What is the pathological significance of tau oligomers?

Biochemical Society Transactions

Volumn 40, Issue 4, 2012, Pages 693-697

  Cowan, Catherine M ^a   Quraishe, Shmma ^a   Mudher, Amritpal ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Alzheimer's disease; Filament; Oligomer; Tangle; Tau; Tauopathy

Indexed keywords

OLIGOMER; TAU PROTEIN;

CONFERENCE PAPER; DROSOPHILA; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RODENT; TAUOPATHY;

ALZHEIMER DISEASE; ANIMALS; HUMANS; PHOSPHORYLATION; TAU PROTEINS; TAUOPATHIES;

RODENTIA;

EID: 84864378643     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120135     Document Type: Conference Paper

References (45)

1. Goedert, M. and Spillantini, M.G. (2011) Pathogenesis of the tauopathies. J. Mol. Neurosci. 45, 425-431
2. Roberson, E.D., Scearce-Levie, K., Palop, J.J., Yan, F., Cheng, I.H., Wu, T., Gerstein, H., Yu, G.Q. and Mucke, L. (2007) Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science 316, 750-754 (Pubitemid 46717684)
3. Shipton, O.A., Leitz, J.R., Dworzak, J., Acton, C.E., Tunbridge, E.M., Denk, F., Dawson, H.N., Vitek, M.P., Wade-Martins, R., Paulsen, O. and Vargas-Caballero, M. (2011) Tau protein is required for amyloid β-induced impairment of hippocampal long-term potentiation. J. Neurosci. 31, 1688-1692
4. Morris, M., Maeda, S., Vossel, K. and Mucke, L. (2011) The many faces of tau. Neuron 70, 410-426
5. Crowther, R.A. and Goedert, M. (2000) Abnormal tau-containing filaments in neurodegenerative diseases. J. Struct. Biol. 130, 271-279
6. Tolnay, M. and Clavaguera, F. (2004) Argyrophilic grain disease: a late-onset dementia with distinctive features among tauopathies. Neuropathology 24, 269-283 (Pubitemid 39664748)
7. Kopke, E., Tung, Y.C., Shaikh, S., Alonso, A.C., Iqbal, K. and Grundke-Iqbal, I. (1993) Microtubule-associated protein tau: abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268, 24374-24384 (Pubitemid 23335430)
8. Santacruz, K., Lewis, J., Spires, T., Paulson, J., Kotilinek, L., Ingelsson, M., Guimaraes, A., DeTure, M., Ramsden, M., McGowan, E. et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481 (Pubitemid 40994688)
9. Wittmann, C.W., Wszolek, M.F., Shulman, J.M., Salvaterra, P.M., Lewis, J., Hutton, M. and Feany, M.B. (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293, 711-714 (Pubitemid 32728676)
10. Williams, D.W., Tyrer, M. and Shepherd, D. (2000) Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J. Comp. Neurol. 428, 630-640
11. Ali, Y.O., Ruan, K. and Zhai, R.G. (2012) NMNAT suppresses tau-induced neurodegeneration by promoting clearance of hyperphosphorylated tau oligomers in a Drosophila model of tauopathy. Hum. Mol. Genet. 21, 237-250
12. Spires-Jones, T.L., Kopeikina, K.J., Koffie, R.M., de Calignon, A. and Hyman, B.T. (2011) Are tangles as toxic as they look? J. Mol. Neurosci. 45, 438-444
13. Van der Jeugd, A., Hochgrafe, K., Ahmed, T., Decker, J.M., Sydow, A., Hofmann, A., Wu, D., Messing, L., Balschun, D., D'Hooge, R. and Mandelkow, E.M. (2012) Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human Tau. Acta Neuropathol. 123, 787-805
14. Maeda, S., Sahara, N., Saito, Y., Murayama, M., Yoshiike, Y., Kim, H., Miyasaka, T., Murayama, S., Ikai, A. and Takashima, A. (2007) Granular tau oligomers as intermediates of tau filaments. Biochemistry 46, 3856-3861 (Pubitemid 46493485)
15. Maeda, S., Sahara, N., Saito, Y., Murayama, S., Ikai, A. and Takashima, A. (2006) Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer's disease. Neurosci. Res. 54, 197-201 (Pubitemid 43276078)
16. Berger, Z., Roder, H., Hanna, A., Carlson, A., Rangachari, V., Yue, M., Wszolek, Z., Ashe, K., Knight, J., Dickson, D. et al. (2007) Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J. Neurosci. 27, 3650-3662 (Pubitemid 46557687)
17. 231 precedes the structural change detected by Alz-50 antibody in Alzheimer's disease. J. Alzheimer's Dis. 8, 29-41
18. Goedert, M., Jakes, R., Spillantini, M.G., Hasegawa, M., Smith, M.J. and Crowther, R.A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383, 550-553 (Pubitemid 26346185)
19. Cowan, C.M., Shepherd, D. and Mudher, A. (2010) Insights from Drosophila models of Alzheimer's disease. Biochem. Soc. Trans. 38, 988-992
20. Alonso, A., Zaidi, T., Novak, M., Grundke-Iqbal, I. and Iqbal, K. (2001) Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. U.S.A. 98, 6923-6928 (Pubitemid 32538318)
21. Cowan, C.M., Sealey, M.A., Quraishe, S., Targett, M.T., Marcellus, K., Allan, D. and Mudher, A. (2011) Modelling tauopathies in Drosophila: insights from the fruit fly. Int. J. Alzheimer's Dis. 2011, 598157
22. Mudher, A., Shepherd, D., Newman, T.A., Mildren, P., Jukes, J.P., Squire, A., Mears, A., Drummond, J.A., Berg, S., MacKay, D. et al. (2004) GSK-3β inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiatry 9, 522-530 (Pubitemid 38903508)
23. Cowan, C.M., Bossing, T., Page, A., Shepherd, D. and Mudher, A. (2010) Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo. Acta Neuropathol. 120, 593-604
24. Kosmidis, S., Grammenoudi, S., Papanikolopoulou, K. and Skoulakis, E.M. (2010) Differential effects of Tau on the integrity and function of neurons essential for learning in Drosophila. J. Neurosci. 30, 464-477
25. Nishimura, I., Yang, Y. and Lu, B. (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116, 671-682 (Pubitemid 38326726)
26. Kimura, T., Yamashita, S., Fukuda, T., Park, J.M., Murayama, M., Mizoroki, T., Yoshiike, Y., Sahara, N. and Takashima, A. (2007) Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J. 26, 5143-5152 (Pubitemid 350261280)
27. Patterson, K.R., Remmers, C., Fu, Y., Brooker, S., Kanaan, N.M., Vana, L., Ward, S., Reyes, J.F., Philibert, K., Glucksman, M.J. and Binder, L.I. (2011) Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease. J. Biol. Chem. 286, 23063-23076
28. Makrides, V., Shen, T.E., Bhatia, R., Smith, B.L., Thimm, J., Lal, R. and Feinstein, S.C. (2003) Microtubule-dependent oligomerization of tau: implications for physiological tau function and tauopathies. J. Biol. Chem. 278, 33298-33304 (Pubitemid 37055780)
29. Lasagna-Reeves, C.A., Castillo-Carranza, D.L., Guerrero-Muoz, M.J., Jackson, G.R. and Kayed, R. (2010) Preparation and characterization of neurotoxic tau oligomers. Biochemistry 49, 10039-10041
30. Sahara, N., Maeda, S., Murayama, M., Suzuki, T., Dohmae, N., Yen, S.H. and Takashima, A. (2007) Assembly of two distinct dimers and higher-order oligomers from full-length tau. Eur. J. Neurosci. 25, 3020-3029 (Pubitemid 46888808)
31. Patterson, K.R., Ward, S.M., Combs, B., Voss, K., Kanaan, N.M., Morfini, G., Brady, S.T., Gamblin, T.C. and Binder, L.I. (2011) Heat shock protein 70 prevents both tau aggregation and the inhibitory effects of preexisting tau aggregates on fast axonal transport. Biochemistry 50, 10300-10310
32. Lasagna-Reeves, C.A., Castillo-Carranza, D.L., Sengupta, U., Clos, A.L., Jackson, G.R. and Kayed, R. (2011) Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Mol. Neurodegener. 6, 39
33. Lasagna-Reeves, C.A., Castillo-Carranza, D.L., Sengupta, U., Sarmiento, J., Troncoso, J., Jackson, G.R. and Kayed, R. (2012) Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J. 26, 1946-1959
34. Henkins, K.M., Sokolow, S., Miller, C.A., Vinters, H.V., Poon, W., Cornwell, L.B., Saing, T. and Gylys, K.H. (2012) Extensive p-tau pathology and SDS-stable p-tau oligomers in Alzheimer's cortical synapses. Brain Pathol., doi:10.1111/j.1750-3639.2012.00598.x
35. Sahara, N., Maeda, S., Yoshiike, Y., Mizoroki, T., Yamashita, S., Murayama, M., Park, J.M., Saito, Y., Murayama, S. and Takashima, A. (2007) Molecular chaperone-mediated tau protein metabolism counteracts the formation of granular tau oligomers in human brain. J. Neurosci. Res. 85, 3098-3108 (Pubitemid 350057365)
36. Nagy, Z., Esiri, M.M., Jobst, K.A., Morris, J.H., King, E.M., McDonald, B., Litchfield, S., Smith, A., Barnetson, L. and Smith, A.D. (1995) Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria. Dementia 6, 21-31
37. Goedert, M., Crowther, R.A. and Spillantini, M.G. (1998) Tau mutations cause frontotemporal dementias. Neuron 21, 955-958 (Pubitemid 29018067)
38. Spires, T.L., Orne, J.D., SantaCruz, K., Pitstick, R., Carlson, G.A., Ashe, K.H. and Hyman, B.T. (2006) Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol. 168, 1598-1607
39. Le Corre, S., Klafki, H.W., Plesnila, N., Hubinger, G., Obermeier, A., Sahagun, H., Monse, B., Seneci, P., Lewis, J., Eriksen, J. et al. (2006) An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 103, 9673-9678 (Pubitemid 43955883)
40. Chee, F.C., Mudher, A., Cuttle, M.F., Newman, T.A., MacKay, D., Lovestone, S. and Shepherd, D. (2005) Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Neurobiol. Dis. 20, 918-928 (Pubitemid 41619367)
41. Mershin, A., Pavlopoulos, E., Fitch, O., Braden, B.C., Nanopoulos, D.V. and Skoulakis, E.M. (2004) Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn. Mem. 11, 277-287 (Pubitemid 38697893)
42. Holmes, C., Boche, D., Wilkinson, D., Yadegarfar, G., Hopkins, V., Bayer, A., Jones, R.W., Bullock, R., Love, S., Neal, J.W. et al. (2008) Long-term effects of Aβ42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372, 216-223 (Pubitemid 351978111)
43. Kazemi-Esfarjani, P. and Benzer, S. (2000) Genetic suppression of polyglutamine toxicity in Drosophila. Science 287, 1837-1840 (Pubitemid 30143971)
44. Goldberg, M.S. and Lansbury, Jr, P.T. (2000) Is there a cause-and-effect relationship between α-synuclein fibrillization and Parkinson's disease? Nat. Cell Biol. 2, E115-E119
45. Auluck, P.K. and Bonini, N.M. (2002) Pharmacological prevention of Parkinson disease in Drosophila. Nat. Med. 8, 1185-1186 (Pubitemid 35373534)