Insights from molecular dynamics simulations for computational protein design

Molecular Systems Design and Engineering

Volumn 2, Issue 1, 2017, Pages 9-33

  Childers, Matthew Carter ^a   Daggett, Valerie ^a  

^a University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL CHEMISTRY; CONFORMATIONS; MOLECULAR DYNAMICS; PROTEINS;

AMINO ACID SEQUENCE; CLASSICAL DYNAMICS; COMPUTATIONAL PROTEIN DESIGN; CONFORMATIONAL TRANSITIONS; EXPERIMENTAL TECHNIQUES; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN DATA BANK; STRUCTURAL BIOLOGY;

STRUCTURAL DESIGN;

EID: 85028047204     PISSN: None     EISSN: 20589689     Source Type: Journal    
DOI: 10.1039/c6me00083e     Document Type: Review

References (223)

1. B. A. Gutte Synthetic 70-amino acid residue analog of ribonuclease S-protein with enzymic activity J. Biol. Chem. 1975 250 889 904
2. B. Gutte Study of RNase A mechanism and folding by means of synthetic 63-residue analogs J. Biol. Chem. 1977 252 663 670
3. M. Levitt J. Greer Automatic identification of secondary structure in globular proteins J. Mol. Biol. 1977 114 181 239
4. E. T. Kaiser F. J. Kézdy Secondary structures of proteins and peptides in amphiphilic environments Proc. Natl. Acad. Sci. U. S. A. 1983 80 1137 1143
5. R. Moser et al., Expression of the synthetic gene of an artificial DDT-binding polypeptide in Escherichia coli Protein Eng., Des. Sel. 1987 1 339 343
6. R. Moser R. M. Thomas B. Gutte An artificial crystalline DDT-binding polypeptide FEBS Lett. 1983 157 247 251
7. B. Gutte M. Däumigen E. Wittschieber Design, synthesis and characterisation of a 34-residue polypeptide that interacts with nucleic acids Nature 1979 281 650 655
8. M. Hecht J. Richardson D. Richardson R. Ogden De novo design, expression, and characterization of Felix: a four-helix bundle protein of native-like sequence Science 1990 249 973
9. B. Erickson, et al., in Computer Graphics and Molecular Modeling, ed., R. Fletterick, and, M. Zoller, Cold Spring Harbor Laboratory, 1986, pp. 53-57
10. J. S. Richardson D. C. Richardson The de novo design of protein structures Trends Biochem. Sci. 1989 14 304 309
11. R. L. Dunbrack M. Karplus Backbone-dependent rotamer library for proteins. Application to side-chain prediction J. Mol. Biol. 1993 230 543 574
12. C. Wilson L. M. Gregoret D. A. Agard Modeling side-chain conformation for homologous proteins using an energy-based rotamer search J. Mol. Biol. 1993 229 996 1006
13. B. I. Dahiyat S. L. Mayo De novo protein design: fully automated sequence selection Science 1997 278 82 87
14. B. Kuhlman et al., Design of a novel globular protein fold with atomic-level accuracy Science 2003 302 1364 1368
15. R. Sterner R. Merkl F. M. Raushel Computational Design of Enzymes Chem. Biol. 2008 15 421 423
16. S. Sivaramakrishnan E. Ashley L. Leinwand J. A. Spudich Insights into human beta-cardiac myosin function from single molecule and single cell studies J. Cardiovasc. Transl. Res. 2009 2 426 440
17. E. Z. Eisenmesser et al., Intrinsic dynamics of an enzyme underlies catalysis Nature 2005 438 117 121
18. E. Z. Eisenmesser D. A. Bosco M. Akke D. Kern Enzyme dynamics during catalysis Science 2002 295 1520 1523
19. M. P. Allen and D. J. Tildesley, Computer Simulations of Liquids, Clarendon Press, 1987
20. A. G. Palmer NMR probes of molecular dynamics: Overview and comparison with other techniques Annu. Rev. Biophys. Biomol. Struct. 2001 30 129 155
21. H. van den Bedem J. S. Fraser Integrative, dynamic structural biology at atomic resolution - it's about time Nat. Methods 2015 12 307 318
22. R. O. Dror M. Ø. Jensen D. W. Borhani D. E. Shaw Exploring atomic resolution physiology on a femtosecond to millisecond timescale using molecular dynamics simulations J. Gen. Physiol. 2010 135 555 562
23. T. D. Romo A. Grossfield Unknown unknowns: the challenge of systematic and statistical error in molecular dynamics simulations Biophys. J. 2014 106 1553 1554
24. L. Monticelli and D. P. Tieleman, in Methods in Molecular Biology, 2013, vol. 924, pp. 197-213
25. E. A. Cino W.-Y. Choy M. Karttunen Comparison of Secondary Structure Formation Using 10 Different Force Fields in Microsecond Molecular Dynamics Simulations J. Chem. Theory Comput. 2012 8 2725 2740
26. D. J. Price C. L. Brooks Modern protein force fields behave comparably in molecular dynamics simulations J. Comput. Chem. 2002 23 1045 1057
27. K. Lindorff-Larsen et al., Systematic validation of protein force fields against experimental data PLoS One 2012 7 e32131
28. K. A. Beauchamp Y.-S. Lin R. Das V. S. Pande Are Protein Force Fields Getting Better? A Systematic Benchmark on 524 Diverse NMR Measurements J. Chem. Theory Comput. 2012 8 1409 1414
29. O. F. Lange D. van der Spoel B. L. de Groot Scrutinizing molecular mechanics force fields on the submicrosecond timescale with NMR data Biophys. J. 2010 99 647 655
30. Y. Gu D.-W. W. Li R. Brüschweiler NMR Order Parameter Determination from Long Molecular Dynamics Trajectories for Objective Comparison with Experiment J. Chem. Theory Comput. 2014 10 2599 2607
31. E. S. O'Brien A. J. Wand K. A. Sharp On the ability of molecular dynamics force fields to recapitulate NMR derived protein side chain order parameters Protein Sci. 2016 25 1156 1160
32. D. A. C. Beck R. S. Armen V. Daggett Cutoff size need not strongly influence molecular dynamics results on solvated polypeptides Biochemistry 2005 44 609 616
33. G. Hernández J. S. Anderson D. M. Lemaster Experimentally assessing molecular dynamics sampling of the protein native state conformational distribution Biophys. Chem. 2012 163-164 21 34
34. K. C. Cunha et al., Assessing protein conformational sampling and structural stability via de novo design and molecular dynamics simulations Biopolymers 2015 103 351 361
35. S. D. Bond B. J. Leimkuhler Molecular dynamics and the accuracy of numerically computed averages Acta Numer. 2007 16 1 65
36. D. C. C. Rapaport, The Art of Molecular Dynamics Simulation, Cambridge University Press, 2nd edn, 2004
37. R. D. Skeel, in The Graduate Student's Guide to Numerical Analysis '98, 1999, vol. 26, pp. 119-176
38. M. E. Tuckerman G. J. Martyna Understanding Modern Molecular Dynamics: Techniques and Applications J. Phys. Chem. B 2000 104 159 178
39. M. Levitt M. Hirshberg R. Sharon K. E. Laidig V. Daggett Calibration and Testing of a Water Model for Simulation of the Molecular Dynamics of Proteins and Nucleic Acids in Solution J. Phys. Chem. B 1997 101 5051 5061
40. D. E. Shaw et al., Atomic-level characterization of the structural dynamics of proteins Science 2010 330 341 346
41. K. Lindorff-Larsen P. Maragakis S. Piana D. E. Shaw Picosecond to Millisecond Structural Dynamics in Human Ubiquitin J. Phys. Chem. B 2016 120 8313 8320
42. M. J. Abraham et al., GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers SoftwareX 2015 1 19 25
43. V. S. Pande et al., Atomistic protein folding simulations on the submillisecond time scale using worldwide distributed computing Biopolymers 2003 68 91 109
44. W. F. van Gunsteren J. Dolenc A. E. Mark Molecular simulation as an aid to experimentalists Curr. Opin. Struct. Biol. 2008 18 149 153
45. W. F. van Gunsteren A. E. Mark Validation of molecular dynamics simulation J. Chem. Phys. 1998 108 6109
46. V. Daggett Molecular Dynamics Simulations of the Protein Unfolding/Folding Reaction Acc. Chem. Res. 2002 35 422 429
47. G. D. Haki S. K. Rakshit Developments in industrially important thermostable enzymes: a review Bioresour. Technol. 2003 89 17 34
48. J.-M. Choi S.-S. Han H.-S. Kim Industrial applications of enzyme biocatalysis: Current status and future aspects Biotechnol. Adv. 2015 33 1443 1454
49. C. J. Wilson Rational protein design: developing next-generation biological therapeutics and nanobiotechnological tools Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2015 7 330 341
50. C. N. Pace B. A. Shirley M. McNutt K. Gajiwala Forces contributing to the conformational stability of proteins FASEB J. 1996 10 75 83
51. A. Yokota H. Takahashi T. Takenawa M. Arai Probing the roles of conserved arginine-44 of Escherichia coli dihydrofolate reductase in its function and stability by systematic sequence perturbation analysis Biochem. Biophys. Res. Commun. 2010 391 1703 1707
52. M. Torrado et al., Role of conserved salt bridges in homeodomain stability and DNA binding J. Biol. Chem. 2009 284 23765 23779
53. J.-B. Jomain et al., Structural and thermodynamic bases for the design of pure prolactin receptor antagonists: X-ray structure of Del1-9-G129R-hPRL J. Biol. Chem. 2007 282 33118 33131
54. R. S. Fredricksen C. A. Swenson Relationship between stability and function for isolated domains of troponin C Biochemistry 1996 35 14012 14026
55. A. L. Stouffer V. Nanda J. D. Lear W. F. DeGrado Sequence determinants of a transmembrane proton channel: an inverse relationship between stability and function J. Mol. Biol. 2005 347 169 179
56. M. Masazumi G. Signor B. W. Matthews Substantial increase of protein stability by multiple disulphide bonds Nature 1989 342 291 293
57. T. Sikosek H. S. Chan Biophysics of protein evolution and evolutionary protein biophysics J. R. Soc., Interface 2014 11 20140419
58. S. Kapoor A. Rafiq S. Sharma Protein Engineering and Its Applications in Food Industry Crit. Rev. Food Sci. Nutr. 2015 11 10.1080/10408398.2014.1000481
59. K. Teilum J. G. Olsen B. B. Kragelund Protein stability, flexibility and function Biochim. Biophys. Acta, Proteins Proteomics 2011 1814 969 976
60. J. Clarke A. M. Hounslow C. J. Bond A. R. Fersht V. Daggett The effects of disulfide bonds on the denatured state of barnase Protein Sci. 2000 9 2394 2404
61. S. S. Pendley Y. B. Yu T. E. Cheatham Molecular dynamics guided study of salt bridge length dependence in both fluorinated and non-fluorinated parallel dimeric coiled-coils Proteins 2009 74 612 629
62. S.-H. H. Chao et al., Two structural scenarios for protein stabilization by PEG J. Phys. Chem. B 2014 118 8388 8395
63. S. Xiao et al., Rational modification of protein stability by targeting surface sites leads to complicated results Proc. Natl. Acad. Sci. U. S. A. 2013 110 11337 11342
64. H. M. Berman J. Westbrook Z. Feng G. Gilliland T. N. Bhat H. Weissig I. N. Shindyalov P. E. Bourne The Protein Data Bank Nucleic Acids Res. 2000 28 235 242
65. P. J. Flory Statistical Thermodynamics of Semi-Flexible Chain Molecules Proc. R. Soc. A 1956 234 60 73
66. A. J. Doig D. H. Williams Is the hydrophobic effect stabilizing or destabilizing in proteins?: The contribution of disulphide bonds to protein stability J. Mol. Biol. 1991 217 389 398
67. J. Clarke A. R. Fersht Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation Biochemistry 1993 32 4322 4329
68. C. M. Johnson M. Oliveberg J. Clarke A. R. Fersht Thermodynamics of denaturation of mutants of barnase with disulfide crosslinks J. Mol. Biol. 1997 268 198 208
69. S. F. Betz Disulfide bonds and the stability of globular proteins Protein Sci. 1993 2 1551 1558
70. M. G. Pikkemaat A. B. M. Linssen H. J. C. Berendsen D. B. Janssen Molecular dynamics simulations as a tool for improving protein stability Protein Eng. 2002 15 185 192
71. B. Hazes B. W. Dijkstra Model building of disulfide bonds in proteins with known three-dimensional structure Protein Eng. 1988 2 119 125
72. C. Niu L. Zhu X. Xu Q. Li Rational Design of Disulfide Bonds Increases Thermostability of a Mesophilic 1,3-1,4-β-Glucanase from Bacillus terquilensis PLoS One 2016 11 e0154036
73. H. Yu H. Huang Engineering proteins for thermostability through rigidifying flexible sites Biotechnol. Adv. 2014 32 308 315
74. V. Daggett M. Levitt A model of the molten globule state from molecular dynamics simulations Proc. Natl. Acad. Sci. U. S. A. 1992 89 5142 5146
75. V. Daggett M. Levitt Protein unfolding pathways explored through molecular dynamics simulations J. Mol. Biol. 1993 232 600 619
76. M. Levitt M. Hirshberg R. Sharon V. Daggett Potential Energy Function and Parameters for Simulations of the Molecular Dynamics of Proteins and Nucleic Acids in Solution Comput. Phys. Commun. 1995 91 215 231
77. A. Matouschek J. T. Kellis Jr L. Serrano A. R. Fersht Mapping the transition state and pathway of protein folding by protein engineering Nature 1989 340 122 126
78. V. Daggett A. Li L. S. Itzhaki D. E. Otzen A. R. Fersht Structure of the transition state for folding of a protein derived from experiment and simulation J. Mol. Biol. 1996 257 430 440
79. N. Kulkarni A. Shendye M. Rao Molecular and biotechnological aspects of xylanases FEMS Microbiol. Rev. 1999 23 411 456
80. Q. Beg M. Kapoor L. Mahajan G. S. Hoondal Microbial xylanases and their industrial applications: a review Appl. Microbiol. Biotechnol. 2001 56 326 338
81. T. Collins C. Gerday G. Feller Xylanases, xylanase families and extremophilic xylanases FEMS Microbiol. Rev. 2005 29 3 23
82. J. C. Joo S. Pohkrel S. P. Pack Y. J. Yoo Thermostabilization of Bacillus circulans xylanase via computational design of a flexible surface cavity J. Biotechnol. 2010 146 31 39
83. S. Wells S. Menor B. Hespenheide M. F. Thorpe Constrained geometric simulation of diffusive motion in proteins Phys. Biol. 2005 2 S127 S136
84. J. C. Joo S. P. Pack Y. H. Kim Y. J. Yoo Thermostabilization of Bacillus circulans xylanase: Computational optimization of unstable residues based on thermal fluctuation analysis J. Biotechnol. 2011 151 56 65
85. Y. Liu B. Kuhlman RosettaDesign server for protein design Nucleic Acids Res. 2006 34 W235 W238
86. G. Vogt S. Woell P. Argos Protein thermal stability, hydrogen bonds, and ion pairs J. Mol. Biol. 1997 269 631 643
87. E. D. Merkley W. W. Parson V. Daggett Temperature dependence of the flexibility of thermophilic and mesophilic flavoenzymes of the nitroreductase fold Protein Eng., Des. Sel. 2010 23 327 336
88. A. Szilágyi P. Závodszky Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey Structure 2000 8 493 504
89. K. Yokota K. Satou S.-Y. Ohki Comparative analysis of protein thermostability: differences in amino acid content and substitution at the surfaces and in the core regions of thermophilic and mesophilic proteins Sci. Technol. Adv. Mater. 2006 7 255 262
90. D. S. Vieira L. Degreve An insight into the thermostability of a pair of xylanases: the role of hydrogen bonds Mol. Phys. 2009 107 59 69
91. D. S. Vieira L. Degrève R. J. Ward Characterization of temperature dependent and substrate-binding cleft movements in Bacillus circulans family 11 xylanase: a molecular dynamics investigation Biochim. Biophys. Acta 2009 1790 1301 1306
92. J. S. Alponti R. Fonseca Maldonado R. J. Ward Thermostabilization of Bacillus subtilis GH11 xylanase by surface charge engineering Int. J. Biol. Macromol. 2016 87 522 528
93. J. Chen H. Yu C. Liu J. Liu Z. Shen Improving stability of nitrile hydratase by bridging the salt-bridges in specific thermal-sensitive regions J. Biotechnol. 2012 164 354 362
94. J. Li A. Mahajan M. D. Tsai Ankyrin repeat: A unique motif mediating protein-protein interactions Biochemistry 2006 45 15168 15178
95. L. K. Mosavi T. J. Cammett D. C. Desrosiers Z.-Y. Peng The ankyrin repeat as molecular architecture for protein recognition Protein Sci. 2004 13 1435 1448
96. B. T. Porebski A. M. Buckle Consensus protein design Protein Eng., Des. Sel. 2016 29 245 251
97. H. K. Binz M. T. Stumpp P. Forrer P. Amstutz A. Plückthun Designing repeat proteins: Well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins J. Mol. Biol. 2003 332 489 503
98. P. Forrer M. T. Stumpp H. K. Binz A. Plückthun A novel strategy to design binding molecules harnessing the modular nature of repeat proteins FEBS Lett. 2003 539 2 6
99. G. Interlandi S. K. Wetzel G. Settanni A. Plückthun A. Caflisch Characterization and further stabilization of designed ankyrin repeat proteins by combining molecular dynamics simulations and experiments J. Mol. Biol. 2008 375 837 854
100. P. Alfarano et al., Optimization of designed armadillo repeat proteins by molecular dynamics simulations and NMR spectroscopy Protein Sci. 2012 21 1298 1314
101. A.-S. Yang B. Honig On the pH Dependence of Protein Stability J. Mol. Biol. 1993 231 459 474
102. C. Oinonen J. Rouvinen Structural comparison of Ntn-hydrolases Protein Sci. 2000 9 2329 2337
103. M. Arroyo I. de la Mata C. Acebal M. P. Castillón Biotechnological applications of penicillin acylases: state-of-the-art Appl. Microbiol. Biotechnol. 2003 60 507 514
104. D. T. Guranda T. S. Volovik V. K. Svedas pH Stability of penicillin acylase from Escherichia coli Biochemistry 2004 69 1386 1390
105. D. Suplatov et al., Computational design of a pH stable enzyme: understanding molecular mechanism of penicillin acylase's adaptation to alkaline conditions PLoS One 2014 9 e100643
106. S. Leone et al., Molecular Dynamics Driven Design of pH-Stabilized Mutants of MNEI, a Sweet Protein PLoS One 2016 11 e0158372
107. M. Strumillo P. Beltrao Towards the computational design of protein post-translational regulation Bioorg. Med. Chem. 2015 23 2877 2882
108. K.-Y. Huang et al., dbPTM 2016: 10-year anniversary of a resource for post-translational modification of proteins Nucleic Acids Res. 2016 44 D435 D446
109. G. A. Khoury et al., Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database Sci. Rep. 2011 1 4 8
110. R. J. Solá K. Griebenow Effects of glycosylation on the stability of protein pharmaceuticals J. Pharm. Sci. 2009 98 1223 1245
111. R. Apweiler H. Hermjakob N. Sharon On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database Biochim. Biophys. Acta 1999 1473 4 8
112. A. M. Sinclair S. Elliott Glycoengineering: The effect of glycosylation on the properties of therapeutic proteins J. Pharm. Sci. 2005 94 1626 1635
113. J. L. Baker E. Çelik M. P. DeLisa Expanding the glycoengineering toolbox: the rise of bacterial N-linked protein glycosylation Trends Biotechnol. 2013 31 313 323
114. H. W. Hellinga Rational protein design: combining theory and experiment Proc. Natl. Acad. Sci. U. S. A. 1997 94 10015 10017
115. I. N. Berezovsky K. B. Zeldovich E. I. Shakhnovich Positive and negative design in stability and thermal adaptation of natural proteins PLoS Comput. Biol. 2007 3 e52
116. M. Samoudi et al., Rational design of hyper-glycosylated interferon beta analogs: A computational strategy for glycoengineering J. Mol. Graphics Modell. 2015 56 31 42
117. J. A. Davey A. M. Damry C. K. Euler N. K. Goto R. A. Chica Prediction of Stable Globular Proteins Using Negative Design with Non-native Backbone Ensembles Structure 2015 23 2011 2021
118. R. Fonseca-Maldonado et al., Engineering the pattern of protein glycosylation modulates the thermostability of a GH11 xylanase J. Biol. Chem. 2013 288 25522 25534
119. G. N. Ramachandran C. Ramakrishnan V. Sasisekharan Stereochemistry of polypeptide chain configurations J. Mol. Biol. 1963 7 95 99
120. C.-L. Towse G. Hopping I. Vulovic V. Daggett Nature versus design: the conformational propensities of D-amino acids and the importance of side chain chirality Protein Eng., Des. Sel. 2014 27 447 455
121. A. Rodriguez-Granillo S. Annavarapu L. Zhang R. L. Koder V. Nanda Computational design of thermostabilizing D-amino acid substitutions J. Am. Chem. Soc. 2011 133 18750 18759
122. B. Imperiali R. A. Moats S. L. Fisher T. J. Prins A conformational study of peptides with the general structure Ac-L-Xaa-Pro-D-Xaa-L-Xaa-NH2: spectroscopic evidence for a peptide with significant beta-turn character in water and in dimethyl sulfoxide J. Am. Chem. Soc. 1992 114 3182 3188
123. G. Hopping et al., Designed α-sheet peptides inhibit amyloid formation by targeting toxic oligomers eLife 2014 3 e01681
124. J. Kellock G. Hopping B. Caughey V. Daggett Peptides Composed of Alternating L- and D-Amino Acids Inhibit Amyloidogenesis in Three Distinct Amyloid Systems Independent of Sequence J. Mol. Biol. 2016 428 2317 2328
125. S. Rana B. Kundu S. Durani Stereospecific peptide folds. A rationally designed molecular bracelet Chem. Commun. 2004 2462 2463
126. S. Rana B. Kundu S. Durani A small peptide stereochemically customized as a globular fold with a molecular cleft Chem. Commun. 2005 207 209
127. F. I. Valiyaveetil M. Sekedat R. Mackinnon T. W. Muir Glycine as a D-amino acid surrogate in the K(+)-selectivity filter Proc. Natl. Acad. Sci. U. S. A. 2004 101 17045 17049
128. K. M. Makwana R. Mahalakshmi Capping β-hairpin with N-terminal d-amino acid stabilizes peptide scaffold Biopolymers 2016 106 260 266
129. E. M. Anderson K. M. Larsson O. Kirk One biocatalyst - many applications: the use of Candida antarctica B-lipase in organic synthesis Biocatal. Biotransform. 1998 16 181 204
130. H. J. Park K. Park Y. H. Kim Y. J. Yoo Computational approach for designing thermostable Candida antarctica lipase B by molecular dynamics simulation J. Biotechnol. 2014 192 Pt A 66 70
131. I. de la Mata et al., The impact of R53C mutation on the three-dimensional structure, stability, and DNA-binding properties of the human Hesx-1 homeodomain ChemBioChem 2002 3 726 740
132. S. Kinet S. Bernichtein P. A. Kelly J. A. Martial V. Goffin Biological properties of human prolactin analogs depend not only on global hormone affinity, but also on the relative affinities of both receptor binding sites J. Biol. Chem. 1999 274 26033 26043
133. M. Zakrzewska D. Krowarsch A. Wiedlocha S. Olsnes J. Otlewski Highly stable mutants of human fibroblast growth factor-1 exhibit prolonged biological action J. Mol. Biol. 2005 352 860 875
134. K. Julenius E. Thulin S. Linse B. E. Finn Hydrophobic core substitutions in calbindin D9k: effects on stability and structure Biochemistry 1998 37 8915 8925
135. 2+ binding and dissociation Biochemistry 1998 37 8926 8937
136. A. Morin J. Meiler L. S. Mizoue Computational design of protein-ligand interfaces: potential in therapeutic development Trends Biotechnol. 2011 29 159 166
137. S. Liang et al., Exploring the molecular design of protein interaction sites with molecular dynamics simulations and free energy calculations Biochemistry 2009 48 399 414
138. B. J. C. Janssen E. F. Halff J. D. Lambris P. Gros Structure of compstatin in complex with complement component C3c reveals a new mechanism of complement inhibition J. Biol. Chem. 2007 282 29241 29247
139. D. Ricklin J. D. Lambris Compstatin: a complement inhibitor on its way to clinical application Adv. Exp. Med. Biol. 2008 632 273 292
140. A. Sahu D. Morikis J. D. Lambris Compstatin, a peptide inhibitor of complement, exhibits species-specific binding to complement component C3 Mol. Immunol. 2003 39 557 566
141. P. Tamamis et al., Design of a modified mouse protein with ligand binding properties of its human analog by molecular dynamics simulations: The case of C3 inhibition by compstatin Proteins: Struct., Funct., Bioinf. 2011 79 3166 3179
142. P. Tamamis D. Morikis C. A. Floudas G. Archontis Species specificity of the complement inhibitor compstatin investigated by all-atom molecular dynamics simulations Proteins: Struct., Funct., Bioinf. 2010 78 2655 2667
143. P. Tamamis et al., Molecular Dynamics in Drug Design: New Generations of Compstatin Analogs Chem. Biol. Drug Des. 2012 79 703 718
144. 5: implications for protein-protein recognition Biochemistry 1995 34 9682 9693
145. J. Moult Comparison of database potentials and molecular mechanics force fields Curr. Opin. Struct. Biol. 1997 7 194 199
146. 5 Biochemistry 1999 38 5054 5064
147. 1H-NMR Experiments Biochemistry 1999 38 5065 5075
148. S. Michielssens et al., A designed conformational shift to control protein binding specificity Angew. Chem., Int. Ed. 2014 53 10367 10371
149. S. C. Dodani et al., Structural, functional, and spectroscopic characterization of the substrate scope of the novel nitrating cytochrome P450 TxtE ChemBioChem 2014 15 2259 2267
150. S. C. Dodani et al., Discovery of a regioselectivity switch in nitrating P450s guided by molecular dynamics simulations and Markov models Nat. Chem. 2016 8 419 425
151. fold-like calculations Biophys. J. 2007 93 3382 3391
152. D. S. Kemp M. L. Casey Physical Organic Chemistry of Benzisoxazoles. II. Linearity of the Brönsted Free Energy Relationship for the Base-Catalyzed Decomposition of Benzisoxazoles J. Am. Chem. Soc. 1973 95 6670 6680
153. D. Röthlisberger et al., Kemp elimination catalysts by computational enzyme design Nature 2008 453 190 195
154. S. N. Thorn R. G. Daniels M. T. Auditor D. Hilvert Large rate accelerations in antibody catalysis by strategic use of haptenic charge Nature 1995 373 228 230
155. F. Hollfelder A. J. Kirby D. S. Tawfik Off-the-shelf proteins that rival tailor-made antibodies as catalysts Nature 1996 383 60 62
156. I. V. Korendovych et al., Design of a switchable eliminase Proc. Natl. Acad. Sci. U. S. A. 2011 108 6823 6827
157. A. Zanghellini et al., New algorithms and an in silico benchmark for computational enzyme design Protein Sci. 2006 15 2785 2794
158. H. K. Privett et al., Iterative approach to computational enzyme design Proc. Natl. Acad. Sci. U. S. A. 2012 109 3790 3795
159. E. W. Debler et al., Structural origins of efficient proton abstraction from carbon by a catalytic antibody Proc. Natl. Acad. Sci. U. S. A. 2005 102 4984 4989
160. L. Jiang et al., De novo computational design of retro-aldol enzymes Science 2008 319 1387 1391
161. B. List C. F. Barbas R. A. Lerner Aldol sensors for the rapid generation of tunable fluorescence by antibody catalysis Proc. Natl. Acad. Sci. U. S. A. 1998 95 15351 15355
162. J. Z. Ruscio J. E. Kohn K. A. Ball T. Head-Gordon The influence of protein dynamics on the success of computational enzyme design J. Am. Chem. Soc. 2009 131 14111 14115
163. L. Wang et al., Structural analyses of covalent enzyme-substrate analog complexes reveal strengths and limitations of de novo enzyme design J. Mol. Biol. 2012 415 615 625
164. G. Kiss V. S. Pande K. N. Houk Molecular dynamics simulations for the ranking, evaluation, and refinement of computationally designed proteins Methods Enzymol. 2013 523 145 170
165. G. Kiss D. Röthlisberger D. Baker K. N. Houk Evaluation and ranking of enzyme designs Protein Sci. 2010 19 1760 1773
166. S. Bjelic et al., Computational design of enone-binding proteins with catalytic activity for the Morita-Baylis-Hillman reaction ACS Chem. Biol. 2013 8 749 757
167. P. A. Alexander D. A. Rozak J. Orban P. N. Bryan Directed Evolution of Highly Homologous Proteins with Different Folds by Phage Display: Implications for the Protein Folding Code Biochemistry 2005 44 14045 14054
168. Y. He D. C. Yeh P. Alexander P. N. Bryan J. Orban Solution NMR structures of IgG binding domains with artificially evolved high levels of sequence identity but different folds Biochemistry 2005 44 14055 14061
169. K. A. Scott V. Daggett Folding mechanisms of proteins with high sequence identity but different folds Biochemistry 2007 46 1545 1556
170. A. Morrone M. E. McCully P. N. Bryan M. Brunori S. Gianni V. Daggett C. Travaglini-Allocatelli The denatured state dictates the topology of two proteins with almost identical sequence but different native structure and function J. Biol. Chem. 2011 286 3863 3872
171. R. Day V. Daggett Direct observation of microscopic reversibility in protein folding J. Mol. Biol. 2007 366 677 686
172. M. E. McCully D. A. C. Beck V. Daggett Microscopic reversibility of protein folding in molecular dynamics simulations of the engrailed homeodomain Biochemistry 2008 47 4079 7089
173. A. Li V. Daggett Characterization of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2 Proc. Natl. Acad. Sci. U. S. A. 1994 91 10430 10434
174. A. Li V. Daggett Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations J. Mol. Biol. 1996 257 412 429
175. A. G. Ladurner L. S. Itzhaki V. Daggett A. R. Fersht Synergy between simulation and experiment in describing the energy landscape of protein folding Proc. Natl. Acad. Sci. U. S. A. 1998 95 8473 8478
176. M. Levitt Molecular dynamics of native protein, II. Analysis and nature of motion J. Mol. Biol. 1983 168 621 657
177. S. Piana et al., Computational design and experimental testing of the fastest-folding β-sheet protein J. Mol. Biol. 2011 405 43 48
178. M. J. Cocco J. T. Lecomte Characterization of hydrophobic cores in apomyoglobin: a proton NMR spectroscopy study Biochemistry 1990 29 11067 11072
179. P. A. Jennings P. E. Wright Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin Science 1993 262 892 896
180. R. M. Ballew J. Sabelko M. Gruebele Direct observation of fast protein folding: the initial collapse of apomyoglobin Proc. Natl. Acad. Sci. U. S. A. 1996 93 5759 5764
181. R. M. Ballew J. Sabelko M. Gruebele Observation of distinct nanosecond and microsecond protein folding events Nat. Struct. Biol. 1996 3 923 926
182. J. S. Goodman S. H. Chao T. V. Pogorelov M. Gruebele Filling up the heme pocket stabilizes apomyoglobin and speeds up its folding J. Phys. Chem. B 2014 118 6511 6518
183. C. Garcia C. Nishimura S. Cavagnero H. J. Dyson P. E. Wright Changes in the apomyoglobin folding pathway caused by mutation of the distal histidine residue Biochemistry 2000 39 11227 11237
184. P. Picotti et al., Modulation of the structural integrity of helix F in apomyoglobin by single amino acid replacements Protein Sci. 2004 13 1572 1585
185. U. Mayor C. M. Johnson J. G. Grossmann S. Sato G. S. Jas S. M. V. Freund N. R. Guydosh D. O. V. Alonso V. Daggett A. R. Fersht The Complete Folding Pathway of a Protein from Nanoseconds to Microseconds Nature 2003 421 863 867
186. U. Mayor C. M. Johnson V. Daggett A. R. Fersht Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation Proc. Natl. Acad. Sci. U. S. A. 2000 97 13518 13522
187. M. L. DeMarco D. O. V. Alonso V. Daggett Diffusing and colliding: The atomic level folding/unfolding pathway of a small helical protein J. Mol. Biol. 2004 341 1109 1124
188. S. Gianni N. R. Guydosh F. Khan T. D. Caldas U. Mayor G. W. N. White M. L. DeMarco V. Daggett A. R. Fersht Unifying features in protein-folding mechanisms Proc. Natl. Acad. Sci. U. S. A. 2003 100 13286 13291
189. m Biochemistry 2008 47 7079 7089
190. T. D. Sharpe A. L. Jonsson T. J. Rutherford V. Daggett A. R. Fersht The role of the turn in β-hairpin formation during WW domain folding Protein Sci. 2007 16 2233 2239
191. T. L. Religa J. S. Markson U. Mayor S. M. V. Freund A. R. Fersht Solution structure of a protein denatured state and folding intermediate Nature 2005 437 1053 1056
192. G. W. N. White S. Gianni J. G. Grossman P. Jemth A. R. Fersht V. Daggett Simulation and Experiment Conspire to reveal Cryptic Intermediates and the Slide from the Nucleation-Condensation to Framework Mechanism of Folding J. Mol. Biol. 2005 350 757 775
193. Q. Peng et al., Mechanical design of the third FnIII domain of tenascin-C J. Mol. Biol. 2009 386 1327 1342
194. S. P. Ng et al., Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation J. Mol. Biol. 2005 350 776 789
195. Y. Cao T. Yoo H. Li Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins Proc. Natl. Acad. Sci. U. S. A. 2008 105 11152 11157
196. S. Zhuang Q. Peng Y. Cao H. Li Modulating the Mechanical Stability of Extracellular Matrix Protein Tenascin-C in a Controlled and Reversible Fashion J. Mol. Biol. 2009 390 820 829
197. K. Rutherford V. Daggett Polymorphisms and Disease: Hotspots of Inactivation in Methyltransferases Trends Biochem. Sci. 2010 35 531 538
198. F. Chiti C. M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 2006 75 333 366
199. C. Haass D. J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 2007 8 101 112
200. J. D. Sipe et al., Amyloid fibril proteins and amyloidosis: chemical identification and clinical classification International Society of Amyloidosis 2016 Nomenclature Guidelines Amyloid 2016 23 209 213
201. D. O. V. Alonso S. DeArmond F. Cohen V. Daggett Mapping the Early Steps in the Conversion of the Prion Protein Proc. Natl. Acad. Sci. U. S. A. 2001 98 2985 2989
202. D. O. V. Alons C. An V. Daggett Simulations of Biomolecules: Characterization of the Early Steps in the pH-Induced Conformational Conversion of the Hamster, Bovine, and Human Forms of the Prion Protein Philos. Trans. R. Soc., A 2002 360 1165 1178
203. R. S. Armen D. O. V. Alonso V. Daggett Anatomy of an amyloidogenic intermediate: Conversion of β-sheet to α-sheet structure in transthyretin at acidic pH Structure 2004 12 1847 1863
204. R. S. Armen M. L. DeMarco D. O. V. Alonso V. Daggett Pauling and Corey's alpha-pleated sheet structure may define the prefibrillar amyloidogenic intermediate in amyloid disease Proc. Natl. Acad. Sci. U. S. A. 2004 101 11622 11627
205. R. E. Steward R. S. Armen V. Daggett Different disease-causing mutations in transthyretin trigger the same conformational conversion Protein Eng., Des. Sel. 2008 21 187 195
206. M. Yang M. Lei B. Yordanov S. Huo Peptide plane can flip in two opposite directions: Implication in amyloid formation of transthyretin J. Phys. Chem. B. 2006 110 5829 5833
207. S. L. Kazmirski V. Daggett Non-native interactions in protein folding intermediates: molecular dynamics simulations of hen lysozyme J. Mol. Biol. 1998 284 793 806
208. R. S. Armen V. Daggett Characterization of two distinct beta2-microglobulin unfolding intermediates that may lead to amyloid fibrils of different morphology Biochemistry 2005 44 16098 16107
209. R. S. Armen B. M. Bernard R. Day D. O. V. Alonso V. Daggett Characterization of a possible amyloidogenic precursor in glutamine-repeat neurodegenerative diseases Proc. Natl. Acad. Sci. U. S. A. 2005 102 13433 13438
210. V. Babin C. Roland C. Sagui The α-sheet: A missing-in-action secondary structure? Proteins 2011 79 937 946
211. L. Pauling R. B. Corey The pleated sheet, a new layer configuration of polypeptide chains Proc. Natl. Acad. Sci. U. S. A. 1951 37 251 256
212. V. Daggett α-sheet: The toxic conformer in amyloid diseases? Acc. Chem. Res. 2006 39 594 602
213. D. A. C. Beck D. O. V. Alonso D. Inoyama V. Daggett The intrinsic conformational propensities of the twenty naturally occurring amino acids and reflection of these propensities in proteins Proc. Natl. Acad. Sci. U. S. A. 2008 105 12259 12264
214. C.-L. Towse J. Vymetal J. Vondrasek V. Daggett Insights into unfolded proteins from the intrinsic φ/ψ propensities of the AAXAA host-guest series Biophys. J. 2016 110 348 361
215. C.-L. Towse G. Hopping I. Vulovic V. Daggett Nature versus design: The conformational propensities of D-amino acids and the importance of side chain chirality Protein Eng., Des. Sel. 2014 27 447 455
216. M. C. Childers C.-L. Towse V. Daggett The effect of chirality and steric hindrance on intrinsic backbone conformational propensities: Tools for protein design Protein Eng., Des. Sel. 2016 29 271 280
217. C.-L. Towse S. J. Rysavy I. M. Vulovic V. Daggett New Dynamic Rotamer Libraries: Data-Driven Analysis of Side Chain Conformational Propensities Structure 2016 24 187 199
218. M. C. Childers, C. L. Towse and V. Daggett, Molecular dynamics-derived rotamer libraries for D-amino acids, 2016
219. D. A. C. Beck A. L. Jonsson D. Schaeffer K. A. Scott R. Day R. D. Toofanny D. O. V. Alonso V. Daggett Dynameomics: Mass annotation of protein dynamics and unfolding in water by high-throughput atomistic molecular dynamics simulations Protein Eng., Des. Sel. 2008 21 353 368
220. M. W. Van der Kamp P. C. Anderson D. A. C. Beck N. C. Benson A. L. Jonsson E. D. Merkley R. D. Schaeffer A. D. Scouras A. Simms R. D. Toofanny V. Daggett Dynameomics: A comprehensive database of protein dynamics Structure 2010 18 423 435
221. C. Camilloni et al., Rational design of mutations that change the aggregation rate of a protein while maintaining its native structure and stability Sci. Rep. 2016 6 25559
222. F. Fogolari et al., Molecular dynamics simulation suggests possible interaction patterns at early steps of beta2-microglobulin aggregation Biophys. J. 2007 92 1673 1681
223. G. Esposito et al., The Controlling Roles of Trp60 and Trp95 in β2-Microglobulin Function, Folding and Amyloid Aggregation Properties J. Mol. Biol. 2008 378 885 895