TDP-43 prions

Cold Spring Harbor Perspectives in Medicine

Volumn 8, Issue 3, 2018, Pages

  Nonaka, Takashi ^a   Hasegawa, Masato ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN AGGREGATE; TAR DNA BINDING PROTEIN; DNA BINDING PROTEIN; PRION PROTEIN; TDP-43 PROTEIN, HUMAN;

ARTICLE; BRAIN DISEASE; CELL TRANSFER; HUMAN; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRION; PROTEIN AGGREGATION; PROTEIN TRANSPORT; TDP 43 PROTEINOPATHY; ANIMAL; BRAIN; CHEMISTRY; DEGENERATIVE DISEASE; DISEASE MODEL; GENETICS; METABOLISM; NERVE CELL; PATHOLOGY; PROTEINOSIS; PROTEOSTASIS DEFICIENCY;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; PRION PROTEINS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEOSTASIS DEFICIENCIES;

EID: 85043584354     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a024463     Document Type: Article

References (61)

1. Amador-Ortiz C, Lin WL, 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, et al. 2006. TDP-43 is a component of ubiquitin-positive taunegative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351: 602–611.
3. Arai T, Mackenzie IR, 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.
4. Ayala YM, De Conti L, Avendaño-Vázquez SE, Dhir A, Romano M, D’Ambrogio A, Tollervey J, Ule J, Baralle M, Buratti E, et al. 2011. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J 30: 277–288.
5. Bigio EH, Wu JY, Deng HX, Bit-Ivan EN, Mao Q, Ganti R, Peterson M, Siddique N, Geula C, Siddique T, et al. 2013. Inclusions in frontotemporal lobar degeneration with TDP-43 proteinopathy (FTLD-TDP) and amyotrophic lateral sclerosis (ALS), but not FTLD with FUS proteinopathy (FTLD-FUS), have properties of amyloid. Acta Neuropathol 125: 463–465.
6. Braak H, Braak E. 1991. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239–259.
7. Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. 2003. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24: 197– 211.
8. Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, Suh E, Van Deerlin VM, Wood EM, Baek Y, et al. 2013. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 74: 20–38.
9. Buratti E, Baralle FE. 2008. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front Biosci 13: 867–878.
10. Carlomagno Y, Zhang Y, Davis M, Lin WL, Cook C, Dunmore J, Tay W, Menkosky K, Cao X, Petrucelli L, et al. 2014. Casein kinase II induced polymerization of soluble TDP-43 into filaments is inhibited by heat shock proteins. PLoS ONE 9: e90452.
11. Chiang PM, Ling J, Jeong YH, Price DL, Aja SM, Wong PC. 2010. Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc Natl Acad Sci 107: 16320–16324.
12. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, et al. 2009. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11: 909–913.
13. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF. 1996. Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature 383: 685–690.
14. de Calignon A, Polydoro M, Suárez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, et al. 2012. Propagation of tau pathology in a model of early Alzheimer’s disease. Neuron 73: 685–697.
15. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, Spencer B, Masliah E, Lee SJ. 2009. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of a-synuclein. Proc Natl Acad Sci 106: 13010–13015.
16. Fevrier B, Vilette D, Archer F, Loew D, Faigle W, Vidal M, Laude H, Raposo G. 2004. Cells release prions in association with exosomes. Proc Natl Acad Sci 101: 9683–9688.
17. Freeman SH, Spires-Jones T, Hyman BT, Growdon JH, Frosch MP. 2008. TAR-DNA binding protein 43 in Pick disease. J Neuropathol Exp Neurol 67: 62–67.
18. Frost B, Jacks RL, Diamond MI. 2009. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284: 12845–12852.
19. Fujishiro H, Uchikado H, Arai T, Hasegawa M, Akiyama H, Yokota O, Tsuchiya K, Togo T, Iseki E, Hirayasu Y. 2009. Accumulation of phosphorylated TDP-43 in brains of patients with argyrophilic grain disease. Acta Neuropathol 117: 151–158.
20. Furukawa Y, Kaneko K, Watanabe S, Yamanaka K, Nukina N. 2011. A seeding reaction recapitulates intracellular formation of Sarkosyl-insoluble transactivation response element (TAR) DNA-binding protein-43 inclusions. J Biol Chem 286: 18664–18672.
21. Geser F, Winton MJ, Kwong LK, Xu Y, Xie SX, Igaz LM, Garruto RM, Perl DP, Galasko D, Lee VM, et al. 2008. Pathological TDP-43 in parkinsonism–dementia complex and amyotrophic lateral sclerosis of Guam. Acta Neuropathol 115: 133–145.
22. Goedert M, Clavaguera F, Tolnay M. 2010. The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33: 317–325.
23. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT, Chenouard N, de Chaumont F, Martino A, Enninga J, et al. 2009. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 11: 328–336.
24. Guo L, Shorter J. 2016. Biology and pathobiology of TDP-43 and emergent therapeutic strategies. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a024554.
25. Guo W, Chen Y, Zhou X, Kar A, Ray P, Chen X, Rao EJ, Yang M, Ye H, Zhu L, et al. 2011. An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Nat Struct Mol Biol 18: 822–830.
26. Hasegawa M, Arai T, Akiyama H, Nonaka T, Mori H, Hashimoto T, Yamazaki M, Oyanagi K. 2007. TDP-43 is deposited in the Guam parkinsonism–dementia complex brains. Brain 130: 1386–1394.
27. Hasegawa M, Arai T, Nonaka T, Kametani F, Yoshida M, Hashizume Y, Beach TG, Buratti E, Baralle F, Morita M, et al. 2008. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann Neurol 64: 60–70.
28. Hasegawa M, Nonaka T, Tsuji H, Tamaoka A, Yamashita M, Kametani F, Yoshida M, Arai T, Akiyama H. 2011. Molecular dissection of TDP-43 proteinopathies. J Mol Neurosci 45: 480–485.
29. Higashi S, Iseki E, Yamamoto R, Minegishi M, Hino H, Fujisawa K, Togo T, Katsuse O, Uchikado H, Furukawa Y, et al. 2007. Concurrence of TDP-43, tau and a-synuclein pathology in brains of Alzheimer’s disease and dementia with Lewy bodies. Brain Res 1184: 284–294.
30. Igaz LM, Kwong LK, Chen-Plotkin A, Winton MJ, Unger TL, Xu Y, Neumann M, Trojanowski JQ, Lee VM. 2009. Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 284: 8516–8524.
31. Inukai Y, Nonaka T, Arai T, Yoshida M, Hashizume Y, Beach TG, Buratti E, Baralle FE, Akiyama H, Hisanaga S, et al. 2008. Abnormal phosphorylation of Ser409/410 of TDP-43 in FTLD-U and ALS. FEBS Lett 582: 2899–2904.
32. Johnson BS, McCaffery JM, Lindquist S, Gitler AD. 2008. A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc Natl Acad Sci 105: 6439–6444.
33. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW. 2008. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson’s disease. Nat Med 14: 504–506.
34. Kraemer BC, Schuck T, Wheeler JM, Robinson LC, Trojanowski JQ, Lee VM, Schellenberg GD. 2010. Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol 119: 409– 419.
35. Lagier-Tourenne C, Polymenidou M, Cleveland DW. 2010. TDP-43 and FUS/TLS: Emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 19: R46– R64.
36. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Björklund A, et al. 2008. Lewy bodies in grafted neurons in subjects with Parkinson’s disease suggest host-to-graft disease propagation. Nat Med 14: 501–503.
37. Lin WL, Dickson DW. 2008. Ultrastructural localization of TDP-43 in filamentous neuronal inclusions in various neurodegenerative diseases. Acta Neuropathol 116: 205– 213.
38. Ling SC, Polymenidou M, Cleveland DW. 2013. Converging mechanisms in ALS and FTD: Disrupted RNA and protein homeostasis. Neuron 79: 416–438.
39. Liu L, Drouet V, Wu JW, Witter MP, Small SA, Clelland C, Duff K. 2012. Trans-synaptic spread of tau pathology in vivo. PLoS ONE 7: e31302.
40. Luk KC, Song C, O’Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM. 2009. Exogenous a-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci 106: 20051–20056.
41. Luk KC, Kehm V, Carroll J, Zhang B, O’Brien P, Trojanowski JQ, Lee VM. 2012a. Pathological a-synuclein transmission initiates Parkinson-like neurodegeneration in non-transgenic mice. Science 338: 949–953.
42. Luk KC, Kehm VM, Zhang B, O’Brien P, Trojanowski JQ, Lee VM. 2012b. Intracerebral inoculation of pathological a-synuclein initiates a rapidly progressive neurodegenerative a-synucleinopathy in mice. J Exp Med 209: 975–986.
43. Lukavsky PJ, Daujotyte D, Tollervey JR, Ule J, Stuani C, Buratti E, Baralle FE, Damberger FF, Allain FH. 2013. Molecular basis of UG-rich RNA recognition by the human splicing factor TDP-43. Nat Struct Mol Biol 20: 1443–1449.
44. Mackenzie IR, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, Perry RH, Trojanowski JQ, Mann DM, Lee VM. 2011. A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 122: 111–113.
45. Masuda-Suzukake M, Nonaka T, Hosokawa M, Oikawa T, Arai T, Akiyama H, Mann DM, Hasegawa M. 2013. Prion-like spreading of pathological a-synuclein in brain. Brain 136: 1128–1138.
46. Masuda-Suzukake M, Nonaka T, Hosokawa M, Kubo M, Shimozawa A, Akiyama H, Hasegawa M. 2014. Pathological a-synuclein propagates through neural networks. Acta Neuropathol Commun 2: 88.
47. Nakashima-Yasuda H, Uryu K, Robinson J, Xie SX, Hurtig H, Duda JE, Arnold SE, Siderowf A, Grossman M, Leverenz JB, et al. 2007. Co-morbidity of TDP-43 proteinopathy in Lewy body related diseases. Acta Neuropathol 114: 221–229.
48. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, et al. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130–133.
49. Nonaka T, Kametani F, Arai T, Akiyama H, Hasegawa M. 2009. Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Hum Mol Genet 18: 3353–3364.
50. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M. 2010. Seeded aggregation and toxicity of a-synuclein and tau: Cellular models of neurodegenerative diseases. J Biol Chem 285: 34885–34898.
51. Nonaka T, Masuda-Suzukake M, Arai T, Hasegawa Y, Akatsu H, Obi T, Yoshida M, Murayama S, Mann DM, Akiyama H, et al. 2013. Prion-like properties of pathological TDP-43 aggregates from diseased brains. Cell Rep 4: 124–134.
52. Nonaka T, Watanabe S, Masuda M, Hasegawa M. 2016. U.S. Patent PCT/JP2006/324786.
53. Pesiridis GS, Lee VM, Trojanowski JQ. 2009. Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis. Hum Mol Genet 18: R156–R162.
54. Sephton CF, Good SK, Atkin S, Dewey CM, Mayer P III, Herz J, Yu G. 2010. TDP-43 is a developmentally regulated protein essential for early embryonic development. J Biol Chem 285: 6826–6834.
55. Tatom JB, Wang DB, Dayton RD, Skalli O, Hutton ML, Dickson DW, Klein RL. 2009. Mimicking aspects of frontotemporal lobar degeneration and Lou Gehrig’s disease in rats via TDP-43 overexpression. Mol Ther 17: 607–613.
56. Tsuji H, Arai T, Kametani F, Nonaka T, Yamashita M, Suzukake M, Hosokawa M, Yoshida M, Hatsuta H, Takao M, et al. 2012. Molecular analysis and biochemical classification of TDP-43 proteinopathy. Brain 135: 3380–3391.
57. Uryu K, Nakashima-Yasuda H, Forman MS, Kwong LK, Clark CM, Grossman M, Miller BL, Kretzschmar HA, Lee VM, Trojanowski JQ, et al. 2008. Concomitant TAR-DNA-binding protein 43 pathology is present in Alzheimer disease and corticobasal degeneration but not in other tauopathies. J Neuropathol Exp Neurol 67: 555–564.
58. Wang HY, Wang IF, Bose J, Shen CK. 2004. Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 83: 130–139.
59. Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, Cuijt I, Smits V, Ceuterick-de Groote C, Van Broeckhoven C, Kumar-Singh S. 2010. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci 107: 3858–3863.
60. Wu LS, Cheng WC, Hou SC, Yan YT, Jiang ST, Shen CK. 2010. TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 48: 56–62.
61. Yamashita M, Nonaka T, Hirai S, Miwa A, Okado H, Arai T, Hosokawa M, Akiyama H, Hasegawa M. 2014. Distinct pathways leading to TDP-43-induced cellular dysfunctions. Hum Mol Genet 23: 4345–4356.