TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis

Biochemical and Biophysical Research Communications

Volumn 351, Issue 3, 2006, Pages 602-611

  Arai, Tetsuaki ^a   Hasegawa, Masato ^a   Akiyama, Haruhiko ^a   Ikeda, Kenji ^b   Nonaka, Takashi ^a   Mori, Hiroshi ^c   Mann, David ^d   Tsuchiya, Kuniaki ^e   Yoshida, Mari ^f   Hashizume, Yoshio ^f   Oda, Tatsuro ^g  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b Zikei hospital 100 2 Urayasuhonmachi   (Japan)

^c OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e TOKYO METROPOLITAN MATSUZAWA HOSPITAL   (Japan)

^f AICHI MEDICAL UNIVERSITY   (Japan)

^g National Hospital Organization Shimofusa Psychiatric Medical Center   (Japan)

Author keywords

Accumulation; Glia; Immunoblot; Immunohistochemistry; Insoluble; Mass spectrometry; Motoneuron; Neurite; Phosphorylation; Spinal cord

Indexed keywords

NUCLEAR PROTEIN; TAR DNA BINDING PROTEIN OF 43 KDA; TAU PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ADULT; AGED; ALTERNATIVE RNA SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN DEGENERATION; BRAIN NERVE CELL; CELL INCLUSION; CHEMICAL ANALYSIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GENETIC TRANSCRIPTION; GLIA CELL; HUMAN; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR WEIGHT; MOTOR NEURON DISEASE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; SPINAL CORD;

AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; DEMENTIA; DNA-BINDING PROTEINS; FEMALE; HUMANS; INCLUSION BODIES; MALE; MIDDLE AGED; TAU PROTEINS; TISSUE DISTRIBUTION; UBIQUITIN;

EID: 33750716074     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.10.093     Document Type: Article

References (53)

1. McKhann G.M., Albert M.S., Grossman M., Miller B., Dickson D., and Trojanowski J.Q. Clinical and pathological diagnosis of frontotemporal dementia: report of the work group on frontotemporal dementia and Pick's disease. Arch. Neurol. 58 (2001) 1803-1809
2. Mitsuyama Y., and Takamiya S. Presenile dementia with motor neuron disease in Japan. A new entity?. Arch. Neurol. 36 (1979) 592-593
3. Nakano I. Temporal lobe lesions in amyotrophic lateral sclerosis with dementia-lesions in the apical cortex and some deeper structures of the temporal lobes. Neuropathology 12 (1992) 69-77
4. Wightman G., Anderson V.E.R., Martin A.J., Swash M., Anderson B.H., Neary D., Mann D., Luthert P., and Leigh P.N. Hippocampal and neocortical ubiquitin-immunoreactive inclusions in amyotrophic lateral sclerosis with dementia. Neurosci. Lett. 139 (1992) 269-274
5. Jackson M., Lennox G., and Lowe J. Motor neuron disease-inclusion dementia. Neurodegeneration 5 (1996) 339-350
6. Iseki E., Li F., Odawara T., Hino H., Suzuki K., Kosaka K., Akiyama H., Ikeda K., and Kato M. Ubiquitin-immunohistochemical investigation of atypical Pick's disease without Pick bodies. J. Neurol. Sci. 159 (1998) 194-201
7. Ikeda K. Neuropathological discrepancy between Japanese Pick's disease without Pick bodies and frontal lobe degeneration type of frontotemporal dementia proposed by Lund and Manchester group. Neuropathology 20 (2000) 76-82
8. Knopman D.S., Mastri A.R., Frey W.H., Sung J.H., and Rustan T. Dementia lacking distinctive histologic features: a common non-Alzheimer degenerative dementia. Neurology 40 (1990) 251-256
9. Lipton A.M., White III C.L., and Bigio E.H. Frontotemporal lobar degeneration with motor neuron disease-type inclusions predominates in 76 cases of frontotemporal degeneration. Acta Neuropathol. (Berl.) 108 (2004) 379-385
10. Okamoto K., Hirai S., Yamazaki T., Sun X., and Nakazato Y. New ubiquitin-positive intraneuronal inclusions in the extra-motor cortices in patients with amyotrophic lateral sclerosis. Neurosci. Lett. 129 (1991) 233-236
11. Okamoto K., Murakami N., Kusada H., Yoshida M., Hashizume Y., Nakazato Y., Matsubara E., and Hirai S. Ubiquitin-positive intraneuronal inclusions in the extramotor cortices of presenile dementia patients with motor neuron disease. J. Neurol. 239 (1992) 426-430
12. Bergmann M., Kuchelmeister K., Schmid K.W., Kretzschmar H.A., and Schröder R. Different variants of frontotemporal dementia: a neuropathological and immunohistochemical study. Acta Neuropathol. (Berl.) 92 (1996) 170-179
13. Ikeda K., Akiyama H., Arai T., Ueno H., Tsuchiya K., and Kosaka K. Morphometrical reappraisal of motor neuron system of Pick's disease and amyotrophic lateral sclerosis with dementia. Acta Neuropathol. (Berl.) 104 (2002) 21-28
14. Mackenzie I.R.A., and Feldman H.H. Ubiquitin immunohistochemistry suggests classic motor neuron disease, motor neuron disease with dementia, and frontotemporal dementia of the motor neuron disease type represent a clinicopathological spectrum. J. Neuropathol. Exp. Neurol. 64 (2005) 730-739
15. Arai T., Nonaka T., Hasegawa M., Akiyama H., Yoshida M., Hashizume Y., Tsuchiya K., Oda T., and Ikeda K. Neuronal and glial inclusions in frontotemporal dementia with or without motor neuron disease are immunopositive for p62. Neurosci. Lett. 342 (2003) 41-44
16. Mori F., Nishie M., Piao Y.S., Kito K., Kamitani T., Takahashi H., and Wakabayashi K. Accumulation of NEDD8 in neuronal and glial inclusions of neurodegenerative disorders. Neuropathol. Appl. Neurobiol. 31 (2005) 53-61
17. Kuusisto E., Salminen A., and Alafuzoff I. Ubiquitin-binding protein p62 is present in neuronal and glial inclusions in human tauopathies and synucleinopathies. Neuroreport 12 (2001) 2085-2090
18. Rosso S.M., Kamphorst W., de Graaf G., Willemsen R., Ravid R., Niermeijer M.F., Spillantini M.G., Heutink P., and van Swieten J.C. Familial frontotemporal dementia with ubiquitin-positive inclusions is linked to chromosome 17q21-22. Brain 124 (2001) 1948-1957
19. Woulfe J., Kertesz A., and Munoz D.G. Frontotemporal dementia with ubiquitinated cytoplasmic and intranuclear inclusions. Acta Neuropathol. (Berl.) 102 (2001) 94-102
20. Vance C., Al-Chalabi A., Ruddy D., Smith B.N., Hu X., Sreedharan J., Siddique T., Schelhaas H.J., Kusters B., Troost D., Baas F., de Jong V., and Shaw C.E. Familial amyotrophic lateral sclerosis with frontotemporal dementia is linked to a locus on chromosome 9p13.2-21.3. Brain 129 (2006) 868-875
21. Forman M.S., Mackenzie I.R., Cairns N.J., Swanson E., Boyer P.J., Drachman D.A., Jhaveri B.S., Karlawish J.H., Pestronk A., Smith T.W., Tu P., Watts G.D.J., Markesbery W.R., Smith C.D., and Kimonis V.E. Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J. Neuropathol. Exp. Neurol. 65 (2006) 571-581
22. Cruts M., Gijselinck I., van der Zee J., Engelborghs S., Wils H., Pirici D., Rademakers R., Vandenberghe R., Dermaut B., Martin J., van Duijin C., Peeters K., Sciot R., Santens P., De Pooter T., Mattheijssens M., Van den Broeck M., Cuijt I., Vennekens K., De Deyn P.P., Kumar-Singh S., and Van Broeckhoven C. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442 (2006) 920-924
23. Baker M., Mackenzie I.R., Pickering-Brown S.M., Gass J., Rademakers R., Lindholm C., Snowden J., Adamson J., Sadovnick A.D., Rollinson S., Cannon A., Dwosh E., Neary D., Melquist S., Richardson A., Dickson D., Berger Z., Eriksen J., Robinson T., Zehr C., Dickey C.A., Crook R., McGowan E., Mann D., Boeve B., Feldman H., and Hutton M. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442 (2006) 916-919
24. Mukherjee O., Pastor P., Cairns N.J., Chakraverty S., Kauwe J.S.K., Shears S., Behrens M.I., Budde J., Hinrichs A.L., Norton J., Levitch D., Taylor-Reinwald L., Gitcho M., Tu P.-H., Grinberg L.T., Liscic R.M., Armendariz J., Morris J.C., and Goate A.M. 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 (2006) 314-322
25. J. Gass, A. Cannon, I.R. Mackenzie, B. Boeve, M. Baker, J. Adamson, R. Crook, S. Melquist, K. Kuntz, R. Peterson, K. Josephs, S.-P. Brown, N. Graff-Radford, R. Uitti, D. Dickson, Z. Wzsolek, J. Gonzalez, T.G. Beach, E. Bigio, N. Johnson, S. Weintraub, M. Mesulam, C.L. White III, B. Woodruff, R. Caselli, G.-Y. Hsiung, H. Feldman, D. Knopman, M. Hutton, R. Rademakers, Mutations in progranulin are a major cause of ubiquitin-positive frontotemporal lobar degeneration, Hum. Mol. Genet., advance online publication, doi:10.1093/hmg/ddl241 (2006).
26. Watts G.D.J., Wymer J., Kovach M.J., Mehta S.G., Mumm S., Darvish D., Pestronk A., Whyte M.P., and Kimonis V.E. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36 (2004) 377-381
27. Ou S.H., Wu F., Harrich D., García-Martínez L.F., and 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 (1995) 3584-3596
28. Wang H.-Y., Wang I.-F., Bose J., and Shen C.-K.J. Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 83 (2004) 130-139
29. Mori H., Kondo J., and Ihara Y. Ubiquitin is a component of paired helical filaments in Alzheimer's disease. Science 235 (1987) 1641-1644
30. Fujiwara H., Hasegawa M., Dohmae N., Kawashima A., Masliah E., Goldberg M.S., Shen J., Takio K., and Iwatsubo T. α-Synuclein is phosphorylated in synucleinopathy lesions. Nat. Cell. Biol. 4 (2002) 160-164
31. Goedert M., Spillantini M.G., Cairns N.J., and Crowther R.A. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8 (1992) 159-168
32. Lowe J., Lennox G., Jefferson D., Morrell K., McQuire D., Gray T., Landon M., Doherty F.J., and Mayer R.J. A filamentous inclusion body within anterior horn neurones in motor neurone disease defined by immunocytochemical localization of ubiquitin. Neurosci. Lett. 94 (1988) 203-210
33. Leigh P.N., Whitwell H., Garofalo O., Buller J., Swash M., Martin J.E., Gallo J.-M., Weller R.O., and Anderton B.H. Ubiquitin-immunoreactive intraneuronal inclusions in amyotrophic lateral sclerosis. Brain 114 (1991) 775-788
34. Buratti E., Brindisi A., Giombi M., Tisminetzky S., Ayala Y.M., and Baralle F.E. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail. J. Biol. Chem. 280 (2005) 37572-37584
35. Wang I.-F., Reddy N.M., and Shen C.-K.J. Higher order arrangement of the eukaryotic nuclear bodies. Proc. Natl. Acad. Sci. USA 99 (2002) 13583-13588
36. Hasegawa M., Morishima-Kawashima M., Takio K., Suzuki M., Titani K., and Ihara Y. Protein sequence and mass spectrometric analyses of tau in the Alzheimer's disease brain. J. Biol. Chem. 267 (1992) 17047-17054
37. Ihara Y., Abraham C., and Selkoe D.J. Antibodies to paired helical filaments in Alzheimer's disease do not recognize normal brain proteins. Nature 304 (1983) 727-730
38. Endoh R., Ogawara M., Iwatsubo T., Nakano I., and Mori H. Lack of the carboxyl terminal sequence of tau in ghost tangle of Alzheimer's disease. Brain Res. 601 (1993) 164-172
39. Watanabe A., Takio K., and Ihara Y. Deamidation and isoaspartate formation in smeared tau in paired helical filaments. J. Biol. Chem. 274 (1999) 7368-7378
40. Arai T., Ikeda K., Akiyama H., Tsuchiya K., Iritani S., Ishiguro K., Yagishita S., Oda T., Odawara T., and Iseki E. Different immunoreactivities of the microtubule-binding region of tau and its molecular basis in brains from patients with Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol. (Berl.) 105 (2003) 489-498
41. Hu J.H., Zhang H., Wagey R., Krieger C., and Pelech S.L. Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord. J. Neurochem. 85 (2003) 432-442
42. Bendotti C., Atzori C., Piva R., Tortarolo M., Strong M.J., Debiasi S., and Migheli A. Activated p38MAPK is a novel component of the intracellular inclusions found in human amyotrophic lateral sclerosis and mutant SOD1 transgenic mice. J. Neuropathol. Exp. Neurol. 63 (2004) 113-119
43. Noda K., Katayama S., Watanabe C., Yamamura Y., and Nakamura S. Gallyas- and tau-positive glial structures in motor neuron disease with dementia. Clin. Neuropathol. 18 (1999) 218-225
44. Forno L.S., Langston J.W., Herrick M.K., Wilson J.D., and Murayama S. Ubiquitin-positive neuronal and tau 2-positive glial inclusions in frontotemporal dementia of motor neuron type. Acta Neuropathol. (Berl.) 103 (2002) 599-606
45. Yang W., Sopper M.M., Leystra-Lanz C., and Strong M.J. Microtubule-associated tau protein positive neuronal and glial inclusions in ALS. Neurology 61 (2003) 1766-1773
46. Kakita A., Oyanagi K., Nagai H., and Takahashi H. Eosinophilic intranuclear inclusions in the hippocampal pyramidal neurons of a patient with amyotrophic lateral sclerosis. Acta Neuropathol. (Berl.) 93 (1997) 532-536
47. Seilhean D., Takahashi J., El Hachimi K.H., Fujigasaki H., Lebre A.-S., Biancalana V., Dürr A., Salachas F., Hogenhuis J., de Thé H., Hauw J.-J., Meininger V., Brice A., and Duyckaerts C. Amyotrophic lateral sclerosis with neuronal intranuclear protein inclusions. Acta Neuropathol. (Berl.) 108 (2004) 81-87
48. Hudson A.J. Amyotrophic lateral sclerosis and its association with dementia, parkinsonism and other neurological disorders: a review. Brain 104 (1981) 217-247
49. Portet F., Cadihac C., Touchon J., and Camu W. Cognitive impairment in motor neuron disease with bulbar onset. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2 (2001) 23-29
50. Lomen-Hoerth C., Anderson T., and Miller B. The overlap of amyotrophic lateral sclerosis and frontotemporal dementia. Neurology 59 (2002) 1077-1079
51. Schreiber H., Gaigalat T., Wiedemuth-Catrinescu U., Graf M., Utter I., Muche R., and Ludolph A.C. Cognitive function in bulbar- and spinal-onset amyotrophic lateral sclerosis. A longitudinal study in 52 patients. J. Neurol. 252 (2005) 772-781
52. Hosler B.A., Siddique T., Sapp P.C., Sailor W., Huang M.C., Hossain A., Daube J.R., Nance M., Fan C., Kaplan J., Hung W.-Y., McKenna-Yasek D., Haines J.L., Pericak-Vance M.A., Horvitz H.R., and Brown Jr. R.H. Linkage of familial amyotrophic lateral sclerosis with frontotemporal dementia to chromosome 9q21-q22. JAMA 284 (2000) 1664-1669
53. Morita M., Al-Chalabi A., Anderson P.M., Hosler B., Sapp P., Englund E., Mitchell J.E., Habgood J.J., de Belleroche J., Xi J., Jongjaroenprasert W., Horvitz H.R., Gunnarsson L.-G., and Brown Jr. R.H. A locus on chromosome 9p confers susceptibility to ALS and frontotemporal dementia. Neurology 66 (2006) 839-844