Mass spectrometric analysis of accumulated TDP-43 in amyotrophic lateral sclerosis brains

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kametani, Fuyuki ^a   Obi, Tomokazu ^b   Shishido, Takeo ^b   Akatsu, Hiroyasu ^c   Murayama, Shigeo ^d   Saito, Yuko ^e   Yoshida, Mari ^f   Hasegawa, Masato ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b SHIZUOKA INSTITUTE OF EPILEPSY AND NEUROLOGICAL DISORDERS   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

^d Tokyo Metropolitan Geriatric Hospital and Institute of Gerontology   (Japan)

^e NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^f AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; PEPTIDE FRAGMENT; TDP-43 PROTEIN, HUMAN;

AGED; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; FEMALE; HUMAN; MALE; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; PROTEIN PROCESSING; TANDEM MASS SPECTROMETRY;

AGED; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; DNA-BINDING PROTEINS; FEMALE; HUMANS; MALE; MIDDLE AGED; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TANDEM MASS SPECTROMETRY;

EID: 84961771361     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23281     Document Type: Article

References (52)

1. Buratti, E. et al. TDP-43 Binds Heterogeneous Nuclear Ribonucleoprotein A/B through Its C-terminal Tail: An important region for the inhibition of cystic fibrosis transmembrane conductance regulatior exon 9 splicing. J. Biol. Chem. 280, 37572-37584, doi: 10.1074/jbc.M505557200 (2005).
2. Baralle, M., Buratti, E. & Baralle, F. E. The role of TDP-43 in the pathogenesis of ALS and FTLD. Biochem Soc Trans 41, 1536-1540, doi: 10.1042/bst20130186 (2013).
3. Ayala, Y. M., Misteli, T. & Baralle, F. E. TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclindependent kinase 6 expression. Proc Natl Acad Sci USA 105, 3785-3789, doi: 10.1073/pnas.0800546105 (2008).
4. Ayala, Y. M., Pagani, F. & Baralle, F. E. TDP43 depletion rescues aberrant CFTR exon 9 skipping. FEBS Lett 580, 1339-1344, doi: 10.1016/j.febslet.2006.01.052 (2006).
5. Corrado, L. et al. High frequency of TARDBP gene mutations in Italian patients with amyotrophic lateral sclerosis. Human Mutation 30, 688-694 (2009).
6. Buratti, E. & Baralle, F. E. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front Biosci 13, 867-878 (2008).
7. Buratti, E. et al. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J 20, 1774-1784, doi: 10.1093/emboj/20.7.1774 (2001).
8. Bose, J. K., Wang, I. F., Hung, L., Tarn, W.-Y. & Shen, C. K. J. TDP-43 overexpression enhances exon-7 inclusion during SMN PremRNA splicing. J. Biol. Chem. 283, 28852-28859, doi: 10.1074/jbc.M805376200 (2008).
9. Ou, S. H., Wu, F., Harrich, D., Garcia-Martinez, L. F. & Gaynor, R. B. 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 (1995).
10. Wang, H.-Y., Wang, I. F., Bose, J. & Shen, C. K. J. Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 83, 130-139 (2004).
11. Wang, I. F., Reddy, N. M. & Shen, C. K. Higher order arrangement of the eukaryotic nuclear bodies. Proc Natl Acad Sci USA 99, 13583-13588, doi: 10.1073/pnas.212483099 (2002).
12. Sephton, C. F. et al. TDP-43 Is a Developmentally Regulated Protein Essential for Early Embryonic Development. Journal of Biological Chemistry 285, 6826-6834, doi: 10.1074/jbc.M109.061846 (2010).
13. Wu, L.-S. et al. TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. genesis 48, 56-62, doi: 10.1002/dvg.20584 (2010).
14. Neumann, M. et al. Ubiquitinated TDP-43 in Frontotemporal Lobar Degeneration and Amyotrophic Lateral Sclerosis. Science 314, 130-133, doi: 10.1126/science.1134108 (2006).
15. Arai, T. et al. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochemical and Biophysical Research Communications 351, 602-611 (2006).
16. Yokota, O. et al. Phosphorylated TDP-43 pathology and hippocampal sclerosis in progressive supranuclear palsy. Acta Neuropathol 120, 55-66, doi: 10.1007/s00401-010-0702-1 (2010).
17. Arai, T. et al. Phosphorylated TDP-43 in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathol 117, 125-136, doi: 10.1007/s00401-008-0480-1 (2009).
18. Hasegawa, M. et al. TDP-43 is deposited in the Guam parkinsonism-dementia complex brains. Brain 130, 1386-1394, doi: 10.1093/brain/awm065 (2007).
19. Tan, C. F. et al. Selective occurrence of TDP-43-immunoreactive inclusions in the lower motor neurons in Machado-Joseph disease. Acta Neuropathol 118, 553-560, doi: 10.1007/s00401-009-0552-x (2009).
20. Toyoshima, Y. et al. Spinocerebellar ataxia type 2 (SCA2) is associated with TDP-43 pathology. Acta Neuropathol 122, 375-378, doi: 10.1007/s00401-011-0862-7 (2011).
21. Kabashi, E. et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 40, 572-574 (2008).
22. Sreedharan, J. et al. TDP-43 Mutations in Familial and Sporadic Amyotrophic Lateral Sclerosis. Science 319, 1668-1672, doi: 10.1126/science.1154584 (2008).
23. Mackenzie, I. R., Rademakers, R. & Neumann, M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9, 995-1007, doi: 10.1016/S1474-4422(10)70195-2 (2010).
24. Tamaoka, A. et al. TDP-43 M337V mutation in familial amyotrophic lateral sclerosis in Japan. Intern Med 49, 331-334 (2010).
25. Pesiridis, G. S., Lee, V. M. & Trojanowski, J. Q. Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis. Hum Mol Genet 18, R156-162, doi: 10.1093/hmg/ddp303 (2009).
26. Tsuji, H. et al. Molecular analysis and biochemical classification of TDP-43 proteinopathy. Brain 135, 3380-3391, doi: 10.1093/brain/aws230 (2012).
27. Hasegawa, M. et al. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Annals of Neurology 64, 60-70 (2008).
28. Neumann, M., Kwong, L. K., Sampathu, D. M., Trojanowski, J. Q. & Lee, V. M. TDP-43 proteinopathy in frontotemporal lobar degeneration and amyotrophic lateral sclerosis: protein misfolding diseases without amyloidosis. Arch Neurol 64, 1388-1394, doi: 10.1001/archneur.64.10.1388 (2007).
29. Neumann, M. et al. TDP-43 in the ubiquitin pathology of frontotemporal dementia with VCP gene mutations. J Neuropathol Exp Neurol 66, 152-157, doi: 10.1097/nen.0b013e31803020b9 (2007).
30. Zhang, Y. J. et al. Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc Natl Acad Sci USA 106, 7607-7612, doi: 10.1073/pnas.0900688106 (2009).
31. Hasegawa, M. et al. Molecular analysis and biochemical classification of TDP-43 proteinopathy. Dementia and Geriatric Cognitive Disorders 33, 103-104 (2012).
32. Inukai, Y. et al. Abnormal phosphorylation of Ser409/410 of TDP-43 in FTLD-U and ALS. FEBS Letters 582, 2899-2904 (2008).
33. Nonaka, T. et al. Prion-like Properties of Pathological TDP-43 Aggregates from Diseased Brains. Cell Reports 4, 124-134, doi: 10.1016/j.celrep.2013.06.007 (2013).
34. Li, Q., Yokoshi, M., Okada, H. & Kawahara, Y. The cleavage pattern of TDP-43 determines its rate of clearance and cytotoxicity. Nat Commun 6, doi: 10.1038/ncomms7183 (2015).
35. Wang, I. F. et al. The self-interaction of native TDP-43 C terminus inhibits its degradation and contributes to early proteinopathies. Nat Commun 3, 766, doi: 10.1038/ncomms1766 (2012).
36. Yamashita, T. et al. A role for calpain-dependent cleavage of TDP-43 in amyotrophic lateral sclerosis pathology. Nat Commun 3, 1307, doi: 10.1038/ncomms2303 (2012).
37. Aggad, D., Veriepe, J., Tauffenberger, A. & Parker, J. A. TDP-43 toxicity proceeds via calcium dysregulation and necrosis in aging Caenorhabditis elegans motor neurons. J Neurosci 34, 12093-12103, doi: 10.1523/JNEUROSCI.2495-13.2014 (2014).
38. Kametani, F. et al. Identification of casein kinase-1 phosphorylation sites on TDP-43. Biochemical and Biophysical Research Communications 382, 405-409, doi: 10.1016/j.bbrc.2009.03.038 (2009).
39. Cohen, T. J. et al. An acetylation switch controls TDP-43 function and aggregation propensity. Nat Commun 6, doi: 10.1038/ncomms6845 (2015).
40. Suzuki, H., Lee, K. & Matsuoka, M. TDP-43-induced death is associated with altered regulation of BIM and Bcl-xL and attenuated by caspase-mediated TDP-43 cleavage. J Biol Chem 286, 13171-13183, doi: 10.1074/jbc.M110.197483 (2011).
41. Chew, J. et al. C9ORF72 repeat expansions in mice cause TDP-43 pathology, neuronal loss, and behavioral deficits. Science 348, 1151-1154, doi: 10.1126/science.aaa9344 (2015).
42. Fang, Y. S. et al. Full-length TDP-43 forms toxic amyloid oligomers that are present in frontotemporal lobar dementia-TDP patients. Nat Commun 5, 4824, doi: 10.1038/ncomms5824 (2014).
43. Janssens, J. et al. Overexpression of ALS-associated p.M337V human TDP-43 in mice worsens disease features compared to wildtype human TDP-43 mice. Mol Neurobiol 48, 22-35, doi: 10.1007/s12035-013-8427-5 (2013).
44. Igaz, L. M. et al. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J Clin Invest 121, 726-738, doi: 10.1172/JCI44867 (2011).
45. D'Alton, S. et al. Divergent Phenotypes in Mutant TDP-43 Transgenic Mice Highlight Potential Confounds in TDP-43 Transgenic Modeling. PLoS ONE 9, e86513, doi: 10.1371/journal.pone.0086513 (2014).
46. Igaz, L. M. et al. Expression Of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J. Biol. Chem. 284, 8516-8524, M809462200, doi: 10.1074/jbc.M809462200 (2009).
47. Nonaka, T., Kametani, F., Arai, T., Akiyama, H. & Hasegawa, M. Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Hum. Mol. Genet. 18, 3353-3364, doi: 10.1093/hmg/ddp275 (2009).
48. Igaz, L. M. et al. 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, doi: 10.2353/ajpath.2008.080003 (2008).
49. Lee, E. B., Lee, V. M. Y. & Trojanowski, J. Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat Rev Neurosci 13, 38-50 (2012).
50. Guo, W. et al. An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Nat Struct Mol Biol 18, 822-830, doi: 10.1038/nsmb.2053 (2011).
51. Chen, A. K. et al. Induction of amyloid fibrils by the C-terminal fragments of TDP-43 in amyotrophic lateral sclerosis. J Am Chem Soc 132, 1186-1187, doi: 10.1021/ja9066207 (2010).
52. Wang, Y.-T. et al. The Truncated C-terminal RNA Recognition Motif of TDP-43 Protein Plays a Key Role in Forming Proteinaceous Aggregates. Journal of Biological Chemistry 288, 9049-9057, doi: 10.1074/jbc.M112.438564 (2013).