Structural characterization of a soluble amyloid β-peptide oligomer

Biochemistry

Volumn 48, Issue 9, 2009, Pages 1870-1877

  Yu, Liping ^a,c   Edalji, Rohinton ^a   Harlan, John E ^a   Holzman, Thomas F ^a,d   Lopez, Ana Pereda ^a   Labkovsky, Boris ^a   Hillen, Heinz ^b   Barghorn, Stefan ^b   Ebert, Ulrich ^b   Richardson, Paul L ^a   Miesbauer, Laura ^a   Solomon, Larry ^a   Bartley, Diane ^a   Walter, Karl ^a   Johnson, Robert W ^a   Hajduk, Philip J ^a   Olejniczak, Edward T ^a  

^a ABBOTT LABORATORIES   (United States)

^b ABBOTT GMBH AND CO KG   (Germany)

^c UNIVERSITY OF IOWA   (United States)

^d Nanosphere Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALIPHATIC HYDROCARBONS; ALZHEIMER'S; ALZHEIMER'S DISEASE; DISEASE PROGRESSIONS; DISULFIDE BONDS; IN-VITRO; INSOLUBLE FIBRILS; NEURODEGENERATIVE DISORDERS; NMR DATUM; PEPTIDE OLIGOMERS; SHEET STRUCTURES; STRUCTURAL CHARACTERIZATIONS; STRUCTURAL DATUM;

FATTY ACIDS; GLYCOPROTEINS; HYDROCARBONS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERS; PEPTIDES; POLYMERS; SOAPS (DETERGENTS);

AMINES;

AMYLOID BETA PROTEIN; GLOBULOMER; OLIGOMER; PREGLOBULOMER; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; BINDING AFFINITY; CONFORMATION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME LINKED IMMUNOSORBENT ASSAY; NERVE CONDUCTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; STRUCTURE ANALYSIS; SYNAPSE;

AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PROTEIN; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY;

EID: 64549140676     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802046n     Document Type: Article

References (40)

1. Mattson, M. P. (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639.
2. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
3. Klein, W. L., Krafft, G. A., and Finch, C. E. (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224.
4. 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.
5. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., and Katzman, R. (1991) Physical basis of cognitive alterations in alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
6. Kuo, Y.-M., Emmerling, M. R., Vigo-Pelfrey, C., Kasunic, T. C., Kirkpatrick, J. B., Murdoch, G. H., Ball, M. J., and Roher, A. E. (1996) Water-soluble Abeta(N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 271, 4077-4081.
7. Lue, L.-F., Kuo, Y.-M., Roher, A. E., Brachova, L., Shen, Y., Sue, L., Beach, T., Kurth, J. H., Rydel, R. E., and Rogers, J. (1999) Soluble amyloid {beta} peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862.
8. 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 neurode-generation in Alzheimer's disease. Ann. Neurol. 46, 860-866.
9. Arispe, N., Rojas, E., and Pollard, H. (1993) Alzheimer disease amyloid {beta} protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. U.S.A. 90, 567-571.
10. Lashuel, H. A., Hartley, D., Petre, B. M., Walz, T., and Lansbury, P. T. (2002) Neurodegenerative disease: Amyloid pores from pathogenic mutations. Nature 418, 291.
11. 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 Abeta 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453.
12. (a) Barghorn, S., Nimmrich, V., Striebinger, A., Krantz, C., Keller, P., Janson, B., Bahr, M., Schmidt, M., Bitner, R. S., Harlan, J., Barlow, E., Ebert, U., and Hillen, H. (2005) Globular amyloid beta-peptide oligomers - a homogenous and stable neu-ropathological protein in Alzheimer's disease. J. Neurochem. 95, 834-847.
13. (b) Barghorn, S., Striebinger, A., Giaisi, S., Gaalen, M., Bespalov, A., Labkobsky, B., Ebert, U., and Hillen, H. (2008) in International Conference on Alzheimer's Disease 2008, Chicago, IL.
14. Olofsson, A., Sauer-Eriksson, A. E., and Ohman, A. (2006) The solvent protection of Alzheimer amyloid-{beta}-(1-42) fibrils as determined by solution NMR spectroscopy. J. Biol. Chem. 281, 477-483.
15. Petkova, A. T., Yau, W.-M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer's amyloid fibrils. Biochemistry 45, 498-512.
16. Makin, O. S., and Serpell, L. C. (2005) Structures for amyloid fibrils. FEBS J. 272, 5950-5961.
17. Ferguson, N., Becker, J., Tidow, H., Tremmel, S., Sharpe, T. D., Krause, G., Flinders, J., Petrovich, M., Berriman, J., Oschkinat, H., and Fersht, A. R. (2006) General structural motifs of amyloid protofilaments. Proc. Natl. Acad. Sci. U.S.A. 103, 16248-16253.
18. Eisenberg, D., Nelson, R., Sawaya, M. R., Balbirnie, M., Sambashivan, S., Ivanova, M. I., Madsen, A. O., and Riekel, C. (2006) The structural biology of protein aggregation diseases: Fundamental questions and some answers. Acc. Chem. Res. 39, 568-575.
19. Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc. Natl. Acad. Sci. U.S.A. 102, 17342-17347.
20. Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747.
21. Kirschner, D. A., Abraham, C., and Selkoe, D. J. (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proc. Natl. Acad. Sci. U.S.A. 83, 503-507.
22. 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 Alzheimer's beta-amyloid. Nat. Struct. Mol. Biol. 14, 1157-1164.
23. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular cloningsa laboratory manual, Cold Spring Harbor Laboratory Press, New York.
24. 2H-labeled proteins with high sensitivity. J. Am. Chem. Soc. 116, 11655-11666.
25. 2H-labeled proteins. J. Biomol. NMR 13, 369-374.
26. Clore, G. M., and Gronenborn, A. M. (1994) Multidimensional heteronuclear magnetic resonance of proteins. Methods Enzymol. 239, 349-363.
27. Ikura, M., and Bax, A. (1992) Isotope-filtered 2D NMR of a protein-peptide complex: study of a skeletal muscle myosin light chain kinase fragment bound to calmodulin. J. Am. Chem. Soc. 114, 2433-2440.
28. Nilges, M., Clore, G. M., and Gronenborn, A. M. (1988) Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Lett. 229, 317-324.
29. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D54 (Part 5), 905-921.
30. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302.
31. Alexandrescu, A. T. (2001) An NMR-based quenched hydrogen exchange investigation of model amyloid fibrils formed by cold shock protein A. Pacific Symp. Biocomput. 6, 67-78.
32. Nishimura, C., Dyson, H. J., and Wright, P. E. (2005) Enhanced picture of protein-folding intermediates using organic solvents in H/D exchange and quench-flow experiments. Proc. Natl. Acad. Sci. U.S.A. 102, 4765-4770.
33. Gellermann, G. P., Byrnes, H, Striebinger, A., Ullrich, K., Mueller, R., Hillen, H., and Barghorn, S. (2008) A beta-globulomers are formed independently of the fibril pathway. Neurobiol. Dis. 30, 212-220.
34. Ma, B., and Nussinov, R. (2006) Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Curr. Opin. Chem. Biol. 10, 445-452.
35. Lazo, N. D., Grant, M. A., Condron, M. C., Rigby, A. C., and Teplow, D. B. (2005) On the nucleation of amyloid beta-protein monomer folding. Protein Sci. 14, 1581-1596.
36. Grant, M. A., Lazo, N. D., Lomakin, A., Condron, M. M., Arai, H., Yamin, G., Rigby, A. C., and Teplow, D. B. (2007) Familial Alzheimer's disease mutations alter the stability of the amyloid beta-protein monomer folding nucleus. Proc. Natl. Acad. Sci. U.S.A. 104, 16522-16527.
37. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G., and Dobson, C. M. (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci. U.S.A. 96, 3590-3594.
38. Martins, I. C., Kuperstein, I., Wilkinson, H., Maes, E., Vanbrabant, M., Jonckheere, W., Van Gelder, P., Hartmann, D., D'Hooge, R., De Strooper, B., Schymkowitz, J., and Rousseau, F. (2008) Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. Embo J. 27, 224-233.
39. Selkoe, D. J. (2003) Folding proteins in fatal ways. Nature 426, 900-904.
40. Glabe, C. G. (2008) Structural classification of toxic amyloid oligomers. J. Biol. Chem. 283, 29639-29643.