Proteolytic processing of TAR DNA binding protein-43 by caspases produces C-terminal fragments with disease defining properties independent of progranulin

Journal of Neurochemistry

Volumn 110, Issue 3, 2009, Pages 1082-1094

  Dormann, Dorothee ^a   Capell, Anja ^a   Carlson, Aaron M ^a   Shankaran, Sunita S ^b   Rodde, Ramona ^a   Neumann, Manuela ^c   Kremmer, Elisabeth ^d   Matsuwaki, Takashi ^e   Yamanouchi, Keitaro ^e   Nishihara, Masugi ^e   Haass, Christian ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

Dementia; Frontotemporal lobar degeneration; FTLD U; Neurodegeneration; Progranulin; TAR DNA binding protein 43

Indexed keywords

CASPASE; PROGRANULIN; SMALL INTERFERING RNA; TAR DNA BINDING PROTEIN; UBIQUITIN;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INCLUSION; CONTROLLED STUDY; ENZYME ACTIVATION; FRONTOTEMPORAL DEMENTIA; GLIA CELL; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

ANIMALS; CASPASES; CELL LINE, TUMOR; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT;

MUS;

EID: 67650432367     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06211.x     Document Type: Article

References (54)

1. Aguzzi A. Haass C. (2003) Games played by rogue proteins in prion disorders and Alzheimer's disease. Science 302, 814 818. (Pubitemid 37339613)
2. Ahmed Z., Mackenzie I. R., Hutton M. L. Dickson D. W. (2007) Progranulin in frontotemporal lobar degeneration and neuroinflammation. J. Neuroinflammation 4, 7.
3. Arai T., Hasegawa M., Akiyama H. et al. (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)
4. Arai T., Mackenzie I. R., Hasegawa M., Nonoka T., Niizato K., Tsuchiya K., Iritani S., Onaya M. Akiyama H. (2009) Phosphorylated TDP-43 in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathol. 117, 125 136.
5. Ayala Y. M., Misteli T. Baralle F. E. (2008) TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc. Natl Acad. Sci. USA 105, 3785 3789. (Pubitemid 351723476)
6. Baker M., Mackenzie I. R., Pickering-Brown S. M. et al. (2006) Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442, 916 919. (Pubitemid 44285946)
7. Benajiba L., Le Ber I., Camuzat A. et al. (2009) TARDBP mutations in motoneuron disease with frontotemporal lobar degeneration. Ann. Neurol. 65, 470 473.
8. Bose J. K., Wang I. F., Hung L., Tarn W. Y. Shen C. K. (2008) TDP-43 overexpression enhances exon-7 inclusion during SMN Pre-mRNA splicing. J. Biol. Chem. 283, 28852 28859.
9. Buratti E. 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.
10. Buratti E., Brindisi A., Pagani F. 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)
11. Buratti E., Brindisi A., Giombi M., Tisminetzky S., Ayala Y. M. 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. (Pubitemid 41642366)
12. Corrado L., Ratti A., Gellera C. et al. (2009) High frequency of TARDBP gene mutations in Italian patients with amyotrophic lateral sclerosis. Hum. Mutat. 30, 688 694.
13. Cruts M., Gijselinck I., van der Zee J. et al. (2006) Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442, 920 924. (Pubitemid 44285947)
14. Daoud H., Valdmanis P. N., Kabashi E., Dion P., Dupre N., Camu W., Meininger V. Rouleau G. A. (2009) Contribution of TARDBP mutations to sporadic amyotrophic lateral sclerosis. J. Med. Genet. 46, 112 114.
15. Del Bo R., Ghezzi S., Corti S. et al. (2009) TARDBP (TDP-43) sequence analysis in patients with familial and sporadic ALS: identification of two novel mutations. Eur. J. Neurol. 16, 727 732.
16. Farrer M. J., Hulihan M. M., Kachergus J. M. et al. (2009) DCTN1 mutations in Perry syndrome. Nat. Genet. 41, 163 165.
17. Finch N., Baker M., Crook R. et al. (2009) Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members. Brain 132, 583 591.
18. Ghidoni R., Benussi L., Glionna M., Franzoni M. Binetti G. (2008) Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration. Neurology 71, 1235 1239.
19. Gijselinck I., Van Broeckhoven C. Cruts M. (2008) Granulin mutations associated with frontotemporal lobar degeneration and related disorders: an update. Hum. Mutat. 29, 1373 1386. (Pubitemid 352774891)
20. Gitcho M. A., Baloh R. H., Chakraverty S. et al. (2008) TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol. 63, 535 538. (Pubitemid 351614720)
21. Gregory R. I., Yan K. P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N. Shiekhattar R. (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235 240. (Pubitemid 39545855)
22. Haass C. Selkoe D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 8, 101 112. (Pubitemid 46432529)
23. Hasegawa M., Arai T., Nonaka T. et al. (2008) Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann. Neurol. 64, 60 70.
24. Igaz L. M., Kwong L. K., Xu Y. et al. (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)
25. Igaz L. M., Kwong L. K., Chen-Plotkin A., Winton M. J., Unger T. L., Xu Y., Neumann M., Trojanowski J. Q. Lee V. M. (2009) Expression Of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J. Biol. Chem. 284, 8516 8524.
26. Inukai Y., Nonaka T., Arai T. et al. (2008) Abnormal phosphorylation of Ser409/410 of TDP-43 in FTLD-U and ALS. FEBS Lett. 582, 2899 2904.
27. Kabashi E., Valdmanis P. N., Dion P. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40, 572 574. (Pubitemid 351601218)
28. Kamada M., Maruyama H., Tanaka E. et al. (2009) Screening for TARDBP mutations in Japanese familial amyotrophic lateral sclerosis. J. Neurol. Sci. [Epub ahead of print, Y., Chiba S., Suzuki M. et al. (2007) Alteration of behavioural phenotype in mice by targeted disruption of the progranulin gene. Behav. Brain Res. 185, 110 118.
29. Kuhnlein P., Sperfeld A. D., Vanmassenhove B., Van Deerlin V., Lee V. M., Trojanowski J. Q., Kretzschmar H. A., Ludolph A. C. Neumann M. (2008) Two German kindreds with familial amyotrophic lateral sclerosis due to TARDBP mutations. Arch. Neurol. 65, 1185 1189.
30. Lemmens R., Race V., Hersmus N. et al. (2009) TDP-43 M311V mutation in familial amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 80, 354 355.
31. Mercado P. A., Ayala Y. M., Romano M., Buratti E. Baralle F. E. (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. (Pubitemid 41742619)
32. Moisse K., Volkening K., Leystra-Lantz C., Welch I., Hill T. Strong M. J. (2009) Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Brain Res. 1249, 202 211.
33. Mukherjee O., Pastor P., Cairns N. J. et al. (2006) HDDD2 is a familial frontotemporal lobar degeneration with ubiquitin-positive, tau-negative inclusions caused by a missense mutation in the signal peptide of progranulin. Ann. Neurol. 60, 314 322. (Pubitemid 44520234)
34. Mukherjee O., Wang J., Gitcho M. et al. (2008) Molecular characterization of novel progranulin (GRN) mutations in frontotemporal dementia. Hum. Mutat. 29, 512 521.
35. Neumann M., Sampathu D. M., Kwong L. K. et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130 133. (Pubitemid 44547757)
36. Neumann M., Kwong L. K., Truax A. C. et al. (2007) TDP-43-positive white matter pathology in frontotemporal lobar degeneration with ubiquitin-positive inclusions. J. Neuropathol. Exp. Neurol. 66, 177 183. (Pubitemid 46673273)
37. Neumann M., Kwong L. K., Lee E. B. et al. (2009) Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies. Acta Neuropathol. 117, 137 149.
38. Ou S. H., Wu F., Harrich D., Garcia-Martinez L. F. Gaynor R. B. (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.
39. Parkinson N., Ince P. G., Smith M. O. et al. (2006) ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67, 1074 1077. (Pubitemid 44454610)
40. Rademakers R. Hutton M. (2007) The genetics of frontotemporal lobar degeneration. Curr. Neurol. Neurosci. Rep. 7, 434 442. (Pubitemid 47422786)
41. Rutherford N. J., Zhang Y. J., Baker M. et al. (2008) Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet 4, e1000193.
42. Schymick J. C., Yang Y., Andersen P. M. et al. (2007) Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-frontotemporal dementia phenotypes. J. Neurol. Neurosurg. Psychiatry 78, 754 756. (Pubitemid 46998853)
43. Shankaran S. S., Capell A., Hruscha A. T., Fellerer K., Neumann M., Schmid B. Haass C. (2008) Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J. Biol. Chem. 283, 1744 1753.
44. Skibinski G., Parkinson N. J., Brown J. M. et al. (2005) Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet. 37, 806 808. (Pubitemid 41077105)
45. Sleegers K., Brouwers N., Van Damme P. et al. (2009) Serum biomarker for progranulin-associated frontotemporal lobar degeneration. Ann. Neurol. 65, 603 609.
46. Sreedharan J., Blair I. P., Tripathi V. B. et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319, 1668 1672.
47. Van Deerlin V. M., Leverenz J. B., Bekris L. M. et al. (2008) TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 7, 409 416.
48. Watts G. D., Wymer J., Kovach M. J., Mehta S. G., Mumm S., Darvish D., Pestronk A., Whyte M. P. Kimonis V. E. (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377 381. (Pubitemid 38437260)
49. Watts G. D., Thomasova D., Ramdeen S. K. et al. (2007) Novel VCP mutations in inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia. Clin. Genet. 72, 420 426. (Pubitemid 47570695)
50. Winton M. J., Igaz L. M., Wong M. M., Kwong L. K., Trojanowski J. Q. 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.
51. Yokoseki A., Shiga A., Tan C. F. et al. (2008) TDP-43 mutation in familial amyotrophic lateral sclerosis. Ann. Neurol. 63, 538 542. (Pubitemid 351614721)
52. van der Zee J., Le Ber I., Maurer-Stroh S. et al. (2007) Mutations other than null mutations producing a pathogenic loss of progranulin in frontotemporal dementia. Hum. Mutat. 28, 416.
53. Zhang Y. J., Xu Y. F., Dickey C. A., Buratti E., Baralle F., Bailey R., Pickering-Brown S., Dickson D. Petrucelli L. (2007) Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J. Neurosci. 27, 10530 10534. (Pubitemid 47501990)
54. Zhang Y. J., Xu Y. F., Cook C. et al. (2009) Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc. Natl Acad. Sci. USA 106, 7607 7612.