RNA-Processing Protein TDP-43 Regulates FOXO-Dependent Protein Quality Control in Stress Response

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Zhang, Tao ^a,b   Baldie, Gerard ^a,b   Periz, Goran ^a,b   Wang, Jiou ^a,b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN 14 3 3; SOMATOMEDIN BINDING PROTEIN; TAR DNA BINDING PROTEIN; TRANSCRIPTION FACTOR FOXO; CAENORHABDITIS ELEGANS PROTEIN; DAF-16 PROTEIN, C ELEGANS; DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; FOXO3 PROTEIN, HUMAN; RNA BINDING PROTEIN; TDP-1 PROTEIN, C ELEGANS; TDP-43 PROTEIN, HUMAN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1;

ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; DOWN REGULATION; GENE FREQUENCY; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; LONGEVITY; MOLECULAR DYNAMICS; NONHUMAN; OLIGOMERIZATION; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA METABOLISM; RNA PROCESSING; SIGNAL TRANSDUCTION; STRESS; UPREGULATION; ANIMAL; CAENORHABDITIS ELEGANS; CYTOPLASM; FEMALE; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TRANSGENIC ANIMAL;

14-3-3 PROTEINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOPLASM; DNA-BINDING PROTEINS; FEMALE; FORKHEAD BOX PROTEIN O1; FORKHEAD BOX PROTEIN O3; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HUMANS; LONGEVITY; RNA-BINDING PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84908336837     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004693     Document Type: Article

References (80)

1. Martin DE, Soulard A, Hall MN, (2004) TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969–979.
2. Bergkessel M, Whitworth GB, Guthrie C, (2011) Diverse environmental stresses elicit distinct responses at the level of pre-mRNA processing in yeast. RNA 17: 1461–1478.
3. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099–1108.
4. Holcik M, Sonenberg N, (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6: 318–327.
5. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519–529.
6. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, et al. (2006) Ubiquitinated TDP-43 in Frontotemporal Lobar Degeneration and Amyotrophic Lateral Sclerosis. Science 314: 130–133.
7. 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: 1668–1672.
8. Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH, (2009) TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci USA 106: 18809–18814.
9. Johnson BS, Snead D, Lee JJ, McCaffery JM, Shorter J, et al. (2009) TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. J Biol Chem 284: 20329–20339.
10. Zhang Y-J, Xu Y-F, Cook C, Gendron TF, Roettges P, et al. (2009) Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc Natl Acad Sci USA 106: 7607–7612.
11. Kabashi E, Lin L, Tradewell ML, Dion PA, Bercier V, et al. (2009) Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 19: 671–683.
12. Caccamo A, Majumder S, Deng JJ, Bai Y, Thornton FB, et al. (2009) Rapamycin rescues TDP-43 mislocalization and the associated low molecular mass neurofilament instability. J Biol Chem 284: 27416–27424.
13. Guo W, Chen Y, Zhou X, Kar A, Ray P, et al. (2011) An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Nat Struct Mol Biol 18: 822–830.
14. Hanson KA, Kim SH, Wassarman DA, Tibbetts RS, (2010) Ubiquilin Modifies TDP-43 Toxicity in a Drosophila Model of Amyotrophic Lateral Sclerosis (ALS). J Biol Chem 285: 11068–11072.
15. Ash PEA, Zhang Y-J, Roberts CM, Saldi T, Hutter H, et al. (2010) Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum Mol Genet 19: 3206–3218.
16. Liachko NF, Guthrie CR, Kraemer BC, (2010) Phosphorylation Promotes Neurotoxicity in a Caenorhabditis elegans Model of TDP-43 Proteinopathy. J Neurosci 30: 16208–16219.
17. Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, et al. (2010) TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci USA 107: 3858–3863.
18. Stallings NR, Puttaparthi K, Luther CM, Burns DK, Elliott JL, (2010) Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol Dis 40: 404–414.
19. Xu Y-F, Gendron TF, Zhang Y-J, Lin W-L, D'Alton S, et al. (2010) Wild-Type Human TDP-43 Expression Causes TDP-43 Phosphorylation, Mitochondrial Aggregation, Motor Deficits, and Early Mortality in Transgenic Mice. J Neurosci 30: 10851–10859.
20. Shan X, Chiang P, Price D, Wong PC, (2010) Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc Natl Acad Sci USA 107: 16325–16330.
21. Zhou H, Huang C, Chen H, Wang D, Landel CP, et al. (2010) Transgenic Rat Model of Neurodegeneration Caused by Mutation in the TDP Gene. PLoS Genet 6: e1000887.
22. Fiesel FC, Voigt A, Weber SS, Van den Haute C, Waldenmaier A, et al. (2010) Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J 29: 209–221.
23. Barmada SJ, Skibinski G, Korb E, Rao EJ, Wu JY, et al. (2010) Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis. J Neurosci 30: 639–649.
24. Swarup V, Phaneuf D, Dupre N, Petri S, Strong M, et al. (2011) Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor kappaB-mediated pathogenic pathways. J Exp Med 208: 2429–2447.
25. Bose JK, Huang CC, Shen CK, (2011) Regulation of autophagy by neuropathological protein TDP-43. J Biol Chem 286: 44441–44448.
26. 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 15: 1488–1497.
27. Schmid B, Hruscha A, Hogl S, Banzhaf-Strathmann J, Strecker K, et al. (2013) Loss of ALS-associated TDP-43 in zebrafish causes muscle degeneration, vascular dysfunction, and reduced motor neuron axon outgrowth. Proc Natl Acad Sci USA 110: 4986–4991.
28. Serio A, Bilican B, Barmada SJ, Ando DM, Zhao C, et al. (2013) Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proc Natl Acad Sci USA 110: 4697–4702.
29. Kim HJ, Raphael AR, LaDow ES, McGurk L, Weber RA, et al. (2014) Therapeutic modulation of eIF2alpha phosphorylation rescues TDP-43 toxicity in amyotrophic lateral sclerosis disease models. Nat Genet 46: 152–160.
30. Yang C, Wang H, Qiao T, Yang B, Aliaga L, et al. (2014) Partial loss of TDP-43 function causes phenotypes of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 111: E1121–1129.
31. Alami NH, Smith RB, Carrasco MA, Williams LA, Winborn CS, et al. (2014) Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron 81: 536–543.
32. Austin JA, Wright GSA, Watanabe S, Grossmann JG, Antonyuk SV, et al. (2014) Disease causing mutants of TDP-43 nucleic acid binding domains are resistant to aggregation and have increased stability and half-life. Proc Natl Acad Sci USA 111: 4309–4314.
33. He F, Krans A, Freibaum BD, Taylor JP, Todd PK, (2014) TDP-43 suppresses CGG repeat-induced neurotoxicity through interactions with HnRNP A2/B1. Hum Mol Genet 23: 5036–5051.
34. Galloway JN, Shaw C, Yu P, Parghi D, Poidevin M, et al. (2014) CGG repeats in RNA modulate expression of TDP-43 in mouse and fly models of fragile X tremor ataxia syndrome. Hum Mol Genet E-pub ahead of print. Doi:10.1093/hmg/ddu314.
35. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG, (1993) hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62: 289–321.
36. Buratti E, Baralle FE, (2012) TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Trends Biochem Sci 37: 237–247.
37. 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.
38. Abhyankar MM, Urekar C, Reddi PP, (2007) A Novel CpG-free Vertebrate Insulator Silences the Testis-specific SP-10 Gene in Somatic Tissues. J Biol Chem 282: 36143–36154.
39. Ou S, Wu F, Harrich D, Garcia-Martinez L, Gaynor R, (1995) Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J Virol 69: 3584–3596.
40. Bose JK, Wang I-F, Hung L, Tarn W-Y, Shen C-KJ, (2008) TDP-43 Overexpression Enhances Exon 7 Inclusion during the Survival of Motor Neuron Pre-mRNA Splicing. J Biol Chem 283: 28852–28859.
41. Mercado PA, Ayala YM, Romano M, Buratti E, Baralle FE, (2005) Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res 33: 6000–6010.
42. Strong MJ, Volkening K, Hammond R, Yang W, Strong W, et al. (2007) TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol Cell Neurosci 35: 320–327.
43. Volkening K, Leystra-Lantz C, Yang W, Jaffee H, Strong MJ, (2009) Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS). Brain Res 1305: 168–182.
44. Kawahara Y, Mieda-Sato A, (2012) TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci USA 109: 3347–3352.
45. King OD, Gitler AD, Shorter J, (2012) The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res 1462: 61–80.
46. Kwiatkowski TJ, JrBosco 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.
47. 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.
48. Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, et al. (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495: 467–473.
49. Dewey CM, Cenik B, Sephton CF, Dries DR, Mayer P, 3rdet al. (2011) TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol Cell Biol 31: 1098–1108.
50. McDonald KK, Aulas A, Destroismaisons L, Pickles S, Beleac E, et al. (2011) TAR DNA-binding protein 43 (TDP-43) regulates stress granule dynamics via differential regulation of G3BP and TIA-1. Hum Mol Genet 20: 1400–1410.
51. Liu-Yesucevitz L, Bilgutay A, Zhang YJ, Vanderwyde T, Citro A, et al. (2010) Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS One 5: e13250.
52. 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.
53. 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.
54. Guil S, Long JC, Caceres JF, (2006) hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol Cell Biol 26: 5744–5758.
55. Zhang T, Hwang HY, Hao H, Talbot C, JrWang J, (2012) Caenorhabditis elegans RNA-processing protein TDP-1 regulates protein homeostasis and life span. J Biol Chem 287: 8371–8382.
56. Vaccaro A, Tauffenberger A, Ash PE, Carlomagno Y, Petrucelli L, et al. (2012) TDP-1/TDP-43 regulates stress signaling and age-dependent proteotoxicity in Caenorhabditis elegans. PLoS Genet 8: e1002806.
57. Salih DA, Brunet A, (2008) FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20: 126–136.
58. Berryman DE, Christiansen JS, Johannsson G, Thorner MO, Kopchick JJ, (2008) Role of the GH/IGF-1 axis in lifespan and healthspan: lessons from animal models. Growth Horm IGF Res 18: 455–471.
59. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277–283.
60. Zhang T, Mullane PC, Periz G, Wang J, (2011) TDP-43 neurotoxicity and protein aggregation modulated by heat shock factor and insulin/IGF-1 signaling. Hum Mol Genet 20: 1952–1965.
61. Alfieri RR, Petronini PG, (2007) Hyperosmotic stress response: comparison with other cellular stresses. Pflugers Arch 454: 173–185.
62. Burkewitz K, Choe K, Strange K, (2011) Hypertonic stress induces rapid and widespread protein damage in C. elegans. Am J Physiol Cell Physiol 301: C566–576.
63. Choe KP, Strange K, (2008) Genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged proteins as an essential hypertonic stress response. Am J Physiol Cell Physiol 295: C1488–1498.
64. Nunes P, Ernandez T, Roth I, Qiao X, Strebel D, et al. (2013) Hypertonic stress promotes autophagy and microtubule-dependent autophagosomal clusters. Autophagy 9: 550–567.
65. Wang J, Farr G, Hall D, Li F, Furtak K, et al. (2009) An ALS-linked mutant SOD1 produces a locomotor defect associated with aggregation and synaptic dysfunction when expressed in neurons of Caenorhabditis elegans. PLoS Genet 5: e1000350.
66. Tzivion G, Dobson M, Ramakrishnan G, (2011) FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta 1813: 1938–1945.
67. van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, et al. (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol 8: 1064–1073.
68. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, et al. (2003) The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160: 823–831.
69. Rena G, Prescott AR, Guo S, Cohen P, Unterman TG, (2001) Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem J 354: 605–612.
70. Brunet A, Kanai F, Stehn J, Xu J, Sarbassova D, et al. (2002) 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol 156: 817–828.
71. Obsilova V, Vecer J, Herman P, Pabianova A, Sulc M, et al. (2005) 14-3-3 Protein interacts with nuclear localization sequence of forkhead transcription factor FoxO4. Biochemistry 44: 11608–11617.
72. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, et al. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458–471.
73. Zhao J, Brault JJ, Schild A, Goldberg AL, (2008) Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4: 378–380.
74. van der Vos KE, Eliasson P, Proikas-Cezanne T, Vervoort SJ, van Boxtel R, et al. (2012) Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat Cell Biol 14: 829–837.
75. Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, et al. (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet 12: 2753–2764.
76. Kedersha N, Anderson P, (2007) Mammalian stress granules and processing bodies. Methods Enzymol 431: 61–81.
77. Zhao Y, Yang J, Liao W, Liu X, Zhang H, et al. (2010) Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 12: 665–675.
78. Eijkelenboom A, Burgering BM, (2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14: 83–97.
79. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. Embo J 10: 3959–3970.
80. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857–868.