Hydrogen-deuterium (H/D) exchange mapping of Aβ1-40 amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy

Biochemistry

Volumn 44, Issue 11, 2005, Pages 4434-4441

  Whittemore, Neil A ^a   Mishra, Rajesh ^a   Kheterpal, Indu ^b   Williams, Angela D ^b   Wetzel, Ronald ^b   Serpersu, Engin H ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF TENNESSEE GRADUATE SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM; HYDROGEN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORGANIC ACIDS; PROTONS; SOLVENTS;

AMIDES; AMYLOID FIBRILS; DIMETHYL SULFOXIDE (DMSO); RESIDUES;

POLYPEPTIDES;

AMIDE; AMYLOID BETA PROTEIN[1-40]; DEUTERIUM; DICHLOROACETIC ACID; DIMETHYL SULFOXIDE; GLYCINE; PROTON; SERINE; SOLVENT;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL REACTION KINETICS; DEUTERIUM HYDROGEN EXCHANGE; HETERONUCLEAR SINGLE QUANTUM COHERENCE SPECTROSCOPY; HYDROGEN BOND; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; TECHNIQUE;

AMYLOID BETA-PROTEIN; DEUTERIUM EXCHANGE MEASUREMENT; DICHLOROACETATE; DIMETHYL SULFOXIDE; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTONS; SOLVENTS;

EID: 15544388942     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048292u     Document Type: Article

References (41)

1. Turner, G. C., and Varshavsky, A. (2000) Detecting and measuring cotranslational protein degradation in vivo, Science 289, 2117-2120.
2. Martin, J. B. (1999) Molecular basis of the neurodegenerative disorders [published erratum appears in (1999) N. Engl. J. Med. 341, 1407], N. Engl. J. Med. 340, 1970-1980.
3. Martin, J. B. (1999) Molecular basis of the neurodegenerative disorders [published erratum appears in (1999) N. Engl. J. Med. 341, 1407], N. Engl. J. Med. 340, 1970-1980.
4. Tycko, R. (2004) Progress towards a molecular-level structural understanding of amyloid fibrils, Curr. Opin. Struct. Biol. 14, 96-103.
5. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. F. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction, J. Mol. Biol. 273, 729-739.
6. Kheterpal, I., Williams, A., Murphy, C., Bledsoe, B., and Wetzel, R. (2001) Structural features of the Aβ amyloid fibril elucidated by limited proteolysis, Biochemistry 40, 11757-11767.
7. Kheterpal, I., Zhou, S., Cook, K. D., and Wetzel, R. (2000) Aβ amyloid fibrils possess a core structure highly resistant to hydrogen exchange, Proc. Natl. Acad. Sci. U.S.A. 97, 13597-13601.
8. Kheterpal, I., Lashuel, H. A., Hartley, D. M., Walz, T., Lansbury, P. T., and Wetzel, R. (2003) Aβ protofibrils possess a stable core structure resistant to hydrogen exchange, Biochemistry 42, 14092-14098.
9. Petkova, A. T., Leapman, R. D., Yau, W. M., and Tycko, R. (2004) Structural investigations of Alzheimer's β-amyloid fibrils by solid-state NMR, Biophys. J. 86, 506A.
10. Benzinger, T. L., Gregory, D. M., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Botto, R. E., and Meredith, S. C. (1998) Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register, Proc. Natl. Acad. Sci. U.S.A. 95, 13407-13412.
11. Antzutkin, O. N., Leapman, R. D., Balbach, J. J., and Tycko, R. (2002) Supramolecular structural constraints on Alzheimer's β-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance, Biochemistry 41, 15436-15450.
12. Torok, M., Milton, S., Kayed, R., Wu, P., McIntire, T., Glabe, C. G., and Langen, R. (2002) Structural and dynamic features of Alzheimer's A β peptide in amyloid fibrils studied by site-directed spin labeling, J. Biol. Chem. 277, 40810-40815.
13. Williams, A. D., Portelius, E., Kheterpal, I., Guo, J. T., Cook, K. D., Xu, Y., and Wetzel, R. (2004) Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis, J. Mol. Biol. 335, 833-842.
14. Wang, S. S. S., Tobler, S. A., Good, T. A., and Fernandez, E. J. (2003) Hydrogen exchange-mass spectrometry analysis of β-amyloid peptide structure, Biochemistry 42, 9507-9514.
15. Milne, J. S., Mayne, L., Roder, H., Wand, A. J., and Englander, S. W. (1998) Determinants of protein hydrogen exchange studied in equine cytochrome c, Protein Sci. 7, 739-745.
16. Englander, S. W., Sosnick, T. R., Englander, J. J., and Mayne, L. (1996) Mechanisms and uses of hydrogen exchange, Curr. Opin. Struct. Biol. 6, 18-23.
17. Hoshino, M., Katou, H., Hagihara, Y., Hasegawa, K., Naiki, H., and Goto, Y. (2002) Mapping the core of the β(2)-microglobulin amyloid fibril by H/D exchange, Nat. Struct. Biol. 9, 332-336.
18. Ippel, J. H., Olofsson, A., Schleucher, J., Lundgren, E., and Wijmenga, S. S. (2002) Probing solvent accessibility of amyloid fibrils by solution NMR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 99, 8648-8653.
19. Kuwata, K., Matumoto, T., Cheng, H., Nagayama, K., James Thomas, L., and Roder, H. (2003) NMR-detected hydrogen exchange and molecular dynamics simulations provide structural insight into fibril formation of prion protein fragment 106-126, Proc. Natl. Acad. Sci. U.S.A. 100, 14790-14795.
20. Olofsson, A., Ippel, J. H., Wijmenga, S. S., Lundgren, E., and Ohman, A. (2004) Probing solvent accessibility of transthyretin amyloid by solution NMR spectroscopy, J. Biol. Chem. 279, 5699-5707.
21. Mishra, R., Whittemore, N. A., Kheterpal, I., Wetzel, R., and Serpersu, E. (2004) in National Meeting of the Protein Society, San Diego, CA.
22. States, D. J., Haberkorn, R. A., and Ruben, D. J. (1982) A two-dimensional nuclear Overhauser experiment with pure absorption phase in 4 quadrants, J. Magn. Reson. 48, 286-292.
23. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy, J. Chem. Phys. 71, 4546-4553.
24. Shaka, A. J., Lee, C. J., and Pines, A. (1988) Iterative schemes for bilinear operators-Application to spin decoupling, J. Magn. Reson. 77, 274-293.
25. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
26. 15N chemical-shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
27. Bax, A., Vuister, G. W., Grzesiek, S., Delaglio, F., Wang, A. C., Tschudin, R., and Zhu, G. (1994) Measurement of homonuclear and heteronuclear J-couplings from quantitative J-correlation, Methods Enzymol. 239, 79-105.
28. Yamaguchi, K. I., Katou, H., Hoshino, M., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Core and heterogeneity of β(2)-microglobulin amyloid fibrils as revealed by H/D exchange, J. Mol. Biol. 338, 559-571.
29. Hirota-Nakaoka, N., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Dissolution of β(2)-microglobulin amyloid fibrils by dimethylsulfoxide, J. Biochem. 134, 159-164.
30. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
31. Redfield, C. (1993) in NMR of Macromolecules, A Practical Approach (Roberts, G. C. K., Ed.) pp 71-101, IRL Press, Oxford, U.K.
32. Mikros, E., Benaki, D., Humpfer, E., Spraul, M., Loukas, S., Stassinopoulou, C. I., and Pelecanou, M. (2001) High-resolution NMR spectroscopy of the β-amyloid(1-28) fibril typical for Alzheimer's disease, Angew. Chem. 40, 3603-3605.
33. Coles, M., Bicknell, W., Watson, A. A., Fairlie, D. P., and Craik, D. J. (1998) Solution structure of amyloidβ peptide(1-40) in a water-micelle environment. Is the membrane-spanning domain where we think it is? Biochemistry 37, 11064-11077.
34. Kheterpal, I., Wetzel, R., Cook, K. (2003) Enhanced correction methods for hydrogen exchange-mass spectrometry studies of amyloid fibrils, Protein Sci. 12, 635-643.
35. Jarrett, J. T., Berger, E. P., and Lansbury, P. T. Jr. (1993) The carboxy terminus of the β-amyloid protein is critical for the seeding of amyloid formation. Implications for the pathogenesis of Alzheimer's disease, Biochemistry 32, 4693-4697.
36. Selkoe, D. J. (1999) Translating cell biology into therapeutic advances in Alzheimer's disease, Nature 399, A23-A31.
37. Kirkitadze, M. D., Bitan, G., and Teplow, D. B. (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: The emerging role of oligomeric assemblies, J. Neurosci. Res. 69, 567-577.
38. Caughey, B., and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders, Annu. Rev. Neurosci. 26, 267-298.
39. Esler, W. P., Stimson, E. R., Ghilardi, J. R., Lu, Y. A., Felix, A. M., Vinters, H. V., Mantyh, P. W., Lee, J. P., Maggio, J. E. (1996) Point substitution in the central hydrophobic cluster of a human β-amyloid congener disrupts peptide folding and abolishes plaque competence, Biochemistry 35, 13914-13921.
40. Petkova, A. T., Leapman, R. D., Quo, Z., Yau, W.-M., Mattson, M. P., Tycko, R. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils, Science 307, 262-265.
41. Shivaprasad, S. and Wetzel, R. (2004) An intersheet packing interaction in Aβ fibrils mapped by disulfide crosslinking, Biochemistry 43, 15310-15317.