Aberrant assembly of RNA recognition motif 1 links to pathogenic conversion of TAR DNA-binding protein of 43 kDa (TDP-43)

Journal of Biological Chemistry

Volumn 288, Issue 21, 2013, Pages 14886-14905

  Shodai, Akemi ^a   Morimura, Toshifumi ^a   Ido, Akemi ^a   Uchida, Tsukasa ^a,b   Ayaki, Takashi ^b   Takahashi, Rina ^c   Kitazawa, Soichiro ^c   Suzuki, Sakura ^d   Shirouzu, Mikako ^d   Kigawa, Takanori ^d   Muto, Yutaka ^d   Yokoyama, Shigeyuki ^d   Takahashi, Ryosuke ^b   Kitahara, Ryo ^c   Ito, Hidefumi ^b,e   Fujiwara, Noriko ^f   Urushitani, Makoto ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RITSUMEIKAN UNIVERSITY   (Japan)

^d RIKEN   (Japan)

^e WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^f HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATE FORMATION; AMYLOID FIBRIL; AMYOTROPHIC LATERAL SCLEROSIS; DNA-BINDING PROTEIN; MASS SPECTROMETRIC ANALYSIS; MISLOCALIZATION; RNA-RECOGNITION MOTIFS; UBIQUITINATION;

AMINO ACIDS; CONFORMATIONS; NEURONS; OLIGOMERS; PROTEINS; RNA; TAR;

AGGREGATES;

AMYLOID BETA PROTEIN; CYSTEINE; SERINE; TAR DNA BINDING PROTEIN; TAR DNA BINDING PROTEIN OF 43 KDA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CASE REPORT; CONTROLLED STUDY; CYTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MASS SPECTROMETRY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN MOTIF; RNA RECOGNITION MOTIF 1;

AMYOTROPHIC LATERAL SCLEROSIS (LOU GEHRIG'S DISEASE); CELL BIOLOGY; PROTEIN CHEMICAL MODIFICATION; PROTEIN MISFOLDING; STRUCTURAL BIOLOGY; TAR DNA-BINDING PROTEIN 43 KDA;

AMINO ACID MOTIFS; AMYLOID; AMYOTROPHIC LATERAL SCLEROSIS; DNA-BINDING PROTEINS; FEMALE; HEK293 CELLS; HUMANS; INTRANUCLEAR INCLUSION BODIES; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEURONS; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RNA SPLICING; UBIQUITINATION;

EID: 84878224074     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451849     Document Type: Article

References (45)

1. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y., and Oda, T. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351, 602-611 (Pubitemid 44708852)
2. 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 (Pubitemid 44547757)
3. Baloh, R. H. (2012) How do the RNA-binding proteins TDP-43 and FUS relate to amyotrophic lateral sclerosis and frontotemporal degeneration, and to each other? Curr. Opin. Neurol. 25, 701-707
4. Pesiridis, G. S., Lee, V. M., and Trojanowski, J. Q. (2009) Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis. Hum. Mol. Genet. 18, R156-R162
5. Gendron, T. F., Josephs, K. A., and Petrucelli, L. (2010) Review. Transactive response DNA-binding protein 43 (TDP-43). Mechanisms of neurodegeneration. Neuropathol. Appl. Neurobiol. 36, 97-112
6. Cohen, T. J., Lee, V. M., and Trojanowski, J. Q. (2011) TDP-43 functions and pathogenic mechanisms implicated in TDP-43 proteinopathies. Trends Mol. Med. 17, 659-667
7. Winton, M. J., Igaz, L. M., Wong, M. M., Kwong, L. K., Trojanowski, J. Q., and Lee, V. M. (2008) Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. J. Biol. Chem. 283, 13302-13309
8. Kuo, P. H., Doudeva, L. G., Wang, Y. T., Shen, C. K., and Yuan, H. S. (2009) Structural insights into TDP-43 in nucleic acid binding and domain interactions. Nucleic Acids Res. 37, 1799-1808
9. Furukawa, Y., Kaneko, K., Watanabe, S., Yamanaka, K., and Nukina, N. (2011) A seeding reaction recapitulates intracellular formation of Sarkosyl-insoluble transactivation response element (TAR) DNA-binding protein-43 inclusions. J. Biol. Chem. 286, 18664-18672
10. Budini, M., Buratti, E., Stuani, C., Guarnaccia, C., Romano, V., De Conti, L., and Baralle, F. E. (2012) Cellular model of TAR DNA-binding protein 43 (TDP-43) aggregation based on its C-terminal Gln/Asn-rich region. J. Biol. Chem. 287, 7512-7525
11. Hasegawa, M., Arai, T., Nonaka, T., Kametani, F., Yoshida, M., Hashizume, Y., Beach, T. G., Buratti, E., Baralle, F., Morita, M., Nakano, I., Oda, T., Tsuchiya, K., and Akiyama, H. (2008) Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann. Neurol. 64, 60-70
12. Ash, P. E., Zhang, Y. J., Roberts, C. M., Saldi, T., Hutter, H., Buratti, E., Petrucelli, L., and Link, C. D. (2010) Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum. Mol. Genet. 19, 3206-3218
13. Shodai, A., Ido, A., Fujiwara, N., Ayaki, T., Morimura, T., Oono, M., Uchida, T., Takahashi, R., Ito, H., and Urushitani, M. (2012) Conserved acidic amino acid residues in a second RNA recognition motif regulate assembly and function of TDP-43. PloS One 7, e52776
14. Bentmann, E., Neumann, M., Tahirovic, S., Rodde, R., Dormann, D., and Haass, C. (2012) Requirements for stress granule recruitment of fused in sarcoma (FUS) and TAR DNA-binding protein of 43 kDa (TDP-43). J. Biol. Chem. 287, 23079-23094
15. Higashi, S., Kabuta, T., Nagai, Y., Tsuchiya, Y., Akiyama, H., and Wada, K. (2013) TDP-43 associates with stalled ribosomes and contributes to cell survival during cellular stress. J. Neurochem. 10.1111/jnc.12194
16. Buratti, E., and Baralle, F. E. (2001) Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem. 276, 36337-36343
17. Polymenidou, M., Lagier-Tourenne, C., Hutt, K. R., Huelga, S. C., Moran, J., Liang, T. Y., Ling, S. C., Sun, E., Wancewicz, E., Mazur, C., Kordasiewicz, H., Sedaghat, Y., Donohue, J. P., Shiue, L., Bennett, C. F., Yeo, G. W., and Cleveland, D. W. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 14, 459-468
18. Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Zupunski, V., Patani, R., Chandran, S., Rot, G., Zupan, B., Shaw, C. E., and Ule, J. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 14, 452-458
19. Xiao, S., Sanelli, T., Dib, S., Sheps, D., Findlater, J., Bilbao, J., Keith, J., Zinman, L., Rogaeva, E., and Robertson, J. (2011) RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol. Cell. Neurosci. 47, 167-180
20. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (Pubitemid 44118036)
21. Kuwata, K., Nishida, N., Matsumoto, T., Kamatari, Y. O., Hosokawa-Muto, J., Kodama, K., Nakamura, H. K., Kimura, K., Kawasaki, M., Takakura, Y., Shirabe, S., Takata, J., Kataoka, Y., and Katamine, S. (2007) Hot spots in prion protein for pathogenic conversion. Proc. Natl. Acad. Sci. U.S.A. 104, 11921-11926 (Pubitemid 47185606)
22. Torrent, J., Alvarez-Martinez, M. T., Liautard, J. P., and Lange, R. (2006) Modulation of prion protein structure by pressure and temperature. Biochim. Biophys. Acta 1764, 546-551
23. Chang, C. K., Wu, T. H., Wu, C. Y., Chiang, M. H., Toh, E. K., Hsu, Y. C., Lin, K. F., Liao, Y. H., Huang, T. H., and Huang, J. J. (2012) The N-terminus of TDP-43 promotes its oligomerization and enhances DNA binding affinity. Biochem. Biophys. Res. Commun. 425, 219-224
24. 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
25. Akasaka, K. (2006) Probing conformational fluctuation of proteins by pressure perturbation. Chem. Rev. 106, 1814-1835
26. Ramjeesingh, M., Huan, L. J., Garami, E., and Bear, C. E. (1999) Novel method for evaluation of the oligomeric structure of membrane proteins. Biochem. J. 342, 119-123 (Pubitemid 29410857)
27. Matusica, D., Fenech, M. P., Rogers, M. L., and Rush, R. A. (2008) Characterization and use of the NSC-34 cell line for study of neurotrophin receptor trafficking. J. Neurosci. Res. 86, 553-565 (Pubitemid 351204469)
28. Che, M. X., Jiang, Y. J., Xie, Y. Y., Jiang, L. L., and Hu, H. Y. (2011) Aggregation of the 35-kDa fragment of TDP-43 causes formation of cytoplasmic inclusions and alteration of RNA processing. FASEB J. 25, 2344-2353
29. Kitahara, R., Yamaguchi, Y., Sakata, E., Kasuya, T., Tanaka, K., Kato, K., Yokoyama, S., and Akasaka, K. (2006) Evolutionally conserved intermediates between ubiquitin and NEDD8. J. Mol. Biol. 363, 395-404 (Pubitemid 44436251)
30. 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
31. 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
32. 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 (Pubitemid 351601218)
33. Nonaka, T., Arai, T., Buratti, E., Baralle, F. E., Akiyama, H., and Hasegawa, M. (2009) Phosphorylated and ubiquitinated TDP-43 pathological inclusions in ALS and FTLD-U are recapitulated in SH-SY5Y cells. FEBS Lett. 583, 394-400
34. Iguchi, Y., Katsuno, M., Takagi, S., Ishigaki, S., Niwa, J., Hasegawa, M., Tanaka, F., and Sobue, G. (2012) Oxidative stress induced by glutathione depletion reproduces pathological modifications of TDP-43 linked to TDP-43 proteinopathies. Neurobiol. Dis. 45, 862-870
35. Biswas, S., Chida, A. S., and Rahman, I. (2006) Redox modifications of protein-thiols. emerging roles in cell signaling. Biochem. Pharmacol. 71, 551-564 (Pubitemid 43121989)
36. Swarup, V., Phaneuf, D., Dupré, N., Petri, S., Strong, M., Kriz, J., and Julien, J. P. (2011) Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor κB-mediated pathogenic pathways. J. Exp. Med. 208, 2429-2447
37. 111 in human copper-zinc superoxide dismutase. J. Biol. Chem. 282, 35933-35944
38. Akhtar, M. W., Sunico, C. R., Nakamura, T., and Lipton, S. A. (2012) Redox regulation of protein function via cysteine S-nitrosylation and its relevance to neurodegenerative diseases. Int. J. Cell Biol. 2012, 463756
39. Pesiridis, G. S., Tripathy, K., Tanik, S., Trojanowski, J. Q., and Lee, V. M. (2011) A "two-hit" hypothesis for inclusion formation by carboxyl-terminal fragments of TDP-43 protein linked to RNA depletion and impaired microtubule-dependent transport. J. Biol. Chem. 286, 18845-18855
40. Buratti, E., Brindisi, A., Pagani, F., and Baralle, F. E. (2004) Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipping of exon 9. A functional link with disease penetrance. Am. J. Hum. Genet. 74, 1322-1325 (Pubitemid 38669335)
41. Swarup, V., Phaneuf, D., Bareil, C., Robertson, J., Rouleau, G. A., Kriz, J., and Julien, J. P. (2011) Pathological hallmarks of amyotrophic lateral sclerosis/frontotemporal lobar degeneration in transgenic mice produced with TDP-43 genomic fragments. Brain 134, 2610-2626
42. Igaz, L. M., Kwong, L. K., Lee, E. B., Chen-Plotkin, A., Swanson, E., Unger, T., Malunda, J., Xu, Y., Winton, M. J., Trojanowski, J. Q., and Lee, V. M. (2011) Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest. 121, 726-738
43. Zhang, T., Mullane, P. C., Periz, G., and 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
44. Caccamo, A., Majumder, S., and Oddo, S. (2012) Cognitive decline typical of frontotemporal lobar degeneration in transgenic mice expressing the 25-kDa C-terminal fragment of TDP-43. Am. J. Pathol. 180, 293-302
45. Igaz, L. M., Kwong, L. K., Xu, Y., Truax, A. C., Uryu, K., Neumann, M., Clark, C. M., Elman, L. B., Miller, B. L., Grossman, M., McCluskey, L. F., Trojanowski, J. Q., and Lee, V. M. (2008) Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Am. J. Pathol. 173, 182-194 (Pubitemid 351947966)