Hydrogen/deuterium exchange-protected oligomers populated during β fibril formation correlate with neuronal cell death

ACS Chemical Biology

Volumn 9, Issue 11, 2014, Pages 2678-2685

  Serra Vidal, Bernat ^a   Pujadas, Lluís ^b   Rossi, Daniela ^b   Soriano, Eduardo ^b,c   Madurga, Sergio ^b   Carulla, Natàlia ^a  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; OLIGOMER; BIOPOLYMER; DEUTERIUM; HYDROGEN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL DEATH; CELL HETEROGENEITY; DEUTERIUM HYDROGEN EXCHANGE; ELECTROSPRAY MASS SPECTROMETRY; FIBER; GEL PERMEATION CHROMATOGRAPHY; MOUSE; NERVE CELL; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; CHEMISTRY; CYTOLOGY; METABOLISM;

AMYLOID BETA-PEPTIDES; BIOPOLYMERS; CELL DEATH; DEUTERIUM; HYDROGEN; NEURONS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84914145237     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500621x     Document Type: Article

References (32)

1. Masters, C. L. and Selkoe, D. J. (2012) Biochemistry of amyloid beta-protein and amyloid deposits in Alzheimer disease Cold Spring Harbor Perspect. Med. 2, a006262
2. Serpell, L. C. (2000) Alzheimers amyloid fibrils: structure and assembly Biochim. Biophys. Acta 1502, 16-30
3. Dickson, D. W., Crystal, H. A., Bevona, C., Honer, W., Vincent, I., and Davies, P. (1995) Correlations of synaptic and pathological markers with cognition of the elderly Neurobiol. Aging 16, 285-298
4. McLean, C. A., Cherny, R. A., Fraser, F. W., Fuller, S. J., Smith, M. J., Beyreuther, K., Bush, A. I., and Masters, C. L. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimers disease Ann. Neurol. 46, 860-866
5. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimers amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112
6. Benilova, I., Karran, E., and De Strooper, B. (2012) The toxic Abeta oligomer and Alzheimers disease: an emperor in need of clothes Nat. Neurosci. 15, 349-357
7. Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L., Wals, P., Zhang, C., Finch, C. E., Krafft, G. A., and Klein, W. L. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
8. Chimon, S., Shaibat, M. A., Jones, C. R., Calero, D. C., Aizezi, B., and Ishii, Y. (2007) Evidence of fibril-like beta-sheet structures in a neurotoxic amyloid intermediate of Alzheimers beta-amyloid Nat. Struct. Mol. Biol. 14, 1157-1164
9. Yu, L., Edalji, R., Harlan, J. E., Holzman, T. F., Lopez, A. P., Labkovsky, B., Hillen, H., Barghorn, S., Ebert, U., Richardson, P. L., Miesbauer, L., Solomon, L., Bartley, D., Walter, K., Johnson, R. W., Hajduk, P. J., and Olejniczak, E. T. (2009) Structural characterization of a soluble amyloid beta-peptide oligomer Biochemistry 48, 1870-1877
10. Ahmed, M., Davis, J., Aucoin, D., Sato, T., Ahuja, S., Aimoto, S., Elliott, J. I., Van Nostrand, W. E., and Smith, S. O. (2010) Structural conversion of neurotoxic amyloid-beta(1-42) oligomers to fibrils Nat. Struct. Mol. Biol. 17, 561-567
11. Haupt, C., Leppert, J., Ronicke, R., Meinhardt, J., Yadav, J. K., Ramachandran, R., Ohlenschlager, O., Reymann, K. G., Gorlach, M., and Fandrich, M. (2012) Structural basis of beta-amyloid-dependent synaptic dysfunctions Angew. Chem., Int. Ed. 51, 1576-1579
12. Cohen, S. I., Linse, S., Luheshi, L. M., Hellstrand, E., White, D. A., Rajah, L., Otzen, D. E., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. J. (2013) Proliferation of amyloid-beta42 aggregates occurs through a secondary nucleation mechanism Proc. Natl. Acad. Sci. U.S.A. 110, 9758-9763
13. Wogulis, M., Wright, S., Cunningham, D., Chilcote, T., Powell, K., and Rydel, R. E. (2005) Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death J. Neurosci. 25, 1071-1080
14. Jan, A., Adolfsson, O., Allaman, I., Buccarello, A. L., Magistretti, P. J., Pfeifer, A., Muhs, A., and Lashuel, H. A. (2011) Abeta42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Abeta42 species J. Biol. Chem. 286, 8585-8596
15. 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-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimers disease Nat. Chem. 1, 326-331
16. Narayan, P., Orte, A., Clarke, R. W., Bolognesi, B., Hook, S., Ganzinger, K. A., Meehan, S., Wilson, M. R., Dobson, C. M., and Klenerman, D. (2012) The extracellular chaperone clusterin sequesters oligomeric forms of the amyloid-beta(1-40) peptide Nat. Struct. Mol. Biol. 19, 79-83
17. Konermann, L., Vahidi, S., and Sowole, M. A. (2014) Mass spectrometry methods for studying structure and dynamics of biological macromolecules Anal. Chem. 86, 213-232
18. Kheterpal, I., Lashuel, H. A., Hartley, D. M., Walz, T., Lansbury, P. T., Jr., and Wetzel, R. (2003) Abeta protofibrils possess a stable core structure resistant to hydrogen exchange Biochemistry 42, 14092-14098
19. Pan, J., Han, J., Borchers, C. H., and Konermann, L. (2011) Conformer-specific hydrogen exchange analysis of Abeta(1-42) oligomers by top-down electron capture dissociation mass spectrometry Anal. Chem. 83, 5386-5393
20. Pan, J., Han, J., Borchers, C. H., and Konermann, L. (2012) Structure and dynamics of small soluble Abeta(1-40) oligomers studied by top-down hydrogen exchange mass spectrometry Biochemistry 51, 3694-3703
21. Mysling, S., Betzer, C., Jensen, P. H., and Jorgensen, T. J. D. (2013) Characterizing the dynamics of alpha-synuclein oligomers using hydrogen/deuterium exchange monitored by mass spectrometry Biochemistry 52, 9097-9103
22. Paslawski, W., Mysling, S., Thomsen, K., Jorgensen, T. J. D., and Otzen, D. E. (2014) Co-existence of two different alpha-synuclein oligomers with different core structures determined by hydrogen/deuterium exchange mass spectrometry Angew. Chem., Int. Ed. 53, 7560-7563
23. Zhang, Y., Rempel, D. L., Zhang, J., Sharma, A. K., Mirica, L. M., and Gross, M. L. (2013) Pulsed hydrogen-deuterium exchange mass spectrometry probes conformational changes in amyloid beta (Abeta) peptide aggregation Proc. Natl. Acad. Sci. U.S.A. 110, 14604-14609
24. Carulla, N., Zhou, M., Arimon, M., Gairi, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2009) Experimental characterization of disordered and ordered aggregates populated during the process of amyloid fibril formation Proc. Natl. Acad. Sci. U.S.A. 106, 7828-7833
25. Jan, A., Hartley, D. M., and Lashuel, H. A. (2010) Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimers disease research Nat. Protoc. 5, 1186-1209
26. Reinke, A. A. and Gestwicki, J. E. (2011) Insight into amyloid structure using chemical probes Chem. Biol. Drug Des. 77, 399-411
27. Sanchez, L., Madurga, S., Pukala, T., Vilaseca, M., Lopez-Iglesias, C., Robinson, C. V., Giralt, E., and Carulla, N. (2011) Abeta40 and Abeta42 amyloid fibrils exhibit distinct molecular recycling properties J. Am. Chem. Soc. 133, 6505-6508
28. Kheterpal, I., Zhou, S., Cook, K. D., and Wetzel, R. (2000) Abeta amyloid fibrils possess a core structure highly resistant to hydrogen exchange Proc. Natl. Acad. Sci. U.S.A. 97, 13597-13601
29. Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimers amyloid-beta(1-42) fibrils Proc. Natl. Acad. Sci. U.S.A. 102, 17342-17347
30. Campioni, S., Mannini, B., Zampagni, M., Pensalfini, A., Parrini, C., Evangelisti, E., Relini, A., Stefani, M., Dobson, C. M., Cecchi, C., and Chiti, F. (2010) A causative link between the structure of aberrant protein oligomers and their toxicity Nat. Chem. Biol. 6, 140-147
31. Serio, T. R., Cashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F., and Lindquist, S. L. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289, 1317-1321
32. Cremades, N., Cohen, S. I., Deas, E., Abramov, A. Y., Chen, A. Y., Orte, A., Sandal, M., Clarke, R. W., Dunne, P., Aprile, F. A., Bertoncini, C. W., Wood, N. W., Knowles, T. P. J., Dobson, C. M., and Klenerman, D. (2012) Direct observation of the interconversion of normal and toxic forms of alpha-synuclein Cell 149, 1048-1059