Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-β

Nature

Volumn 485, Issue 7400, 2012, Pages 651-655

  Nussbaum, Justin M ^a   Schilling, Stephan ^b   Cynis, Holger ^b   Silva, Antonia ^a   Swanson, Eric ^a   Wangsanut, Tanaporn ^a   Tayler, Kaycie ^a   Wiltgen, Brian ^a   Hatami, Asa ^c   Rönicke, Raik ^d   Reymann, Klaus ^d   Hutter Paier, Birgit ^e   Alexandru, Anca ^f   Jagla, Wolfgang ^f   Graubner, Sigrid ^f   Glabe, Charles G ^c   Demuth, Hans Ulrich ^b,f   Bloom, George S ^a,g  

^a UNIVERSITY OF VIRGINIA   (United States)

^b PROBIODRUG AG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e JSW Life Sciences GmbH   (Austria)

^f Ingenium Pharmaceuticals GmbH   (Germany)

^g UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; MONOMER; OLIGOMER; PRION PROTEIN; PYROGLUTAMIC ACID; TAU PROTEIN; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); GLUTAMIC ACID; MUTANT PROTEIN; PEPTIDE FRAGMENT;

HISTOPATHOLOGY; NERVOUS SYSTEM DISORDER; RODENT; TOXICITY;

ALZHEIMER DISEASE; ARTICLE; CELL VIABILITY; CYTOTOXICITY; FREEZE DRYING; GEL CHROMATOGRAPHY; GLIOSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL CULTURE; OLIGOMERIZATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; WESTERN BLOTTING; ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; MOUSE; PRION; TRANSGENIC MOUSE;

MUS;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; GLUTAMIC ACID; HUMANS; MICE; MICE, TRANSGENIC; MUTANT PROTEINS; PEPTIDE FRAGMENTS; PRIONS; TAU PROTEINS;

EID: 84863762839     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11060     Document Type: Article

References (30)

1. Gandy, S. et al. Days to criterion as an indicator of toxicity associated with human Alzheimer amyloid-b oligomers. Ann. Neurol. 68, 220-230 (2010).
2. Walsh, D. M. & Selkoe, D. J. Ab oligomers-a decade of discovery. J. Neurochem. 101, 1172-1184 (2007).
3. Rapoport, M., Dawson, H. N., Binder, L. I., Vitek, M. P.&Ferreira, A. Tau is essential to b-amyloid-induced neurotoxicity. Proc.Natl Acad. Sci.USA 99,6364-6369(2002).
4. King, M. E. et al. Tau-dependent microtubule disassembly initiated by pre-fibrillar b-amyloid. J. Cell Biol. 175, 541-546 (2006).
5. Roberson, E. D. et al. Reducing endogenous tau ameliorates amyloid b-induced deficits in an Alzheimer's disease mouse model. Science 316, 750-754 (2007).
6. Jin, M. et al. Soluble amyloid b-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl Acad. Sci. USA 108, 5819-5824 (2011).
7. Mori, H., Takio, K., Ogawara,M.&Selkoe, D. J.Mass spectrometry of purifiedamyloid b protein in Alzheimer's disease. J. Biol. Chem. 267, 17082-17086 (1992).
8. Saido, T. C. et al.Dominantand differential depositionof distinct b-amyloidpeptide species, AbN3(pE), in senile plaques. Neuron 14, 457-466 (1995).
9. Jawhar, S., Wirths, O.&Bayer, T. A. Pyroglutamateamyloid-b (Ab): a hatchetman in Alzheimer disease. J. Biol. Chem. 286, 38825-38832 (2011).
10. Schilling, S. et al. Glutaminyl cyclase inhibition attenuates pyroglutamate Ab and Alzheimer's disease-like pathology. Nature Med. 14, 1106-1111 (2008).
11. Tabaton, M. et al. Soluble amyloid b-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid. Biochem. Biophys. Res. Commun. 200, 1598-1603 (1994).
12. Russo, C. et al. Pyroglutamate-modifiedamyloid b-peptides-AbN3(pE)- strongly affect cultured neuron and astrocyte survival. J. Neurochem. 82, 1480-1489 (2002).
13. Schilling, S. et al. On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45, 12393-12399 (2006).
14. Schlenzig, D. et al. Pyroglutamate formation influences solubility and amyloidogenicity of amyloid peptides. Biochemistry 48, 7072-7078 (2009).
15. Levine, H. III. Thioflavine T interaction with synthetic Alzheimer's disease b-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci. 2, 404-410 (1993).
16. Wang, X. M. et al. A new microcellular cytotoxicity test based on calceinAMrelease. Hum. Immunol. 37, 264-270 (1993).
17. Scudiero, D. A. et al. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res. 48, 4827-4833 (1988).
18. Alexandru, A. et al. Selective hippocampal neurodegeneration in transgenic mice expressing small amounts of truncated Ab is induced by pyroglutamate-Ab formation. J. Neurosci. 31, 12790-12801 (2011).
19. Tucker, K. L., Meyer, M. & Barde, Y. A. Neurotrophins are required for nerve growth during development. Nature Neurosci. 4, 29-37 (2001).
20. Rockenstein, E., Mallory, M., Mante, M., Sisk, A. & Masliaha, E. Early formation of matureamyloid-b protein deposits in amutantAPP transgenicmodel depends on levels of Ab1-42. J. Neurosci. Res. 66, 573-582 (2001).
21. Jawhar, S. et al. Overexpression of glutaminyl cyclase, the enzyme responsible for pyroglutamate Ab formation, induces behavioral deficits, and glutaminyl cyclase knock-out rescues the behavioral phenotype in 5XFAD mice. J. Biol. Chem. 286, 4454-4460 (2011).
22. Tanghe, A. et al.Pathological hallmarks, clinical parallels, and value for drug testing in Alzheimer's disease of the APP[V717I] London transgenic mouse model. Int. J. Alzheimers Dis. 2010 (2010).
23. Wilcock, D. M. et al. Progression of amyloid pathology to Alzheimer's disease pathology in anamyloid precursor protein transgenicmouse model by removal of nitric oxide synthase 2. J. Neurosci. 28, 1537-1545 (2008).
24. He, W.& Barrow, C. J. The Ab 3-pyroglutamyl and 11-pyroglutamyl peptides found in senile plaque have greater b-sheet forming and aggregation propensities in vitro than full-length Ab. Biochemistry 38, 10871-10877 (1999).
25. Wirths, O. et al. Intraneuronal pyroglutamate-Ab 3-42 triggers neurodegeneration and lethal neurological deficits in a transgenic mouse model. Acta Neuropathol. 118, 487-496 (2009).
26. Gü ntert, A., Dobeli, H. & Bohrmann, B. High sensitivity analysis of amyloid-b peptide composition in amyloid deposits from human and PS2APP mouse brain. Neuroscience 143, 461-475 (2006).
27. Piccini, A. et al. b-Amyloid is different in normal aging and in Alzheimer disease. J. Biol. Chem. 280, 34186-34192 (2005).
28. Hartlage-Rübsamen, M. et al. Glutaminyl cyclase contributes to the formation of focal and diffuse pyroglutamate (pGlu)-Ab deposits in hippocampus via distinct cellular mechanisms. Acta Neuropathol. 121, 705-719 (2011).
29. Vossel, K. A. et al. Tau reduction prevents Ab-induced defects in axonal transport. Science 330, 198 (2010).
30. Wilcox, K. C., Lacor, P. N., Pitt, J. & Klein, W. L. Ab oligomer-induced synapse degeneration in Alzheimer's disease. Cell. Mol. Neurobiol. 31, 939-948 (2011).