Orientations of residues along the β-arch of self-assembled amylin fibril-like structures lead to polymorphism

Biomacromolecules

Volumn 16, Issue 1, 2015, Pages 156-165

  Wineman Fisher, Vered ^a   Atsmon Raz, Yoav ^a   Miller, Yifat ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOMERS; PEPTIDES; PROTEINS;

AMYLOID DEPOSITS; ATOMIC LEVELS; CRYSTAL MODELS; EXPERIMENTAL MODELS; EXTRACELLULAR; SELF-ASSEMBLED; SIDE-CHAINS; TYPE-2 DIABETES;

ARCHES;

AMYLIN; HYDROGEN; AMYLOID;

ARTICLE; CHEMICAL STRUCTURE; FIBER; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN POLYMORPHISM; X RAY CRYSTALLOGRAPHY; CHEMISTRY; PROTEIN SECONDARY STRUCTURE;

AMYLOID; ISLET AMYLOID POLYPEPTIDE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84921019880     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm501326y     Document Type: Article

References (73)

1. Diabetes Atlas, 5th ed.; International Diabetes Federation: Brussels, Belgium, 2011.
2. Clark, A.; Cooper, G. J.; Lewis, C. E.; Morris, J. F.; Willis, A. C.; Reid, K. B.; Turner, R. C. Islet amyloid formed from diabetes-associated peptide may be pathogenic in type-2 diabetes. Lancet 1987, 2, 231-4.
3. Clark, A.; de Koning, E. J.; Hattersley, A. T.; Hansen, B. C.; Yajnik, C. S.; Poulton, J. Pancreatic pathology in non-insulin dependent diabetes (NIDDM). Diabetes Res. Clin. Pract. 1995, 28, S39-47.
4. Westermark, P.; Wernstedt, C.; Wilander, E.; Hayden, D. W.; O'Brien, T. D.; Johnson, K. H. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 3881-5.
5. Westermark, P.; Wilander, E.; Johnson, K. H. Islet amyloid polypeptide. Lancet 1987, 2, 623.
6. Westermark, P.; Grimelius, L. The pancreatic islet cells in insular amyloidosis in human diabetic and non-diabetic adults. Acta Pathol. Microbiol. Scand., Sect. A 1973, 81, 291-300.
7. Caughey, B.; Lansbury, P. T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 2003, 26, 267-98.
8. Cleary, J. P.; Walsh, D. M.; Hofmeister, J. J.; Shankar, G. M.; Kuskowski, M. A.; Selkoe, D. J.; Ashe, K. H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 2005, 8, 79-84.
9. Haass, C.; Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8, 101-12.
10. Hardy, J.; Selkoe, D. J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297, 353-6.
11. 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, 1317-21.
12. Wei, L.; Jiang, P.; Xu, W.; Li, H.; Zhang, H.; Yan, L.; Chan-Park, M. B.; Liu, X. W.; Tang, K.; Mu, Y.; Pervushin, K. The molecular basis of distinct aggregation pathways of islet amyloid polypeptide. J. Biol. Chem. 2011, 286, 6291-300.
13. Jayasinghe, S. A.; Langen, R. Identifying structural features of fibrillar islet amyloid polypeptide using site-directed spin labeling. J. Biol. Chem. 2004, 279, 48420-5.
14. Bedrood, S.; Li, Y.; Isas, J. M.; Hegde, B. G.; Baxa, U.; Haworth, I. S.; Langen, R. Fibril structure of human islet amyloid polypeptide. J. Biol. Chem. 2012, 287, 5235-41.
15. Kajava, A. V.; Aebi, U.; Steven, A. C. The parallel superpleated beta-structure as a model for amyloid fibrils of human amylin. J. Mol. Biol. 2005, 348, 247-52.
16. Luca, S.; Yau, W. M.; Leapman, R.; Tycko, R. Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochem 2007, 46, 13505-22.
17. Wang, L.; Middleton, C. T.; Singh, S.; Reddy, A. S.; Woys, A. M.; Strasfeld, D. B.; Marek, P.; Raleigh, D. P.; de Pablo, J. J.; Zanni, M. T.; Skinner, J. L. 2DIR spectroscopy of human amylin fibrils reflects stable beta-sheet structure. J. Am. Chem. Soc. 2011, 133, 16062-71.
18. Wiltzius, J. J.; Sievers, S. A.; Sawaya, M. R.; Cascio, D.; Popov, D.; Riekel, C.; Eisenberg, D. Atomic structure of the cross-beta spine of islet amyloid polypeptide (amylin). Protein Sci. 2008, 17, 1467-74.
19. Hu, R.; Zhang, M.; Patel, K.; Wang, Q.; Chang, Y.; Gong, X.; Zhang, G.; Zheng, J. Cross-sequence interactions between human and rat islet amyloid polypeptides. Langmuir 2014, 30, 5193-201.
20. Liang, G.; Zhao, J.; Yu, X.; Zheng, J. Comparative molecular dynamics study of human islet amyloid polypeptide (IAPP) and rat IAPP oligomers. Biochemistry 2013, 52, 1089-100.
21. Zhao, J.; Hu, R.; Sciacca, M. F.; Brender, J. R.; Chen, H.; Ramamoorthy, A.; Zheng, J. Non-selective ion channel activity of polymorphic human islet amyloid polypeptide (amylin) double channels. Phys. Chem. Chem. Phys. 2014, 16, 2368-77.
22. Zhao, J.; Yu, X.; Liang, G.; Zheng, J. Structural polymorphism of human islet amyloid polypeptide (hIAPP) oligomers highlights the importance of interfacial residue interactions. Biomacromolecules 2011, 12, 210-20.
23. Zhao, J.; Yu, X.; Liang, G.; Zheng, J. Heterogeneous triangular structures of human islet amyloid polypeptide (amylin) with internal hydrophobic cavity and external wrapping morphology reveal the polymorphic nature of amyloid fibrils. Biomacromolecules 2011, 12, 1781-94.
24. Qi, R.; Luo, Y.; Ma, B.; Nussinov, R.; Wei, G. Conformational distribution and alpha-helix to beta-sheet transition of human amylin fragment dimer. Biomacromolecules 2014, 15, 122-31.
25. Andrews, M. N.; Winter, R. Comparing the structural properties of human and rat islet amyloid polypeptide by MD computer simulations. Biophys. Chem. 2011, 156, 43-50.
26. Dupuis, N. F.; Wu, C.; Shea, J. E.; Bowers, M. T. The amyloid formation mechanism in human IAPP: dimers have beta-strand monomer-monomer interfaces. J. Am. Chem. Soc. 2011, 133, 7240-3.
27. Bernhardt, N. A.; Berhanu, W. M.; Hansmann, U. H. Mutations and seeding of amylin fibril-like oligomers. J. Phys. Chem. B 2013, 117, 16076-85.
28. Berhanu, W. M.; Hansmann, U. H. Inter-species cross-seeding: stability and assembly of rat-human amylin aggregates. PLoS One 2014, 9, e97051.
29. Xu, W.; Su, H.; Zhang, J. Z.; Mu, Y. Molecular dynamics simulation study on the molecular structures of the amylin fibril models. J. Phys. Chem. B 2012, 116, 13991-9.
30. Kalé, L.; Skeel, R.; Bhandarkar, M.; Brunner, R.; Gursoy, A.; Krawetz, N.; Phillips, J.; Shinozaki, A.; Varadarajan, K.; Schulten, K. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 1999, 151, 283.
31. MacKerell, A. D.; Bashford, D.; Bellott, R. L.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Straub, J.; Watanabe, M.; Wiórkiewicz-Kuczera, J.; Yin, D.; Karplus, M. all-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102, 3586.
32. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4, 187-217.
33. Cino, E. A.; Choy, W. Y.; Karttunen, M. Comparison of secondary structure formation using 10 different force fields in microsecond molecular dynamics simulations. J. Chem. Theory Comput. 2012, 8, 2725-2740.
34. Mackerell, A. D., Jr.; Feig, M.; Brooks, C. L., III Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 2004, 25, 1400-15.
35. Best, R. B.; Buchete, N. V.; Hummer, G. Are current molecular dynamics force fields too helical? Biophys. J. 2008, 95, L07-9.
36. Freddolino, P. L.; Park, S.; Roux, B.; Schulten, K. Force field bias in protein folding simulations. Biophys. J. 2009, 96, 3772-80.
37. Lindorff-Larsen, K.; Maragakis, P.; Piana, S.; Eastwood, M. P.; Dror, R. O.; Shaw, D. E. Systematic validation of protein force fields against experimental data. PLoS One 2012, 7, e32131.
38. Best, R. B.; Mittal, J.; Feig, M.; MacKerell, A. D., Jr. Inclusion of many-body effects in the additive CHARMM protein CMAP potential results in enhanced cooperativity of alpha-helix and beta-hairpin formation. Biophys. J. 2012, 103, 1045-51.
39. Mahoney, M. W.; Jorgensen, W. L. A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J. Chem. Phys. 2000, 112, 8910-8922.
40. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79, 926-935.
41. Tu, K.; Tobias, D. J.; Klein, M. L. Constant pressure and temperature molecular dynamics simulation of a fully hydrated liquid crystal phase dipalmitoylphosphatidylcholine bilayer. Biophys. J. 1995, 69, 2558-62.
42. Feller, S. E.; Zhang, Y.; Pastor, R. W.; Brooks, B. R. Constant pressure molecular dynamics simulation: the Langevin piston method. J. Chem. Phys. 1995, 103, 4613-21.
43. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103, 8577-93.
44. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: an N· log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-92.
45. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327.
46. Lee, M. S.; Feig, M.; Salsbury, F. R., Jr.; Brooks, C. L., III New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations. J. Comput. Chem. 2003, 24, 1348-56.
47. Lee, M. S.; Salsbury, J. F. R.; Brooks, C. L., III Novel generalized Born methods. J. Chem. Phys. 2002, 116, 10606-10614.
48. Raz, Y.; Miller, Y. Interactions between Abeta and mutated Tau lead to polymorphism and induce aggregation of Abeta-mutated tau oligomeric complexes. PLoS One 2013, 8, e73303.
49. Miller, Y.; Ma, B.; Nussinov, R. Polymorphism of Alzheimer's Abeta17-42 (p3) oligomers: the importance of the turn location and its conformation. Biophys. J. 2009, 97, 1168-77.
50. Miller, Y.; Ma, B.; Nussinov, R. Synergistic interactions between repeats in tau protein and Abeta amyloids may be responsible for accelerated aggregation via polymorphic states. Biochemistry 2011, 50, 5172-81.
51. Raz, Y.; Adler, J.; Vogel, A.; Scheidt, H. A.; Haupl, T.; Abel, B.; Huster, D.; Miller, Y. The influence of the DeltaK280 mutation and Nor C-terminal extensions on the structure, dynamics, and fibril morphology of the tau R2 repeat. Phys. Chem. Chem. Phys. 2014, 16, 7710-7.
52. Miller, Y.; Ma, B.; Tsai, C. J.; Nussinov, R. Hollow core of Alzheimer's Abeta42 amyloid observed by cryoEM is relevant at physiological pH. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 14128-33.
53. Miller, Y.; Ma, B.; Nussinov, R. Zinc ions promote Alzheimer Abeta aggregation via population shift of polymorphic states. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 9490-5.
54. Miller, Y.; Ma, B.; Nussinov, R. Polymorphism in Alzheimer Abeta amyloid organization reflects conformational selection in a rugged energy landscape. Chem. Rev. 2010, 110, 4820-38.
55. Fandrich, M.; Meinhardt, J.; Grigorieff, N. Structural polymorphism of Alzheimer Abeta and other amyloid fibrils. Prion 2009, 3, 89-93.
56. Meinhardt, J.; Sachse, C.; Hortschansky, P.; Grigorieff, N.; Fandrich, M. Abeta(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils. J. Mol. Biol. 2009, 386, 869-77.
57. Pham, J. D.; Demeler, B.; Nowick, J. S. Polymorphism of oligomers of a peptide from beta-amyloid. J. Am. Chem. Soc. 2014, 136, 5432-42.
58. Raz, Y.; Rubinov, B.; Matmor, M.; Rapaport, H.; Ashkenasy, G.; Miller, Y. Effects of mutations in de novo designed synthetic amphiphilic beta-sheet peptides on self-assembly of fibrils. Chem. Commun. 2013, 49, 6561-3.
59. Paravastu, A. K.; Leapman, R. D.; Yau, W. M.; Tycko, R. Molecular structural basis for polymorphism in Alzheimer's betaamyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18349-54.
60. Miller, Y.; Ma, B.; Nussinov, R. The unique Alzheimer's beta-amyloid triangular fibril has a cavity along the fibril axis under physiological conditions. J. Am. Chem. Soc. 2011, 133, 2742-8.
61. Ma, B.; Elkayam, T.; Wolfson, H.; Nussinov, R. Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 5772-7.
62. Porat, Y.; Mazor, Y.; Efrat, S.; Gazit, E. Inhibition of islet amyloid polypeptide fibril formation: a potential role for heteroaromatic interactions. Biochemistry 2004, 43, 14454-62.
63. Azriel, R.; Gazit, E. Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation. J. Biol. Chem. 2001, 276, 34156-61.
64. Marek, P.; Abedini, A.; Song, B.; Kanungo, M.; Johnson, M. E.; Gupta, R.; Zaman, W.; Wong, S. S.; Raleigh, D. P. Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 2007, 46, 3255-61.
65. Thirumalai, D.; Reddy, G.; Straub, J. E. Role of water in protein aggregation and amyloid polymorphism. Acc. Chem. Res. 2012, 45, 83-92.
66. Krone, M. G.; Hua, L.; Soto, P.; Zhou, R.; Berne, B. J.; Shea, J. E. Role of water in mediating the assembly of Alzheimer amyloid-beta Abeta16-22 protofilaments. J. Am. Chem. Soc. 2008, 130, 11066-72.
67. Reddy, G.; Straub, J. E.; Thirumalai, D. Dry amyloid fibril assembly in a yeast prion peptide is mediated by long-lived structures containing water wires. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 21459-64.
68. Yoon, G.; Lee, M.; Kim, J. I.; Na, S.; Eom, K. Role of sequence and structural polymorphism on the mechanical properties of amyloid fibrils. PLoS One 2014, 9, e88502.
69. Sawaya, M. R.; Sambashivan, S.; Nelson, R.; Ivanova, M. I.; Sievers, S. A.; Apostol, M. I.; Thompson, M. J.; Balbirnie, M.; Wiltzius, J. J.; McFarlane, H. T.; Madsen, A. O.; Riekel, C.; Eisenberg, D. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 2007, 447, 453-7.
70. Berryman, J. T.; Radford, S. E.; Harris, S. A. Thermodynamic description of polymorphism in Q- and N-rich peptide aggregates revealed by atomistic simulation. Biophys. J. 2009, 97, 1-11.
71. Berryman, J. T.; Radford, S. E.; Harris, S. A. Systematic examination of polymorphism in amyloid fibrils by moleculardynamics simulation. Biophys. J. 2011, 100, 2234-42.
72. Park, J.; Kahng, B.; Hwang, W. Thermodynamic selection of steric zipper patterns in the amyloid cross-beta spine. PLoS Comput. Biol. 2009, 5, e1000492.
73. Buchanan, L. E.; Dunkelberger, E. B.; Tran, H. Q.; Cheng, P. N.; Chiu, C. C.; Cao, P.; Raleigh, D. P.; de Pablo, J. J.; Nowick, J. S.; Zanni, M. T. Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient beta-sheet. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 19285-90.