Side-chain hydrophobicity and the stability of Aβ16-22 aggregates

Protein Science

Volumn 21, Issue 12, 2012, Pages 1837-1848

  Berhanu, Workalemahu M ^a   Hansmann, Ulrich H E ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Amyloids; Force fields; Hydrophobicity; Molecular dynamics

Indexed keywords

AMINO ACID; AMYLOID BETA PROTEIN[1-40]; OLIGOMER;

ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENE REARRANGEMENT; GENETIC STABILITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; WILD TYPE;

AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN STABILITY;

EID: 84870371359     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2164     Document Type: Article

References (72)

1. Glenner GG, Wong CW (1984) Alzheimers disease - initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
2. 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 69:567-577.
3. Eisenberg D JM (2012) The amyloid state of proteins in human diseases. Cell 148:1188-1203.
4. Balbach JJ, Ishii Y, Antzutkin ON, Leapman RD, Rizzo NW, Dyda F, Reed J, Tycko R (2000) Amyloid fibrilformation by A beta(16-22), a seven-residue fragment of the Alzheimer's beta-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39: 13748-13759.
5. Williams AD, Portelius E, Kheterpal I, Guo JT, Cook KD, Xu Y, Wetzel R (2004) Mapping A beta amyloid fibril secondary structure using scanning proline mutagenesis. J Mol Biol 335:833-842.
6. Findeis MA, Musso GM, Arico-Muendel CC, Benjamin HW, Hundal AM, Lee JJ, Chin J, Kelley M, Wakefield J, Hayward NJ, Molineaux SM (1999) Modified-peptide inhibitors of amyloid beta-peptide polymerization. Biochemistry 38:6791-6800.
7. Soto C, Sigurdsson EM, Morelli L, Kumar RA, Castano EM, Frangione B (1998) Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy. Nat Med 4: 822-826.
8. Gazit E (2007) Self assembly of short aromatic peptides into amyloid fibrils and related nanostructures. Prion 1:32-35.
9. Adler-Abramovich L, Vaks L, Carny O, Trudler D, Magno A, Caflisch A, Frenkel D, Gazit E (2012) Phenylalanine assembly into toxic fibrils suggests amyloid etiology in phenylketonuria. Nat Chem Biol 8:701-706.
10. Armstrong AH, Chen J, McKoy AF, Hecht MH (2011) Mutations that replace aromatic side chains promote aggregation of the Alzheimer's A beta peptide. Biochemistry 50:4058-4067.
11. Senguen FT, Doran TM, Anderson EA, Nilsson BL (2011) Clarifying the influence of core amino acid hydrophobicity, secondary structure propensity, and molecular volume on amyloid-beta 16-22 self-assembly. Mol Biosyst 7:497-510.
12. Berhanu WM, Masunov AM (2012) Unique example of amyloid aggregates stabilized by main chain H-bond instead of the steric zipper: molecular dynamics study of the amyloidogenic segment of amylin wild-type and mutants. J Mol Model 18:891-903.
13. Berhanu WM, Masunov AM (2012) Controlling the aggregation and rate of release in order to improve insulin formulation: molecular dynamics study of fulllength insulin amyloid oligomer models. J Mol Model 18:1129-1142.
14. Workalemahu M, Berhanu AM, Masunov AE (2012) Alternative packing modes leading to amyloid polymorphism in five fragments studied with molecular dynamics. Peptide Sci 98:131-144.
15. Berhanu WM, Masunov AE (2010) Natural polyphenols as inhibitors of amyloid aggregation. Molecular dynamics study of GNNQQNY heptapeptide decamer. Biophys Chem 149:12-21.
16. Berhanu WM, Masunov AE (2011) Can molecular dynamics simulations assist in design of specific inhibitors and imaging agents of amyloid aggregation? Structure, stability and free energy predictions for amyloid oligomers of VQIVYK, MVGGVV and LYQLEN. J Mol Model 1:2423-2442.
17. Friedman R (2011) Aggregation of amyloids in a cellular context: modelling and experiment. Biochem J 438: 415-426.
18. Jun-tao Guo CKH, Xu Y, Wetzel R, Modeling protein aggregate assembly and structure. In: Ying Xu, Dong Xu, Jie Liang, Eds. (2007) Computational Methods for Protein Structure Prediction and Modeling. New York: Springer, pp 279-318.
19. Adcock SA, McCammon J A (2006) Molecular dynamics: Survey of methods for simulating the activity of proteins. Chem Rev 106:1589-1615.
20. Durrant JD, McCammon JA (2011) Molecular dynamics simulations and drug discovery. BMC Biol 9:9.
21. Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, Merz KM, Onufriev A, Simmerling C, Wang B, Woods RJ (2005) The Amber biomolecular simulation programs. J Comput Chem 26:1668-1688.
22. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616.
23. Christen M, Hunenberger PH, Bakowies D, Baron R, Burgi R, Geerke DP, Heinz TN, Kastenholz MA, Krautler V, Oostenbrink C, Peter C, Trzesniak D, Van Gunsteren WF (2005) The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 26:1719-1751.
24. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J Phys Chem B 105:6474-6487.
25. Todorova N, Legge FS, Treutlein H, Yarovsky I (2008) Systematic comparison of empirical forcefields for molecular dynamic simulation of insulin. J Phys Chem B 112:11137-11146.
26. Feig M, MacKerell AD, Brooks CL (2003) Force field influence on the observation of pi-helical protein structures in molecular dynamics simulations. J Phys Chem B 107:2831-2836.
27. Mu YG, Kosov DS, Stock G. (2003) Conformational dynamics of trialanine in water. 2. Comparison of AMBER, CHARMM, GROMOS, and OPLS force fields to NMR and infrared experiments. J Phys Chem B 107:5064-5073.
28. Yoda T, Sugita Y, Okamoto Y (2004) Comparisons of force fields for proteins by generalized-ensemble simulations. Chem Phys Lett 386:460-467.
29. Nguyen PH, Li MS, Derreumaux P (2011) Effects of all-atom force fields on amyloid oligomerization: replica exchange molecular dynamics simulations of the A beta(16-22) dimer and trimer. Phys Chem Chem Phys 13:9778-9788.
30. Anand P, Hansmann UHE (2011) Internal and environmental effects on folding and dimerisation of Alzheimer's beta-amyloid peptide. Mol Simulat 37:440-448.
31. Huet A, Derreumaux P (2006) Impact of the mutation A21G (Flemish variant) on Alzheimer's beta-amyloid dimers by molecular dynamics simulations. Biophys J 91:3829-3840.
32. Baumketner A, Krone MG, Shea JE (2008) Role of the familial Dutch mutation E22Q in the folding and aggregation of the 15-28 fragment of the Alzheimer amyloid-beta protein. Proc Natl Acad Sci USA 105: 6027-6032.
33. Fawzi NL, Kohlstedt KL, Okabe Y, Head-Gordon T (2008) Protofibril assemblies of the arctic, Dutch, and Flemish mutants of the Alzheimer's A beta(1-40) peptide. Biophys J 94:2007-2016.
34. Berhanu WM HU (2012) Structure and dynamics of amyloid-β segmental polymorphisms. PLoS One 7:e41479.
35. Chebaro Y, Derreumaux P (2009) Targeting the early steps of A beta 16-22 protofibril disassembly by N-methylated inhibitors: A numerical study. Proteins 75:442-452.
36. Takeda T, Klimov DK (2008) Temperature-induced dissociation of A beta monomers from amyloid fibril. Biophys J 95:1758-1772.
37. Takeda T, Klimov DK. (2007) Dissociation of A beta(16-22) amyloid fibrils probed by molecular dynamics. J Mol Biol 368:1202-1213.
38. Chebaro Y JP, Zang T, Mu Y, Nguyen PH, Mousseau N, Derreumaux P (2012) Structures of Aβ17-42 trimers in isolation and with five small-molecule drugs using a hierarchical computational procedure. J Phys Chem B 116:8412-8422.
39. Takeda T, Klimov DK (2009) Replica exchange simulations of the thermodynamics of a beta fibril growth. Biophys J 96:442-452.
40. Takeda T, Klimov DK (2009) Probing energetics of a beta fibril elongation by molecular dynamics simulations. Biophys J 96:4428-4437.
41. Han M, Hansmann UHE (2011) Replica exchange molecular dynamics of the thermodynamics of fibril growth of Alzheimer's A beta(42) peptide. J Chem Phys 135:6.
42. Rojas A, Liwo A, Browne D, Scheraga HA (2010) Mechanism of fiber assembly: Treatment of a beta peptide aggregation with a coarse-grained united-residue force field. J Mol Biol 404:537-552.
43. Li MS, Co NT, Reddy G, Hu CK, Straub JE, Thirumalai D (2010) Factors governing fibrillogenesis of polypeptide chains revealed by lattice models. Phys Rev Lett 105:4.
44. Wei GH, Mousseau N, Derreumaux P (2007) Computational simulations of the early steps of protein aggregation. Prion 1:3-8.
45. Ma BY, Nussinov (2006) Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Curr Opin Struct Biol 10:445-452.
46. Blinov N, Dorosh L, Wishart D, Kovalenko A (2010) Association thermodynamics and conformational stability of beta-sheet amyloid beta(17-42) oligomers: Effects of E22Q (Dutch) mutation and charge neutralization. Biophys J 98:282-296.
47. Cruz L, Urbanc B, Borreguero JM, Lazo ND, Teplow DB, Stanley HE (2005) Solvent and mutation effects on the nucleation of amyloid beta-protein folding. Proc Natl Acad Sci USA 102:18258-18263.
48. Massi F, Klimov D, Thirumalai D, Straub JE (2002) Charge states rather than propensity for beta-structure determine enhanced fibrillogenesis in wild-type Alzheimer's beta-amyloid peptide compared to E22Q Dutch mutant. Protein Sci 11:1639-1647.
49. Berhanu WM, Mikhailov IA, Masunov AE (2010) Are density functional theory predictions of the Raman spectra accurate enough to distinguish conformational transitions during amyloid formation? J Mol Model 16: 1093-1101.
50. Fernandez A, Scheraga HA (2003) Insufficiently dehydrated hydrogen bonds as determinants of protein interactions. Proc Natl Acad Sci USA 100:113-118.
51. Straub JE, Thirumalai D (2010) Principles governing oligomer formation in amyloidogenic peptides. Curr Opin Struct Biol 20:187-195.
52. Rohrig UF, Laio A, Tantalo N, Parrinello M, Petronzio R (2006) Stability and structure of oligomers of the Alzheimer peptide A beta(16-22): from the dimer to the 32-mer. Biophys J 91:3217-3229.
53. Chelli R, Gervasio FL, Procacci P, Schettino V (2002) Stacking and T-shape competition in aromatic-aromatic amino acid interactions. J Am Chem Soc 124:6133-6143.
54. Kuznicki T, Masliyah JH, Bhattacharjee S (2009) Aggregation and partitioning of model asphaltenes at toluene-water interfaces: Molecular dynamics simulations. Energy Fuels 23:5027-5035.
55. Zgarbova M, Otyepka M, Sponer J, Hobza P, Jurecka P (2010) Large-scale compensation of errors in pairwise-additive empirical force fields: comparison of AMBER intermolecular terms with rigorous DFT-SAPT calculations. Phys Chem Chem Phys 12:10476-10493.
56. Van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC (2005) GROMACS: fast, flexible, and free. J Comput Chem 26:1701-1718.
57. Massi F, Peng JW, Lee JP, Straub JE (2001) Simulation study of the structure and dynamics of the Alzheimer's amyloid peptide congener in solution. Biophys J 80: 31-44.
58. Berhanu WM, Masunov AE (2011) Molecular dynamic simulation of wild type and mutants of the polymorphic amyloid NNQNTF segments of elk prion: Structural stability and thermodynamic of association. Biopolymers 95:573-590.
59. 10-35): Sequence effects. Proc Natl Acad Sci USA 99:14126-14131.
60. Fauchere JL, Pliska V (1983) hydrophobic parameterspi of amino-acid side-chains from the partitioning of n-acetyl-amino-acid amides. Eur J Med Chem 18: 369-375.
61. Costantini S, Colonna G, Facchiano AM (2006) Amino acid propensities for secondary structures are influenced by the protein structural class. Biochem Biophys Res Commun 342:441-451.
62. Colletier JP, Laganowsky A, Landau M, Zhao ML, Soriaga AB, Goldschmidt L, Flot D, Cascio D, Sawaya MR, Eisenberg D (2011) Molecular basis for amyloid-beta polymorphism. Proc Natl Acad Sci USA 108: 16938-16943.
63. Tycko R, Sciarretta KL, Orgel J, Meredith SC (2009) Evidence for novel beta-sheet structures in Iowa mutant beta-amyloid fibrils. Biochemistry 48:6072-6084.
64. Darden T, York D, Pedersen L (1993) Particle Mesh Ewald - an N.log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092.
65. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577-8593.
66. Hess B (2008) P-LINCS: A parallel linear constraint solver for molecular simulation. J Chem Theory Comput 4:116-122.
67. Miyamoto S, Kollman PA (1992) Settle - an analytical version of the shake and rattle algorithm for rigid water models. J Comput Chem 13:952-962.
68. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126:7.
69. Parrinello M, Rahman A (1981) Polymorphic transitions in single-crystals - a new molecular-dynamics method. J Appl Phys 52:7182-7190.
70. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78:1950-1958.
71. Meersman F, Dobson CM (2006) Probing the pressuretemperature stability of amyloid fibrils provides new insights into their molecular properties. Biochim Biophys Acta 1764:452-460.
72. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graphics 14:33-38.