Z-Phe-Ala-diazomethylketone (PADK) disrupts and remodels early oligomer states of the Alzheimer disease Aβ42 protein

Journal of Biological Chemistry

Volumn 287, Issue 9, 2012, Pages 6084-6088

  Zheng, Xueyun ^a   Gessel, Megan M ^a   Wisniewski, Meagan L ^b   Viswanathan, Kishore ^c,d   Wright, Dennis L ^c   Bahr, Ben A ^b   Bowers, Michael T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT PEMBROKE   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d Synaptic Dynamics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; AMYLOID DISEASE; ELECTRON MICROSCOPY IMAGES; FIBRIL FORMATION; ION MOBILITY; ION MOBILITY SPECTROMETRY; MASS SPECTRA; OLIGOMERIC STATE; PROTECTIVE EFFECTS; SMALL MOLECULES; THERAPEUTIC STRATEGY; TRANSGENIC MICE;

GLYCOPROTEINS; MASS SPECTROMETRY; MOLECULES; NEURODEGENERATIVE DISEASES; OLIGOMERIZATION; PROTEINS;

OLIGOMERS;

AMYLOID BETA PROTEIN[1-42]; BENZYLOXYCARBONYLPHENYLALANYL DIAZOMETHYL KETONE; MONOMER; N 1040; NOOTROPIC AGENT; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG PROTEIN BINDING; ION MOBILITY SPECTROMETRY; MASS SPECTROMETRY; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOIDOSIS; ANIMALS; DIAZOMETHANE; DIMERIZATION; DISEASE MODELS, ANIMAL; DRUG DESIGN; HUMANS; MASS SPECTROMETRY; MICE; MICROSCOPY, ELECTRON; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY;

MUS MUSCULUS;

EID: 84857483279     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C111.328575     Document Type: Article

References (42)

1. Mattson, M. P. (2004) Pathways toward and away from Alzheimer disease. Nature 430, 631-639
2. Stokin, G. B., Lillo, C., Falzone, T. L., Brusch, R. G., Rockenstein, E., Mount, S. L., Raman, R., Davies, P., Masliah, E., Williams, D. S., and Goldstein, L. S. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer disease. Science 307, 1282-1288 (Pubitemid 40299973)
3. Roychaudhuri, R., Yang, M., Hoshi, M. M., and Teplow, D. B. (2009) Amyloid-β protein assembly and Alzheimer disease. J. Biol. Chem. 284, 4749-4753
4. Billings, L. M., Oddo, S., Green, K. N., McGaugh, J. L., and LaFerla, F. M. (2005) Intraneuronal Aβ causes the onset of early Alzheimer disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688 (Pubitemid 40320703)
5. Klein, W. L., Krafft, G. A., and Finch, C. E. (2001) Targeting small Aβ oligomers: the solution to an Alzheimer disease conundrum? Trends Neurosci. 24, 219-224 (Pubitemid 32204378)
6. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid-β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (Pubitemid 34288854)
7. Kirkitadze, M. D., Bitan, G., and Teplow, D. B. (2002) Paradigm shifts in Alzheimer disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J. Neurosci. Res. 69, 567-577 (Pubitemid 34966869)
8. Ono, K., Condron, M. M., and Teplow, D. B. (2009) Structure-neurotoxicity relationships of amyloid-β protein oligomers. Proc. Natl. Acad. Sci. U.S.A. 106, 14745-14750
9. Bitan, G., Lomakin, A., and Teplow, D. B. (2001) Amyloid-β protein oligomerization: prenucleation interactions revealed by photo-induced crosslinking of unmodified proteins. J. Biol. Chem. 276, 35176-35184
10. Teplow, D. B., Lazo, N. D., Bitan, G., Bernstein, S., Wyttenbach, T., Bowers, M. T., Baumketner, A., Shea, J. E., Urbanc, B., Cruz, L., Borreguero, J., and Stanley, H. E. (2006) Elucidating amyloid-β protein folding and assembly: a multidisciplinary approach. Acc. Chem. Res. 39, 635-645
11. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid-β protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U.S.A. 100, 330-335 (Pubitemid 36078074)
12. Bernstein, S. L., Wyttenbach, T., Baumketner, A., Shea, J. E., Bitan, G., Teplow, D. B., and Bowers, M. T. (2005) Amyloid-β protein: monomer structure and early aggregation states of Aβ42 and its Pro-19 alloform. J. Am. Chem. Soc. 127, 2075-2084 (Pubitemid 40270509)
13. Bernstein, S. L., Dupuis, N. F., Lazo, N. D., Wyttenbach, T., Condron, M. M., Bitan, G., Teplow, D. B., Shea, J. E., Ruotolo, B. T., Robinson, C. V., and Bowers, M. T. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the etiology of Alzheimer disease. Nat. Chem. 1, 326-331
14. Bitan, G., Vollers, S. S., and Teplow, D. B. (2003) Elucidation of primary structure elements controlling early amyloid-β protein oligomerization. J. Biol. Chem. 278, 34882-34889 (Pubitemid 37102247)
15. Lesné, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440, 352-357
16. Bates, K. A., Verdile, G., Li, Q. X., Ames, D., Hudson, P., Masters, C. L., and Martins, R. N. (2009) Clearance mechanisms of Alzheimer amyloid-β peptide: implications for therapeutic design and diagnostic tests. Mol Psychiatry 14, 469-486
17. Stains, C. I., Mondal, K., and Ghosh, I. (2007) Molecules that target β-amyloid. ChemMedChem 2, 1675-1692
18. Necula, M., Kayed, R., Milton, S., and Glabe, C. G. (2007) Small molecule inhibitors of aggregation indicate that amyloid-β oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 282, 10311-10324 (Pubitemid 47093410)
19. Hawkes, C. A., Ng, V., and McLaurin, J. (2009) Small molecule inhibitors of Aβ-aggregation and neurotoxicity. Drug Develop. Res. 70, 111-124
20. Re, F., Airoldi, C., Zona, C., Masserini, M., La Ferla, B., Quattrocchi, N., and Nicotra, F. (2010) β-amyloid aggregation inhibitors: small molecules as candidate drugs for therapy of Alzheimer disease. Curr. Med. Chem. 17, 2990-3006
21. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J., Simmons, M. R., Ambegaokar, S. S., Chen, P. P., Kayed, R., Glabe, C. G., Frautschy, S. A., and Cole, G. M. (2005) Curcumin inhibits formation of amyloid-β oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 280, 5892-5901 (Pubitemid 40280072)
22. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., Engemann, S., Pastore, A., and Wanker, E. E. (2008) EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566 (Pubitemid 351799141)
23. De Felice, F. G., Houzel, J. C., Garcia-Abreu, J., Louzada, P. R., Jr., Afonso, R. C., Meirelles, M. N., Lent, R., Neto, V. M., and Ferreira, S. T. (2001) Inhibition of Alzheimer disease β-amyloid aggregation, neurotoxicity, and in vivo deposition by nitrophenols: implications for Alzheimer therapy. FASEB J. 15, 1297-1299
24. Porat, Y., Abramowitz, A., and Gazit, E. (2006) Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug Des. 67, 27-37 (Pubitemid 43881385)
25. Higuchi, M., Iwata, N., and Saido, T. C. (2005) Understanding molecular mechanisms of proteolysis in Alzheimer disease: progress toward therapeutic interventions. Biochim. Biophys. Acta 1751, 60-67 (Pubitemid 41033295)
26. Nixon, R. A., Mathews, P. M., and Cataldo, A. M. (2001) The neuronal endosomal-lysosomal system in Alzheimer disease. J. Alzheimers Dis. 3, 97-107 (Pubitemid 32238256)
27. Bahr, B. A. (2009) Lysosomal modulatory drugs for a broad strategy against protein accumulation disorders. Curr. Alzheimer Res. 6, 438-445
28. Mueller-Steiner, S., Zhou, Y., Arai, H., Roberson, E. D., Sun, B., Chen, J., Wang, X., Yu, G., Esposito, L., Mucke, L., and Gan, L. (2006) Antiamyloidogenic and neuroprotective functions of cathepsin B: implications for Alzheimer disease. Neuron 51, 703-714 (Pubitemid 44374903)
29. Butler, D., Hwang, J., Estick, C., Nishiyama, A., Kumar, S. S., Baveghems, C., Young-Oxendine, H. B., Wisniewski, M. L., Charalambides, A., and Bahr, B. A. (2011) Protective effects of positive lysosomal modulation in Alzheimer disease transgenic mouse models. PLoS ONE 6, e20501
30. Bahr, B. A., Wisniewski, M. L., and Butler, D. (2012) Rejuvenation Res., in press
31. Wyttenbach, T., and Bowers, M. T. (2003) Gas-phase conformations: The ion mobility/ion chromatography method. Top. Curr. Chem. 225, 207-232
32. Dupuis, N. F., Wu, C., Shea, J. E., and Bowers, M. T. (2009) Human islet amyloid polypeptide monomers form ordered β-hairpins: a possible direct amyloidogenic precursor. J. Am. Chem. Soc. 131, 18283-18292
33. Grabenauer, M., Wyttenbach, T., Sanghera, N., Slade, S. E., Pinheiro, T. J., Scrivens, J. H., and Bowers, M. T. (2010) Conformational stability of Syrian hamster prion protein PrP(90-231). J. Am. Chem. Soc. 132, 8816-8818
34. Grabenauer, M., Wu, C., Soto, P., Shea, J. E., and Bowers, M. T. (2010) Oligomers of the prion protein fragment 106-126 are likely assembled from β-hairpins in solution, and methionine oxidation inhibits assembly without altering the peptide's monomeric conformation. J. Am. Chem. Soc. 132, 532-539
35. Baumketner, A., Bernstein, S. L., Wyttenbach, T., Bitan, G., Teplow, D. B., Bowers, M. T., and Shea, J. E. (2006) Amyloid-β protein monomer structure: a computational and experimental study. Protein Sci. 15, 420-428
36. Dupuis, N. F., Wu, C., Shea, J. E., and Bowers, M. T. (2011) The amyloid formation mechanism in human IAPP: dimers have β-strand monomer-monomer interfaces. J. Am. Chem. Soc. 133, 7240-7243
37. Murray, M. M., Bernstein, S. L., Nyugen, V., Condron, M. M., Teplow, D. B., and Bowers, M. T. (2009) Amyloid-β protein: Aβ40 inhibits Aβ42 oligomerization. J. Am. Chem. Soc. 131, 6316-6317
38. Bleiholder, C., Dupuis, N. F., Wyttenbach, T., and Bowers, M. T. (2011) Ion mobility mass spectrometry reveals a conformational conversion from random assembly to β-sheet in amyloid fibril formation. Nat. Chem. 3, 172-177
39. Lomakin, A., Chung, D. S., Benedek, G. B., Kirschner, D. A., and Teplow, D. B. (1996) On the nucleation and growth of amyloid-β protein fibrils: detection of nuclei and quantitation of rate constants. Proc. Natl. Acad. Sci. U.S.A. 93, 1125-1129 (Pubitemid 26054370)
40. Wyttenbach, T., Kemper, P. R., and Bowers, M. T. (2001) Design of a new electrospray ion mobility mass spectrometer. Int. J. Mass Spectrom. 212, 13-23
41. Yang, C. N., Shiao, Y. J., Shie, F. S., Guo, B. S., Chen, P. H., Cho, C. Y., Chen, Y. J., Huang, F. L., and Tsay, H. J. (2011) Mechanism mediating oligomeric Aβ clearance by naive primary microglia. Neurobiol. Dis. 42, 221-230
42. Convertino, M., Vitalis, A., and Caflisch, A. (2011) Disordered binding of small molecules to Aβ12-28. J. Biol. Chem. 286, 41578-41588