UBE2E ubiquitin-conjugating enzymes and ubiquitin isopeptidase y regulate TDP-43 protein ubiquitination

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 19164-19179

  Hans, Friederike ^a,b,c   Fiesel, Fabienne C ^c,g   Strong, Jennifer C ^c   Jackel, Sändra ^c   Rasse, Tobias M ^d   Geisler, Sven ^c   Springer, Wolfdieter ^b,c,g   Schulz, Jörg B ^e,f   Voigt, Aaron ^e   Kahle, Philipp J ^a,b,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c Laboratory of Functional Neurogenetics Department of Neurodegeneration and   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^f JARA Jülich Aachen Research Alliance Future Information Technology   (Germany)

^g MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; PROTEINS;

INTERACTORS; PROTEIN AGGREGATES; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

ENZYMES;

COMPLEMENTARY DNA; PEPTIDASE; PROTEASOME INHIBITOR; TAR DNA BINDING PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN ISOPEPTIDASE Y; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA LIBRARY; DROSOPHILA MELANOGASTER; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; UBIQUITINATION;

AMYOTROPHIC LATERAL SCLEROSIS (ALS) (LOU GEHRIG DISEASE); DROSOPHILA; FRONTOTEMPORAL DEMENTIA; PROTEASOME; PROTEIN AGGREGATION; PROTEIN-PROTEIN INTERACTION; TDP-43; UBIQUITIN-CONJUGATING ENZYME; UBIQUITIN-SPECIFIC PROTEASE; UBIQUITINATION;

ADULT; ANIMALS; BRAIN; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HEK293 CELLS; HUMANS; NEUROTOXINS; PROTEIN TRANSPORT; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN THIOLESTERASE; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84903851882     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561704     Document Type: Article

References (69)

1. Mackenzie, I. R., Rademakers, R., and Neumann, M. (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 9, 995-1007
2. Van Langenhove, T., van der Zee, J., and Van Broeckhoven, C. (2012) The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann. Med. 44, 817-828
3. Fiesel, F. C., and Kahle, P. J. (2011) TDP-43 and FUS/TLS: cellular functions and implications for neurodegeneration. FEBS J. 278, 3550-3568
4. Neumann, M., Sampathu, D. M., Kwong, L. K., Truax, A. C., Micsenyi, M. C., Chou, T. T., Bruce, J., Schuck, T., Grossman, M., Clark, C. M., McCluskey, L. F., Miller, B. L., Masliah, E., Mackenzie, I. R., Feldman, H., Feiden, W., Kretzschmar, H. A., Trojanowski, J. Q., and Lee, V. M. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-133
5. Avendaño-Vázquez, S. E., Dhir, A., Bembich, S., Buratti, E., Proudfoot, N., and Baralle, F. E. (2012) Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev. 26, 1679-1684
6. Ayala, Y. M., De Conti, L., Avendaño-Vázquez, S. E., Dhir, A., Romano, M., D'Ambrogio, A., Tollervey, J., Ule, J., Baralle, M., Buratti, E., and Baralle, F. E. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 30, 277-288
7. Kabashi, E., Valdmanis, P. N., Dion, P., Spiegelman, D., McConkey, B. J., Vande Velde, C., Bouchard, J.-P., Lacomblez, L., Pochigaeva, K., Salachas, F., Pradat, P.-F., Camu, W., Meininger, V., Dupre, N., and Rouleau, G. A. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40, 572-574
8. Rutherford, N. J., Zhang, Y.-J., Baker, M., Gass, J. M., Finch, N. A., Xu, Y.-F., Stewart, H., Kelley, B. J., Kuntz, K., Crook, R. J., Sreedharan, J., Vance, C., Sorenson, E., Lippa, C., Bigio, E. H., Geschwind, D. H., Knopman, D. S., Mitsumoto, H., Petersen, R. C., Cashman, N. R., Hutton, M., Shaw, C. E., Boylan, K. B., Boeve, B., Graff-Radford, N. R., Wszolek, Z. K., Caselli, R. J., Dickson, D. W., Mackenzie, I. R., Petrucelli, L., and Rademakers, R. (2008) Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet. 4, e1000193
9. Zhang, Y.-J., Gendron, T. F., Xu, Y.-F., Ko, L.-W., Yen, S.-H., and Petrucelli, L. (2010) Phosphorylation regulates proteasomal-mediated degradation and solubility ofTARDNAbinding protein-43 C-terminal fragments. Mol. Neurodegener. 5, 33
10. van Eersel, J., Ke, Y. D., Gladbach, A., Bi, M., Götz, J., Kril, J. J., and Ittner, L. M. (2011) Cytoplasmic accumulation and aggregation of TDP-43 upon proteasome inhibition in cultured neurons. PLoS One 6, e22850
11. Caccamo, A., Majumder, S., Deng, J. J., Bai, Y., Thornton, F. B., and Oddo, S. (2009) Rapamycin rescues TDP-43 mislocalization and the associated low molecular mass neurofilament instability. J. Biol. Chem. 284, 27416-27424
12. Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerød, L., Fisher, E. M., Isaacs, A., Brech, A., Stenmark, H., and Simonsen, A. (2007) Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179, 485-500
13. Brady, O. A., Meng, P., Zheng, Y., Mao, Y., and Hu, F. (2011) Regulation of TDP-43 aggregation by phosphorylation and p62/SQSTM1. J. Neurochem. 116, 248-259
14. Scotter, E. L., Vance, C., Nishimura, A. L., Lee, Y.-B., Chen, H.-J., Urwin, H., Sardone, V., Mitchell, J. C., Rogelj, B., Rubinsztein, D. C., and Shaw, C. E. (2014) Differential roles of the ubiquitin proteasome system and autophagy in the clearance of soluble and aggregated TDP-43 species. J. Cell Sci. 127, 1263-1278
15. Urushitani, M., Sato, T., Bamba, H., Hisa, Y., and Tooyama, I. (2010) Synergistic effect between proteasome and autophagosome in the clearance of polyubiquitinated TDP-43. J. Neurosci. Res. 88, 784-797
16. Wang, X., Fan, H., Ying, Z., Li, B., Wang, H., and Wang, G. (2010) Degradation of TDP-43 and its pathogenic form by autophagy and the ubiquitinproteasome system. Neurosci. Lett. 469, 112-116
17. Hebron, M. L., Lonskaya, I., Sharpe, K., Weerasinghe, P. P., Algarzae, N. K., Shekoyan, A. R., and Moussa, C. E. (2013) Parkin ubiquitinates Tar-DNA binding protein-43 (TDP-43) and promotes its cytosolic accumulation via interaction with histone deacetylase 6 (HDAC6). J. Biol. Chem. 288, 4103-4115
18. Wang, I.-F., Reddy, N. M., and Shen, C.-K. (2002) Higher order arrangement of the eukaryotic nuclear bodies. Proc. Natl. Acad. Sci. U. S. A. 99, 13583-13588
19. Fiesel, F. C., Voigt, A., Weber, S. S., Van den Haute, C., Waldenmaier, A., Görner, K., Walter, M., Anderson, M. L., Kern, J. V., Rasse, T. M., Schmidt, T., Springer, W., Kirchner, R., Bonin, M., Neumann, M., Baekelandt, V., Alunni-Fabbroni, M., Schulz, J. B., and Kahle, P. J. (2010) Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J. 29, 209-221
20. Tsuiji, H., Iguchi, Y., Furuya, A., Kataoka, A., Hatsuta, H., Atsuta, N., Tanaka, F., Hashizume, Y., Akatsu, H., Murayama, S., Sobue, G., and Yamanaka, K. (2013) Spliceosome integrity is defective in the motor neuron diseases ALS and SMA. EMBO Mol. Med. 5, 221-234
21. Fallini, C., Bassell, G. J., and Rossoll, W. (2012) The ALS disease protein TDP-43 is actively transported in motor neuron axons and regulates axon outgrowth. Hum. Mol. Genet. 21, 3703-3718
22. Yu, Z., Fan, D., Gui, B., Shi, L., Xuan, C., Shan, L., Wang, Q., Shang, Y., and Wang, Y. (2012) Neurodegeneration-associated TDP-43 interacts with fragile X mental retardation protein (FMRP)/Staufen (STAU1) and regulates SIRT1 expression in neuronal cells. J. Biol. Chem. 287, 22560-22572
23. Buratti, E., Brindisi, A., Giombi, M., Tisminetzky, S., Ayala, Y. M., and Baralle, F. E. (2005) 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. J. Biol. Chem. 280, 37572-37584
24. D'Ambrogio, A., Buratti, E., Stuani, C., Guarnaccia, C., Romano, M., Ayala, Y. M., and Baralle, F. E. (2009) Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. Nucleic Acids Res. 37, 4116-4126
25. Freibaum, B. D., Chitta, R. K., High, A. A., and Taylor, J. P. (2010) Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J. Proteome Res. 9, 1104-1120
26. Ling, S.-C., Albuquerque, C. P., Han, J. S., Lagier-Tourenne, C., Tokunaga, S., Zhou, H., and Cleveland, D. W. (2010) ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/ TLS. Proc. Natl. Acad. Sci. U. S. A. 107, 13318-13323
27. Buratti, E., and Baralle, F. E. (2010) The multiple roles of TDP-43 in pre-mRNA processing and gene expression regulation. RNA Biol. 7, 420-429
28. Liu-Yesucevitz, L., Bilgutay, A., Zhang, Y.-J., Vanderweyde, T., Citro, A., Mehta, T., Zaarur, N., McKee, A., Bowser, R., Sherman, M., Petrucelli, L., and Wolozin, B. (2010) Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS One 5, e13250
29. Kim, S. H., Shanware, N. P., Bowler, M. J., and Tibbetts, R. S. (2010) Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J. Biol. Chem. 285, 34097-34105
30. Kawahara, Y., and Mieda-Sato, A. (2012) TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl. Acad. Sci. U. S. A. 109, 3347-3352
31. Buratti, E., De Conti, L., Stuani, C., Romano, M., Baralle, M., and Baralle, F. (2010) Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 277, 2268-2281
32. Shiina, Y., Arima, K., Tabunoki, H., and Satoh, J. (2010) TDP-43 dimerizes in human cells in culture. Cell. Mol. Neurobiol. 30, 641-652
33. Wang, I.-F., Chang, H.-Y., Hou, S.-C., Liou, G.-G., Way, T.-D., and Shen, C.-K. (2012) The self-interaction of native TDP-43 C terminus inhibits its degradation and contributes to early proteinopathies. Nat. Commun. 3, 766
34. Fuentealba, R. A., Udan, M., Bell, S., Wegorzewska, I., Shao, J., Diamond, M. I., Weihl, C. C., and Baloh, R. H. (2010) Interaction with polyglutamine aggregates reveals a Q/N-rich domain in TDP-43. J. Biol. Chem. 285, 26304-26314
35. Cohen, T. J., Hwang, A. W., Unger, T., Trojanowski, J. Q., and Lee, V. M. (2012) Redox signalling directly regulates TDP-43 via cysteine oxidation and disulphide cross-linking. EMBO J. 31, 1241-1252
36. Furukawa, Y., Kaneko, K., and Nukina, N. (2011) Molecular properties of TAR DNA binding protein-43 fragments are dependent upon its cleavage site. Biochim. Biophys. Acta 1812, 1577-1583
37. Voigt, A., Herholz, D., Fiesel, F. C., Kaur, K., Müller, D., Karsten, P., Weber, S. S., Kahle, P. J., Marquardt, T., and Schulz, J. B. (2010) TDP-43- mediated neuron loss in vivo requires RNA-binding activity. PLoS One 5, e12247
38. Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., and Springer, W. (2010) PINK1/Parkin-mediated mitophagy isdependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131
39. Hoffman, C. S., and Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57, 267-272
40. Ayala, Y. M., Zago, P., D'Ambrogio, A., Xu, Y.-F., Petrucelli, L., Buratti, E., and Baralle, F. E. (2008) Structural determinants of the cellular localization and shuttling of TDP-43. J. Cell Sci. 121, 3778-3785
41. Clague, M. J., and Urbé, S. (2006) Endocytosis: the DUB version. Trends Cell Biol. 16, 551-559
42. Tharun, S. (2009) Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell Mol. Biol. 272, 149-189
43. Collins, M., Riascos, D., Kovalik, T., An, J., Krupa, K., Krupa, K., Hood, B. L., Conrads, T. P., Renton, A. E., Traynor, B. J., and Bowser, R. (2012) The RNA-binding motif 45 (RBM45) protein accumulates in inclusion bodies in amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration with TDP-43 inclusions (FTLD-TDP) patients. Acta Neuropathol. 124, 717-732
44. Ohn, T., Kedersha, N., Hickman, T., Tisdale, S., and Anderson, P. (2008)A functional RNAi screen links O -GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10, 1224-1231
45. Arimoto, K., Fukuda, H., Imajoh-Ohmi, S., Saito, H., and Takekawa, M. (2008) Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 10, 1324-1332
46. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E., Vijayadamodar, G., Pochart, P., Machineni, H., Welsh, M., Kong, Y., Zerhusen, B., Malcolm, R., Varrone, Z., Collis, A., Minto, M., Burgess, S., McDaniel, L., Stimpson, E., Spriggs, F., Williams, J., Neurath, K., Ioime, N., Agee, M., Voss, E., Furtak, K., Renzulli, R., Aanensen, N., Carrolla, S., Bickelhaupt, E., Lazovatsky, Y., DaSilva, A., Zhong, J., Stanyon, C. A., Finley, R. L., Jr., White, K. P., Braverman, M., Jarvie, T., Gold, S., Leach, M., Knight, J., Shimkets, R. A., McKenna, M. P., Chant, J., and Rothberg, J. M. (2003) A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736
47. Dammer, E. B., Fallini, C., Gozal, Y. M., Duong, D. M., Rossoll, W., Xu, P., Lah, J. J., Levey, A. I., Peng, J., Bassell, G. J., and Seyfried, N. T. (2012) Coaggregation of RNA-binding proteins in a model of TDP-43 proteinopathy with selective RGG motif methylation and a role for RRM1 ubiquitination. PLoS One 7, e38658
48. Row, P. E., Prior, I. A., McCullough, J., Clague, M. J., and Urbé, S. (2006) The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618-12624
49. Avvakumov, G. V., Walker, J. R., Xue, S., Finerty, P. J., Jr., Mackenzie, F., Newman, E. M., and Dhe-Paganon, S. (2006) Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8). J. Biol. Chem. 281, 38061-38070
50. Lattante, S., Rouleau, G. A., and Kabashi, E. (2013) TARDBP and FUS mutations associated with amyotrophic lateral sclerosis: summary and update. Hum. Mutat. 34, 812-826
51. Kovacs, G. G., Murrell, J. R., Horvath, S., Haraszti, L., Majtenyi, K., Molnar, M. J., Budka, H., Ghetti, B., and Spina, S. (2009) TARDBP variation associated with frontotemporal dementia, supranuclear gaze palsy, and chorea. Mov. Disord. 24, 1843-1847
52. Nollen, E. A., Garcia, S. M., van Haaften, G., Kim, S., Chavez, A., Morimoto, R. I., and Plasterk, R. H. (2004) Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc. Natl. Acad. Sci. U. S. A. 101, 6403-6408
53. Taatjes, D. J. (2010) The human Mediator complex: a versatile, genomewide regulator of transcription. Trends Biochem. Sci. 35, 315-322
54. Sato, S., Tomomori-Sato, C., Parmely, T. J., Florens, L., Zybailov, B., Swanson, S. K., Banks, C. A., Jin, J., Cai, Y., Washburn, M. P., Conaway, J. W., and Conaway, R. C. (2004) A set of consensus mammalian mediator subunits identified by multidimensional protein identification technology. Mol. Cell 14, 685-691
55. Gibson, T. J. (2012) RACK1 researchships passing in the night? FEBS Lett. 586, 2787-2789
56. Imai, Y., Soda, M., and Takahashi, R. (2000) Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 275, 35661-35664
57. Zhang, Y., Gao, J., Chung, K. K., Huang, H., Dawson, V. L., and Dawson, T. M. (2000) Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl. Acad. Sci. U. S. A. 97, 13354-13359
58. Buchwald, G., van der Stoop, P., Weichenrieder, O., Perrakis, A., van Lohuizen, M., and Sixma, T. K. (2006) Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 25, 2465-2474
59. Clague, M. J., and Urbé, S. (2010) Ubiquitin: same molecule, different degradation pathways. Cell 143, 682-685
60. Komander, D., and Rape, M. (2012) The ubiquitin code. Annu. Rev. Biochem. 81, 203-229
61. van Wijk, S. J., and Timmers, H. T. (2010) The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J. 24, 981-993
62. Tai, H.-C., and Schuman, E. M. (2008) Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 9, 826-838
63. Lehman, N. L. (2009) The ubiquitin proteasome system in neuropathology. Acta Neuropathol. 118, 329-347
64. Metzger, M. B., Pruneda, J. N., Klevit, R. E., and Weissman, A. M. (2014) RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 1843, 47-60
65. Fiesel, F. C., Weber, S. S., Supper, J., Zell, A., and Kahle, P. J. (2012) TDP-43 regulates global translational yield by splicing of exon junction complex component SKAR. Nucleic Acids Res. 40, 2668-2682
66. Hong, S., Lee, S., Cho, S.-G., and Kang, S. (2008) UbcH6 interacts with and ubiquitinates the SCA1 gene product ataxin-1. Biochem. Biophys. Res. Commun. 371, 256-260
67. Seiberlich, V., Goldbaum, O., Zhukareva, V., and Richter-Landsberg, C. (2012) The small molecule inhibitor PR-619 of deubiquitinating enzymes affects the microtubule network and causes protein aggregate formation in neural cells: implications for neurodegenerative diseases. Biochim. Biophys. Acta 1823, 2057-2068
68. Lukavsky, P. J., Daujotyte, D., Tollervey, J. R., Ule, J., Stuani, C., Buratti, E., Baralle, F. E., Damberger, F. F., and Allain, F. H. (2013) Molecular basis of UG-rich RNA recognition by the human splicing factor TDP-43. Nat. Struct. Mol. Biol. 20, 1443-1449
69. Tashiro, Y., Urushitani, M., Inoue, H., Koike, M., Uchiyama, Y., Komatsu, M., Tanaka, K., Yamazaki, M., Abe, M., Misawa, H., Sakimura, K., Ito, H., and Takahashi, R. (2012) Motor neuron-specific disruption of proteasomes, but not autophagy, replicates amyotrophic lateral sclerosis. J. Biol. Chem. 287, 42984-42994