Interaction of amyloid inhibitor proteins with amyloid beta peptides: Insight from molecular dynamics simulations

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Das, Payel ^a   Kang, Seung Gu ^a   Temple, Sally ^b   Belfort, Georges ^c  

^a IBM T J WATSON RESEARCH CENTER   (United States)

^b Neural Stem Cell Institute   (United States)

^c Rensselaer Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; AMYLOID BETA PROTEIN; AMYLOID INHIBITOR PROTEIN; BETA CRYSTALLIN; INHIBITOR PROTEIN; MONOMER; OLIGOMER; UNCLASSIFIED DRUG; LYSOZYME; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; LYSOSOME; MOLECULAR DYNAMICS; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STATIC ELECTRICITY; AMINO ACID SEQUENCE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEINOSIS;

ALPHA-CRYSTALLIN B CHAIN; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; BINDING SITES; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MURAMIDASE; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING;

EID: 84912525082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113041     Document Type: Article

References (97)

1. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-766.
2. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, et al. (2007) Natural Oligomers of the Alzheimer Amyloid-beta Protein Induce Reversible Synapse Loss by Modulating an NMDA-Type Glutamate Receptor-Dependent Signaling Pathway. J Neurosci 27: 2866-2875.
3. Quist A, Doudevski I, Lin H, Azimova R, Ng D, et al. (2005) Amyloid ion channels: A common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 102: 10427-10432.
4. Bonda DJ, Wang X, Perry G, Nunomura A, Tabaton M, et al. (2010) Oxidative stress in Alzheimer disease: A possibility for prevention. Neuropharmacology 59: 290-294.
5. Sakono M, Zako T (2010) Amyloid oligomers: formation and toxicity of Ab oligomers. FEBS J 277: 1348-1358.
6. Vandersteen A, Hubin E, Sarroukh R, De Baets G, Schymkowitz J, et al. (2012) A comparative analysis of the aggregation behavior of amyloid-beta peptide variants. FEBS Lett 586: 4088-4093.
7. Tycko R, Thomas L. James VDt, Uli S (2001) [19] Solid-state nuclear magnetic resonance techniques for structural studies of amyloid fibrils. Method Enzymol: Academic Press. pp. 390-413.
8. Petkova AT, Yau W-M, Tycko R (2005) Experimental Constraints on Quaternary Structure in Alzheimer's beta-Amyloid Fibrils. Biochemistry 45: 498-512.
9. Sato T, Kienlen-Campard P, Ahmed M, Liu W, Li H, et al. (2006) Inhibitors of Amyloid Toxicity Based on beta-sheet Packing of Abeta-40 and Abeta-42 Biochemistry 45: 5503-5516.
10. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, et al. (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci USA 102: 17342-17347.
11. Petkova AT, Ishii Y, Balbach JJ, Antzutkin ON, Leapman RD, et al. (2002) A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99: 16742-16747.
12. Yoo BC, Kim SH, Cairns N, Fountoulakis M, Lubec G (2001) Deranged Expression of Molecular Chaperones in Brains of Patients with Alzheimer's Disease. Biochem Biophys Res Commun 280: 249-258.
13. Shinohara H, Inaguma Y, Goto S, Inagaki T, Kato K (1993) alphaB crystallin and HSP28 are enhanced in the cerebral cortex of patients with Alzheimer's disease. J Neurol Sci 119: 203-208.
14. Wilhelmus MMM, Otte-Höller I, Wesseling P, De Waal RMW, Boelens WC, et al. (2006) Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropath Appl Neuro 32: 119-130.
15. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12: 842-846.
16. Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89: 10449-10453.
17. Basha E, O'Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37: 106-117.
18. Bhat SP, Nagineni CN (1989) alphaB subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158: 319-325.
19. Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci USA 79: 2360-2364.
20. Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, et al. (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24: 3633-3642.
21. Peschek J, Braun N, Franzmann TM, Georgalis Y, Haslbeck M, et al. (2009) The eye lens chaperone alpha-crystallin forms defined globular assemblies. Proc Natl Acad Sci USA 106: 13272-13277.
22. Nahomi RB, Wang B, Raghavan CT, Voss O, Doseff AI, et al. (2013) Chaperone Peptides of alpha- Crystallin Inhibit Epithelial Cell Apoptosis, Protein Insolubilization, and Opacification in Experimental Cataracts. J Biol Chem 288: 13022-13035.
23. Ohto-Fujita E, Fujita Y, Atomi Y (2007) Analysis of the aB-crystallin domain responsible for inhibiting tubulin aggregation. Cell Stress Chaperon 12: 163-171.
24. Ghosh JG, Houck SA, Clark JI (2008) Interactive sequences in the molecular chaperone, human alphaB crystallin modulate the fibrillation of amyloidogenic proteins. Int J Biochem Cell Biol 40: 954-967.
25. Hochberg GKA, Ecroyd H, Liu C, Cox D, Cascio D, et al. (2014) The structured core domain of alphaB-crystallin can prevent amyloid fibrillation and associated toxicity. Proc Natl Acad Sci USA 111: 1562-1570.
26. Goldstein LE, Muffat JA, Cherny RA, Moir RD, Ericsson MH, et al. (2003) Cytosolic beta-amyloid deposition and supranuclear cataracts in lenses from people with Alzheimer's disease. Lancet 361: 1258-1265.
27. Stege GJJ, Renkawek K, Overkamp PSG, Verschuure P, van Rijk AF, et al. (1999) The Molecular Chaperone alphaB-crystallin Enhances Amyloid beta Neurotoxicity. Biochem Biophys Res Commun 262: 152-156.
28. Liang JJN (2000) Interaction between beta-amyloid and lens alphaB-crystallin. FEBS Lett 484: 98-101.
29. Kudva YC, Hiddinga HJ, Butler PC, Mueske CS, Eberhardt NL (1997) Small heat shock proteins inhibit in vitro Abeta-42 amyloidogenesis. FEBS Lett 416: 117-121.
30. Wilhelmus MMM, Boelens WC, Otte-Höller I, Kamps B, de Waal RMW, et al. (2006) Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloidbeta protein toxicity. Brain Res 1089: 67-78.
31. Raman B, Ban T, Sakai M, Pasta SY, Ramakrishna T, et al. (2005) AlphaB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid beta-peptide and beta2-microglobulin. Biochem J 392: 573-581.
32. Shammas Sarah L, Waudby Christopher A, Wang S, Buell Alexander K, Knowles Tuomas PJ, et al. (2011) Binding of the Molecular Chaperone alphaB-Crystallin to Abeta Amyloid Fibrils Inhibits Fibril Elongation. Biophysical J 101: 1681-1689.
33. Narayan P, Meehan S, Carver JA, Wilson MR, Dobson CM, et al. (2012) Amyloid-beta Oligomers are Sequestered by both Intracellular and Extracellular Chaperones. Biochemistry 51: 9270-9276.
34. Narayan P, Ganzinger KA, McColl J, Weimann L, Meehan S, et al. (2013) Single Molecule Characterization of the Interactions between Amyloid-beta Peptides and the Membranes of Hippocampal Cells. J Am Chem Soc 135: 1491-1498.
35. Narayanan S, Kamps B, Boelens WC, Reif B (2006) alphaB-crystallin competes with Alzheimer's disease beta-amyloid peptide for peptide-peptide interactions and induces oxidation of Abeta-Met35. FEBS Lett 580: 5941-5946.
36. Dehle F, Ecroyd H, Musgrave I, Carver J (2010) alphaB-Crystallin inhibits the cell toxicity associated with amyloid fibril formation by k-casein and the amyloid-beta peptide. Cell Stress Chaperon 15: 1013-1026.
37. Mannini B, Cascella R, Zampagni M, van Waarde-Verhagen M, Meehan S, et al. (2012) Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc Natl Acad Sci USA 109: 12479-12484.
38. Assarsson A, Hellstrand E, Cabaleiro-Lago C, Linse S (2014) Charge Dependent Retardation of Amyloid beta Aggregation by Hydrophilic Proteins. ACS Chem Neurosci 5: 266-274.
39. Luo J, Warmlander SKTS, Graslund A, Abrahams JP (2013) Human lysozyme inhibits the in vitro aggregation of Abeta peptides, which in vivo are associated with Alzheimer's disease. Chem Comm 49: 6507-6509.
40. Ma B, Nussinov R (2006) Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Curr Opin Chem Biol 10: 445-452.
41. Kirshenbaum K, Daggett V (1995) pH-Dependent Conformations of the Amyloid.beta.(1-28) Peptide Fragment Explored Using Molecular Dynamics. Biochemistry 34: 7629-7639.
42. Baumketner A, Shea J-E (2007) The Structure of the Alzheimer Amyloid-beta 10-35 Peptide Probed through Replica-Exchange Molecular Dynamics Simulations in Explicit Solvent. J Mol Biol 366: 275-285.
43. Rojas AV, Liwo A, Scheraga HA (2013) A Study of the alpha-Helical Intermediate Preceding the Aggregation of the Amino-Terminal Fragment of the beta Amyloid Peptide (Abeta1-28). J Phys Chem B 115: 12978-12983.
44. Ball KA, Phillips AH, Nerenberg PS, Fawzi NL, Wemmer DE, et al. (2011) Homogeneous and heterogeneous tertiary structure ensembles of amyloid-beta peptides. Biochemistry 50: 7612-7628.
45. Flöck D, Colacino S, Colombo G, Di Nola A (2006) Misfolding of the amyloid β-protein: A molecular dynamics study. Proteins 62: 183-192.
46. Gnanakaran S, Nussinov R, García AE (2006) Atomic-Level Description of Amyloid beta-Dimer Formation. J Am Chem Soc 128: 2158-2159.
47. Zhu X, Bora RP, Barman A, Singh R, Prabhakar R (2012) Dimerization of the Full-Length Alzheimer Amyloid beta-Peptide (Abeta42) in Explicit Aqueous Solution: A Molecular Dynamics Study. J Phys Chem B 116: 4405-4416.
48. Fawzi NL, Kohlstedt KL, Okabe Y, Head-Gordon T (2008) Protofibril Assemblies of the Arctic, Dutch, and Flemish Mutants of the Alzheimer's Abeta1-40 Peptide. Biophysical J 94: 2007-2016.
49. Buchete N-V, Tycko R, Hummer G (2005) Molecular Dynamics Simulations of Alzheimer's beta- Amyloid Protofilaments. J Mol Biol 353: 804-821.
50. Convertino M, Pellarin R, Catto M, Carotti A, Caflisch A (2009) 9,10-Anthraquinone hinders β-aggregation: How does a small molecule interfere with Aβ-peptide amyloid fibrillation? Prot Sci 18: 792-800.
51. Chebaro Y, Jiang P, Zang T, Mu Y, Nguyen PH, et al. (2012) Structures of Abeta17-42 Trimers in Isolation and with Five Small-Molecule Drugs Using a Hierarchical Computational Procedure. J Phys Chem B 116: 8412-8422.
52. Eskici G, Gur M (2013) Computational design of new peptide inhibitors for amyloid beta (Aβ) aggregation in Alzheimer's disease: application of a novel methodology. Plos One 8: e66178.
53. Xu Y, Shen J, Luo X, Zhu W, Chen K, et al. (2005) Conformational transition of amyloid beta-peptide. Proc Natl Acad Sci USA 102: 5403-5407.
54. Jang H, Zheng J, Nussinov R (2007) Models of beta-Amyloid Ion Channels in the Membrane Suggest That Channel Formation in the Bilayer Is a Dynamic Process. Biophysical J 93: 1938-1949.
55. Jang H, Connelly L, Teran Arce F, Ramachandran S, Kagan BL, et al. (2013) Mechanisms for the Insertion of Toxic, Fibril-like beta-Amyloid Oligomers into the Membrane. J Chem Theory Comput 9: 822-833.
56. Gowing E, Roher AE, Woods AS, Cotter RJ, Chaney M, et al. (1994) Chemical characterization of A beta 17-42 peptide, a component of diffuse amyloid deposits of Alzheimer disease. J Biol Chem 269: 10987-10990.
57. Lalowski M, Golabek A, Lemere CA, Selkoe DJ, Wisniewski HM, et al. (1996) The "Nonamyloidogenic" p3 Fragment (Amyloid beta17-42) Is a Major Constituent of Down's Syndrome Cerebellar Preamyloid. J Biol Chem 271: 33623-33631.
58. Wei W, Norton DD, Wang X, Kusiak JW (2002) Abeta17-42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis. Brain 125: 2036-2043.
59. Jang H, Arce FT, Ramachandran S, Capone R, Azimova R, et al. (2010) Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer's Disease and Down syndrome. Proc Natl Acad Sci USA 107: 6538-6543.
60. Streltsov VA, Varghese JN, Masters CL, Nuttall SD (2011) Crystal structure of the amyloid-β p3 fragment provides a model for oligomer formation in Alzheimer's disease. J Neurosci 31: 1419-1426.
61. Nguyen PH, Tarus B, Derreumaux P (2014) Familial Alzheimer A2 V Mutation Reduces the Intrinsic Disorder and Completely Changes the Free Energy Landscape of the Abeta1-28 Monomer. J Phys Chem B 118: 501-510.
62. Baumketner A, Bernstein SL, Wyttenbach T, Lazo ND, Teplow DB, et al. (2006) Structure of the 21-30 fragment of amyloid beta protein. Prot Sci 15: 1239-1247.
63. Han W, Wu Y-D (2005) A strand-loop-strand structure is a possible intermediate in fibril elongation: Long time simulations of amyloid-b peptide (10-35). J Am Chem Soc 127: 15408-15416.
64. Ahmad B, Chen Y, Lapidus LJ (2012) Aggregation of alpha-synuclein is kinetically controlled by intramolecular diffusion. Proc Natl Acad Sci USA 109: 2336-2341.
65. Houck SA, Landsbury A, Clark JI, Quinlan RA (2011) Multiple Sites in aB-Crystallin Modulate Its Interactions with Desmin Filaments Assembled In Vitro. Plos One 6: e25859.
66. Sciarretta KL, Gordon DJ, Petkova AT, Tycko R, Meredith SC (2005) Ab40-Lactam(D23/K28) Models a Conformation Highly Favorable for Nucleation of Amyloid†. Biochemistry 44: 6003-6014.
67. Bertz M, Chen J, Feige MJ, Franzmann TM, Buchner J, et al. (2010) Structural and Mechanical Hierarchies in the alpha-Crystallin Domain Dimer of the Hyperthermophilic Small Heat Shock Protein Hsp16.5. J Mol Biol 400: 1046-1056.
68. Wen-Hui X, Wen-Fei L, Wei W (2012) Modulation of Amyloid-beta Conformation by Charge State of N-Terminal Disordered Region. Chin Phys Lett 29: 0887021-0887024.
69. Yu L, Edalji R, Harlan JE, Holzman TF, Lopez AP, et al. (2009) Structural characterization of a soluble amyloid beta-peptide oligomer. Biochemistry 48: 1870-1877.
70. Urbanc B, Cruz L, Yun S, Buldyrev SV, Bitan G, et al. (2004) In silico study of amyloid beta-protein folding and oligomerization. Proc Natl Acad Sci USA 101: 17345-17350.
71. Aquilina JA, Watt SJ (2007) The N-terminal domain of αB-crystallin is protected from proteolysis by bound substrate. Biochem Biophys Res Commun 353: 1115-1120.
72. Bhattacharyya J, Padmanabha Udupa E, Wang J, Sharma KK (2006) Mini-αB-crystallin: a functional element of αB-crystallin with chaperone-like activity. Biochemistry 45: 3069-3076.
73. Zou K, Gong J-S, Yanagisawa K, Michikawa M (2002) A Novel Function of Monomeric Amyloid beta- Protein Serving as an Antioxidant Molecule against Metal-Induced Oxidative Damage. J Neurosci 22: 4833-4841.
74. Giuffrida ML, Caraci F, Pignataro B, Cataldo S, De Bona P, et al. (2009) b-Amyloid Monomers Are Neuroprotective. J Neurosci 29: 10582-10587.
75. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, et al. (2009) Structural conversion of neurotoxic amyloid-[beta]1-42 oligomers to fibrils. Nat Struct Mol Biol 17: 561-567.
76. Hung LW, Ciccotosto GD, Giannakis E, Tew DJ, Perez K, et al. (2008) Amyloid-beta Peptide (Abeta) Neurotoxicity Is Modulated by the Rate of Peptide Aggregation: Abeta Dimers and Trimers Correlate with Neurotoxicity. J Neurosci 28: 11950-11958.
77. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-[beta] protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84.
78. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci USA 106: 14745-14750.
79. Luo J, Wärmländer SKTS, Gräslund A, Abrahams JP (2014) Non-chaperone Proteins Can Inhibit Aggregation and Cytotoxicity of Alzheimer Amyloid β Peptide. J Biol Chem 289: 27766-27775.
80. Bagnéris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, et al. (2009) Crystal Structures of alpha-Crystallin Domain Dimers of alphaB-Crystallin and Hsp20. J Mol Biol 392: 1242-1252.
81. Deserno M, Holm C (1998) How to mesh up Ewald sums. II. An accurate error estimate for the particle-particle- particle-mesh algorithm. J Chem Phys 109: 7694-7701.
82. MacKerell AD, Bashford D, Bellott M, Dunbrack R, Evanseck J, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
83. MacKerell AD, Feig M, Brooks CL (2004) 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 Comp Chem 25: 1400-1415.
84. Das P, King JA, Zhou R (2011) Aggregation of γ-crystallins associated with human cataracts via domain swapping at the C-terminal β-strands. Proc Natl Acad Sci USA 108: 10514-10519.
85. Eleftheriou M, Germain RS, Royyuru AK, Zhou R (2006) Thermal denaturing of mutant lysozyme with both the OPLSAA and the CHARMM force fields. J Am Chem Soc 128: 13388-13395.
86. Lockhart C, Kim S, Klimov DK (2014) Explicit Solvent Molecular Dynamics Simulations of Abeta Peptide Interacting with Ibuprofen Ligands. J Phys Chem B 116: 12922-12932.
87. Kent A, Jha AK, Fitzgerald JE, Freed KF (2008) Benchmarking Implicit Solvent Folding Simulations of the Amyloid beta(10-35) Fragment. J Phys Chem B 112: 6175-6186.
88. Dai B, Kang S-g, Huynh T, Lei H, Castelli M, et al. (2013) Salts drive controllable multilayered upright assembly of amyloid-like peptides at mica/water interface. Proc Natl Acad Sci USA 110: 8543-8548.
89. Lemmin T, Dimitrov M, Fraering PC, Dal Peraro M (2014) Perturbations of the Straight Transmembrane alpha-Helical Structure of the Amyloid Precursor Protein Affect its Processing by gamma-Secretase. J Biol Chem.
90. Ito M, Johansson J, Strömberg R, Nilsson L (2011) Unfolding of the Amyloid beta-Peptide Central Helix: Mechanistic Insights from Molecular Dynamics Simulations. Plos One 6: e17587.
91. Liang G, Zhao J, Yu X, Zheng J (2013) Comparative Molecular Dynamics Study of Human Islet Amyloid Polypeptide (IAPP) and Rat IAPP Oligomers. Biochemistry 52: 1089-1100.
92. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
93. Kumar S, Huang C, Zheng G, Bohm E, Bhatele A, et al. (2008) Scalable molecular dynamics with NAMD on the IBM Blue Gene/L system. IBM J Res Dev 52: 177-188.
94. Frishman D, Argos P (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579.
95. García AE, Hummer G (2000) Water penetration and escape in proteins. Proteins 38: 261-272.
96. Rosenman DJ, Connors CR, Chen W, Wang C, Garcia AE (2013) Abeta Monomers Transiently Sample Oligomer and Fibril-Like Configurations: Ensemble Characterization Using a Combined MD/ NMR Approach. J Mol Biol 425: 3338-3359.
97. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.