Structure and dynamics of small soluble Aβ(1-40) oligomers studied by top-down hydrogen exchange mass spectrometry

Biochemistry

Volumn 51, Issue 17, 2012, Pages 3694-3703

  Pan, Jingxi ^a   Han, Jun ^b   Borchers, Christoph H ^b   Konermann, Lars ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; AMMONIUM ACETATE; AMYLOID FIBRIL; BASIC SOLUTIONS; DEUTERATION PATTERNS; DEUTERATIONS; ELECTRON CAPTURE DISSOCIATION; HYDROGEN EXCHANGE; INTERCONVERSIONS; ION SELECTION; LOW SALT CONCENTRATION; MOLE FRACTION; NEUROTOXICITY; SECONDARY STRUCTURES; SPATIAL RESOLUTION; STRUCTURAL CHARACTERIZATION; STRUCTURAL STUDIES; STRUCTURE AND DYNAMICS; TIME-RESOLVED; TOPDOWN;

AMIDES; AMMONIUM COMPOUNDS; CIRCULAR DICHROISM SPECTROSCOPY; DEUTERIUM; DYNAMICS; HYDROGEN; HYDROGEN BONDS; MASS SPECTROMETRY; MOLECULES; PROTEINS;

OLIGOMERS;

AMMONIUM ACETATE; AMYLOID BETA PROTEIN; MONOMER; OLIGOMER; SODIUM CHLORIDE;

ARTICLE; CIRCULAR DICHROISM; GEL PERMEATION CHROMATOGRAPHY; HUMAN; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE;

AMYLOID BETA-PEPTIDES; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; DEUTERIUM EXCHANGE MEASUREMENT; HUMANS; HYDROGEN BONDING; MASS SPECTROMETRY; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84860430705     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3002049     Document Type: Article

References (83)

1. Chiti, F. and Dobson, C. M. (2006) Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 75, 333-366
2. Schnabel, J. (2011) Amyloid: Little Proteins, Big Clues Nature 475, S12-S14
3. 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
4. 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
5. Detoma, A. S., Salamekh, S., Ramamoorthy, A., and Lim, M. H. (2012) Misfolded proteins in Alzheimer's disease and type II diabetes Chem. Soc. Rev. 41, 608-621
6. St. George-Hyslop, P. and Schmitt-Ulms, G. (2010) Alzheimer's disease: Modulating γ-secretase Nature 467, 36-37
7. Hellstrand, E., Boland, B., Walsh, D. M., and Linse, S. (2010) Amyloid β-Protein Aggregation Produces Highly Reproducible Kinetic Data and Occurs by a Two-Phase Process ACS Chem. Neurosci. 1, 13-18
8. 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 β-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747
9. Paravastu, A. K., Leapman, R. D., Yau, W. M., and Tycko, R. (2008) Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 105, 18349-18354
10. Lührs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-β(1-42) fibrils Proc. Natl. Acad. Sci. U.S.A. 102, 17342-17347
11. Kim, W. and Hecht, M. H. (2005) Sequence Determinants of Enhanced Amyloidogenicity of Alzheimer Aβ42 Peptide Relative to Aβ40 J. Biol. Chem. 280, 35069-35076
12. 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
13. Fawzi, N. L., Ying, J., Ghirlando, R., Torchiam, D. A., and Clore, G. M. (2011) Atomic-resolution dynamics on the surface of amyloid-β protofibrils probed by solution NMR Nature 480, 268-272
14. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid β-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112
15. 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
16. 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 β-peptide oligomer Biochemistry 48, 1870-1877
17. Huang, T. H., Yang, D. S., Plaskos, N. P., Go, S., Yip, C. M., Fraser, P. E., and Chakrabartty, A. (2000) Structural studies of soluble oligomers of the Alzheimer β-amyloid peptide J. Mol. Biol. 297, 73-87
18. Glabe, C. G. (2008) Structural Classification of Toxic Amyloid Oligomers J. Biol. Chem. 283, 29639-29643
19. Lesne, 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
20. Koffie, R. M., Meyer-Luehmann, M., Hashimoto, T., Adams, K. W., Mielke, M. L., Garcia-Alloza, M., Micheva, K. D., Smith, S. J., Kim, M. L., Lee, V. M., Hyman, B. T., and Spires-Jones, T. L. (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques Proc. Natl. Acad. Sci. U.S.A. 106, 4012-4017
21. Jin, M., Shepardson, N., Yang, T., Chen, G., Walsh, D., and Selkoe, D. J. (2011) Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration Proc. Natl. Acad. Sci. U.S.A. 108, 5819-5824
22. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14, 837-842
23. Cerf, E., Sarroukh, R., Tamamizu-Kato, S., Breydo, L., Derclaye, S., Dufrêne, Y. F., Narayanaswami, V., Goormaghtigh, E., Ruysschaert, J. M., and Raussens, V. (2009) Antiparallel β-sheet: A signature structure of the oligomeric amyloid β-peptide Biochem. J. 421, 415-423
24. 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
25. Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., and Strittmatter, S. M. (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers Nature 457, 1128-1132
26. Colletier, J. P., Laganowsky, A., Landau, M., Zhao, M., Soriaga, A. B., Goldschmidt, L., Flot, D., Cascio, D., Sawaya, M. R., and Eisenberg, D. (2011) Molecular basis for amyloid-β polymorphism Proc. Natl. Acad. Sci. U.S.A. 108, 16938-16943
27. 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-β(1-40) peptide Nat. Struct. Mol. Biol. 19, 79-83
28. 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 aetiology of Alzheimer's disease Nat. Chem. 1, 326-331
29. Chimon, S., Shaibat, M. A., Jones, C. R., Calero, D. C., Aizezi, B., and Ishii, Y. (2007) Evidence of fibril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's β-amyloid Nat. Struct. Mol. Biol. 14, 1157-1164
30. Chromy, B. A., Nowak, R. J., Lambert, M. P., Viola, K. L., Chang, L., Velasco, P. T., Jones, B. W., Fernandez, S. J., Lacor, P. N., Horowitz, P., Finch, C. E., Krafft, G. A., and Klein, W. L. (2003) Self-assembly of Aβ(1-42) into globular neurotoxins Biochemistry 42, 12749-12760
31. Shafrir, Y., Durell, S. R., Anishkin, A., and Guy, H. R. (2010) β-Barrel models of soluble amyloid β oligomers and annular protofibrils Proteins 78, 3458-3472
32. Pan, J., Han, J., Borchers, C. H., and Konermann, L. (2011) Conformer-Specific Hydrogen Exchange Analysis of Aß(1-42) Oligomers by Top-Down Electron Capture Dissociation Mass Spectrometry Anal. Chem. 83, 5386-5393
33. Haupt, C., Leppert, J., Ronicke, R., Meinhardt, J., Yadav, J. K., Ramachandran, R., Ohlenschlager, O., Reymann, K. G., Gorlach, M., and Fändrich, M. (2012) Structural Basis of β-Amyloid Dependent Synaptic Dysfunctions Angew. Chem., Int. Ed. 51, 1576-1579
34. Abelein, A., Bolognesi, B., Dobson, C. M., Graslund, A., and Lendel, C. (2012) Hydrophobicity and Conformational Change as Mechanistic Determinants for Nonspecific Modulators of Amyloid β Self-Assembly Biochemistry 51, 126-137
35. Ashcroft, A. E. (2010) Mass Spectrometry and the Amyloid Problem: How Far Can We Go in the Gas Phase? J. Am. Soc. Mass Spectrom. 21, 1087-1096
36. 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
37. Smith, A. M., Jahn, T. R., Ashcroft, A. E., and Radford, S. E. (2006) Direct Observation of Oligomeric Species formed in the Early Stages of Amyloid Formation using Electrospray Ionization Mass Spectrometry J. Mol. Biol. 364, 9-19
38. Smith, D. P., Radford, S. E., and Ashcroft, A. E. (2010) Elongated oligomers in β2-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry Proc. Natl. Acad. Sci. U.S.A. 107, 6794-6798
39. Kloniecki, M., Jablonowska, A., Poznanski, J., Langridge, J., Hughes, C., Campuzano, I., Giles, K., and Dadlez, M. (2011) Ion Mobility Separation Coupled with MS Detects Two Structural States of Alzheimer's Disease Aß1-40 Peptide Oligomers J. Mol. Biol. 407, 110-124
40. Englander, S. W. (2006) Hydrogen Exchange and Mass Spectrometry: A Historical Perspective J. Am. Soc. Mass Spectrom. 17, 1481-1489
41. Kaltashov, I. A., Engen, J. R., and Gross, M. L. (2006) Hydrogen Exchange and Covalent Modification: Focus on Biomolecular Structure, Dynamics, and Function. 18th Sanibel Conference on Mass Spectrometry J. Am. Soc. Mass Spectrom. 17, i-ii
42. Smith, D. L., Deng, Y., and Zhang, Z. (1997) Probing the Noncovalent Structure of Proteins by Amide Hydrogen Exchange Mass Spectrometry J. Mass Spectrom. 32, 135-146
43. Busenlehner, L. S. and Armstrong, R. N. (2005) Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry Arch. Biochem. Biophys. 433, 34-46
44. Lu, X., Wintrode, P. L., and Surewicz, W. K. (2007) β-Sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange Proc. Natl. Acad. Sci. U.S.A. 104, 1510-1515
45. Del Mar, C., Greenbaum, E. A., Mayne, L., Englander, S. W., and Woods, V. L. (2005) Structure and properties of α-synuclein and other amyloids determined at the amino acid level Proc. Natl. Acad. Sci. U.S.A. 102, 15477-15482
46. Sanchez, L., Madurga, S., Pukala, T., Vilaseca, M., Lopez-Iglesias, C., Robinson, C. V., Giralt, E., and Carulla, N. (2011) Aβ40 and Aβ42 Amyloid Fibrils Exhibit Distinct Molecular Recycling Properties J. Am. Chem. Soc. 133, 6505-6508
47. Kheterpal, I., Lashuel, H. A., Hartley, D. M., Walz, T., Lansbury, P. T. J., and Wetzel, R. (2003) Aβ protofibrils possess a stable core structure resistant to hydrogen exchange Biochemistry 42, 14092-14098
48. Zhang, A., Qi, W., Good, T. A., and Fernandez, E. J. (2009) Structural Differences between Aβ(1-40) Intermediate Oligomers and Fibrils Elucidated by Proteolytic Fragmentation and Hydrogen/Deuterium Exchange Biophys. J. 96, 1091-1104
49. Kheterpal, I., Chen, M., Cook, K. D., and Wetzel, R. (2006) Structural Differences in Aβ Amyloid Protofibrils and Fibrils Mapped by Hydrogen Exchange-Mass Spectrometry with On-line Proteolytic Fragmentation J. Mol. Biol. 361, 785-795
50. Rand, K. D., Bache, N., Nedertoft, M. M., and Jørgensen, T. J. D. (2011) Spatially Resolved Protein Hydrogen Exchange Measured by Matrix-Assisted Laser Desorption Ionization In-Source Decay Anal. Chem. 83, 8859-8862
51. Zubarev, R. A., Zubarev, A. R., and Savitski, M. M. (2008) Electron Capture/Transfer versus Collisionally Activted/Induced Dissociations: Solo or Duet? J. Am. Soc. Mass Spectrom. 19, 753-761
52. Coon, J. J. (2009) Collisions or Electrons? Protein Sequence Analysis in the 21st Century Anal. Chem. 81, 3208-3215
53. Rand, K. D., Adams, C. M., Zubarev, R. A., and Jørgensen, T. J. D. (2008) Electron Capture Dissociation Proceeds with a Low Degree of Intramolecular Migration of Peptide Amide Hydrogens J. Am. Chem. Soc. 130, 1341-1349
54. Zehl, M., Rand, K. D., Jensen, O. N., and Jørgensen, T. J. D. (2008) Electron Transfer Dissociation Facilitates the Measurement of Deuterium Incorporation into Selectively Labeled Peptides with Single Residue Resolution J. Am. Chem. Soc. 130, 17453-17459
55. Pan, J., Han, J., Borchers, C. H., and Konermann, L. (2009) Hydrogen/Deuterium Exchange Mass Spectrometry with Top-Down Electron Capture Dissociation for Characterizing Structural Transitions of a 17 kDa Protein J. Am. Chem. Soc. 131, 12801-12808
56. Rand, K. D., Zehl, M., Jensen, O. N., and Jørgensen, T. J. D. (2009) Protein Hydrogen Exchange Measured at Single-Residue Resolution by Electron Transfer Dissociation Mass Spectrometry Anal. Chem. 81, 5577-5584
57. Landgraf, R. R., Chalmers, M. J., and Griffin, P. R. (2012) Automated Hydrogen/Deuterium Exchange Electron Transfer Dissociation High Resolution Mass Spectrometry Measured at Single-Amide Resolution J. Am. Soc. Mass Spectrom. 23, 301-309
58. Huang, R. Y., Garai, K., Frieden, C., and Gross, M. L. (2011) Hydrogen/Deuterium Exchange and Electron-Transfer Dissociation Mass Spectrometry Determine the Interface and Dynamics of Apolipoprotein E Oligomerization Biochemistry 50, 9273-9282
59. Konermann, L., Pan, J., and Liu, Y. (2011) Hydrogen Exchange Mass Spectrometry for Studying Protein Structure and Dynamics Chem. Soc. Rev. 40, 1224-1234
60. Abzalimov, R. R., Kaplan, D. A., Easterling, M. L., and Kaltashov, I. A. (2009) Protein conformations can be probed in top-down HDX MS experiments utilizing electron transfer dissociation of protein ions without hydrogen scrambling J. Am. Soc. Mass Spectrom. 20, 1514-1517
61. Kaltashov, I. A., Bobst, C. E., and Abzalimov, R. R. (2009) H/D Exchange and Mass Spectrometry in the Studies of Protein Conformation and Dynamics: Is There a Need for a Top-Down Approach? Anal. Chem. 81, 7892-7899
62. Stine, W. B., Jr., Dahlgren, K. N., Krafft, G. A., and LaDu, M. J. (2003) In vitro characterization of conditions for amyloid-β peptide oligomerization and fibrillogenesis J. Biol. Chem. 278, 11612-11622
63. Xiao, H., Hoerner, J. K., Eyles, S. J., Dobo, A., Voigtman, E., Melcuk, A. I., and Kaltashov, I. A. (2005) Mapping protein energy landscapes with amide hydrogen exchange and mass spectrometry: I. A generalized model for a two-state protein and comparison with experiment Protein Sci. 14, 543-557
64. Cech, N. B. and Enke, C. G. (2001) Practical Implication of Some Recent Studies in Electrospray Ionization Fundamentals Mass Spectrom. Rev. 20, 362-387
65. Slysz, G. W., Percy, A. J., and Schriemer, D. C. (2008) Restraining Expansion of the Peak Envelope in H/D Exchange-MS and Its Application in Detecting Perturbations of Protein Structure/Dynamics Anal. Chem. 80, 7004-7011
66. Kruger, N. A., Zubarev, R. A., Carpenter, B. K., Kelleher, N. L., Horn, D. M., and McLafferty, F. W. (1999) Electron capture versus energetic dissociation of protein ions Int. J. Mass Spectrom. 182/183, 1-5
67. Hoerner, J. K., Xiao, H., and Kaltashov, I. A. (2005) Structural and Dynamic Characteristics of a Partially Folded State of Ubiquitin Revealed by Hydrogen Exchange Mass Spectrometry Biochemistry 44, 11286-11294
68. Cooper, H. J., Hakansson, K., and Marshall, A. G. (2005) The Role of Electron capture Dissociation in Biomolecular Analysis Mass Spectrom. Rev. 24, 201-222
69. Kruger, N. A., Zubarev, R. A., Horn, D. M., and McLafferty, F. W. (1999) Electron capture dissociation of multiply charged peptide cations Int. J. Mass Spectrom. 185-187, 787-793
70. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairí, M., Feliz, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils Nature 436, 554-558
71. 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
72. Miranker, A., Robinson, C. V., Radford, S. E., and Dobson, C. M. (1996) Investigation of protein folding by mass spectrometry FASEB J. 10, 93-101
73. Kim, M.-Y., Maier, C. S., Reed, D. J., and Deinzer, M. L. (2002) Conformational changes in chemically modified Escherichia coli thioredoxin monitored by H/D exchange and electrospray mass spectrometry Protein Sci. 11, 1320-1329
74. Krishna, M. M. G., Hoang, L., Lin, Y., and Englander, S. W. (2004) Hydrogen exchange methods to study protein folding Methods 34, 51-64
75. Kuprowski, M. C. and Konermann, L. (2007) Signal Response of Co-Existing Protein Conformers in Electrospray Mass Spectrometry Anal. Chem. 79, 2499-2506
76. Peschke, M., Verkerk, U. H., and Kebarle, P. (2004) Features of the ESI Mechanism that Affect the Observation of Multiply Charged Noncovalent Protein Complexes and the Determination of the Association Constant by the Titration Method J. Am. Soc. Mass Spectrom. 15, 1424-1434
77. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary Structure Effects on Peptide Group Hydrogen Exchange Proteins: Struct., Funct., Genet. 17, 75-86
78. Chetty, P. S., Mayne, L., Lund-Katz, S., Stranz, D. D., Englander, S. W., and Phillips, M. C. (2009) Helical structure and stability in human apolipoprotein A-I by hydrogen exchange and mass spectrometry Proc. Natl. Acad. Sci. U.S.A. 106, 19005-19010
79. Fersht, A. R. (1999) Structure and Mechanism in Protein Science, W. H. Freeman & Co., New York.
80. Chou, K.-C. (2000) Prediction of Tight Turns and Their Types in Proteins Anal. Biochem. 286, 1-16
81. Laganowsky, A., Liu, C., Sawaya, M. R., Whitelegge, J. P., Park, J., Zhao, M., Pensalfini, A., Soriaga, A. B., Landau, M., Teng, P. K., Cascio, D., Glabe, C., and Eisenberg, D. (2012) Atomic view of a toxic amyloid small oligomer Science 335, 1228-1231
82. 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
83. Liu, T., Pantazatos, D., Li, S., Hamuro, Y., Hilser, V. J., and Woods, V. L. (2012) Quantitative assessment of protein structural models by comparison of H/D exchange MS data with exchange behavior accurately predicted by DXCOREX J. Am. Soc. Mass Spectrom. 23, 43-56