A coarse-grained model for peptide aggregation on a membrane surface

Journal of Physical Chemistry B

Volumn 118, Issue 28, 2014, Pages 8420-8432

  Morriss Andrews, Alex ^a   Brown, Frank L H ^a   Shea, Joan Emma ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID BILAYERS; PEPTIDES;

AGGREGATE STRUCTURES; BENDING RIGIDITY; COARSE GRAINED MODELS; COARSE-GRAINED MOLECULAR DYNAMICS; FIBRILLAR AGGREGATES; IMPLICIT SOLVENTS; MORPHOLOGY TRANSITIONS; PEPTIDE AGGREGATION;

AGGREGATES;

LIPID BILAYER; PEPTIDE;

CHEMISTRY; LIPID BILAYER; THEORETICAL MODEL;

LIPID BILAYERS; MODELS, THEORETICAL; PEPTIDES;

EID: 84902099700     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp502871m     Document Type: Article

References (92)

1. Thirumalai, D.; Klimov, D.; Dima, R. Emerging Ideas on the Molecular Basis of Protein and Peptide Aggregation Curr. Opin. Struct. Biol. 2003, 13, 146-159
2. Straub, J.; Thirumalai, D. Principles Governing Oligomer Formation in Amyloidogenic Peptides Curr. Opin. Struct. Biol. 2010, 20, 187-195
3. Chiti, F.; Dobson, C. Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 2006, 75, 333-366
4. Stefani, M. Protein Misfolding and Aggregation: New Examples in Medicine and Biology of the Dark Side of the Protein World Biochim. Biophys. Acta, Mol. Basis Dis. 2004, 1739, 5-25
5. 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
6. Zhu, M.; Han, S.; Zhou, F.; Carter, S. A.; Fink, A. L. Annular Oligomeric Amyloid Intermediates Observed by in Situ Atomic Force Microscopy J. Biol. Chem. 2004, 279, 24452-24459
7. Serpell, L. C. Alzheimer's Amyloid Fibrils: Structure and Assembly Biochim. Biophys. Acta, Mol. Basis Dis. 2000, 1502, 16-30
8. Sabate, R.; Estelrich, J. Evidence of the Existence of Micelles in the Fibrillogenesis of β-Amyloid Peptide J. Phys. Chem. B 2005, 109, 11027-11032
9. Seubert, P.; Vigo-Pelfrey, C.; Esch, F.; Lee, M.; Dovey, H.; Davis, D.; Sinha, S.; Schlossmaker, M.; Whaley, J. Isolation and Quantification of Soluble Alzheimer's -Peptide from Biological Fluids Nature 1992, 359, 325-327
10. Aisenbrey, C.; Borowik, T.; Byström, R.; Bokvist, M.; Lindström, F.; Misiak, H.; Sani, M.; Gröbner, G. How Is Protein Aggregation in Amyloidogenic Diseases Modulated by Biological Membranes? Eur. Biophys. J. 2008, 37, 247-255
11. Knight, J. D.; Miranker, A. D. Phospholipid Catalysis of Diabetic Amyloid Assembly J. Mol. Biol. 2004, 341, 1175-1187
12. Choo-Smith, L.-P.; Garzon-Rodriguez, W.; Glabe, C. G.; Surewicz, W. K. Acceleration of Amyloid Fibril Formation by Specific Binding of A-(1-40) Peptide to Ganglioside-Containing Membrane Vesicles J. Biol. Chem. 1997, 272, 22987-22990
13. Gorbenko, G. P.; Kinnunen, P. K. The Role of Lipid-Protein Interactions in Amyloid-Type Protein Fibril Formation Chem. Phys. Lipids 2006, 141, 72-82
14. Watkins, H. M.; Vallee-Belisle, A.; Ricci, F.; Makarov, D. E.; Plaxco, K. W. Entropic and Electrostatic Effects on the Folding Free Energy of a Surface-Attached Biomolecule: An Experimental and Theoretical Study J. Am. Chem. Soc. 2012, 134, 2120-2126
15. Zhu, M.; Souillac, P.; Ionescu-Zanetti, C.; Carter, S.; Fink, A. Surface-Catalyzed Amyloid Fibril Formation J. Biol. Chem. 2002, 277, 50914-50922
16. Giacomelli, C. E.; Norde, W. Influence of Hydrophobic Teflon Particles on the Structure of Amyloid β-Peptide Biomacromolecules 2003, 4, 1719-1726
17. Linse, S.; Cabaleiro-Lago, C.; Xue, W.; Lynch, I.; Lindman, S.; Thulin, E.; Radford, S.; Dawson, K. Nucleation of Protein Fibrillation by Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 8691-8696
18. Kowalewski, T.; Holtzman, D. M. In Situ Atomic Force Microscopy Study of Alzheimer's β-Amyloid Peptide on Different Substrates: New Insights into Mechanism of β-Sheet Formation Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3688-3693
19. Sasahara, K.; Morigaki, K.; Shinya, K. Effects of Membrane Interaction and Aggregation of Amyloid β-Peptide on Lipid Mobility and Membrane Domain Structure Phys. Chem. Chem. Phys. 2013, 15, 8929-8939
20. Seeliger, J.; Evers, F.; Jeworrek, C.; Kapoor, S.; Weise, K.; Andreetto, E.; Tolan, M.; Kapurniotu, A.; Winter, R. Cross-Amyloid Interaction of Aβ and IAPP at Lipid Membranes Angew. Chem., Int. Ed. 2012, 51, 679-683
21. Shen, L.; Adachi, T.; Vanden Bout, D.; Zhu, X.-Y. A Mobile Precursor Determines Amyloid-β Peptide Fibril Formation at Interfaces J. Am. Chem. Soc. 2012, 134, 14172-14178
22. Zhang, L.; Zhong, J.; Huang, L.; Wang, L.; Hong, Y.; Sha, Y. Parallel-Oriented Fibrogenesis of a β-Sheet Forming Peptide on Supported Lipid Bilayers J. Phys. Chem. B 2008, 112, 8950-8954
23. Kremer, J. J.; Murphy, R. M. Kinetics of Adsorption of β-Amyloid Peptide Aβ (1-40) to Lipid Bilayers J. Biochem. Biophys. Methods 2003, 57, 159-169
24. Kremer, J. J.; Pallitto, M. M.; Sklansky, D. J.; Murphy, R. M. Correlation of β-Amyloid Aggregate Size and Hydrophobicity with Decreased Bilayer Fluidity of Model Membranes Biochemistry 2000, 39, 10309-10318
25. Lopes, D.; Meister, A.; Gohlke, A.; Hauser, A.; Blume, A.; Winter, R. Mechanism of Islet Amyloid Polypeptide Fibrillation at Lipid Interfaces Studied by Infrared Reflection Absorption Spectroscopy Biophys. J. 2007, 93, 3132-3141
26. Bucciantini, M.; Rigacci, S.; Stefani, M. Amyloid Aggregation: Role of Biological Membranes and the Aggregate-Membrane System J. Phys. Chem. Lett. 2014, 5, 517-527
27. Khandelia, H.; Ipsen, J. H.; Mouritsen, O. G. The Impact of Peptides on Lipid Membranes Biochim. Biophys. Acta, Biomembr. 2008, 1778, 1528-1536
28. Butterfield, S.; Lashuel, H. Amyloidogenic Protein-Membrane Interactions: Mechanistic Insight from Model Systems Angew. Chem., Int. Ed. 2010, 49, 5628-5654
29. Lashuel, H. A.; Lansbury, P. T. Are Amyloid Diseases Caused by Protein Aggregates That Mimic Bacterial Pore-Forming Toxins? Q. Rev. Biophys. 2006, 39, 167-201
30. Jang, H.; Arce, F. T.; Ramachandran, S.; Capone, R.; Lal, R.; Nussinov, R. β-Barrel Topology of Alzheimer's β-Amyloid Ion Channels J. Mol. Biol. 2010, 404, 917-934
31. Connelly, L.; Jang, H.; Teran Arce, F.; Ramachandran, S.; Kagan, B. L.; Nussinov, R.; Lal, R. Effects of Point Substitutions on the Structure of Toxic Alzheimers β-Amyloid Channels: Atomic Force Microscopy and Molecular Dynamics Simulations Biochemistry 2012, 51, 3031-3038
32. Kastorna, A.; Trusova, V.; Gorbenko, G.; Kinnunen, P. Membrane Effects of Lysozyme Amyloid Fibrils Chem. Phys. Lipids 2012, 165, 331-337
33. Engel, M. F.; Khemtémourian, L.; Kleijer, C. C.; Meeldijk, H. J.; Jacobs, J.; Verkleij, A. J.; de Kruijff, B.; Killian, J. A.; Höppener, J. W. Membrane Damage by Human Islet Amyloid Polypeptide Through Fibril Growth at the Membrane Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 6033-6038
34. Milanesi, L.; Sheynis, T.; Xue, W.-F.; Orlova, E. V.; Hellewell, A. L.; Jelinek, R.; Hewitt, E. W.; Radford, S. E.; Saibil, H. R. Direct Three-Dimensional Visualization of Membrane Disruption by Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 20455-20460
35. Burke, K. A.; Yates, E. A.; Legleiter, J. Amyloid-Forming Proteins Alter the Local Mechanical Properties of Lipid Membranes Biochemistry 2013, 52, 808-817
36. Lee, M. K.; Stirling, W.; Xu, Y.; Xu, X.; Qui, D.; Mandir, A. S.; Dawson, T. M.; Copeland, N. G.; Jenkins, N. A.; Price, D. L. Human α-Synuclein- Harboring Familial Parkinson's Disease-Linked Ala-53 Thr Mutation Causes Neurodegenerative Disease with α-Synuclein Aggregation in Transgenic Mice Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 8968-8973
37. Nikolic, A.; Baud, S.; Rauscher, S.; Pomès, R. Molecular Mechanism of β-Sheet Self-Organization at Water-Hydrophobic Interfaces Proteins 2011, 79, 1-22
38. Kim, S.; Klimov, D. K. Binding to the Lipid Monolayer Induces Conformational Transition in Aβ Monomer J. Mol. Model. 2013, 19, 737-750
39. Yu, X.; Wang, Q.; Pan, Q.; Zhou, F.; Zheng, J. Molecular Interactions of Alzheimer Amyloid-β Oligomers with Neutral and Negatively Charged Lipid Bilayers Phys. Chem. Chem. Phys. 2013, 15, 8878-8889
40. Yu, X.; Zheng, J. Cholesterol Promotes the Interaction of Alzheimer β-Amyloid Monomer with Lipid Bilayer J. Mol. Biol. 2012, 421, 561-571
41. Lemkul, J. A.; Bevan, D. R. Lipid Composition Influences the Release of Alzheimer's Amyloid β-Peptide from Membranes Protein Sci. 2011, 20, 1530-1545
42. Gupta, K.; Jang, H.; Harlen, K.; Puri, A.; Nussinov, R.; Schneider, J. P.; Blumenthal, R. Mechanism of Membrane Permeation Induced by Synthetic β-Hairpin Peptides Biophys. J. 2013, 105, 2093-2103
43. Arce, F. T.; Jang, H.; Ramachandran, S.; Landon, P. B.; Nussinov, R.; Lal, R. Polymorphism of Amyloid β Peptide in Different Environments: Implications for Membrane Insertion and Pore Formation Soft Matter 2011, 7, 5267-5273
44. Strodel, B.; Lee, J. W.; Whittleston, C. S.; Wales, D. J. Transmembrane Structures for Alzheimer's Aβ1- 42 Oligomers J. Am. Chem. Soc. 2010, 132, 13300-13312
45. Miyashita, N.; Straub, J.; Thirumalai, D. Structures of β-Amyloid Peptide 1-40, 1-42, and 1-55 the 672-726 Fragment of APP in a Membrane Environment with Implications for Interactions with γ-Secretase J. Am. Chem. Soc. 2009, 131, 17843-17852
46. Panahi, A.; Feig, M. Dynamic Heterogeneous Dielectric Generalized Born (DHDGB): An Implicit Membrane Model with a Dynamically Varying Bilayer Thickness J. Chem. Theory Comput. 2013, 9, 1709-1719
47. Parton, D. L.; Klingelhoefer, J. W.; Sansom, M. S. Aggregation of Model Membrane Proteins, Modulated by Hydrophobic Mismatch, Membrane Curvature, and Protein Class Biophys. J. 2011, 101, 691-699
48. Hall, B. A.; Chetwynd, A. P.; Sansom, M. S. Exploring Peptide-Membrane Interactions with Coarse-Grained MD Simulations Biophys. J. 2011, 100, 1940-1948
49. 2H-NMR Experiments on the Orientation of the Transmembrane Helix WALP23 by Computer Simulations Biophys. J. 2010, 99, 1455-1464
50. Holdbrook, D. A.; Leung, Y. M.; Piggot, T. J.; Marius, P.; Williamson, P. T.; Khalid, S. Stability and Membrane Orientation of the Fukutin Transmembrane Domain: A Combined Multiscale Molecular Dynamics and Circular Dichroism Study Biochemistry 2010, 49, 10796-10802
51. Poojari, C.; Kukol, A.; Strodel, B. How the Amyloid- Peptide and Membranes Affect Each Other: An Extensive Simulation Study Biochim. Biophys. Acta, Biomembr. 2013, 1828, 327-339
52. Friedman, R.; Pellarin, R.; Caflisch, A. Amyloid Aggregation on Lipid Bilayers and Its Impact on Membrane Permeability J. Mol. Biol. 2009, 387, 407-415
53. Illya, G.; Deserno, M. Coarse-Grained Simulation Studies of Peptide-Induced Pore Formation Biophys. J. 2008, 95, 4163-4173
54. Zhang, Y.; Luo, Y.; Deng, Y.; Mu, Y.; Wei, G. Lipid Interaction and Membrane Perturbation of Human Islet Amyloid Polypeptide Monomer and Dimer by Molecular Dynamics Simulations PLoS One 2012, 7, e38191
55. Zhao, L. N.; Chiu, S.-W.; Benoit, J.; Chew, L. Y.; Mu, Y. Amyloid β Peptides Aggregation in a Mixed Membrane Bilayer: A Molecular Dynamics Study J. Phys. Chem. B 2011, 115, 12247-12256
56. Davis, C. H.; Berkowitz, M. L. A Molecular Dynamics Study of the Early Stages of Amyloid-β (1-42) Oligomerization: The Role of Lipid Membranes Proteins 2010, 78, 2533-2545
57. Davis, C.; Berkowitz, M. Interaction Between Amyloid-Beta(1-42) Peptide and Phospholipid Bilayers: A Molecular Dynamics Study Biophys. J. 2009, 96, 785-797
58. Nguyen, P.; Derreumaux, P. Understanding Amyloid Fibril Nucleation and Aβ Oligomer/Drug Interactions from Computer Simulations Acc. Chem. Res. 2013, 47, 603-611
59. Phelps, E. M.; Hall, C. K. Structural Transitions and Oligomerization Along Polyalanine Fibril Formation Pathways from Computer Simulations Proteins 2012, 80, 1582-1597
60. Wu, C.; Shea, J.-E. Coarse-Grained Models for Protein Aggregation Curr. Opin. Struct. Biol. 2011, 21, 209-220
61. Levy, Y.; Onuchic, J. N. Mechanisms of Protein Assembly: Lessons from Minimalist Models Acc. Chem. Res. 2006, 39, 135-142
62. Bellesia, G.; Shea, J.-E. Self-Assembly of β-Sheet Forming Peptides into Chiral Fibrillar Aggregates J. Chem. Phys. 2007, 126, 245104
63. Bellesia, G.; Shea, J.-E. Diversity of Kinetic Pathways in Amyloid Fibril Formation J. Chem. Phys. 2009, 131, 111102
64. Bellesia, G.; Shea, J.-E. Effect of β-Sheet Propensity on Peptide Aggregation J. Chem. Phys. 2009, 130, 145103
65. Morriss-Andrews, A.; Bellesia, G.; Shea, J.-E. Effects of Surface Interactions on Peptide Aggregate Morphology J. Chem. Phys. 2011, 135, 085102
66. Morriss-Andrews, A.; Shea, J. Kinetic Pathways to Peptide Aggregation on Surfaces: The Effects of β-Sheet Propensity and Surface Attraction J. Chem. Phys. 2012, 136, 065103
67. Morriss-Andrews, A.; Bellesia, G.; Shea, J. β-Sheet Propensity Controls the Kinetic Pathways and Morphologies of Seeded Peptide Aggregation J. Chem. Phys. 2012, 137, 145104
68. Brannigan, G.; Philips, P.; Brown, F. Flexible Lipid Bilayers in Implicit Solvent Phys. Rev. E 2005, 72, 011915
69. Watson, M.; Penev, E.; Welch, P.; Brown, F. Thermal Fluctuations in Shape, Thickness, and Molecular Orientation in Lipid Bilayers J. Chem. Phys. 2011, 135, 244701
70. Watson, M. C.; Morriss-Andrews, A.; Welch, P. M.; Brown, F. L. Thermal Fluctuations in Shape, Thickness, and Molecular Orientation in Lipid Bilayers. II. Finite Surface Tensions J. Chem. Phys. 2013, 139, 084706
71. Watson, M. C.; Brandt, E. G.; Welch, P. M.; Brown, F. L. Determining Biomembrane Bending Rigidities from Simulations of Modest Size Phys. Rev. Lett. 2012, 109, 028102
72. Brannigan, G.; Brown, F. Contributions of Gaussian Curvature and Nonconstant Lipid Volume to Protein Deformation of Lipid Bilayers Biophys. J. 2007, 92, 864-876
73. Brannigan, G.; Brown, F. A Consistent Model for Thermal Fluctuations and Protein-Induced Deformations in Lipid Bilayers Biophys. J. 2006, 90, 1501-1520
74. Balbirnie, M.; Grothe, R.; Eisenberg, D. S. An Amyloid-Forming Peptide from the Yeast Prion Sup35 Reveals a Dehydrated -Sheet Structure for Amyloid Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 2375-2380
75. Tjernberg, L.; Hosia, W.; Bark, N.; Thyberg, J.; Johansson, J. Charge Attraction and Propensity Are Necessary for Amyloid Fibril Formation from Tetrapeptides J. Biol. Chem. 2002, 277, 43243-43246
76. Straub, J. E.; Thirumalai, D. Membrane-Protein Interactions Are Key to Understanding Amyloid Formation J. Phys. Chem. Lett. 2014, 5, 633-635
77. Evangelisti, E.; Cecchi, C.; Cascella, R.; Sgromo, C.; Becatti, M.; Dobson, C. M.; Chiti, F.; Stefani, M. Membrane Lipid Composition and Its Physicochemical Properties Define Cell Vulnerability to Aberrant Protein Oligomers J. Cell Sci. 2012, 125, 2416-2427
78. Mueller, H.; Butt, H.-J.; Bamberg, E. Adsorption of Membrane-Associated Proteins to Lipid Bilayers Studied with an Atomic Force Microscope: Myelin Basic Protein and Cytochrome C J. Phys. Chem. B 2000, 104, 4552-4559
79. Marrink, S. J.; de Vries, A. H.; Mark, A. E. Coarse Grained Model for Semiquantitative Lipid Simulations J. Phys. Chem. B 2004, 108, 750-760
80. Cecchini, M.; Rao, F.; Seeber, M.; Caflisch, A. Replica Exchange Molecular Dynamics Simulations of Amyloid Peptide Aggregation J. Chem. Phys. 2004, 121, 10748
81. Nguyen, P.; Li, M.; Stock, G.; Straub, J.; Thirumalai, D. Monomer Adds to Preformed Structured Oligomers of Abeta-Peptides by a Two-Stage Dock-Lock Mechanism Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 111-116
82. Straub, J.; Thirumalai, D. Toward a Molecular Theory of Early and Late Events in Monomer to Amyloid Fibril Formation Annu. Rev. Phys. Chem. 2011, 62, 437-463
83. Feller, S. E.; Pastor, R. W. Constant Surface Tension Simulations of Lipid Bilayers: The Sensitivity of Surface Areas and Compressibilities J. Chem. Phys. 1999, 111, 1281-1287
84. Safran, S. A. Statistical Thermodynamics of Surfaces, Interfaces and Membranes; Westview Press: Boulder, CO, 1994.
85. Brown, F. L. H. Continuum Simulations of Biomembrane Dynamics and the Importance of Hydrodynamic Effects Q. Rev. Biophys. 2011, 44, 391-432
86. Netz, R. R.; Pincus, P. Inhomogeneous Fluid Membranes: Segregation, Ordering, and Effective Rigidity Phys. Rev. E 1995, 52, 4114-4128
87. Sigurdsson, J. K.; Brown, F. L. H.; Atzberger, P. J. Hybrid Continuum-Particle Method for Fluctuating Lipid Bilayer Membranes with Diffusing Protein Inclusions J. Comput. Phys. 2013, 252, 65-85
88. Khelashvili, G.; Kollmitzer, B.; Heftberger, P.; Pabst, G.; Harries, D. Calculating the Bending Modulus for Multicomponent Lipid Membranes in Different Thermodynamic Phases J. Chem. Theory Comput. 2013, 9, 3866-3871
89. Gorbenko, G.; Trusova, V. Protein Aggregation in a Membrane Environment Adv. Protein Chem. Struct. Biol. 2011, 84, 113-142
90. Lee, H.-J.; Choi, C.; Lee, S.-J. Membrane-Bound -Synuclein Has a High Aggregation Propensity and the Ability to Seed the Aggregation of the Cytosolic Form J. Biol. Chem. 2002, 277, 671-678
91. Matsuzaki, K.; Horikiri, C. Interactions of Amyloid β-Peptide (1- 40) with Ganglioside-Containing Membranes Biochemistry 1999, 38, 4137-4142
92. Zhang, Y.-J.; Shi, J.-M.; Bai, C.-J.; Wang, H.; Li, H.-Y.; Wu, Y.; Ji, S.-R. Intra-Membrane Oligomerization and Extra-Membrane Oligomerization of Amyloid-β Peptide Are Competing Processes As a Result of Distinct Patterns of Motif Interplay J. Biol. Chem. 2012, 287, 748-756