Pyroglutamylated amyloid-β peptide reverses cross β-sheets by a prion-like mechanism

Journal of Physical Chemistry B

Volumn 118, Issue 21, 2014, Pages 5637-5643

  Matos, Jason O ^a   Goldblatt, Greg ^a   Jeon, Jaekyun ^a   Chen, Bo ^a   Tatulian, Suren A ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; GLYCOPROTEINS; ISOTOPES; OLIGOMERS; TRANSMISSION ELECTRON MICROSCOPY;

ALZHEIMER'S DISEASE; FIBRILLOGENESIS; FTIR SPECTROSCOPY; HELICAL STRUCTURES; MOLAR FRACTIONS; SHEET FORMATION; STRUCTURAL DIFFERENCES; STRUCTURAL MECHANISMS;

PEPTIDES;

AMYLOID BETA PROTEIN; GLUTAMIC ACID; PRION; PROTEIN AGGREGATE;

ALZHEIMER DISEASE; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PATHOLOGY; PRION; PROTEIN SECONDARY STRUCTURE; PROTEINOSIS; ULTRASTRUCTURE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; GLUTAMIC ACID; HUMANS; MODELS, MOLECULAR; PRIONS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN STRUCTURE, SECONDARY;

EID: 84901682732     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp412743s     Document Type: Article

References (53)

1. Hardy, J.; Allsop, D. Amyloid Deposition as the Central Event in the Aetiology of Alzheimer's Disease Trends Pharmacol. Sci. 1991, 12, 383-388
2. Pike, C. J.; Burdick, D.; Walencewicz, A. J.; Glabe, C. G.; Cotman, C. W. Neurodegeneration Induced by β-Amyloid Peptides in vitro: The Role of Peptide Assembly State J. Neurosci. 1993, 13, 1676-1687 (Pubitemid 23095409)
3. Hardy, J.; Selkoe, D. J. The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics Science 2002, 297, 353-356 (Pubitemid 34790756)
4. Kirkitadze, M. D.; Bitan, G.; Teplow, D. B. Paradigm Shifts in Alzheimer's Disease and Other Neurodegenerative Disorders: The Emerging Role of Oligomeric Assemblies J. Neurosci. Res. 2002, 69, 567-577 (Pubitemid 34966869)
5. Klein, W. L.; Stine, W. B.; Teplow, D. B. Small Assemblies of Unmodified Amyloid β-Protein Are the Proximate Neurotoxin in Alzheimer's Disease Neurobiol. Aging 2004, 25, 569-580 (Pubitemid 38686476)
6. 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.; Bowers, M. T. Amyloid-β Protein Oligomerization and the Importance of Tetramers and Dodecamers in the Aetiology of Alzheimer's Disease Nat. Chem. 2009, 1, 326-331
7. Masters, C. L.; Selkoe, D. J. Biochemistry of Amyloid β-Protein and Amyloid Deposits in Alzheimer Disease Cold Spring Harb. Perspect. Med. 2012, 2 (a006262) 1-24
8. Benilova, I.; Karran, E.; De Strooper, B. The Toxic Aβ Oligomer and Alzheimer's Disease: An Emperor in Need of Clothes Nat. Neurosci. 2012, 15, 349-357
9. Tomaselli, S.; Esposito, V.; Vangone, P.; van Nuland, N. A.; Bonvin, A. M.; Guerrini, R.; Tancredi, T.; Temussi, P. A.; Picone, D. The α-to-β Conformational Transition of Alzheimer's Aβ-(1-42) Peptide in Aqueous Media is Reversible: A Step by Step Conformational Analysis Suggests the Location of β Conformation Seeding ChemBioChem 2006, 7, 257-267 (Pubitemid 43220939)
10. Eanes, E. D.; Glenner, G. G. X-Ray Diffraction Studies on Amyloid Filaments J. Histochem. Cytochem. 1968, 16, 673-677
11. Kirschner, D. A.; Inouye, H.; Duffy, L. K.; Sinclair, A.; Lind, M.; Selkoe, D. J. Synthetic Peptide Homologous to Beta Protein from Alzheimer Disease Forms Amyloid-Like Fibrils in vitro Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 6953-6957
12. Petkova, A. T.; Buntkowsky, G.; Dyda, F.; Leapman, R. D.; Yau, W. M.; Tycko, R. Solid State NMR Reveals a pH-Dependent Antiparallel β-Sheet Registry in Fibrils Formed by a β-Amyloid Peptide J. Mol. Biol. 2004, 335, 247-260 (Pubitemid 37494976)
13. Chaney, M. O.; Webster, S. D.; Kuo, Y. M.; Roher, A. E. Molecular Modeling of the Aβ1-42 Peptide from Alzheimer's Disease Protein Eng. 1998, 11, 761-767 (Pubitemid 28434485)
14. Petkova, A. T.; Ishii, Y.; Balbach, J. J.; Antzutkin, O. N.; Leapman, R. D.; Delaglio, F.; Tycko, R. A Structural Model for Alzheimer's β-Amyloid Fibrils Based on Experimental Constraints from Solid State NMR Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16742-16747 (Pubitemid 36034043)
15. Paravastu, A. K.; Leapman, R. D.; Yau, W. M.; Tycko, R. Molecular Structural Basis for Polymorphism in Alzheimer's β-Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18349-18354
16. Goldsbury, C. S.; Wirtz, S.; Müller, S. A.; Sunderji, S.; Wicki, P.; Aebi, U.; Frey, P. Studies on the in vitro Assembly of Aβ 1-40: Implications for the Search for Aβ Fibril Formation Inhibitors J. Struct. Biol. 2000, 130, 217-231
17. Török, M.; Milton, S.; Kayed, R.; Wu, P.; McIntire, T.; Glabe, C. G.; Langen, R. Structural and Dynamic Features of Alzheimer's Aβ Peptide in Amyloid Fibrils Studied by Site-Directed Spin Labeling J. Biol. Chem. 2002, 277, 40810-40815 (Pubitemid 35215666)
18. 1-42 Fibrils Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17342-17347
19. Kim, Y. S.; Liu, L.; Axelsen, P. H.; Hochstrasser, R. M. Two-Dimensional Infrared Spectra of Isotopically Diluted Amyloid Fibrils from Aβ40 Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 7720-7725 (Pubitemid 351872705)
20. Paul, C.; Axelsen, P. H. β Sheet Structure in Amyloid β Fibrils and Vibrational Dipolar Coupling J. Am. Chem. Soc. 2005, 127, 5754-5755 (Pubitemid 40577610)
21. Cerf, E.; Sarroukh, R.; Tamamizu-Kato, S.; Breydo, L.; Derclaye, S.; Dufrêne, Y. F.; Narayanaswami, V.; Goormaghtigh, E.; Ruysschaert, J. M.; Raussens, V. Antiparallel β-Sheet: A Signature Structure of the Oligomeric Amyloid β-Peptide Biochem. J. 2009, 421, 415-423
22. Schilling, S.; Lauber, T.; Schaupp, M.; Manhart, S.; Scheel, E.; Böhm, G.; Demuth, H. U. On the Seeding and Oligomerization of pGlu-Amyloid Peptides (in vitro) Biochemistry 2006, 45, 12393-12399 (Pubitemid 44583682)
23. Schlenzig, D.; Manhart, S.; Cinar, Y.; Kleinschmidt, M.; Hause, G.; Willbold, D.; Funke, S. A.; Schilling, S.; Demuth, H. U. Pyroglutamate Formation Influences Solubility and Amyloidogenicity of Amyloid Peptides Biochemistry 2009, 48, 7072-7078
24. Schlenzig, D.; Rönicke, R.; Cynis, H.; Ludwig, H. H.; Scheel, E.; Reymann, K.; Saido, T.; Hause, G.; Schilling, S.; Demuth, H. U. N-Terminal Pyroglutamate Formation of Aβ38 and Aβ40 Enforces Oligomer Formation and Potency To Disrupt Hippocampal Long-Term Potentiation J. Neurochem. 2012, 121, 774-784
25. He, W.; Barrow, C. J. The Aβ 3-Pyroglutamyl and 11-Pyroglutamyl Peptides Found in Senile Plaque Have Greater β-Sheet Forming and Aggregation Propensities in vitro than Full-Length Aβ Biochemistry 1999, 38, 10871-10877
26. Wirths, O.; Erck, C.; Martens, H.; Harmeier, A.; Geumann, C.; Jawhar, S.; Kumar, S.; Multhaup, G.; Walter, J.; Ingelsson, M.; Degerman-Gunnarsson, M.; Kalimo, H.; Huitinga, I.; Lannfelt, L.; Bayer, T. A. Identification of Low Molecular Weight Pyroglutamate Aβ Oligomers in Alzheimer Disease: A Novel Tool for Therapy and Diagnosis J. Biol. Chem. 2010, 285, 41517-41524
27. Nussbaum, J. M.; Schilling, S.; Cynis, H.; Silva, A.; Swanson, E.; Wangsanut, T.; Tayler, K.; Wiltgen, B.; Hatami, A.; Rönicke, R.; Reymann, K.; Hutter-Paier, B.; Alexandru, A.; Jagla, W.; Graubner, S.; Glabe, C. G.; Demuth, H. U.; Bloom, G. S. Prion-Like Behaviour and Tau-Dependent Cytotoxicity of Pyroglutamylated Amyloid-β Nature 2012, 485, 651-655
28. pE - Strongly Affect Cultured Neuron and Astrocyte Survival J. Neurochem. 2002, 82, 1480-1489
29. Sun, N.; Hartmann, R.; Lecher, J.; Stoldt, M.; Funke, S. A.; Gremer, L.; Ludwig, H. H.; Demuth, H. U.; Kleinschmidt, M.; Willbold, D. Structural Analysis of the Pyroglutamate-Modified Isoform of the Alzheimer's Disease-Related Amyloid-β Using NMR Spectroscopy J. Pept. Sci. 2012, 18, 691-695
30. Tekirian, T. L.; Yang, A. Y.; Glabe, C.; Geddes, J. W. Toxicity of Pyroglutaminated Amyloid β-Peptides 3pE-40 and -42 is Similar to that of Aβ 1-40 and -42 J. Neurochem. 1999, 73, 1584-1589 (Pubitemid 29440160)
31. Sanders, H. M.; Lust, R.; Teller, J. K. Amyloid-β Peptide Aβp3-42 Affects Early Aggregation of Full-Length Aβ1-42 Peptides 2009, 30, 849-854
32. Petkova, A. T.; Leapman, R. D.; Guo, Z.; Yau, W. M.; Mattson, M. P.; Tycko, R. Self-Propagating, Molecular-Level Polymorphism in Alzheimer's β-Amyloid Fibrils Science 2005, 307, 262-265 (Pubitemid 40116242)
33. Jeong, J. S.; Ansaloni, A.; Mezzenga, R.; Lashuel, H. A.; Dietler, G. Novel Mechanistic Insight into the Molecular Basis of Amyloid Polymorphism and Secondary Nucleation during Amyloid Formation J. Mol. Biol. 2013, 425, 1765-1781
34. pE, in Senile Plaques Neuron 1995, 14, 457-466
35. Wu, G.; Miller, R. A.; Connolly, B.; Marcus, J.; Renger, J.; Savage, M. J. Pyroglutamate-Modified Amyloid-β Protein Demonstrates Similar Properties in an Alzheimer's Disease Familial Mutant Knock-In Mouse and Alzheimer's Disease Brain Neurodegener. Dis. 2013, Oct 23, 1-14
36. Nilsson, M. R. Techniques To Study Amyloid Fibril Formation in vitro Methods 2004, 34, 151-160 (Pubitemid 38993215)
37. Tatulian, S. A.; Garg, G.; Nemec, K. N.; Chen, B.; Khaled, A. R. Molecular Basis for Membrane Pore Formation by Bax Protein Carboxyl Terminus Biochemistry 2012, 51, 9406-9419
38. D'Arrigo, C.; Tabaton, M.; Perico, A. N-Terminal Truncated Pyroglutamyl β Amyloid Peptide Aβpy3-42 Shows a Faster Aggregation Kinetics than the Full-Length Aβ1-42 Biopolymers 2009, 91, 861-873
39. Galante, D.; Corsaro, A.; Florio, T.; Vella, S.; Pagano, A.; Sbrana, F.; Vassalli, M.; Perico, A.; D'Arrigo, C. Differential Toxicity, Conformation and Morphology of Typical Initial Aggregation States of Aβ1-42 and Aβpy3-42 Beta-Amyloids Int. J. Biochem. Cell Biol. 2012, 44, 2085-2093
40. Sreerama, N.; Woody, R. W. Circular Dichroism of Peptides and Proteins. In Circular Dichroism: Principles and Applications; Berova, N.; Nakanishi, K.; Woody, R. W., Eds.; John Wiley & Sons: Hoboken, NJ, 2000; pp 601-620.
41. Bakshi, K.; Liyanage, M. R.; Volkin, D. B.; Middaugh, C. R. Circular Dichroism of Peptides Methods Mol. Biol. 2014, 1088, 247-253
42. Sreerama, N.; Venyaminov, S. Y.; Woody, R. W. Estimation of the Number of α-Helical and β-Strand Segments in Proteins Using Circular Dichroism Spectroscopy Protein Sci. 1999, 8, 370-380 (Pubitemid 29072437)
43. Decatur, S. M. Elucidation of Residue-Level Structure and Dynamics of Polypeptides via Isotope-Edited Infrared Spectroscopy Acc. Chem. Res. 2006, 39, 169-175
44. Haris, P. I. Probing Protein-Protein Interaction in Biomembranes Using Fourier Transform Infrared Spectroscopy Biochim. Biophys. Acta 2013, 1828, 2265-2271
45. Tatulian, S. A. Structural Characterization of Membrane Proteins and Peptides by FTIR and ATR-FTIR Spectroscopy Methods Mol. Biol. 2013, 974, 177-218
46. Goormaghtigh, E.; Cabiaux, V.; Ruysschaert, J. M. Determination of Soluble and Membrane Protein Structure by Fourier Transform Infrared Spectroscopy. III. Secondary Structures Subcell. Biochem. 1994, 23, 405-450
47. Bakshi, K.; Liyanage, M. R.; Volkin, D. B.; Middaugh, C. R. Fourier Transform Infrared Spectroscopy of Peptides Methods Mol. Biol. 2014, 1088, 255-269
48. 16-22 Peptide J. Am. Chem. Soc. 2005, 127, 13488-13489 (Pubitemid 41401188)
49. Petty, S. A.; Decatur, S. M. Intersheet Rearrangement of Polypeptides during Nucleation of β-Sheet Aggregates Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 14272-14277 (Pubitemid 41429688)
50. Kim, Y. S.; Liu, L.; Axelsen, P. H.; Hochstrasser, R. M. 2D IR Provides Evidence for Mobile Water Molecules in β-Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 17751-17756
51. Benilova, I.; De Strooper, B. Promiscuous Alzheimer's Amyloid: Yet Another Partner Science 2013, 341, 1354-1355
52. Deshpande, A.; Mina, E.; Glabe, C.; Busciglio, J. Different Conformations of Amyloid β Induce Neurotoxicity by Distinct Mechanisms in Human Cortical Neurons J. Neurosci. 2006, 26, 6011-6018 (Pubitemid 44318367)
53. Manczak, M.; Calkins, M. J.; Reddy, P. H. Impaired Mitochondrial Dynamics and Abnormal Interaction of Amyloid β with Mitochondrial Protein Drp1 in Neurons from Patients with Alzheimer's Disease: Implications for Neuronal Damage Hum. Mol. Genet. 2011, 20, 2495-2509