Effects of confinement on the structure and dynamics of an intrinsically disordered peptide: A molecular-dynamics study

Journal of Physical Chemistry B

Volumn 117, Issue 14, 2013, Pages 3707-3719

  Rao, J Srinivasa ^a   Cruz, Luis ^a  

^a DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; HYDROGEN BONDS; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; PEPTIDES; PHASE SPACE METHODS; PROTEIN FOLDING;

CELLULAR COMPONENTS; HYDROPHILIC AND HYDROPHOBIC; HYDROPHOBIC PORE; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; PEPTIDE-SURFACE INTERACTIONS; STRUCTURE AND DYNAMICS; TURN STRUCTURE;

DYNAMICS;

EID: 84876229882     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp310623x     Document Type: Article

References (101)

1. Zhou, H. X.; Rivas, G. N.; Minton, A. P. Macromolecular Crowding and Confinement: Biochemical, Biophysical, and Potential Physiological Consequences Annu. Rev. Biophys. 2008, 37, 375-397
2. Eggers, D. K.; Valentine, J. S. Molecular Confinement Influences Protein Structure and Enhances Thermal Protein Stability Protein Sci. 2001, 10 (2) 250-261
3. Jarvet, J.; Danielsson, J.; Damberg, P.; Oleszczuk, M.; Graeslund, A. Positioning of the Alzheimer a Beta(1-40) Peptide in Sds Micelles Using NMR and Paramagnetic Probes J. Biomol. NMR 2007, 39 (1) 63-72
4. Kumar, C. V.; Chaudhari, A. Proteins Immobilized at the Galleries of Layered Alpha-Zirconium Phosphate: Structure and Activity Studies J. Am. Chem. Soc. 2000, 122 (5) 830-837
5. Peterson, R. W.; Anbalagan, K.; Tommos, C.; Wand, A. J. Forced Folding and Structural Analysis of Metastable Proteins J. Am. Chem. Soc. 2004, 126 (31) 9498-9499
6. Wei, Y.; Xu, J. G.; Feng, Q. W.; Dong, H.; Lin, M. D. Encapsulation of Enzymes in Mesoporous Host Materials Via the Nonsurfactant-Templated Sol-Gel Process Mater. Lett. 2000, 44 (1) 6-11
7. Baumketner, A.; Jewett, A.; Shea, J. E. Effects of Confinement in Chaperonin Assisted Protein Folding: Rate Enhancement by Decreasing the Roughness of the Folding Energy Landscape J. Mol. Biol. 2003, 332 (3) 701-713
8. Bhattacharya, A.; Best, R. B.; Mittal, J. Smoothing of the Gb1 Hairpin Folding Landscape by Interfacial Confinement Biophys. J. 2012, 103 (3) 596-600
9. Cheung, M. S.; Klimov, D.; Thirumalai, D. Molecular Crowding Enhances Native State Stability and Refolding Rates of Globular Proteins Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (13) 4753-4758
10. Cheung, M. S.; Thirumalai, D. Effects of Crowding and Confinement on the Structures of the Transition State Ensemble in Proteins J. Phys. Chem. B 2007, 111 (28) 8250-8257
11. England, J.; Lucent, D.; Pande, V. Rattling the Cage: Computational Models of Chaperonin-Mediated Protein Folding Curr. Opin. Struct. Biol. 2008, 18 (2) 163-169
12. England, J. L.; Lucent, D.; Pande, V. S. A Role for Confined Water in Chaperonin Function J. Am. Chem. Soc. 2008, 130 (36) 11838-11839
13. Friedel, M.; Sheeler, D. J.; Shea, J. E. Effects of Confinement and Crowding on the Thermodynamics and Kinetics of Folding of a Minimalist Beta-Barrel Protein J. Chem. Phys. 2003, 118 (17) 8106-8113
14. Garcia, A. E.; Onuchic, J. N. Folding a Protein in a Computer: An Atomic Description of the Folding/Unfolding of Protein A Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (24) 13898-13903
15. Hatters, D. M.; Minton, A. P.; Howlett, G. J. Macromolecular Crowding Accelerates Amyloid Formation by Human Apolipoprotein C-Ii J. Biol. Chem. 2002, 277 (10) 7824-7830
16. Hayer-Hartl, M.; Minton, A. P. A Simple Semiempirical Model for the Effect of Molecular Confinement Upon the Rate of Protein Folding Biochemistry 2006, 45 (44) 13356-13360
17. Jewett, A. I.; Baumketner, A.; Shea, J. E. Accelerated Folding in the Weak Hydrophobic Environment of a Chaperonin Cavity: Creation of an Alternate Fast Folding Pathway Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (36) 13192-13197
18. Klimov, D. K.; Newfield, D.; Thirumalai, D. Simulations of Beta-Hairpin Folding Confined to Spherical Pores Using Distributed Computing Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (12) 8019-8024
19. Lucent, D.; England, J.; Pande, V. Inside the Chaperonin Toolbox: Theoretical and Computational Models for Chaperonin Mechanism Phys. Biol. 2009, 6 (1) 015003-015010
20. O'Brien, E. P.; Stan, G.; Thirumalai, D.; Brooks, B. R. Factors Governing Helix Formation in Peptides Confined to Carbon Nanotubes Nano Lett. 2008, 8 (11) 3702-3708
21. Rathore, N.; Knotts, T. A.; de Pablo, J. J. Confinement Effects on the Thermodynamics of Protein Folding: Monte Carlo Simulations Biophys. J. 2006, 90 (5) 1767-1773
22. Sorin, E. J.; Pande, V. S. Nanotube Confinement Denatures Protein Helices J. Am. Chem. Soc. 2006, 128 (19) 6316-6317
23. Tian, J. H.; Garcia, A. E. Simulation Studies of Protein Folding/Unfolding Equilibrium under Polar and Nonpolar Confinement J. Am. Chem. Soc. 2011, 133 (38) 15157-15164
24. Tian, J. H.; Garcia, A. E. Simulations of the Confinement of Ubiquitin in Self-Assembled Reverse Micelles J. Chem. Phys. 2011, 134 (22) 225101-225111
25. Ziv, G.; Haran, G.; Thirumalai, D. Ribosome Exit Tunnel Can Entropically Stabilize Alpha-Helices Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (52) 18956-18961
26. Kim, Y. C.; Best, R. B.; Mittal, J. Macromolecular Crowding Effects on Protein-Protein Binding Affinity and Specificity J. Chem. Phys. 2010, 133 (20) 205101-205107
27. Mittal, J.; Best, R. B. Dependence of Protein Folding Stability and Dynamics on the Density and Composition of Macromolecular Crowders Biophys. J. 2010, 98 (2) 315-320
28. Mittal, J.; Hummer, G. Interfacial Thermodynamics of Confined Water near Molecularly Rough Surfaces Faraday Discuss. 2010, 146, 341-352
29. Rosen, J.; Kim, Y. C.; Mittal, J. Modest Protein-Crowder Attractive Interactions Can Counteract Enhancement of Protein Association by Intermolecular Excluded Volume Interactions J. Phys. Chem. B 2011, 115 (11) 2683-2689
30. Rosen, J.; Kim, Y. C.; Mittal, J. Macromolecular Crowding Effects on Multiprotein Binding Equilibria: Molecular Simulation and Theory Biophys. J. 2011, 100 (3) 614-614
31. Takagi, F.; Koga, N.; Takada, S. How Protein Thermodynamics and Folding Mechanisms Are Altered by the Chaperonin Cage: Molecular Simulations Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (20) 11367-11372
32. Minton, A. P. Confinement as a Determinant of Macromolecular Structure and Reactivity Biophys. J. 1992, 63 (4) 1090-1100
33. Zimmerman, S. B.; Minton, A. P. Macromolecular Crowding-Biochemical, Biophysical, and Physiological Consequences Annu. Rev. Biophys. Biomol. Struct. 1993, 22, 27-65
34. Minton, A. P. Effects of Macromolecular Crowding on Molecular Recognition Biophys. J. 1994, 66 (2) A68-A68
35. Minton, A. P. Macromolecular Crowding-A Foreword Biophys. Chem. 1995, 57 (1) 1-2
36. Minton, A. P. Implications of Macromolecular Crowding for Protein Assembly Curr. Opin. Struct. Biol. 2000, 10 (1) 34-39
37. Minton, A. P. The Influence of Macromolecular Crowding and Macromolecular Confinement on Biochemical Reactions in Physiological Media J. Biol. Chem. 2001, 276 (14) 10577-10580
38. Minton, A. P.; Colclasure, G. C.; Parker, J. C. Model for the Role of Macromolecular Crowding in Regulation of Cellular-Volume Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (21) 10504-10506
39. Minton, A. P.; Wilf, J. Effect of Macromolecular Crowding Upon the Structure and Function of an Enzyme-Glyceraldehyde-3-Phosphate Dehydrogenase Biochemistry 1981, 20 (17) 4821-4826
40. Zhou, H. X. Polymer Models of Protein Stability, Folding, and Interactions Biochemistry 2004, 43 (8) 2141-2154
41. Zhou, H. X. Helix Formation inside a Nanotube: Possible Influence of Backbone-Water Hydrogen Bonding by the Confining Surface through Modulation of Water Activity J. Chem. Phys. 2007, 127 (24) 245101-245104
42. Zhou, H. X. Protein Folding in Confined and Crowded Environments Arch. Biochem. Biophys. 2008, 469 (1) 76-82
43. Zhou, H. X.; Dill, K. A. Stabilization of Proteins in Confined Spaces Biochemistry 2001, 40 (38) 11289-11293
44. Tang, Y. C.; Chang, H. C.; Roeben, A.; Wischnewski, D.; Wischnewski, N.; Kerner, M. J.; Hartl, F. U.; Hayer-Hartl, M. Structural Features of the GroEL-GroES Nano-Cage Required for Rapid Folding of Encapsulated Protein Cell 2006, 125 (5) 903-914
45. Thirumalai, D.; Klimov, D. K.; Lorimer, G. H. Caging Helps Proteins Fold Proc.. Natl. Acad. Sci. U.S.A. 2003, 100 (20) 11195-11197
46. Lucent, D.; Vishal, V.; Pande, V. S. Protein Folding under Confinement: A Role for Solvent Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (25) 10430-10434
47. Lucent, D.; Snow, C. D.; Aitken, C. E.; Pande, V. S. Non-Bulk-Like Solvent Behavior in the Ribosome Exit Tunnel PLoS Comput. Biol. 2010, 6 (10) 1000963-1000968
48. Zuo, G. H.; Hu, J.; Fang, H. P. Effect of the Ordered Water on Protein Folding: An Off-Lattice Gō-Like Model Study Phys. Rev. E. 2009, 79 (3) 031925-031930
49. Hummer, G.; Rasaiah, J. C.; Noworyta, J. P. Water Conduction through the Hydrophobic Channel of a Carbon Nanotube Nature 2001, 414 (6860) 188-190
50. Yin, H.; Feng, G. G.; Clore, G. M.; Hummer, G.; Rasaiah, J. C. Water in the Polar and Nonpolar Cavities of the Protein Interleukin-1 Beta J. Phys. Chem. B 2010, 114 (49) 16290-16297
51. Yin, H.; Hummer, G.; Rasaiah, J. C. Metastable Water Clusters in the Nonpolar Cavities of the Thermostable Protein Tetrabrachion J. Am. Chem. Soc. 2007, 129 (23) 7369-7377
52. Lane, J. M. D.; Chandross, M.; Stevens, M. J.; Grest, G. S. Water in Nanoconfinement between Hydrophilic Self-Assembled Monolayers Langmuir 2008, 24 (10) 5209-5212
53. Meng, L. Y.; Li, Q. K.; Shuai, Z. G. Effects of Size Constraint on Water Filling Process in Nanotube J. Chem. Phys. 2008, 128 (13) 134703-134710
54. Won, C. Y.; Joseph, S.; Aluru, N. R. Effect of Quantum Partial Charges on the Structure and Dynamics of Water in Single-Walled Carbon Nanotubes J. Chem. Phys. 2006, 125 (11) 114701-114709
55. Athawale, M. V.; Jamadagni, S. N.; Garde, S. How Hydrophobic Hydration Responds to Solute Size and Attractions: Theory and Simulations J. Chem. Phys. 2009, 131 (11) 115102-115110
56. Jamadagni, S. N.; Godawat, R.; Dordick, J. S.; Garde, S. How Interfaces Affect Hydrophobically Driven Polymer Folding J. Phys. Chem. B 2009, 113 (13) 4093-4101
57. Jamadagni, S. N.; Godawat, R.; Garde, S. How Surface Wettabitity Affects the Binding, Folding, and Dynamics of Hydrophobic Polymers at Interfaces Langmuir 2009, 25 (22) 13092-13099
58. Lorenz, C. D.; Lane, J. M. D.; Chandross, M.; Stevens, M. J.; Grest, G. S. Molecular Dynamics Simulations of Water Confined between Matched Pairs of Hydrophobic and Hydrophilic Self-Assembled Monolayers Langmuir 2009, 25 (8) 4535-4542
59. Sansom, M. S. P.; Kerr, I. D.; Breed, J.; Sankararamakrishnan, R. Water in Channel-Like Cavities: Structure and Dynamics Biophys. J. 1996, 70 (2) 693-702
60. Garner, E.; Guilliot, S.; Dunker, A. K.; Romero, P.; Obradovic, Z. Predicting Long Disordered Regions in Protein from Amino Acid Sequence Biophys. J. 1998, 74 (2) A281-A281
61. Obradovic, Z.; Peng, K.; Vucetic, S.; Radivojac, P.; Brown, C. J.; Dunker, A. K. Predicting Intrinsic Disorder from Amino Acid Sequence Proteins 2003, 53 (6) 566-572
62. Dyson, H. J.; Wright, P. E. Insights into the Structure and Dynamics of Unfolded Proteins from Nuclear Magnetic Resonance Unfolded Proteins 2002, 62, 311-340
63. Tompa, P. The Interplay between Structure and Function in Intrinsically Unstructured Proteins FEBS Lett. 2005, 579 (15) 3346-3354
64. Uversky, V. N. Natively Unfolded Proteins: A Point Where Biology Waits for Physics Protein Sci. 2002, 11 (4) 739-756
65. Uversky, V. N. Amyloidogenesis of Natively Unfolded Proteins Curr. Alzheimer Res. 2008, 5 (3) 260-287
66. Wright, P. E.; Dyson, H. J. Intrinsically Unstructured Proteins: Re-Assessing the Protein Structure-Function Paradigm J. Mol. Biol. 1999, 293 (2) 321-331
67. Yang, M. F.; Teplow, D. B. Amyloid Beta-Protein Monomer Folding: Free-Energy Surfaces Reveal Alloform-Specific Differences J. Mol. Biol. 2008, 384 (2) 450-464
68. Urbanc, B.; Cruz, L.; Teplow, D. B.; Stanley, H. E. Computer Simulations of Alzheimer's Amyloid Beta-Protein Folding and Assembly Curr. Alzheimer Res. 2006, 3 (5) 493-504
69. Baumketner, A.; Bernstein, S. L.; Wyttenbach, T.; Bitan, G.; Teplow, D. B.; Bowers, M. T.; Shea, J. E. Amyloid Beta-Protein Monomer Structure: A Computational and Experimental Study Protein Sci. 2006, 15 (3) 420-428
70. Bernstein, S. L.; Wyttenbach, T.; Baumketner, A.; Shea, J. E.; Bitan, G.; Teplow, D. B.; Bowers, M. T. Amyloid Beta-Protein: Monomer Structure and Early Aggregation States of a Beta 42 and Its Pro(19) Alloform J. Am. Chem. Soc. 2005, 127 (7) 2075-2084
71. Urbanc, B.; Cruz, L.; Yun, S.; Buldyrev, S. V.; Bitan, G.; Teplow, D. B.; Stanley, H. E. In Silico Study of Amyloid Beta-Protein Folding and Oligomerization Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (50) 17345-17350
72. Lazo, N. D.; Grant, M. A.; Condron, M. C.; Rigby, A. C.; Teplow, D. B. On the Nucleation of Amyloid Beta-Protein Monomer Folding Protein Sci. 2005, 14 (6) 1581-1596
73. Lee, J. P.; Stimson, E. R.; Ghilardi, J. R.; Mantyh, P. W.; Lu, Y. A.; Felix, A. M.; Llanos, W.; Behbin, A.; Cummings, M.; Van Criekinge, M. 1H NMR of a Beta Amyloid Peptide Congeners in Water Solution. Conformational Changes Correlate with Plaque Competence Biochemistry 1995, 34 (15) 5191-5200
74. Zhang, S.; Iwata, K.; Lachenmann, M. J.; Peng, J. W.; Li, S.; Stimson, E. R.; Lu, Y.; Felix, A. M.; Maggio, J. E.; Lee, J. P. The Alzheimer's Peptide a Beta Adopts a Collapsed Coil Structure in Water J. Struct. Biol. 2000, 130 (2-3) 130-141
75. Balbach, J. J.; Ishii, Y.; Antzutkin, O. N.; Leapman, R. D.; Rizzo, N. W.; Dyda, F.; Reed, J.; Tycko, R. Amyloid Fibril Formation by a Beta 16-22, a Seven-Residue Fragment of the Alzheimer's Beta-Amyloid Peptide, and Structural Characterization by Solid State NMR Biochemistry 2000, 39 (45) 13748-13759
76. Ma, B.; Nussinov, R. Stabilities and Conformations of Alzheimer's Beta -Amyloid Peptide Oligomers (Abeta 16-22, Abeta 16-35, and Abeta 10-35): Sequence Effects Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (22) 14126-14131
77. Serpell, L. C. Alzheimer's Amyloid Fibrils: Structure and Assembly Biochim. Biophys. Acta 2000, 1502 (1) 16-30
78. Wei, G.; Shea, J. E. Effects of Solvent on the Structure of the Alzheimer Amyloid-Beta(25-35) Peptide Biophys. J. 2006, 91 (5) 1638-1647
79. Zanuy, D.; Ma, B.; Nussinov, R. Short Peptide Amyloid Organization: Stabilities and Conformations of the Islet Amyloid Peptide Nfgail Biophys. J. 2003, 84 (3) 1884-1894
80. Cruz, L.; Urbanc, B.; Borreguero, J. M.; Lazo, N. D.; Teplow, D. B.; Stanley, H. E. Solvent and Mutation Effects on the Nucleation of Amyloid Beta-Protein Folding Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (51) 18258-18263
81. Baumketner, A.; Bernstein, S. L.; Wyttenbach, T.; Lazo, N. D.; Teplow, D. B.; Bowers, M. T.; Shea, J. E. Structure of the 21-30 Fragment of Amyloid Beta-Protein Protein Sci. 2006, 15 (6) 1239-1247
82. Jorgensen, W. L.; Madura, J. D. Temperature and Size Dependence for Monte-Carlo Simulations of TIP4P Water Mol. Phys. 1985, 56 (6) 1381-1392
83. Kaminski, G. A.; Friesner, R. A.; Tirado-Rives, J.; Jorgensen, W. L. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins Via Comparison with Accurate Quantum Chemical Calculations on Peptides J. Phys. Chem. B 2001, 105 (28) 6474-6487
84. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A Package for Molecular Simulation and Trajectory Analysis J. Mol. Model. 2001, 7 (8) 306-317
85. Berendsen, H. J. C.; Vanderspoel, D.; Vandrunen, R. GROMACS-A Message-Passing Parallel Molecular-Dynamics Implementation Comput. Phys. Commun. 1995, 91 (1-3) 43-56
86. Cruz, L.; Rao, J. S.; Teplow, D. B.; Urbanc, B. Dynamics of Metastable Beta-Hairpin Structures in the Folding Nucleus of Amyloid Beta-Protein J. Phys. Chem. B 2012, 116 (22) 6311-6325
87. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81 (8) 3684-3690
88. Miyamoto, S.; Kollman, P. A. SETTLE-An Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13 (8) 952-962
89. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18 (12) 1463-1472
90. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G.; Smooth, A. Particle Mesh Ewald Method J. Chem. Phys. 1995, 103 (19) 8577-8593
91. Scott, K. A.; Alonso, D. O. V.; Sato, S.; Fersht, A. R.; Daggett, V. Conformational Entropy of Alanine Versus Glycine in Protein Denatured States Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (8) 2661-2666
92. Frishman, D.; Argos, P. Knowledge-Based Protein Secondary Structure Assignment Proteins 1995, 23 (4) 566-579
93. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14 (1) 33-38
94. Betancourt, M. R.; Thirumalai, D. Exploring the Kinetic Requirements for Enhancement of Protein Folding Rates in the GroEL Cavity J. Mol. Biol. 1999, 287 (3) 627-644
95. Cheung, M. S.; Thirumalai, D. Nanopore-Protein Interactions Dramatically Alter Stability and Yield of the Native State in Restricted Spaces J. Mol. Biol. 2006, 357 (2) 632-643
96. Ojeda, P.; Garcia, M. E.; Londono, A.; Chen, N. Y. Monte Carlo Simulations of Proteins in Cages: Influence of Confinement on the Stability of Intermediate States Biophys. J. 2009, 96 (3) 1076-1082
97. Sigler, P. B.; Xu, Z. H.; Rye, H. S.; Burston, S. G.; Fenton, W. A.; Horwich, A. L. Structure and Function in GroEL-Mediated Protein Folding Annu. Rev. Biochem. 1998, 67, 581-608
98. Faeder, J.; Ladanyi, B. M. Molecular Dynamics Simulations of the Interior of Aqueous Reverse Micelles J. Phys. Chem. B 2000, 104 (5) 1033-1046
99. Chimon, S.; Ishii, Y. Capturing Intermediate Structures of Alzheimer's Beta-Amyloid, Abeta(1-40), by Solid-State NMR Spectroscopy J. Am. Chem. Soc. 2005, 127 (39) 13472-13473
100. Petkova, A. T.; Ishii, Y.; Balbach, J. J.; Antzutkin, O. N.; Leapman, R. D.; Delaglio, F.; Tycko, R. A Structural Model for Alzheimer's BetaAmyloid Fibrils Based on Experimental Constraints from Solid State NMR Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (26) 16742-16747
101. Antzutkin, O. N.; Leapman, R. D.; Balbach, J. J.; Tycko, R. Supramolecular Structural Constraints on Alzheimer's Beta-Amyloid Fibrils from Electron Microscopy and Solid-State Nuclear Magnetic Resonance Biochemistry 2002, 41 (51) 15436-15450