Trp-Cage Folding on Organic Surfaces

Journal of Physical Chemistry B

Volumn 119, Issue 33, 2015, Pages 10417-10425

  Levine, Zachary A ^a   Fischer, Sean A ^b   Shea, Joan Emma ^a   Pfaendtner, Jim ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; CONFORMATIONS; HYDROPHOBICITY; MOLECULAR DYNAMICS;

AROMATIC GROUP; ELECTROSTATIC ATTRACTIONS; HYDROPHOBIC INTERACTIONS; ORGANIC SURFACES; POLY PROLINES; PROTEIN CONFORMATION; REPLICA EXCHANGE MOLECULAR DYNAMICS; SOLID-STATE SURFACE;

SELF ASSEMBLED MONOLAYERS;

ORGANIC COMPOUND; PEPTIDE; TRP-CAGE PEPTIDE;

AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMISTRY; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SURFACE PROPERTY;

AMINO ACID SEQUENCE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; ORGANIC CHEMICALS; PEPTIDES; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SURFACE PROPERTIES;

EID: 84939604118     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b04213     Document Type: Article

References (60)

1. Neidigh, J. W.; Fesinmeyer, R. M.; Andersen, N. H. Designing a 20-Residue Protein Nat. Struct. Biol. 2002, 9, 425-430 10.1038/nsb798
2. Hudaky, P.; Straner, P.; Farkas, V.; Varadi, G.; Toth, G.; Perczel, A. Cooperation Between a Salt Bridge and the Hydrophobic Core Triggers Fold Stabilization in a Trp-Cage Miniprotein Biochemistry 2008, 47, 1007-1016 10.1021/bi701371x
3. Streicher, W. W.; Makhatadze, G. I. Unfolding Thermodynamics of Trp-Cage, a 20 Residue Miniprotein, Studied by Differential Scanning Calorimetry and Circular Dichroism Spectroscopy Biochemistry 2007, 46, 2876-2880 10.1021/bi602424x
4. Qiu, L. L.; Pabit, S. A.; Roitberg, A. E.; Hagen, S. J. Smaller and Faster: The 20-Residue Trp-Cage Protein Folds in 4 Mu S J. Am. Chem. Soc. 2002, 124, 12952-12953 10.1021/ja0279141
5. Neuweiler, H.; Doose, S.; Sauer, M. A Microscopic View of Miniprotein Folding: Enhanced Folding Efficiency Through Formation of an Intermediate Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 16650-16655 10.1073/pnas.0507351102
6. Ahmed, Z.; Beta, I. A.; Mikhonin, A. V.; Asher, S. A. Uv-Resonance Raman Thermal Unfolding Study of Trp-Cage Shows That It Is Not a Simple Two-State Miniprotein J. Am. Chem. Soc. 2005, 127, 10943-10950 10.1021/ja050664e
7. Barua, B.; Lin, J. C.; Williams, V. D.; Kummler, P.; Neidigh, J. W.; Andersen, N. H. The Trp-Cage: Optimizing the Stability of a Globular Miniprotein Protein Eng., Des. Sel. 2008, 21, 171-185 10.1093/protein/gzm082
8. Wafer, L. N. R.; Streicher, W. W.; Makhatadze, G. I. Thermodynamics of the Trp-Cage Miniprotein Unfolding in Urea Proteins: Struct., Funct., Genet. 2010, 78, 1376-1381 10.1002/prot.22681
9. Pitera, J. W.; Swope, W. Understanding Folding and Design: Replica-Exchange Simulations of "Trp-Cage" Fly Miniproteins Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 7587-7592 10.1073/pnas.1330954100
10. Piana, S.; Laio, A. A Bias-Exchange Approach to Protein Folding J. Phys. Chem. B 2007, 111, 4553-4559 10.1021/jp067873l
11. Paschek, D.; Hempel, S.; Garcia, A. E. Computing the Stability Diagram of the Trp-Cage Miniprotein Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 17754-17759 10.1073/pnas.0804775105
12. Day, R.; Paschek, D.; Garcia, A. E. Microsecond Simulations of the Folding/Unfolding Thermodynamics of the Trp-Cage Miniprotein Proteins: Struct., Funct., Genet. 2010, 78, 1889-1899 10.1002/prot.22702
13. English, C. A.; Garcia, A. E. Folding and Unfolding Thermodynamics of the Tc10b Trp-Cage Miniprotein Phys. Chem. Chem. Phys. 2014, 16, 2748-2757 10.1039/c3cp54339k
14. Snow, C. D.; Zagrovic, B.; Pande, V. S. The Trp Cage: Folding Kinetics and Unfolded State Topology Via Molecular Dynamics Simulations J. Am. Chem. Soc. 2002, 124, 14548-14549 10.1021/ja028604l
15. Marinelli, F.; Pietrucci, F.; Laio, A.; Piana, S. A Kinetic Model of Trp-Cage Folding from Multiple Biased Molecular Dynamics Simulations PLoS Comput. Biol. 2009, 5, e1000452 10.1371/journal.pcbi.1000452
16. Marinelli, F. Following Easy Slope Paths on a Free Energy Landscape: The Case Study of the Trp-Cage Folding Mechanism Biophys. J. 2013, 105, 1236-1247 10.1016/j.bpj.2013.07.046
17. Juraszek, J.; Bolhuis, P. G. Sampling the Multiple Folding Mechanisms of Trp-Cage in Explicit Solvent Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 15859-15864 10.1073/pnas.0606692103
18. Paschek, D.; Nymeyer, H.; Garcia, A. E. Replica Exchange Simulation of Reversible Folding/Unfolding of the Trp-Cage Miniprotein in Explicit Solvent: On the Structure and Possible Role of Internal Water J. Struct. Biol. 2007, 157, 524-533 10.1016/j.jsb.2006.10.031
19. Zhou, R. H. Trp-Cage: Folding Free Energy Landscape in Explicit Water Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 13280-13285 10.1073/pnas.2233312100
20. Chowdhury, S.; Lee, M. C.; Xiong, G. M.; Duan, Y. Ab Initio Folding Simulation of the Trp-Cage Mini-Protein Approaches NMR Resolution J. Mol. Biol. 2003, 327, 711-717 10.1016/S0022-2836(03)00177-3
21. Zhan, L. X.; Chen, J. Z. Y.; Liu, W. K. Computational Study of the Trp-Cage Miniprotein Based on the ECEPP/3 Force Field Proteins: Struct., Funct., Genet. 2007, 66, 436-443 10.1002/prot.21157
22. Peter, E. K.; Shea, J.-E. A Hybrid MD
23. Juraszek, J.; Bolhuis, P. G. Rate Constant and Reaction Coordinate of Trp-Cage Folding in Explicit Water Biophys. J. 2008, 95, 4246-4257 10.1529/biophysj.108.136267
24. Paschek, D.; Day, R.; Garcia, A. E. Influence of Water-Protein Hydrogen Bonding on the Stability of Trp-Cage Miniprotein. A Comparison between the TIP3P and Tip4p-Ew Water Models Phys. Chem. Chem. Phys. 2011, 13, 19840-19847 10.1039/c1cp22110h
25. Mei, Y.; Wei, C. Y.; Yip, Y. M.; Ho, C. Y.; Zhang, J. Z. H.; Zhang, D. W. Folding and Thermodynamic Studies of Trp-Cage Based on Polarized Force Field Theor. Chem. Acc. 2012, 131, 1168 10.1007/s00214-012-1168-0
26. Marino, K. A.; Bolhuis, P. G. Confinement-Induced States in the Folding Landscape of the Trp-Cage Miniprotein J. Phys. Chem. B 2012, 116, 11872-11880 10.1021/jp306727r
27. Tian, J. H.; Garcia, A. E. Simulation Studies of Protein Folding/Unfolding Equilibrium under Polar and Nonpolar Confinement J. Am. Chem. Soc. 2011, 133, 15157-15164 10.1021/ja2054572
28. Kannan, S.; Zacharias, M. Folding Simulations of Trp-Cage Mini Protein in Explicit Solvent Using Biasing Potential Replica-Exchange Molecular Dynamics Simulations Proteins: Struct., Funct., Genet. 2009, 76, 448-460 10.1002/prot.22359
29. Lockhart, C.; Klimov, D. K. Alzheimer's Abeta10-40 Peptide Binds and Penetrates Dmpc Bilayer: An Isobaric-Isothermal Replica Exchange Molecular Dynamics Study J. Phys. Chem. B 2014, 118, 2638-48 10.1021/jp412153s
30. Godawat, R.; Jamadagni, S. N.; Garde, S. Characterizing Hydrophobicity of Interfaces by Using Cavity Formation, Solute Binding, and Water Correlations Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 15119-15124 10.1073/pnas.0902778106
31. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters Proteins: Struct., Funct., Genet. 2006, 65, 712-725 10.1002/prot.21123
32. Showalter, S. A.; Bruschweiler, R. Validation of Molecular Dynamics Simulations of Biomolecules Using NMR Spin Relaxation as Benchmarks: Application to the Amber99sb Force Field J. Chem. Theory Comput. 2007, 3, 961-975 10.1021/ct7000045
33. Best, R. B.; Hummer, G. Optimized Molecular Dynamics Force Fields Applied to the Helix-Coil Transition of Polypeptides J. Phys. Chem. B 2009, 113, 9004-9015 10.1021/jp901540t
34. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved Side-Chain Torsion Potentials for the Amber FF99sb Protein Force Field Proteins: Struct., Funct., Genet. 2010, 78, 1950-1958 10.1002/prot.22711
35. Beauchamp, K. A.; Lin, Y.-S.; Das, R.; Pande, V. S. Are Protein Force Fields Getting Better? A Systematic Benchmark on 524 Diverse NMR Measurements J. Chem. Theory Comput. 2012, 8, 1409-1414 10.1021/ct2007814
36. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
37. 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 10.1063/1.445869
38. 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, 3684-3690 10.1063/1.448118
39. Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling J. Chem. Phys. 2007, 126, 014101 10.1063/1.2408420
40. 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, 1463-1472 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
41. Miyamoto, S.; Kollman, P. A. Settle-an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962 10.1002/jcc.540130805
42. 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, 8577-8593 10.1063/1.470117
43. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151 10.1016/S0009-2614(99)01123-9
44. Bonomi, M.; Branduardi, D.; Bussi, G.; Camilloni, C.; Provasi, D.; Raiteri, P.; Donadio, D.; Marinelli, F.; Pietrucci, F.; Broglia, R. A. et al. Plumed: A Portable Plugin for Free-Energy Calculations with Molecular Dynamics Comput. Phys. Commun. 2009, 180, 1961-1972 10.1016/j.cpc.2009.05.011
45. Laio, A.; Parrinello, M. Escaping Free-Energy Minima Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12562-12566 10.1073/pnas.202427399
46. Barducci, A.; Bonomi, M.; Parrinello, M. Metadynamics Wires Comput. Mol. Sci. 2011, 1, 826-843 10.1002/wcms.31
47. Bussi, G.; Gervasio, F. L.; Laio, A.; Parrinello, M. Free-Energy Landscape for Beta Hairpin Folding from Combined Parallel Tempering and Metadynamics J. Am. Chem. Soc. 2006, 128, 13435-13441 10.1021/ja062463w
48. Bonomi, M.; Parrinello, M. Enhanced Sampling in the Well-Tempered Ensemble Phys. Rev. Lett. 2010, 104, 190601 10.1103/PhysRevLett.104.190601
49. Deighan, M.; Bonomi, M.; Pfaendtner, J. Efficient Simulation of Explicitly Solvated Proteins in the Well-Tempered Ensemble J. Chem. Theory Comput. 2012, 8, 2189-21982 10.1021/ct300297t
50. Bonomi, M.; Barducci, A.; Parrinello, M. Reconstructing the Equilibrium Boltzmann Distribution from Well-Tempered Metadynamics J. Comput. Chem. 2009, 30, 1615-1621 10.1002/jcc.21305
51. Ceriotti, M.; Brain, G. A. R.; Riordan, O.; Manolopoulos, D. E. The Inefficiency of Re-Weighted Sampling and the Curse of System Size in High-Order Path Integration Proc. R. Soc. London, Ser. A 2012, 468, 2-17 10.1098/rspa.2011.0413
52. Deighan, M.; Pfaendtner, J. Exhaustively Sampling Peptide Adsorption with Metadynamics Langmuir 2013, 29, 7999-8009 10.1021/la4010664
53. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
54. Daura, X.; Gademann, K.; Schafer, H.; Jaun, B.; Seebach, D.; van Gunsteren, W. F. The Beta-Peptide Hairpin in Solution: Conformational Study of a Beta-Hexapeptide in Methanol by NMR Spectroscopy and MD Simulation J. Am. Chem. Soc. 2001, 123, 2393-404 10.1021/ja003689g
55. Kabsch, W.; Sander, C. Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-Bonded and Geometrical Features Biopolymers 1983, 22, 2577-2637 10.1002/bip.360221211
56. Palazzesi, F.; Prakash, M. K.; Bonomi, M.; Barducci, A. Accuracy of Current All-Atom Force-Fields in Modeling Protein Disordered States J. Chem. Theory Comput. 2015, 11, 2-7 10.1021/ct500718s
57. Henriques, J.; Cragnell, C.; Skepö, M. Molecular Dynamics Simulations of Intrinsically Disordered Proteins: Force Field Evaluation and Comparison with Experiment J. Chem. Theory Comput. 2015, 11, 3420 10.1021/ct501178z
58. English, C. A.; García, A. E. Charged Termini on the Trp-Cage Roughen the Folding Energy Landscape J. Phys. Chem. B 2015, 119, 7874-7881 10.1021/acs.jpcb.5b02040
59. Smeller, L. Pressure-Temperature Phase Diagrams of Biomolecules Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 2002, 1595, 11-29 10.1016/S0167-4838(01)00332-6
60. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T. et al. A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins Based on Condensed-Phase Quantum Mechanical Calculations J. Comput. Chem. 2003, 24, 1999-2012 10.1002/jcc.10349