C-Jun N-terminal kinase controls TDP-43 accumulation in stress granules induced by oxidative stress

Molecular Neurodegeneration

Volumn 6, Issue 1, 2011, Pages

  Meyerowitz, Jodi ^a   Parker, Sarah J ^a   Vella, Laura J ^b   Ng, Dominic Ch ^a,c   Price, Katherine A ^a   Liddell, Jeffrey R ^a   Caragounis, Aphrodite ^a   Li, Qiao Xin ^a,d   Masters, Colin L ^d   Nonaka, Takashi ^e   Hasegawa, Masato ^e   Bogoyevitch, Marie A ^a,c   Kanninen, Katja M ^a   Crouch, Peter J ^a   White, Anthony R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTIN HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

hnRNP; JNK; kinases; oxidative stress; paraquat; stress granules; TDP 43

Indexed keywords

ARSENITE SODIUM; PARAQUAT; STRESS ACTIVATED PROTEIN KINASE; TAR DNA BINDING PROTEIN;

ARTICLE; CELL CULTURE; CELL TYPE; CYTOSOL; ENZYME ACTIVITY; ENZYME INHIBITION; GRANULE CELL; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; TDP 43 PROTEINOPATHY;

EID: 79961117695     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-6-57     Document Type: Article

References (53)

1. Neuron-glia interactions underlie ALS-like axonal cytoskeletal pathology. King AE, Dickson TC, Blizzard CA, Woodhouse A, Foster SS, Chung RS, Vickers JC, Neurobiol Aging 2009 32 459 469 19427060
2. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Barber SC, Shaw PJ, Free Radic Biol Med 2010 48 629 641 10.1016/j.freeradbiomed.2009.11.018 19969067
3. ALS pathogenesis: Recent insights from genetics and mouse models. Swarup V, Julien JP, Prog Neuropsychopharmacol Biol Psychiatry 2010 35 363 369 20728492
4. Pathogenic TARDBP mutations in amyotrophic lateral sclerosis and frontotemporal dementia: disease-associated pathways. Barmada SJ, Finkbeiner S, Rev Neurosci 2010 21 251 272 10.1515/REVNEURO.2010.21.4.251 21086759
5. FTD and ALS: A Tale of Two Diseases. Ferrari R, Kapogiannis D, Huey ED, Momeni P, Curr Alzheimer Res 2011 8 273 294 10.2174/156720511795563700
6. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM, Science 2006 314 130 133 10.1126/science.1134108 17023659 (Pubitemid 44547757)
7. 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, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T, Biochem Biophys Res Commun 2006 351 602 611 10.1016/j.bbrc.2006.10.093 17084815 (Pubitemid 44708852)
8. TAR DNA-binding protein 43 in neurodegenerative disease. Chen-Plotkin AS, Lee VM, Trojanowski JQ, Nat Rev Neurol 2010 6 211 220 10.1038/nrneurol.2010.18 20234357
9. TDP-43 is a culprit in human neurodegeneration, and not just an innocent bystander. Banks GT, Kuta A, Isaacs AM, Fisher EM, Mamm Genome 2008 19 299 305 10.1007/s00335-008-9117-x 18592312
10. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Mackenzie IR, Rademakers R, Neumann M, Lancet Neurol 2010 9 995 1007 10.1016/S1474-4422(10)70195-2 20864052
11. TDP-43: a DNA and RNA binding protein with roles in neurodegenerative diseases. Warraich ST, Yang S, Nicholson GA, Blair IP, Int J Biochem Cell Biol 2010 42 1606 169 10.1016/j.biocel.2010.06.016 20601083
12. Nuclear import impairment causes cytoplasmic trans-activation response DNA-binding protein accumulation and is associated with frontotemporal lobar degeneration. Nishimura AL, Zupunski V, Troakes C, Kathe C, Fratta P, Howell M, Gallo JM, Hortobagyi T, Shaw CE, Rogelj B, Brain 2010 133 1763 1771 10.1093/brain/awq111 20472655
13. Expression of TDP-43 C-terminal Fragments in Vitro Recapitulates Pathological Features of TDP-43 Proteinopathies. Igaz LM, Kwong LK, Chen-Plotkin A, Winton MJ, Unger TL, Xu Y, Neumann M, Trojanowski JQ, Lee VM, J Biol Chem 2009 284 8516 24 19164285
14. Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Zhang YJ, Xu YF, Cook C, Gendron TF, Roettges P, Link CD, Lin WL, Tong J, Castanedes-Casey M, Ash P, Gass J, Rangachari V, Buratti E, Baralle F, Golde TE, Dickson DW, Petrucelli L, Proc Natl Acad Sci USA 2009 106 7607 12 10.1073/pnas.0900688106 19383787
15. Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Nonaka T, Kametani F, Arai T, Akiyama H, Hasegawa M, Hum Mol Genet 2009 18 3353 3364 10.1093/hmg/ddp275 19515851
16. 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, Rouleau GA, Vande Velde C, Hum Mol Genet 2011 20 1400 1410 10.1093/hmg/ddr021 21257637
17. 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, Zaarur N, McKee A, Bowser R, Sherman M, Petrucelli L, Wolozin B, PLoS One 2010 5 13250 10.1371/journal.pone.0013250 20948999
18. Eukaryotic stress granules: the ins and outs of translation. Buchan JR, Parker R, Mol Cell 2009 36 932 941 10.1016/j.molcel.2009.11.020 20064460
19. TDP-43 is recruited to stress granules in conditions of oxidative insult. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, Buratti E, Silani V, Ratti A, J Neurochem 2009 111 1051 1061 10.1111/j.1471-4159.2009.06383.x 19765185
20. 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 Pr, Good SK, Johnson BA, Herz J, Yu G, Mol Cell Biol 2010 31 1098 108 21173160
21. Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Moisse K, Volkening K, Leystra-Lantz C, Welch I, Hill T, Strong MJ, Brain Res 2009 1249 202 211 19046946
22. 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). Volkening K, Leystra-Lantz C, Yang W, Jaffee H, Strong MJ, Brain Res 2009 1305 168 182 19815002
23. Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Ito D, Seki M, Tsunoda Y, Uchiyama H, Suzuki N, Ann Neurol 2011 69 152 162 10.1002/ana.22246 21280085
24. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, Than ME, Mackenzie IR, Capell A, Schmid B, Neumann M, Haass C, EMBO J 2010 29 2841 2857 10.1038/emboj.2010.143 20606625
25. Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. Freibaum BD, Chitta RK, High AA, Taylor JP, J Proteome Res 2010 9 1104 1120 10.1021/pr901076y 20020773
26. Oxidative stress in ALS: A mechanism of neurodegeneration and a therapeutic target. Barber SC, Mead RJ, Shaw PJ, Biochim Biophys Acta 2006 1762 1051 1067 16713195 (Pubitemid 44750575)
27. Phosphorylated and ubiquitinated TDP-43 pathological inclusions in ALS and FTLD-U are recapitulated in SH-SY5Y cells. Nonaka T, Arai T, Buratti E, Baralle FE, Akiyama H, Hasegawa M, FEBS Lett 2009 583 394 400 10.1016/j.febslet.2008.12.031 19111550
28. Zinc induces depletion and aggregation of endogenous TDP-43. Caragounis A, Price KA, Soon CP, Filiz G, Masters CL, Li QX, Crouch PJ, White AR, Free Radic Biol Med 2010 48 1152 1161 10.1016/j.freeradbiomed.2010.01.035 20138212
29. Proteolytic processing of TAR DNA binding protein-43 by caspases produces C-terminal fragments with disease defining properties independent of progranulin. Dormann D, Capell A, Carlson AM, Shankaran SS, Rodde R, Neumann M, Kremmer E, Matsuwaki T, Yamanouchi K, Nishihara M, Haass C, J Neurochem 2009 110 1082 1094 10.1111/j.1471-4159.2009.06211.x 19522733
30. Characterization of alternative isoforms and inclusion body of the TAR DNA-binding protein-43. Nishimoto Y, Ito D, Yagi T, Nihei Y, Tsunoda Y, Suzuki N, J Biol Chem 2010 285 608 619 10.1074/jbc.M109.022012 19887443
31. hnRNP-K is a nuclear target of TCR-activated ERK and required for T-cell late activation. Chang JW, Koike T, Iwashima M, Int Immunol 2009 21 1351 1361 10.1093/intimm/dxp106 19880579
32. Increased expression of the heterogeneous nuclear ribonucleoprotein K in pancreatic cancer and its association with the mutant p53. Zhou R, Shanas R, Nelson MA, Bhattacharyya A, Shi J, Int J Cancer 2010 126 395 404 10.1002/ijc.24744 19609950
33. The Mnks are novel components in the control of TNF alpha biosynthesis and phosphorylate and regulate hnRNP A1. Buxade M, Parra JL, Rousseau S, Shpiro N, Marquez R, Morrice N, Bain J, Espel E, Proud CG, Immunity 2005 23 177 189 10.1016/j.immuni.2005.06.009 16111636 (Pubitemid 41169287)
34. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Habelhah H, Shah K, Huang L, Ostareck-Lederer A, Burlingame AL, Shokat KM, Hentze MW, Ronai Z, Nat Cell Biol 2001 3 325 330 10.1038/35060131 11231586 (Pubitemid 32201331)
35. p38 MAP kinase-dependent regulation of the expression level and subcellular distribution of heterogeneous nuclear ribonucleoprotein A1 and its involvement in cellular senescence in normal human fibroblasts. Shimada N, Rios I, Moran H, Sayers B, Hubbard K, RNA Biol 2009 6 293 304 10.4161/rna.6.3.8497 19430204
36. 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)
37. c-Jun N-terminal kinase (JNK) signaling: recent advances and challenges. Bogoyevitch MA, Ngoei KR, Zhao TT, Yeap YY, Ng DC, Biochim Biophys Acta 2010 1804 463 745 19900593
38. Paraquat activates the IRE1/ASK1/JNK cascade associated with apoptosis in human neuroblastoma SH-SY5Y cells. Yang W, Tiffany-Castiglioni E, Koh HC, Son IH, Toxicol Lett 2009 191 203 210 10.1016/j.toxlet.2009.08.024 19735704
39. JNK3 mediates paraquat- and rotenone-induced dopaminergic neuron death. Choi WS, Abel G, Klintworth H, Flavell RA, Xia Z, J Neuropathol Exp Neurol 2010 69 511 520 10.1097/NEN.0b013e3181db8100 20418776
40. Identification of a new JNK inhibitor targeting the JNK-JIP interaction site. Stebbins JL, De SK, Machleidt T, Becattini B, Vazquez J, Kuntzen C, Chen LH, Cellitti JF, Riel-Mehan M, Emdadi A, Solinas G, Karin M, Pellecchia M, Proc Natl Acad Sci USA 2008 105 16809 16813 10.1073/pnas.0805677105 18922779
41. A novel c-Jun N-terminal kinase (JNK)-binding protein WDR62 is recruited to stress granules and mediates a nonclassical JNK activation. Wasserman T, Katsenelson K, Daniliuc S, Hasin T, Choder M, Aronheim A, Mol Biol Cell 2010 21 117 130 10.1091/mbc.E09-06-0512 19910486
42. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. Buratti E, Brindisi A, Giombi M, Tisminetzky S, Ayala YM, Baralle FE, J Biol Chem 2005 280 37572 37584 10.1074/jbc.M505557200 16157593 (Pubitemid 41642366)
43. Identification of new JNK substrate using ATP pocket mutant JNK and a corresponding ATP analogue. Habelhah H, Shah K, Huang L, Burlingame AL, Shokat KM, Ronai Z, J Biol Chem 2001 276 18090 18095 10.1074/jbc.M011396200 11259409
44. Cytoplasmic accumulation of the RNA binding protein HuR is central to tamoxifen resistance in estrogen receptor positive breast cancer cells. Hostetter C, Licata LA, Witkiewicz A, Costantino CL, Yeo CJ, Brody JR, Keen JC, Cancer Biol Ther 2008 7 1496 1506 10.4161/cbt.7.9.6490 18769129
45. Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. D'Ambrogio A, Buratti E, Stuani C, Guarnaccia C, Romano M, Ayala YM, Baralle FE, Nucleic Acids Res 2009 37 4116 4126 10.1093/nar/gkp342 19429692
46. A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. Perlson E, Jeong GB, Ross JL, Dixit R, Wallace KE, Kalb RG, Holzbaur EL, J Neurosci 2009 29 9903 9917 10.1523/JNEUROSCI.0813-09.2009 19657041
47. Amyotrophic lateral sclerosis: a novel hypothesis involving a gained 'loss of function' in the JNK/SAPK pathway. Zhu X, Perry G, Smith MA, Redox Rep 2003 8 129 133 10.1179/135100003225001494 12935309 (Pubitemid 36874540)
48. Activation of the p38MAPK cascade is associated with upregulation of TNF alpha receptors in the spinal motor neurons of mouse models of familial ALS. Veglianese P, Lo Coco D, Bao Cutrona M, Magnoni R, Pennacchini D, Pozzi B, Gowing G, Julien JP, Tortarolo M, Bendotti C, Mol Cell Neurosci 2006 31 218 231 10.1016/j.mcn.2005.09.009 16219474 (Pubitemid 43214532)
49. Pathological roles of MAPK signaling pathways in human diseases. Kim EK, Choi EJ, Biochim Biophys Acta 2010 1802 396 405 20079433
50. Activation of the JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis. Atzori C, Ghetti B, Piva R, Srinivasan AN, Zolo P, Delisle MB, Mirra SS, Migheli A, J Neuropathol Exp Neurol 2001 60 1190 1197 11764091 (Pubitemid 33117099)
51. Cell stress induces TDP-43 pathological changes associated with ERK1/2 dysfunction: implications in ALS. Ayala V, Granado-Serrano A, Cacabelos D, Naudí A, Ilieva V, Boada J, Caraballo-Miralles V, Lladá J, Ferrer I, Pamplona R, Portero-Otin M, Acta Neuropathol 2011
52. c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. Migheli A, Piva R, Atzori C, Troost D, Schiffer D, J Neuropathol Exp Neurol 1997 56 1314 1322 10.1097/00005072-199712000-00006 9413280 (Pubitemid 28006577)
53. Riluzole protects against glutamate-induced slowing of neurofilament axonal transport. Stevenson A, Yates DM, Manser C, De Vos KJ, Vagnoni A, Leigh PN, McLoughlin DM, Miller CC, Neurosci Lett 2009 454 161 164 10.1016/j.neulet.2009.02.061 19429076