Nuclear carrier and RNA-binding proteins in frontotemporal lobar degeneration associated with fused in sarcoma (FUS) pathological changes

Neuropathology and Applied Neurobiology

Volumn 39, Issue 2, 2013, Pages 157-165

  Davidson, Y S ^a   Robinson, A C ^a   Hu, Q ^a   Mishra, M ^f   Baborie, A ^c   Jaros, E ^d,e   Perry, R H ^e   Cairns, N J ^g   Richardson, A ^a,b   Gerhard, A ^a,b   Neary, D ^a,b   Snowden, J S ^a,b   Bigio, E H ^f   Mann, D M A ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b SALFORD ROYAL NHS FOUNDATION TRUST   (United Kingdom)

^c WALTON CENTRE FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^d ROYAL VICTORIA INFIRMARY   (United Kingdom)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f NORTHWESTERN UNIVERSITY   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ewing's sarcoma protein; Frontotemporal lobar degeneration; Fused in sarcoma; TATA binding protein associated factor 15; TDP 43; Transportins

Indexed keywords

CARRIER PROTEIN; EWING SARCOMA PROTEIN; FUSED IN SARCOMA PROTEIN; RNA BINDING PROTEIN; TATA BINDING PROTEIN ASSOCIATED FACTOR; TATA BINDING PROTEIN ASSOCIATED FACTOR 15; TRANSPORTIN 1; TRANSPORTIN 2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; FUS PROTEIN, HUMAN; KARYOPHERIN BETA; PROTEIN TDP-43; RNA BINDING PROTEIN EWS; TAF15 PROTEIN, HUMAN; TNPO1 PROTEIN, HUMAN; TNPO2 PROTEIN, HUMAN;

ADULT; ARTICLE; CELL INCLUSION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; METABOLISM; MIDDLE AGED;

ADULT; BETA KARYOPHERINS; DNA-BINDING PROTEINS; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; HUMANS; INCLUSION BODIES; MALE; MIDDLE AGED; RNA-BINDING PROTEIN EWS; RNA-BINDING PROTEIN FUS; TATA-BINDING PROTEIN ASSOCIATED FACTORS;

EID: 84873052814     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2012.01274.x     Document Type: Article

References (33)

1. 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. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1998; 51: 1546-54
2. Neary D, Snowden JS, Mann DMA, Northen B, Goulding PJ, MacDermott N. Frontal lobe dementia and motor neurone disease. J Neurol Neurosurg Psychiatry 1990; 53: 23-32
3. Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, Murphy J, Shoesmith C, Rosenfeld J, Leigh PN, Bruijn L, Ince P, Figlewicz D. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2009; 10: 131-46
4. Cairns NJ, Bigio EH, Mackenzie IRA, Neumann M, Lee VMY, Hatanpaa KJ, White CL III, Schneider JA, Tenenholz Grinberg L, 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. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007; 114: 2-22
5. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006; 351: 602-11
6. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar H, Trojanowski JQ, Lee VM. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-3
7. Mackenzie IRA, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, Neary D, Snowden JS, Mann DMA. Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype. Acta Neuropathol 2006; 112: 539-49
8. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micsenyi M, Truax A, Bruce J, Grossman M, Trojanowski JQ, Lee VM. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 2006; 169: 1343-52
9. Baborie A, Griffiths TD, Jaros E, Richardson A, Ferrari R, Moreno J, Momeni P, McKeith IG, Burn DJ, Duplessis D, Pal P, Rollinson S, Pickering-Brown SM, Thompson JC, Neary D, Snowden JS, Perry R, Mann DMA. Pathological correlates of frontotemporal lobar degeneration in the elderly. Acta Neuropathol 2011; 121: 365-71
10. Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, Mackenzie IRA. A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 2009; 132: 2922-31
11. Seelaar H, Klijnsma KY, de Koning I, van der Lugt A, Zheng Chiu W, Azmani A, Rozemuller AJM, Van Swieten JC. Frequency of ubiquitin and FUS-positive, TDP-43-negative frontotemporal lobar degeneration. J Neurol 2010; 257: 747-53
12. Snowden JS, Hu Q, Rollinson S, Halliwell N, Robinson A, Davidson YS, Momeni P, Baborie A, Griffiths TD, Jaros E, Perry RH, Richardson A, Neary D, Pickering-Brown SM, Mann DMA. The most common form of FTLD-FUS (aFTLD-U) is associated with a distinct clinical form of frontotemporal dementia, but not related to mutations in the FUS gene. Acta Neuropathol 2011; 122: 99-110
13. Urwin H, Josephs KA, Rohrer JD, Mackenzie IR, Neumann M, Authier A, Seelaar H, Van Swieten JC, Brown JM, Johannsen P, Nielsen JE, Holm IE, The FReJA Consortium, Dickson DW, Rademakers R, Graff-Radford NR, Parisi JE, Petersen RC, Hatanpaa KJ, White Iii CL, Weiner MF, Geser F, Van Deerlin VM, Trojanowski JQ, Miller BL, Seeley WW, van der Zee J, Kumar-Singh S, Engelborghs S, De Deyn PP, Van Broeckhoven C, Bigio EH, Deng HX, Halliday GM, Kril JJ, Munoz DG, Mann DM, Pickering-Brown SM, Doodeman V, Adamson G, Ghazi-Noori S, Fisher EM, Holton JL, Revesz T, Rossor MN, Collinge J, Mead S, Isaacs AM. FUS pathology defines the majority of tau-and TDP-43-negative frontotemporal lobar degeneration. Acta Neuropathol 2010; 120: 33-41
14. Neumann M, Roeber S, Kretzchmar HA, Rademakers R, Baker M, Mackenzie IRA. Abundant FUS-immunoreactive pathology in neuronal intermediate filament inclusion disease. Acta Neuropathol 2009; 118: 605-16
15. Munoz DG, Neumann M, Kusaka H, Yokota O, Ishihara K, Terada S, Kuroda S, Mackenzie IRA. FUS pathology in basophilic inclusion body disease. Acta Neuropathol 2009; 118: 617-27
16. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, Kril J, Kovacs GG, Ghetti B, Halliday G, Holm IE, Ince PG, Kamphorst W, Revesz T, Rozemuller AJM, Kumar-Singh S, Akiyama H, Baborie A, Spina S, Dickson DW, Trojanowski JQ, Mann DMA. Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations: an update. Acta Neuropathol 2010; 119: 1-4
17. Aman P, Panagopoulos I, Larssen C, Fioretos T, Mencinger M, Toresson H, Hoglund M, Forster A, Rabbitts TH, Ron D, Mandahl N, Mitelman F. Expression pattern of the human sarcoma-associated genes FUS and EWS and the genomic structure of FUS. Genomics 1996; 37: 1-8
18. Yang S, Warraich ST, Nicholson GA, Blair IP. Fused in sarcoma/translocated in liposarcoma: a multifunctional DNA/RNA binding protein. Int J Biochem Cell Biol 2010; 42: 1408-11
19. Andersson MK, Stahlberg A, Arvidsson Y, Olofsson A, Semb H, Stenman G, Nilsson O, Aman P. The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type specific expression patterns and involvement in cell spreading and stress response. BMC Cell Biol 2008; 9: 37
20. Zinszner H, Sok J, Immanuel D, Yin Y, Ron D. TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling. J Cell Sci 1997; 110: 1741-50
21. Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, Than ME, Mackenzie IR, Capell A, Scmid B, Neumann M, Haass C. ALS-associated fused in sarcoma (FUS) mutations disrupttransportin-mediated nuclear import. EMBO J 2010; 29: 2841-57
22. Brellstaff J, Lashley T, Holton JL, Lees AJ, Rossor MN, Bandopadhyay R, Revesz T. Transportin 1: a marker for FTLD-FUS. Acta Neuropathol 2011; 122: 591-600
23. Neumann M, Bentmann E, Dormann D, Jawaid A, DeJesus-Hernandez M, Ansorge O, Roeber S, Kretsscmar HA, Munoz DG, Kusaka H, Yokota O, Ang L-C, Bilbao J, Rademakers R, Haass C, Mackenzie IRA. FET proteins TAF15 and EWS are selective markers that distinguish FTLD with FUS pathology from amyotrophic lateral sclerosis with FUS mutations. Brain 2011; 134: 2595-609
24. Cairns NJ, Grossman M, Arnold SE, Burn DJ, Jaros E, Perry RH, Duyckaerts C, Stankoff B, Pillon B, Skullerud K, Cruz-Sanchez FF, Bigio EH, Mackenzie IR, Gearing M, Juncos JL, Glass JD, Yokoo H, Nakazato Y, Mosaheb S, Thorpe JR, Uryu K, Lee VM, Trojanowski JQ. Clinical and neuropathologic variation in neuronal intermediate filament inclusion disease. Neurology 2004; 63: 1376-84
25. Malnou CE, Salem T, Brockly F, Wodrich H, Piechaczyk M, Jariel-Encontre I. Heterodimerization with Ju8n family members regulates c-fos nucleocytoplasmic traffic. J Biol Chem 2007; 282: 31046-59
26. Kodiha M, Banski P, Cheong H-W, Stochaj U. Dissection of the molecular mechanisms that control the nuclear accumulation of transport factors importin-α and CAS in stressed cells. Cell Mol Life Sci 2008; 65: 1756-67
27. Kovar H. Dr. Jekyll and Mr. Hyde: the two faces of the FUS/EWS/TAF15 protein family. Sarcoma 2011; 2011: 837474. E-pub
28. Law WJ, Cann KL, Hicks GG. TLS, EWS and TAF15: a model for transcriptional integration of gene expression. Brief Funct Genomic Proteomic 2006; 5: 8-14
29. Parlich S, Zakaryan RP, Gehring H. Identification of proteins interacting with protein arginine methyltransferase 8; the Ewing sarcoma (EWS) protein binds independently of its methylation state. Proteins 2008; 72: 1125-37
30. Jobert L, Argentini M, Tora L. PRMT1 mediated methylation of TAF15 is required for its positive gene regulatory function. Exp Cell Res 2009; 315: 1273-86
31. Kwiatkowski TJ, Bosco DA, LeClerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T, Valdmanis P, Rouleau GA, Hosler BA, Cortelli P, de Jong PA, Yoshinaga Y, Haines JL, Pericak-Vance MA, Yan J, Ticozzi N, Siddique T, Kenna-Yasek D, Sapp PC, Horvitz HR, Landers JE, Brown RH Jr. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009; 323: 1205-8
32. Vance C, Roegelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, Ganesalingam J, Williams KL, Tripathi V, Al-Saraj S, Al-Chalabi A, Leigh PN, Blair IP, Nicholson G, de Belleroche J, Gallo JM, Miller CC, Shaw CE. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009; 323: 1208-11
33. Van Langenhove T, van der Zee J, Sleegers K, Engelborghs S, Vandenberghe R, Gijselinck I, Van den Broeck M, Mattheijssens M, Peeters K, De Deyn PP, Cruts M, Van Broeckhoven CM. Genetic contribution of FUS to frontotemporal lobar degeneration. Neurology 2010; 74: 366-71