Alzheimer's amyloid-β oligomers rescue cellular prion protein induced tau reduction via the Fyn pathway

ACS Chemical Neuroscience

Volumn 4, Issue 9, 2013, Pages 1287-1296

  Chen, Rong Jie ^a,b   Chang, Wei Wei ^b   Lin, Yu Chun ^b   Cheng, Pei Lin ^c   Chen, Yun Ru ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

Alzheimer's disease; amyloid ; Fyn; oligomers; PrPC; tau

Indexed keywords

AMYLOID BETA PROTEIN; PRION PROTEIN; PROTEIN KINASE FYN; TAU PROTEIN; UO 126;

ALLELE; ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BUTADIENES; CELL LINE, TUMOR; DOWN-REGULATION; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MUTATION, MISSENSE; NITRILES; PEPTIDE FRAGMENTS; POINT MUTATION; PROTO-ONCOGENE PROTEINS C-FYN; PRPC PROTEINS; PYRIMIDINES; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 84884371831     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn400085q     Document Type: Article

References (42)

1. Lesne, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-beta protein assembly in the brain impairs memory Nature 440 (7082) 352-35
2. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14 (8) 837-842
3. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8 (2) 101-112
4. Morris, M., Maeda, S., Vossel, K., and Mucke, L. (2011) The many faces of tau Neuron 70 (3) 410-426
5. Avila, J., Lucas, J. J., Perez, M., and Hernandez, F. (2004) Role of tau protein in both physiological and pathological conditions Physiol. Rev. 84 (2) 361-384
6. 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 beta-induced deficits in an Alzheimer's disease mouse model Science 316 (5825) 750-754
7. Vossel, K. A., Zhang, K., Brodbeck, J., Daub, A. C., Sharma, P., Finkbeiner, S., Cui, B., and Mucke, L. (2010) Tau reduction prevents Abeta-induced defects in axonal transport Science 330 (6001) 198
8. Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., and Strittmatter, S. M. (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers Nature 457 (7233) 1128-1132
9. Takahashi, R. H., Tobiume, M., Sato, Y., Sata, T., Gouras, G. K., and Takahashi, H. (2011) Accumulation of cellular prion protein within dystrophic neurites of amyloid plaques in the Alzheimer's disease brain Neuropathology 31 (3) 208-214
10. Ferrer, I., Blanco, R., Carmona, M., Puig, B., Ribera, R., Rey, M. J., and Ribalta, T. (2001) Prion protein expression in senile plaques in Alzheimer's disease Acta Neuropathol. 101 (1) 49-56
11. Dermaut, B., Croes, E. A., Rademakers, R., Van den Broeck, M., Cruts, M., Hofman, A., van Duijn, C. M., and Van Broeckhoven, C. (2003) PRNP Val129 homozygosity increases risk for early-onset Alzheimer's disease Ann. Neurol. 53 (3) 409-412
12. Riemenschneider, M., Klopp, N., Xiang, W., Wagenpfeil, S., Vollmert, C., Muller, U., Forstl, H., Illig, T., Kretzschmar, H., and Kurz, A. (2004) Prion protein codon 129 polymorphism and risk of Alzheimer disease Neurology 63 (2) 364-366
13. Chen, S., Yadav, S. P., and Surewicz, W. K. (2010) Interaction between human prion protein and amyloid-beta (Abeta) oligomers: Role of N-terminal residues J. Biol. Chem. 285 (34) 26377-26383
14. Balducci, C., Beeg, M., Stravalaci, M., Bastone, A., Sclip, A., Biasini, E., Tapella, L., Colombo, L., Manzoni, C., Borsello, T., Chiesa, R., Gobbi, M., Salmona, M., and Forloni, G. (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein Proc. Natl. Acad. Sci. U. S. A. 107 (5) 2295-2300
15. Bate, C. and Williams, A. (2011) Amyloid-{beta}-induced synapse damage is mediated via cross-linkage of the cellular prion protein J. Biol. Chem. 286 (44) 37955-37963
16. Chung, E., Ji, Y., Sun, Y., Kascsak, R. J., Kascsak, R. B., Mehta, P. D., Strittmatter, S. M., and Wisniewski, T. (2010) Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse BMC Neurosci. 11 130
17. Barry, A. E., Klyubin, I., Mc Donald, J. M., Mably, A. J., Farrell, M. A., Scott, M., Walsh, D. M., and Rowan, M. J. (2011) Alzheimer's disease brain-derived amyloid-beta-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein J. Neurosci. 31 (20) 7259-7263
18. Freir, D. B., Nicoll, A. J., Klyubin, I., Panico, S., Mc Donald, J. M., Risse, E., Asante, E. A., Farrow, M. A., Sessions, R. B., Saibil, H. R., Clarke, A. R., Rowan, M. J., Walsh, D. M., and Collinge, J. (2011) Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites Nat. Commun. 2, 336
19. Resenberger, U. K., Harmeier, A., Woerner, A. C., Goodman, J. L., Muller, V., Krishnan, R., Vabulas, R. M., Kretzschmar, H. A., Lindquist, S., Hartl, F. U., Multhaup, G., Winklhofer, K. F., and Tatzelt, J. (2011) The cellular prion protein mediates neurotoxic signalling of beta-sheet-rich conformers independent of prion replication EMBO J. 30 (10) 2057-2070
20. Um, J. W., Nygaard, H. B., Heiss, J. K., Kostylev, M. A., Stagi, M., Vortmeyer, A., Wisniewski, T., Gunther, E. C., and Strittmatter, S. M. (2012) Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons Nat. Neurosci. 15 (9) 1227-1235
21. Kessels, H. W., Nguyen, L. N., Nabavi, S., and Malinow, R. (2010) The prion protein as a receptor for amyloid-beta Nature 466 (7308) E3-E4
22. E4-E5.
23. Calella, A. M., Farinelli, M., Nuvolone, M., Mirante, O., Moos, R., Falsig, J., Mansuy, I. M., and Aguzzi, A. (2010) Prion protein and Abeta-related synaptic toxicity impairment EMBO Mol. Med. 2 (8) 306-314
24. Cisse, M., Sanchez, P. E., Kim, D. H., Ho, K., Yu, G. Q., and Mucke, L. (2011) Ablation of cellular prion protein does not ameliorate abnormal neural network activity or cognitive dysfunction in the J20 line of human amyloid precursor protein transgenic mice J. Neurosci. 31 (29) 10427-10431
25. Larson, M. E. and Lesne, S. E. (2012) Soluble Abeta oligomer production and toxicity J. Neurochem. 120 (Suppl 1) 125-139
26. Benilova, I. and De Strooper, B. (2010) Prion protein in Alzheimer's pathogenesis: a hot and controversial issue EMBO Mol. Med. 2 (8) 289-290
27. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways Proc. Natl. Acad. Sci. U. S. A. 100 (1) 330-335
28. Larson, M., Sherman, M. A., Amar, F., Nuvolone, M., Schneider, J. A., Bennett, D. A., Aguzzi, A., and Lesne, S. E. (2012) The complex PrPc-Fyn couples human oligomeric Abeta with pathological tau changes in Alzheimer's disease J. Neurosci. 32 (47) 16857-16871
29. Santuccione, A., Sytnyk, V., Leshchyns'ka, I., and Schachner, M. (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth J. Cell Biol. 169 (2) 341-354
30. Pantera, B., Bini, C., Cirri, P., Paoli, P., Camici, G., Manao, G., and Caselli, A. (2009) PrPc activation induces neurite outgrowth and differentiation in PC12 cells: Role for caveolin-1 in the signal transduction pathway J. Neurochem. 110 (1) 194-207
31. Williamson, R., Usardi, A., Hanger, D. P., and Anderton, B. H. (2008) Membrane-bound beta-amyloid oligomers are recruited into lipid rafts by a fyn-dependent mechanism FASEB J. 22 (5) 1552-1559
32. Caetano, F. A., Beraldo, F. H., Hajj, G. N., Guimaraes, A. L., Jurgensen, S., Wasilewska-Sampaio, A. P., Hirata, P. H., Souza, I., Machado, C. F., Wong, D. Y., De Felice, F. G., Ferreira, S. T., Prado, V. F., Rylett, R. J., Martins, V. R., and Prado, M. A. (2011) Amyloid-beta oligomers increase the localization of prion protein at the cell surface J. Neurochem. 117 (3) 538-553
33. Strom, A., Wang, G. S., Picketts, D. J., Reimer, R., Stuke, A. W., and Scott, F. W. (2011) Cellular prion protein localizes to the nucleus of endocrine and neuronal cells and interacts with structural chromatin components Eur J Cell Biol 90 (5) 414-419
34. Rushworth, J. V., Griffiths, H. H., Watt, N. T., and Hooper, N. M. (2013) Prion protein-mediated toxicity of amyloid-beta oligomers requires lipid rafts and the transmembrane LRP1 J. Biol. Chem. 288 (13) 8935-8951
35. Yang, K., Belrose, J., Trepanier, C. H., Lei, G., Jackson, M. F., and MacDonald, J. F. (2011) Fyn, a potential target for Alzheimer's disease J. Alzheimer's Dis. 27 (2) 243-252
36. Ittner, L. M., Ke, Y. D., Delerue, F., Bi, M., Gladbach, A., van Eersel, J., Wolfing, H., Chieng, B. C., Christie, M. J., Napier, I. A., Eckert, A., Staufenbiel, M., Hardeman, E., and Gotz, J. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models Cell 142 (3) 387-397
37. Andreadis, A., Wagner, B. K., Broderick, J. A., and Kosik, K. S. (1996) A tau promoter region without neuronal specificity J. Neurochem. 66 (6) 2257-2263
38. Heicklen-Klein, A. and Ginzburg, I. (2000) Tau promoter confers neuronal specificity and binds Sp1 and AP-2 J. Neurochem. 75 (4) 1408-1418
39. Xu, K. and Shu, H. K. (2007) EGFR activation results in enhanced cyclooxygenase-2 expression through p38 mitogen-activated protein kinase-dependent activation of the Sp1/Sp3 transcription factors in human gliomas Cancer Res. 67 (13) 6121-6129
40. D'Addario, M., Arora, P. D., and McCulloch, C. A. (2006) Role of p38 in stress activation of Sp1 Gene 379, 51-61
41. Yang, S. H., Sharrocks, A. D., and Whitmarsh, A. J. (2013) MAP kinase signalling cascades and transcriptional regulation Gene 513 (1) 1-13
42. Dahlgren, K. N., Manelli, A. M., Stine, W. B., Jr., Baker, L. K., Krafft, G. A., and LaDu, M. J. (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability J. Biol. Chem. 277 (35) 32046-32053