TDP-43 in ubiquitinated inclusions in the inferior olives in frontotemporal lobar degeneration and in other neurodegenerative diseases: A degenerative process distinct from normal ageing

Acta Neuropathologica

Volumn 118, Issue 3, 2009, Pages 359-369

  Davidson, Yvonne ^a   Amin, Hanan ^a   Kelley, Thomas ^a   Shi, Jing ^a,c   Tian, Jinzhou ^a,c   Kumaran, Ravindran ^d   Lashley, Tammaryn ^d   Lees, Andrew J ^d   DuPlessis, Daniel ^a   Neary, David ^a   Snowden, Julie ^a   Akiyama, Haruhiko ^e   Arai, Tetsuaki ^e   Hasegawa, Masato ^e   Bandopadhyay, Rina ^d   Sikkink, Steve ^b   Pickering Brown, Stuart ^b   Mann, David M A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERNEXIN; NEUROFILAMENT PROTEIN; TAR DNA BINDING PROTEIN; TAU PROTEIN; UBIQUITIN;

ADULT; AGED; AGING; ALZHEIMER DISEASE; ARTICLE; ATROPHY; CELL INCLUSION; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DIFFUSE LEWY BODY DISEASE; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFERIOR OLIVE; MALE; MOTOR NEURON DISEASE; MULTISYSTEM ATROPHY; NERVE DEGENERATION; NEURONAL CYTOPLASMIC INCLUSION; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; TAUOPATHY;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; DEMENTIA; DNA-BINDING PROTEINS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; MALE; MIDDLE AGED; NEURODEGENERATIVE DISEASES; NEURONS; OLIVARY NUCLEUS; UBIQUITIN; UBIQUITINATION;

EID: 68349095164     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-009-0526-z     Document Type: Article

References (47)

1. Amador-Ortiz C, Lin W-L, Ahmed Z, Personett D, Davies P, Duara R, Graff-Radford NR, Hutton ML, Dickson DW (2007) TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease. Ann Neurol 61:435-445
2. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, 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
3. Baker M, Mackenzie IRA, Pickering-Brown SM, Gass J, Rademakers R, Lindholm C, Snowden J, Adamson J, Sadovnick AD, Rollinson S, Cannon A, Dwosh E, Neary D, Melquist S, Richardson A, Dickson D, Eriksen J, Robinson T, Zehr C, Dickey CA, Crook R, McGowan E, Mann D, Boeve B, Feldman H, Hutton M (2006) Mutations in Progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442:916-919
4. Barden H (1970) Relationship of Golgi thiamine pyrophosphatase and lysosomal acid phosphatase to neuromelanin and lipofuscin in cerebral neurones of ageing rhesus monkeys. J Neuropathol Exp Neurol 29:225-240
5. Boeve BF, Baker M, Dickson DW, Parisi JE, Giannini C, Jsephs KA, Hutton M, Pickering-Brown SM, Rademakers R, Tang-Wai D, Jack CR, Kantarci K, Shiung MM, Golde T, Smith GE, Geda YE, Knopman DS, Petersen RC (2006) Frontotemporal dementia and Parkinsonism associated with the IVS1 + 1G → A mutation in progranulin: A clinicopathologic study. Brain 129:3103-3114
6. Brooks B, Miller R, Swash M, Munsat T (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293-299
7. Brun A, Englund E, Gustafson L, Passant U, Mann DMA, Neary D, Snowden JS (1994) Clinical, neuropsychological and neuropathological criteria for fronto-temporal dementia. J Neurol Neurosurg Psychiatry 57:416-418
8. Cairns NJ, Bigio EH, Mackenzie IRA, Neumann M, Lee VM, Hatanpaa KJ, White CL III, Schneider JA, Grinberg LT, Halliday G, Duyckaerts C, Lowe JS, Holm IE, Tolnay M, Okamoto K, Yokoo H, Murayama S, Woulfe J, Munoz DG, Dickson DW, Ince PG, Trojanowski JQ, Mann DMA (2007) Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 114:5-22
9. Cruts M, Gijselinck I, van der Zee J, Engelborghs S, Wils H, Pirici D, Rademakers R, Vandenberghe R, Dermaut B, Martin J-J, van Duijn C, Peeters K, Sciot R, Santens P, De Pooter T, Mattheijssens M, Van den Broeck M, Cujit I, Vennekens K, De Deyn PP, Kumar-Singh S, Van Broeckhoven C (2006) Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442:920-924
10. Davidson Y, Kelley T, Mackenzie IR, Pickering-Brown SM, Du Plessis D, Neary D, Snowden JS, Mann DMA (2007) Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43. Acta Neuropathol 113:521-533
11. Dickson DW, Josephs KA, Amador-Ortiz C (2007) TDP-43 in the differential diagnosis of motor neuron disorders. Acta Neuropathol 114:71-79
12. Dickson DW, Wertin A, Kress Y, Ksiezak-Reding H, Yen S-H (1990) Ubiquitin immunoreactive structures in normal human brains. Lab Invest 63:87-99
13. Forman MS, Farmer J, Johnson JK, Clark CM, Arnold SE, Coslett HB, Chatterjee A, Hurtig HI, Karlawish JH, Rosen HJ, Van Deerlin V, M-Y LeeV, Miller BL, Trojanowski JQ, Grossman M (2006) Frontotemporal dementia: Clinicopathological correlations. Ann Neurol 59:952-962
14. Ii K, Ito H, Tanaka K, Hirano A (1997) Immunocytochemical co-localization of the proteasome in ubiquitinated structures in neurodegenerative diseases and the elderly. J Neuropathol Exp Neurol 56:125-131
15. Josephs KA, Holton JL, Rossor MN, Godbolt AK, Osawa T, Strand K, Khan N, Al-Sarraj S, Revesz T (2004) Frontotemporal lobar degeneration and ubiquitin immunohistochemistry. Neuropathol Appl Neurobiol 30:369-373
16. Josephs KA, Petersen RC, Knopman DS, Boeve BF, Whitwell JL, Duffy JR, Parisi JE, Dickson DW (2006) Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP. Neurology 66:41-48
17. Kato S, Hirano A, Suenaga T, Yen S-H (1990) Ubiquitinated eosinophilic granules in the inferior olivary nucleus. Neuropathol Appl Neurobiol 16:135-139
18. Katsuse O, Dickson DW (2005) Ubiquitin immunohistochemistry of frontotemporal lobar degeneration differentiates cases with and without motor neurone disease. Alzheimer Dis Assoc Disord 19(suppl 1):S37-S43
19. Lasn H, Winblad B, Bogdanovic N (2001) The number of neurons in the inferior olivary nucleus in Alzheimer's disease and normal ageing: A stereological study using the optical fractionator. J Alzheimer's Disease 3:159-168
20. Leigh PN, Anderton BH, Dodson A, Gallo J-M, Swash M, Power DM (1988) Ubiquitin deposits in anterior horn cells in motor neurone disease. Neurosci Lett 93:197-203
21. Lipton AM, White CL III, Bigio EH (2004) Frontotemporal lobar degeneration with motor neuron disease-type inclusions predominates in 76 cases of frontotemporal degeneration. Acta Neuropathol 108:379-385
22. Litvan I, Hauw JJ, Bartko JJ, Lantos PL, Daniel SE, Horoupian DS, McKee A, Dickson D, Bancher C, Tabaton M, Jellinger K, Anderson DW (1996) Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and related disorders. J Neuropath Exp Neurol 55:97-105
23. Lowe JS, Lennox G, Jefferson D, Morrell K, McQuire D, Gray T, Landon M, Doherty FJ, Mayer RJ (1988) A filamentous inclusion body within anterior horn neurones in motor neurone disease detected by immunocytochemical localisation of ubiquitin. Neurosci Lett 94:203-210
24. Mackenzie IRA, Feldman H (2003) The relationship between extramotor ubiquitin-immunoreactive neuronal inclusions and dementia in motor neurone disease. Acta Neuropathol 105:98-102
25. Mackenzie IRA, Feldman HH (2005) Ubiquitin immunohistochemistry suggests classic Motor Neuron Disease, Motor Neuron Disease with dementia and Frontotemporal dementia of the Motor Neuron Disease type represent a clinicopathologic spectrum. J Neuropathol Exp Neurol 64:730-739
26. Mackenzie IRA, Baborie A, Pickering-Brown SM, Du Plessis D, Jaros E, Perry RH, Neary D, Snowden JS, Mann DMA (2006) Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration. Acta Neuropathol 112:539-549
27. Mackenzie IRA, Baker M, Pickering-Brown S, Hsiung G-Y, Lindholm C, Dwosh E, Gass J, Cannon A, Rademakers R, Hutton M, Feldman H (2006) The neuropathology of frontotemporal lobar degeneration caused by mutations in the progranulin gene. Brain 129:3081-3090
28. Mackenzie IRA, Shi J, Shaw CL, Du Pleassis D, Neary D, Snowden D, Mann DMA (2006) dementia lacking distinctive histology (DLDH) revisited. Acta Neuropathol 112:551-559
29. Mackenzie IRA, Neumann M, Bigio E, Cairns NJ, Alafuzoff I, Krill J, Kovacs GG, Ghetti B, Halliday G, Holm IR, Ince PG, Kamphourst W, Revesz T, Rozemuller AJM, Kumar-Singh S, Akiyama H, Baborie A, Spina S, Dickson DW, Trojanowski JQ, Mann DMA (2009) Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: Consensus recommendations. Acta Neuropathol 117:15-18
30. Mann DMA, Sinclair KGA (1978) The quantitative assessment of lipofuscin pigment, cytoplasmic RNA and nucleolar volume in senile dementia. Neuropathol Appl Neurobiol 4:129-135
31. Mann DMA, Yates PO (1974) Ageing in the human nervous system. I The lipofuscin content of nerve cells. Brain 97:481-488
32. Mann DMA, Yates PO, Stamp JE (1978) Relationship of lipofuscin pigment to ageing in the human nervous system. J Neurol Sci 35:83-93
33. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergeron C, Burns A, Miller BL, Lovestone S, Collerton D, Jansen EN, Ballard C, de Vos RA, Wilcock GK, Jellinger KA, Perry RH (1996) Consensus guidelines for the clinical and pathological diagnosis of dementia with Lewy bodies (DLB): Report of the consortium on DLB international workshop. Neurology 47:1113-1124
34. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, Belle G, Berg L (1991) The consortium to establish a registry for Alzheimer's disease. Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41:479-486
35. Moatamed F (1966) Cell frequencies in the human inferior olivary nuclear complex. J Comp Neurol 128:109-116
36. Monagle RD, Brody H (1974) Effects of age upon the main nucleus of the inferior olive in humans. J Comp Neurol 155:61-66
37. Mott RT, Dickson DW, Trojanowski JQ, Zhukareva V, Lee VM, Forman M, Van Deerlin V, Ervin JF, Wang DS, Schmechel DE, Hulette CM (2005) Neuropathologic, biochemical, and molecular characterization of the frontotemporal dementias. J Neuropathol Exp Neurol 64:420-428
38. Mukherjee O, Pastor P, Cairns NJ, Chakraverty S, Kauwe JSK, Shears S, Behrens MJ, Budde J, Hinrichs AL, Norton J, Levich D, Taylor-Reinwald L, Gitcho M, Tu P-H, Grinberg LT, Liscic RM, Armendariz J, Morris JC, Goate AM (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
39. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF (1998) Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology 51:1546-1554
40. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuk T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar H, Trojanowski JQ, Lee VM (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130-133
41. Pickering-Brown SM, Baker M, Gass J, Boeve BF, Loy CT, Brooks WS, Mackenzie IR, Martins RN, Kwok JB, Halliday GM, Kril JJ, Schofield PR, Mann DM, Hutton M (2006) Mutations in progranulin explain atypical phenotypes with variants in MAPT. Brain 129:3124-3126
42. Sandoz P, Meier-Ruge W (1977) Age-related loss of nerve cells from the human inferior olives and unchanged volume of its grey matter. IRCS Med Sci 5:376
43. Shi J, Shaw CL, Richardson AMT, Bailey K, Tian J, Varma AR, Neary D, Snowden JS, Mann DMA (2005) Histopathological changes underlying frontotemporal lobar degeneration with clinicopathological correlation. Acta Neuropathol 110:501-512
44. Snowden JS, Pickering-Brown SM, Mackenzie IR, Richardson AMT, Varma A, Neary D, Mann DMA (2006) Progranulin gene mutations associated with frontotemporal dementia and progressive aphasia. Brain 129:3091-3102
45. Taniguchi S, McDonagh AM, Pickering-Brown SM, Umeda Y, Iwatsubo T, Hasegawa M, Mann DMA (2004) The neuropathology of frontotemporal lobar degeneration with respect to the cytological and biochemical characteristics of tau protein. Neuropathol Appl Neurobiol 30:1-18
46. Trojanowski JQ, Revesz T, Neuropathology Working Group on MS (2007) Proposed neuropathological criteria for the post mortem diagnosis of multiple system atrophy. Neuropathol Appl Neurobiol 33:615-620
47. Woulfe J, Kertesz A, Munoz D (2001) Frontotemporal dementia with ubiquitinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 102:94-102