Simultaneous monitoring of peptide aggregate distributions, structure, and kinetics using amide hydrogen exchange: Application to Aβ(1-40) fibrillogenesis

Biotechnology and Bioengineering

Volumn 100, Issue 6, 2008, Pages 1214-1227

  Qi, Wei ^a   Zhang, Aming ^a   Patel, Dhara ^b   Lee, Sungmun ^b,d   Harrington, Jamie L ^a,e   Zhao, Liming ^c   Schaefer, David ^c   Good, Theresa A ^b   Fernandez, Erik J ^a  

^a University of Virginia   (United States)

^b University of Marylandw Baltimore County   (United States)

^c TOWSON UNIVERSITY   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^e GENZYME CORPORATION   (United States)

Author keywords

Aggregation; Amyloid beta protein (1 40); Hydrogen exchange

Indexed keywords

AGGREGATE STRUCTURES; AGGREGATION; AMIDE HYDROGEN EXCHANGE; AMYLOID BETA; AMYLOID BETA PROTEIN (1-40); FIBRILLOGENESIS; HYDROGEN EXCHANGE; HYDROGEN-DEUTERIUM EXCHANGE; INTERMEDIATE SPECIES; LOW MOLECULAR WEIGHT OLIGOMERS; LOW-MOLECULAR WEIGHT; MASS SPECTRUM; MS APPROACH; MULTI COMPONENTS; OLIGOMER; QUANTITATIVE ANALYSIS; SIMULTANEOUS MONITORING; SOLUBLE AGGREGATES;

AMIDES; AMINES; ATOMIC FORCE MICROSCOPY; CHLORINE COMPOUNDS; DEUTERIUM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN; IMAGE SEGMENTATION; IMAGING TECHNIQUES; LABELING; MASS SPECTROMETERS; MASS SPECTROMETRY; MICROSCOPIC EXAMINATION; MOLECULAR WEIGHT; MONOMERS; NONMETALS; OLIGOMERS; PEPTIDES; POLYMERS; PROTEINS; SCANNING PROBE MICROSCOPY;

AGGREGATES;

AMYLOID; AMYLOID BETA PROTEIN; OLIGOMER;

ARTICLE; ATOMIC FORCE MICROSCOPY; DEUTERIUM HYDROGEN EXCHANGE; MASS SPECTROMETRY; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS;

AMIDES; AMYLOID; AMYLOID BETA-PROTEIN; DEUTERIUM EXCHANGE MEASUREMENT; KINETICS; MASS SPECTROMETRY; MICROSCOPY, ATOMIC FORCE; MOLECULAR WEIGHT; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY;

EID: 48649109730     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.21846     Document Type: Article

References (53)

1. Antzutkin ON, Leapman RD, Balbach JJ, Tycko R. 2002. Supramolecular structural constraints on Alzheimer's β-Amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance. Biochemistry 41(51):15436-15450.
2. Bai Y, Milne JS, Mayne L, Englander WS. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17:75-86.
3. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, Teplow DB. 2003. Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci 100(1):330-335.
4. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416(6880):507-511.
5. Cannon MJ, Williams AD, Wetzel R, Myszka DG. 2004. Kinetic analysis of beta-amyloid fibril elongation. Anal Biochem 328(1):67-75.
6. Carulla N, Caddy GL, Hall DR, Zurdo J, Gairi M, Feliz M, Giralt E, Robinson CV, Dobson CM. 2005. Molecular recycling within amyloid fibrils. Nature 436(7050):554-558.
7. Chen X, Brining S, Nguyen V, Yergey A. 1997. Simultaneous assessment of conformation and aggregation of beta-amyloid peptide using electrospray ionization mass spectrometry. FASEB J 11(10):817-823.
8. Chimon S, Ishii Y. 2005. Capturing intermediate structures of Alzheimer's beta-amyloid, A beta(1-40), by solid-state NMR spectroscopy. J Am Chem Soc 127(39):13472-13473.
9. Dahlgren KN, Manelli AM, Stine WB, Baker LK, Kraffi GA, LaDu MJ. 2002. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 277(35):32046-32053.
10. Demuro A, Mina E, Kayed R, Milton SC, Parker I, Glabe CG. 2005. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J Biol Chem 280(17):17294-17300.
11. Deng YZ, Zhang ZQ, Smith DL. 1999. Comparison of continuous and pulsed labeling amide hydrogen exchange/mass spectrometry for studies of protein dynamics. J Am Soc Mass Spectrom 10(8):675-684.
12. Dzwolak W, Loksztejn A, Smirnovas V. 2006. New insights into the self-assembly of insulin amyloid fibrils: An H-D exchange FT-IR study. Biochemistry 45(26):8143-8151.
13. Fogle JL, O'Connell JP, Fernandez EJ. 2006. Loading, stationary phase, and salt effects during hydrophobic interaction chromatography: [alpha]-Lactalbumin is stabilized at high loadings. J Chromatogr A 1121(2):209-218.
14. Gong YS, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, Klein WL. 2003. Alzheimer's disease-affected brain: Presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100(18):10417-10422.
15. Haass C, Selkoe DJ. 2007. Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8(2):101-112.
16. Hasegawa K, Ono K, Yamada M, Naiki H. 2002. Kinetic modeling and determination of reaction constants of Alzheimer's amyloid fibril extension and dissociation using surface plasmon resonance. Biochemistry 41(46):13489-13498.
17. Hoshino M, Katou H, Hagihara Y, Hasegawa K, Naiki H, Goto Y. 2002. Mapping the core of the beta(2)-microglobulin amyloid fibril by H/D exchange. Nat Struct Biol 9(5):332-336.
18. Hu WP, Chang GL, Chen SJ, Kuo YM. 2006. Kinetic analysis of beta-amyloid peptide aggregation induced by metal ions based on surface plasmon resonance biosensing. J Neurosci Methods 154(1-2):190-197.
19. Jablonowska A, Bakun M, Kupniewska-Kozak A, Dadlez M. 2004. Alzheimer's Disease A[beta] peptide fragment 10-30 forms a spectrum of metastable oligomers with marked preference for N to N and C to C monomer termini proximity. J Mol Biol 344(4):1037-1049.
20. Jorgensen TJD, Gardsvoll H, Dano K, Roepstorff P, Ploug M. 2004. Dynamics of urokinase receptor interaction with peptide antagonists studied by amide hydrogen exchange and mass spectrometry. Biochemistry 43(47):15044-15057.
21. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300(5618):486-489.
22. Kayed R, Sokolov Y, Edmonds B, McIntire TM, Milton SC, Hall JE, Glabe CG. 2004. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J Biol Chem 279(45):46363-46366.
23. Kheterpal I, Zhou S, Cook KD, Wetzel R. 2000. Abeta amyloid fibrils possess a core structure highly resistant to hydrogen exchange. Proc Natl Acad Sci 97(25):13597-13601.
24. Kheterpal I, Lashuel HA, Hartley DM, Wlaz T, Lansbury PT, Wetzel R. 2003a. A beta protofibrils possess a stable core structure resistant to hydrogen exchange. Biochemistry 42(48):14092-14098.
25. Kheterpal I, Wetzel R, Cook KD. 2003b. Enhanced correction methods for hydrogen exchange-mass spectrometric studies of amyloid fibrils. Protein Sci 12(3):635-643.
26. Kheterpal I, Chen M, Cook KD, Wetzel R. 2006. Structural differences in A beta amyloid protofibrils and fibrils mapped by hydrogen exchange - Mass spectrometry with on-line proteolytic fragmentation. J Mol Biol 361(4):785-795.
27. Kirkitadze MD, Bitan G, Teplow DB. 2002. Paradigm shifts in Alzheimer's disease and other neuro degenerative disorders: The emerging role of oligomeric assemblies. J Neurosci Res 69(5):567-577.
28. Klunk WE, Jacob RF, Mason RP. 1999. Quantifying amyloid β-peptide (Aβ) aggregation using the Congo Red-Aβ (CR-Aβ) spectrophotometric assay. Anal Biochem 266:66-76.
29. Kraus M, Bienert M, Krause E. 2003. Hydrogen exchange studies on Alzheimer's amyloid-beta peptides by mass spectrometry using matrix-assisted laser desorption/ionization and electrospray ionization. Rapid Commun Mass Spectrom 17(3):222-228.
30. Kremer JJ, Pallitto MM, Sklansky DJ, Murphy RM. 2000. Correlation of beta-amyloid aggregate size and hydrophobicity with decreased bilayer fluidity of model membranes. Biochemistry 39:10309-10318.
31. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, et al. 1998. Diffusible, nonfibrillar ligands derived from Abeta 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci 95(11):6448-6453.
32. Lee S, Fernandez EJ, Good TA. 2007. Role of aggregation conditions in structure, stability, and toxicity of intermediates in the A beta fibril formation pathway. Protein Sci 16(4):723-732.
33. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH. 2006. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440(7082):352-357.
34. Murphy RM. 2007. Kinetics of amyloid formation and membrane interaction with amyloidogenic proteins. Biochim Biophys Acta 1768:1923-1934.
35. Necula M, Kayed R, Milton S, Glabe CG. 2007. Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrilli-zation pathways are independent and distinct. J Biol Chem 282(14):10311-10324.
36. Nettleton EJ, Tito P, Sunde M, Bouchard M, Dobson CM, Robinson CV. 2000. Characterization of the oligomeric states of insulin in self-assembly and amyloid fibril formation by mass spectrometry. Biophys J 79(2):1053-1065.
37. Olofsson A, Sauer-Eriksson AE, Ohman A. 2006. The solvent protection of Alzheimer Amyloid-{beta}-(1-42) fibrils as determined by solution NMR spectroscopy. J Biol Chem 281(1):477-483.
38. Pallitto MM, Murphy RM. 2001. A Mathematical model of the kinetics of {beta}-Amyloid fibril growth from the denatured state. Biophys J 81(3):1805-1822.
39. Patel D, Good T. 2007. A rapid method to measure beta-amyloid induced neurotoxicity in vitro. J Neurosci Methods 161(1):1-10.
40. Paterson Y, Englander SW, Roder H. 1990. An antibody-binding site on cytochrome-C defined by hydrogen-exchange and 2-dimensional Nmr. Science 249(4970):755-759.
41. Petkova AT, Buntkowsky G, Dyda F, Leapman RD, Yau W-M, Tycko R. 2004. Solid state NMR reveals a pH-dependent Antiparallel [beta]-Sheet Registry in fibrils formed by a [beta]-Amyloid Peptide. J Mol Biol 335(1):247-260.
42. Qian H, Chan SI. 1999. Hydrogen exchange kinetics of proteins in denaturants: A generalized two-process model. I Mol Biol 286(2): 607-616.
43. Soto C. 1999. Plaque busters: Strategies to inhibit amyloid formation in Alzheimer's disease. Mol Med Today 5(8):343-350.
44. Stine WB, Jr., Dahlgren KN, Krafft GA, LaDu MJ. 2003. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278(13):11612-11622.
45. Tobler SA, Fernandez EJ. 2002. Structural features of interferon-gamma aggregation revealed by hydrogen exchange. Protein Sci 11(6):1340-1352.
46. Turner PR, O'Connor K,Tate WP, Abraham WC. 2003. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Progr Neurobiol 70(1):1-32.
47. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB. 1999. Amyloid β-protein fibrillogenesis. J Biol Chem 274:25945-25952.
48. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ. 2002. Naturally secreted oligomers of amyloid [beta] protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416(6880):535-539.
49. Wang SSS, Tobler SA, Good TA, Fernandez EJ. 2003. Hydrogen exchange-mass spectrometry analysis of beta-Amyloid peptide structure. Biochemistry 42(31):9507-9514.
50. Whittemore NA, Mishra R, Kheterpal I, Williams AD, Wetzel R, Serpersu EH. 2005. Hydrogen-deuterium (H/D) exchange mapping of A ss(1-40) amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy. Biochemistry 44(11):4434-4441.
51. Williams AD, Portelius E, Kheterpal I, Guo J-t, Cook KD, Xu Y, Wetzel R. 2004. Mapping A[beta] amyloid fibril secondary structure using scanning proline mutagenesis. J Mol Biol 335(3):833-842.
52. Williams AD, Sega M, Chen ML, Kheterpal I, Geva M, Berthelier V, Kaleta DT, Cook KD, Wetzel R. 2005. Structural properties of A beta protofibrils stabilized by a small molecule. Proc Natl Acad Sci USA 102(20):7115-7120.
53. Yamaguchi KI, Katou H, Hoshino M, Hasegawa K, Naiki H, Goto Y. 2004. Core and heterogeneity of beta(2)-microglobulin amyloid fibrils as revealed by H/D exchange. J Mol Biol 338(3):559-571.