sabbagh M, Provencher P, Lacomblez L, et al. Arch Neurol 2011 68 739 742 10.1001/archneurol.2011.111 21670397
23. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. Liu-Yesucevitz L, Bilgutay A, Zhang YJ, Vanderwyde T, Citro A, Mehta T, et al. PLoS One 2010 5 13250 10.1371/journal.pone.0013250 20948999
24. TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Dewey CM, Cenik B, Sephton CF, Dries DR, Mayer P III, Good SK, et al. Mol Cell Biol 2010 31 1098 1108 21173160
25. TDP-43 is recruited to stress granules in conditions of oxidative insult. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, Buratti E, et al. J Neurochem 2009 111 1051 1061 10.1111/j.1471-4159.2009.06383.x 19765185
26. Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Gal J, Zhang J, Kwinter DM, Zhai J, Jia H, Jia J, et al. Neurobiol Aging 2010 32 2323.e27 2323.e40
27. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, Kwiatkowski TJ Jr, et al. Hum Mol Genet 2010 19 4160 4175 10.1093/hmg/ddq335 20699327
28. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, et al. EMBO J 2010 29 2841 2857 10.1038/emboj.2010.143 20606625
29. Juvenile ALS with basophilic inclusions is a FUS proteinopathy with FUS mutations. Baumer D, Hilton D, Paine SM, Turner MR, Lowe J, Talbot K, et al. Neurology 2010 75 611 618 10.1212/WNL.0b013e3181ed9cde 20668261
30. Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Parker SJ, Meyerowitz J, James JL, Liddell JR, Crouch PJ, Kanninen KM, et al. Neurochem Int 2012 60 415 424 10.1016/j.neuint.2012.01.019 22306778
31. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Lee EB, Lee VM, Trojanowski JQ, Nat Rev Neurosci 2012 13 38 50
32. TDP-43: the relationship between protein aggregation and neurodegeneration in amyotrophic lateral sclerosis and frontotemporal lobar degeneration. Baloh RH, FEBS J 2011 278 3539 3549 10.1111/j.1742-4658.2011. 08256.x 21777387
33. TDP-43-based animal models of neurodegeneration: new insights into ALS pathology and pathophysiology. Wegorzewska I, Baloh RH, Neurodegener Dis 2011 8 262 274 10.1159/000321547 21124004
34. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Science 2006 314 130 133 10.1126/science.1134108 17023659 (Pubitemid 44547757)
35. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, et al. Biochem Biophys Res Commun 2006 351 602 611 10.1016/j.bbrc.2006.10.093 17084815 (Pubitemid 44708852)
36. Regulation of stress granule dynamics by Grb7 and FAK signalling pathway. Tsai NP, Ho PC, Wei LN, EMBO J 2008 27 715 726 10.1038/emboj.2008.19 18273060 (Pubitemid 351506682)
37. Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. Fiesel FC, Voigt A, Weber SS, Van den HC, Waldenmaier A, Gorner K, et al. EMBO J 2010 29 209 221 10.1038/emboj.2009.324 19910924
38. FUS/TLS forms cytoplasmic aggregates, inhibits cell growth and interacts with TDP-43 in a yeast model of amyotrophic lateral sclerosis. Kryndushkin D, Wickner RB, Shewmaker F, Protein Cell 2011 2 223 236 10.1007/s13238-011-1525-0 21452073
39. ALS-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to coregulate HDAC6 mRNA. Kim SH, Shanware N, Bowler MJ, Tibbetts RS, J Biol Chem 2010 286 12766 12774
40. Mutant TDP-43 and FUS Cause Age-Dependent Paralysis and Neurodegeneration in C. elegans. Vaccaro A, Tauffenberger A, Aggad D, Rouleau G, Drapeau P, Parker JA, PLoS One 2012 7 31321 10.1371/journal.pone.0031321 22363618
41. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, Liang TY, et al. Nat Neurosci 2011 14 459 468 10.1038/nn.2779 21358643
42. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. White JP, Cardenas AM, Marissen WE, Lloyd RE, Cell Host Microbe 2007 2 295 305 10.1016/j.chom.2007.08.006 18005751 (Pubitemid 350056396)
43. Stable formation of compositionally unique stress granules in virus-infected cells. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE, J Virol 2010 84 3654 3665 10.1128/JVI.01320-09 20106928
44. Control of fetal growth and neonatal survival by the RasGAP-associated endoribonuclease G3BP. Zekri L, Chebli K, Tourriere H, Nielsen FC, Hansen TV, Rami A, et al. Mol Cell Biol 2005 25 8703 8716 10.1128/MCB.25.19.8703-8716.2005 16166649 (Pubitemid 41369188)
45. Arginine methylation by PRMT1 regulates nuclear-cytoplasmic localization and toxicity of FUS/TLS harbouring ALS-linked mutations. Tradewell ML, Yu Z, Tibshirani M, Boulanger MC, Durham HD, Richard S, Hum Mol Genet 2012 21 136 149 10.1093/hmg/ddr448 21965298
46. Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Damgaard CK, Lykke-Andersen J, Genes Dev 2011 25 2057 2068 10.1101/gad.17355911 21979918
47. A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Tian Q, Streuli M, Saito H, Schlossman SF, Anderson P, Cell 1991 67 629 639 10.1016/0092-8674(91)90536-8 1934064 (Pubitemid 121001476)
48. Local RNA translation at the synapse and in disease. Liu-Yesucevitz L, Bassell GJ, Gitler AD, Hart AC, Klann E, Richter JD, et al. J Neurosci 2011 31 16086 16093 10.1523/JNEUROSCI.4105-11.2011 22072660
49. Dynein motor contributes to stress granule dynamics in primary neurons. Tsai NP, Tsui YC, Wei LN, Neuroscience 2009 159 647 656 10.1016/j.neuroscience. 2008.12.053 19171178