Parallel β-sheet fibril and antiparallel β-sheet oligomer: New insights into amyloid formation of hen egg white lysozyme under heat and acidic condition from FTIR spectroscopy

Journal of Physical Chemistry B

Volumn 117, Issue 15, 2013, Pages 4003-4013

  Zou, Ye ^a   Li, Yiyi ^a   Hao, Wenying ^a   Hu, Xiaoqian ^a   Ma, Gang ^a  

^a HEBEI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GLYCOPROTEINS; OLIGOMERIZATION; OLIGOMERS;

ACIDIC CONDITIONS; AMYLOID FORMATION; ELEVATED TEMPERATURE; HEN EGG WHITE LYSOZYME; PEPTIDE FRAGMENTS; STRUCTURAL INSIGHTS; TEMPERATURE DEPENDENT; TEMPERATURE-DEPENDENT FTIR;

FOURIER TRANSFORM INFRARED SPECTROSCOPY;

EID: 84876491523     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4003559     Document Type: Article

References (63)

1. Sawaya, M. R.; Sambashivan, S.; Nelson, R.; Ivanova, M. I.; Sievers, S. A.; Apostol, M. I.; Thompson, M. J.; Balbirnie, M.; Wiltzius, J. J. W.; McFarlane, H. T. Atomic Structures of Amyloid Cross-Beta Spines Reveal Varied Steric Zippers Nature 2007, 447, 453-457
2. Margittai, M.; Langen, R. Fibrils with Parallel in-Register Structure Constitute a Major Class of Amyloid Fibrils: Molecular Insights from Electron Paramagnetic Resonance Spectroscopy Q. Rev. Biophys. 2008, 41, 265-297
3. Sipe, J. D.; Cohen, A. S. Review: History of the Amyloid Fibril J. Struct. Biol. 2000, 130, 88-98
4. Chiti, F.; Dobson, C. M. Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 2006, 75, 333-366
5. Lansbury, P. T.; Lashuel, H. A. A Century-Old Debate on Protein Aggregation and Neurodegeneration Enters the Clinic Nature 2006, 443, 774-779
6. Lee, J.; Culyba, E. K.; Powers, E. T.; Kelly, J. W. Amyloid-Beta Forms Fibrils by Nucleated Conformational Conversion of Oligomers Nat. Chem. Biol. 2011, 7, 602-609
7. Serio, T. R.; Cashikar, A. G.; Kowal, A. S.; Sawicki, G. J.; Moslehi, J. J.; Serpell, L.; Arnsdorf, M. F.; Lindquist, S. L. Nucleated Conformational Conversion and the Replication of Conformational Information by a Prion Determinant Science 2000, 289, 1317-1321
8. Ahmed, M.; Davis, J.; Aucoin, D.; Sato, T.; Ahuja, S.; Aimoto, S.; Elliott, J. I.; Van Nostrand, W. E.; Smith, S. O. Structural Conversion of Neurotoxic Amyloid-Beta(1-42) Oligomers to Fibrils Nat. Struct. Mol. Biol. 2010, 17, 561-567
9. Auer, S.; Ricchiuto, P.; Kashchiev, D. Two-Step Nucleation of Amyloid Fibrils: Omnipresent or Not? J. Mol. Biol. 2012, 422, 723-730
10. Gellermann, G. P.; Byrnes, H.; Striebinger, A.; Ullrich, K.; Mueller, R.; Hillen, H.; Barghorn, S. Abeta-Globulomers are Formed Independently of the Fibril Pathway Neurobiol. Dis. 2008, 30, 212-220
11. Kayed, R.; Pensalfini, A.; Margol, L.; Sokolov, Y.; Sarsoza, F.; Head, E.; Hall, J.; Glabe, C. Annular Protofibrils are a Structurally and Functionally Distinct Type of Amyloid Oligomer J. Biol. Chem. 2009, 284, 4230-4237
12. Kumar, A.; Paslay, L. C.; Lyons, D.; Morgan, S. E.; Correia, J. J.; Rangachari, V. Specific Soluble Oligomers of Amyloid-Beta Peptide Undergo Replication and Form Non-Fibrillar Aggregates in Interfacial Environments J. Biol. Chem. 2012, 287, 21253-21264
13. Laganowsky, A.; Liu, C.; Sawaya, M. R.; Whitelegge, J. P.; Park, J.; Zhao, M.; Pensalfini, A.; Soriaga, A. B.; Landau, M.; Teng, P. K. Atomic View of a Toxic Amyloid Small Oligomer Science 2012, 335, 1228-1231
14. Glabe, C. G. Structural Classification of Toxic Amyloid Oligomers J. Biol. Chem. 2008, 283, 29639-19643
15. Chiti, F.; Webster, P.; Taddei, N.; Clark, A.; Stefani, M.; Ramponi, G.; Dobson, C. M. Designing Conditions for in Vitro Formation of Amyloid Protofilaments and Fibrils Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3590-3594
16. Dobson, C. M. Protein Folding and Misfolding Nature 2003, 426, 884-890
17. Trexler, A. J.; Nilsson, M. R. The Formation of Amyloid Fibrils from Proteins in the Lysozyme Family Curr. Protein Pept. Sci. 2007, 8, 537-557
18. Krebs, M. R. H.; Wilkins, D. K.; Chung, E. W.; Pitkeathly, M. C.; Chamberlain, A. K.; Zurdo, J.; Robinson, C. V.; Dobson, C. M. Formation and Seeding of Amyloid Fibrils from Wild-Type Hen Lysozyme and a Peptide Fragment from the Beta-Domain J. Mol. Biol. 2000, 300, 541-549
19. Frare, E.; P.; P., D. L.; Zurdo, J.; Dobson, C. M.; Fontana, A. A Highly Amyloidogenic Region of Hen Lysozyme J. Mol. Biol. 2004, 340, 1153-1165
20. Arnaudov, L. N.; de Vries, R. Thermally Induced Fibrillar Aggregation of Hen Egg White Lysozyme Biophys. J. 2005, 88, 515-526
21. Shashilov, V.; Xu, M.; Ermolenkov, V. V.; Fredriksen, L.; Lednev, I. K. Probing a Fibrillation Nucleus Directly by Deep Ultraviolet Raman Spectroscopy J. Am. Chem. Soc. 2007, 129, 6972-6973
22. Mishra, R.; Sorgjerd, K.; Nystrom, S.; Nordigarden, A.; Yu, Y.-C.; Hammarstrom, P. Lysozyme Amyloidogenesis is Accelerated by Specific Nicking and Fragmentation but Decelerated by Intact Protein Binding and Conversion J. Mol. Biol. 2007, 366, 1029-1044
23. Hill, S. E.; Robinson, J.; Matthews, G.; Muschol, M. Amyloid Protofibrils of Lysozyme Nucleate and Grow Via Oligomer Fusion Biophys. J. 2009, 96, 3781-3790
24. Kumar, S.; Ravi, V. K.; Swaminathan, R. How Do Surfactants and DTT Affect the Size, Dynamics, Activity and Growth of Soluble Lysozyme Aggregates? Biochem. J. 2008, 415, 275-288
25. Goda, S.; Takano, K.; Yamagata, Y.; Nagata, R.; Akutsu, H.; Maki, S.; Namba, K.; Yutani, K. Amyloid Protofilament Formation of Hen Egg Lysozyme in Highly Concentrated Ethanol Solution Protein Sci. 2000, 9, 369-375
26. Khan, J. M.; Qadeer, A.; Chaturvedi, S. K.; Ahmad, E.; Rehman, S. A.; Gourinath, S.; Khan, R. H. SDS Can Be Utilized as an Amyloid Inducer: A Case Study on Diverse Proteins PLoS One 2012, 7, e29694
27. Vernaglia, B. A.; Huang, J.; Clark, E. D. Guanidine Hydrochloride Can Induce Amyloid Fibril Formation from Hen Egg-White Lysozyme Biomacromolecules 2004, 5, 1362-1370
28. Sasahara, K.; Yagi, H.; Naiki, H.; Goto, Y. Heat-Induced Conversion of Beta(2)-Microglobulin and Hen Egg-White Lysozyme into Amyloid Fibrils J. Mol. Biol. 2007, 372, 981-991
29. Takase, K.; Higashi, T.; Omura, T. Aggregate Formation and the Structure of the Aggregates of Disulfide-Reduced Proteins J. Protein Chem. 2002, 21, 427-433
30. Stroud, J. C.; Liu, C.; Teng, P. K.; Eisenberg, D. Toxic Fibrillar Oligomers of Amyloid-Beta Have Cross-Beta Structure Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 7717-7722
31. Berthelot, K.; Ta, H. P.; Gean, J.; Lecomte, S.; Cullin, C. In Vivo and in Vitro Analyses of Toxic Mutants of HET-s: FTIR Antiparallel Signature Correlates with Amyloid Toxicity J. Mol. Biol. 2011, 412, 137-152
32. Lumry, R.; Smith, E. L.; Glantz, R. R. Kinetics of Carboxypeptidase Action. I. Effect of Various Extrinsic Factors on Kinetic Parameters J. Am. Chem. Soc. 1951, 73, 4330-4340
33. Aune, K. C.; Tanford, C. Thermodynamics of the Denaturation of Lysozyme by Guanidine Hydrochloride. I. Depdendence on pH at 25 Degrees Biochemistry 1969, 8, 4579-4585
34. Dong, A.; Caughey, W. S. Infrared Methods for Study of Hemoglobin Reactions and Structures Methods Enzymol. 1994, 232, 139-175
35. Sassi, P.; Giugliarelli, A.; Paolantoni, M.; Morresi, A.; Onori, G. Unfolding and Aggregation of Lysozyme: A Thermodynamic and Kinetic Study by FTIR Spectroscopy Biophys. Chem. 2011, 158, 46-53
36. Nielsen, L.; Khurana, R.; Coats, A.; Frokjaer, S.; Brange, J.; Vyas, S.; Uversky, V. N.; Fink, A. L. Effect of Environmental Factors on the Kinetics of Insulin Fibril Formation: Elucidation of the Molecular Mechanism Biochemistry 2001, 40, 6036-6046
37. Harper, J. D.; Lansbury, P. T. J. Models of Amyloid Seeding in Alzheimer's Disease and Scrapie:Mechanistic Truths and Physiological Consequences of the Time-Dependent Solubility of Amyloid Proteins Annu. Rev. Biochem. 1997, 66, 385-407
38. Hortschansky, P.; Schroeckh, V.; Christopeit, T.; Zandomeneghi, G.; Fändrich, M. The Aggregation Kinetics of Alzheimer's Beta-Amyloid Peptide is Controlled by Stochastic Nucleation Protein Sci. 2005, 14, 1753-1759
39. Fu, L.; Ma, G.; Yan, E. C. Y. In Situ Misfolding of Human Islet Amyloid Polypeptide at Interfaces Probed by Vibrational Sum Frequency Generation J. Am. Chem. Soc. 2010, 132, 5405-5412
40. Barth, A.; Zscherp, C. What Vibrations Tell Us About Proteins Q. Rev. Biophys. 2002, 35, 369-430
41. Kubelka, J.; Keiderling, T. A. Differentiation of Beta-Sheet-Forming Structures: Ab Initio-Based Simulations of IR Absorption and Vibrational CD for Model Peptide and Protein Beta-Sheets J. Am. Chem. Soc. 2001, 123, 12048-12058
42. Zandomeneghi, G.; Krebs, M. R.; McCammon, M. G.; Fändrich, M. FTIR Reveals Structural Differences between Native Beta-Sheet Proteins and Amyloid Fibrils Protein Sci. 2004, 13, 3314-3321
43. Decatur, S. M. Elucidation of Residue-Level Structure and Dynamics of Polypeptides via Isotopp-Edited Infrared Spectroscopy Acc. Chem. Res. 2006, 39, 169-175
44. Ling, Y. L.; Strasfeld, D. B.; Shim, S. H.; Raleigh, D. P.; Zanni, M. T. Two-Dimensional Infrared Spectroscopy Provides Evidence of an Intermediate in the Membrane-Catalyzed Assembly of Diabetic Amyloid J. Phys. Chem. B 2009, 113, 2498-2505
45. Guo, Y.; Wang, J. Spectroscopic Evidence for Polymorphic Aggregates Formed by Amyloid-Beta Fragments ChemPhysChem 2012, 13, 3901-3908
46. Chirgadze, Y. N.; Nevskaya, N. A. Infrared-Spectra and Resonance Interaction of Amide-I Vibration of Anti-Parallel-Chain Pleated Sheet Biopolymers 1976, 15, 607-625
47. Peralvarez-Marin, A.; Mateos, L.; Zhang, C.; Singh, S.; Cedazo-Minguez, A.; Visa, N.; Morozova-Roche, L.; Graslund, A.; Barth, A. Influence of Residue 22 on the Folding, Aggregation Profile, and Toxicity of the Alzheimer's Amyloid Beta Peptide Biophys. J. 2009, 97, 277-285
48. Sarroukh, R.; Cerf, E.; Derclaye, S.; Dufrene, Y. F.; Goormaghtigh, E.; Ruysschaert, J.-M.; Raussens, V. Transformation of Amyloid Beta(1-40) Oligomers into Fibrils is Characterized by a Major Change in Secondary Structure Cell. Mol. Life Sci. 2010, 68, 1429-1438
49. Celej, M. S.; Sarroukh, R.; Goormaghtigh, E.; Fidelio, G. D.; Ruysschaert, J.-M.; Raussens, V. Toxic Prefibrillar Alpha-Synuclein Amyloid Oligomers Adopt a Distinctive Antiparallel Beta-Sheet Structure Biochem. J. 2012, 443, 719-726
50. Yamaoki, Y.; Imamura, H.; Fulara, A.; Wójcik, S.; BozÌycki, L.; Kato, M.; Keiderling, T. A.; Dzwolak, W. An FT-IR Study on Packing Defects in Mixed Beta-Aggregates of Poly(L-Glutamic Acid) and Poly(D-Glutamic Acid): A High-Pressure Rescue from a Kinetic Trap J. Phys. Chem. B 2012, 116, 5172-5178
51. Demirdöven, N.; Cheatum, C. M.; Chung, H. S.; Khalil, M.; Knoester, J.; Tokmakoff, A. Two-Dimensional Infrared Spectroscopy of Antiparallel Beta-Sheet Secondary Structure J. Am. Chem. Soc. 2004, 126, 7981-7990
52. Greenfield, N. J. Using Circular Dichroism Spectra to Estimate Protein Secondary Structure Nat. Protoc. 2006, 1, 2876-2890
53. Heinig, M.; Frishman, D. Stride: A Web Server for Secondary Structure Assignment from Known Atomic Coordinates of Proteins Nucleic Acids Res. 2004, 32, W500-W502
54. Stine, W. B. J.; Dahlgren, K. N.; Krafft, G. A.; LaDu, M. J. In Vitro Characterization of Conditions for Amyloid-Beta Peptide Oligomerization and Fibrillogenesis J. Biol. Chem. 2003, 278, 11612-11622
55. Cerf, E.; Sarroukh, R.; Tamamizu-Kato, S.; Breydo, L.; Derclaye, S.; Dufreîne, Y. F.; Narayanaswami, V.; Goormaghtigh, E.; Ruysschaert, J. M.; Raussens, V. Antiparallel Beta-Sheet: A Signature Structure of the Oligomeric Amyloid Beta-Peptide Biochem. J. 2009, 421, 415-423
56. Ma, G.; Li, Y.; Dong, J.; Zou, Y.; Zhang, Z.; Sun, Y. The Dynamic Nature of Incubation Solution after Cooling to Room Temperature in Amyloid Formation of Hen Egg White Lysozyme: An FTIR Assessment Vib. Spectrosc. 2013, 64, 44-50
57. Lührs, T.; Ritter, C.; Adrian, M.; Riek-Loher, D.; Bohrmann, B.; Döbeli, H.; Schubert, D.; Riek, R. 3D Structure of Alzheimer's Amyloid-Beta(1-42) Fibrils Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17342-17347
58. Tycko, R. Molecular Structure of Amyloid Fibrils: Insights from Solid-State NMR Q. Rev. Biophys. 2006, 39, 1-55
59. Luca, S.; Yau, W. M.; Leapman, R.; Tycko, R. Peptide Conformation and Supramolecular Organization in Amylin Fibrils: Constraints from Solid-State NMR Biochemistry 2007, 46, 13505-13522
60. Krimm, S.; Bandekar, J. Vibrational Analysis of Peptides, Polypeptides, and Proteins. V. Normal Vibrations of Beta-Turns Biopolymers 1980, 19, 1-29
61. Strasfeld, D. B.; Ling, Y. L.; Gupta, R.; Raleigh, D. P.; Zanni, M. T. Strategies for Extracting Structural Information from 2D IR Spectroscopy of Amyloid: Application to Islet Amyloid Polypeptide J. Phys. Chem. B 2009, 113, 15679-15691
62. DuBay, K. F.; Pawar, A. P.; Chiti, F.; Zurdo, J.; Dobson, C. M.; Vendruscolo, M. Prediction of the Absolute Aggregation Rates of Amyloidogenic Polypeptide Chains J. Mol. Biol. 2004, 341, 1317-1326
63. Qiang, W.; Yau, W.-M.; Luo, Y.; Mattson, M. P.; Tycko, R. Antiparallel Beta-Sheet Architecture in Iowa-Mutant Beta-Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 4443-4448