A "fuzzy"-logic language for encoding multiple physical traits in biomolecules

Journal of Molecular Biology

Volumn 426, Issue 24, 2014, Pages 4125-4138

  Warszawski, Shira ^a   Netzer, Ravit ^a   Tawfik, Dan S ^a   Fleishman, Sarel J ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

diminishing returns; multistate design; Rosetta; sequence optimization; stability activity tradeoff

Indexed keywords

PROTEIN;

ALGORITHM; BIOLOGY; BIOPHYSICS; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; FUZZY LOGIC; GENETICS; MUTATION; PROCEDURES; PROTEIN ENGINEERING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ALGORITHMS; BIOPHYSICAL PHENOMENA; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; FUZZY LOGIC; MODELS, MOLECULAR; MUTATION; PROTEIN ENGINEERING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 84914127473     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.10.002     Document Type: Article

References (87)

1. M.J. Rooman, and S.J. Wodak Extracting information on folding from the amino acid sequence: consensus regions with preferred conformation in homologous proteins Biochemistry 31 1992 10239 10249
2. P.G. Wolynes Energy landscapes and solved protein-folding problems Philos Trans R Soc A Math Phys Eng Sci 363 2005 453 464
3. W. Li, P.G. Wolynes, and S. Takada Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins Proc Natl Acad Sci U S A 108 2011 3504 3509
4. A. Sali, E. Shakhnovich, and M. Karplus How does a protein fold? Nature 369 1994 248 251
5. J. Kraur How do enzymes work? Science 242 1988 533 539
6. L. Foit, G.J. Morgan, M.J. Kern, L.R. Steimer, A. a von Hacht, and J. Titchmarsh Optimizing protein stability in vivo Mol Cell 36 2009 861 871
7. B.M. Beadle, and B.K. Shoichet Structural bases of stability-function tradeoffs in enzymes J Mol Biol 321 2002 285 296
8. J.D. Bloom, J.J. Silberg, C.O. Wilke, D.A. Drummond, C. Adami, and F.H. Arnold Thermodynamic prediction of protein neutrality Proc Natl Acad Sci U S A 102 2005 606 611
9. E.M. Meiering, L. Serrano, and a R. Fersht Effect of active site residues in barnase on activity and stability J Mol Biol 225 1992 585 589
10. N. Tokuriki, and D.S. Tawfik Stability effects of mutations and protein evolvability Curr Opin Struct Biol 19 2009 596 604
11. N. Tokuriki, F. Stricher, L. Serrano, and D.S. Tawfik How protein stability and new functions trade off PLoS Comput Biol 4 2008 e1000002
12. O. Khersonsky, and D.S. Tawfik Enzyme promiscuity: a mechanistic and evolutionary perspective Annu Rev Biochem 79 2010 471 505
13. X. Wang, G. Minasov, and B.K. Shoichet Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs J Mol Biol 320 2002 85 95
14. A. Zarrinpar, S.-H. Park, and W. a Lim Optimization of specificity in a cellular protein interaction network by negative selection Nature 426 2003 676 680
15. D.S. Tawfik Accuracy-rate tradeoffs: how do enzymes meet demands of selectivity and catalytic efficiency? Curr Opin Chem Biol 21 2014 73 80
16. M. Mohammadi, S.K. Olsen, and O.a Ibrahimi Structural basis for fibroblast growth factor receptor activation Cytokine Growth Factor Rev 16 2005 107 137
17. S.J. Fleishman, and D. Baker Role of the biomolecular energy gap in protein design, structure, and evolution Cell 149 2012 262 273
18. J.U. Bowie, R. Ltcy, and D. Eisenberg A method to identify protein sequences that fold into a known three-dimensional structure Science 253 1990 164 170
19. A. Korkegian, M.E. Black, D. Baker, and B.L. Stoddard Computational thermostabilization of an enzyme Science 308 2005 857 860
20. A.E. Miklos, C. Kluwe, B.S. Der, S. Pai, A. Sircar, and R. a Hughes Structure-based design of supercharged, highly thermoresistant antibodies Chem Biol 19 2012 449 455
21. B. Kuhlman, G. Dantas, G.C. Ireton, G. Varani, B.L. Stoddard, and D. Baker Design of a novel globular protein fold with atomic-level accuracy Science 302 2003 1364 1368
22. N. Koga, R. Tatsumi-Koga, G. Liu, R. Xiao, T.B. Acton, and G.T. Montelione Principles for designing ideal protein structures Nature 491 2012 222 227
23. D. Röthlisberger, O. Khersonsky, A.M. Wollacott, L. Jiang, J. DeChancie, and J. Betker Kemp elimination catalysts by computational enzyme design Nature 453 2008 190 195
24. L. Jiang, E. a Althoff, F.R. Clemente, L. Doyle, D. Röthlisberger, and A. Zanghellini De novo computational design of retro-aldol enzymes Science 319 2008 1387 1391
25. N.P. King, W. Sheffler, M.R. Sawaya, B.S. Vollmar, J.P. Sumida, and I. André Computational design of self-assembling protein nanomaterials with atomic level accuracy Science 336 2012 1171 1174
26. R.K. Jha, A. Leaver-Fay, S. Yin, Y. Wu, G.L. Butterfoss, and T. Szyperski Computational design of a PAK1 binding protein J Mol Biol 400 2010 257 270
27. J. Karanicolas, J.E. Corn, I. Chen, L.a Joachimiak, O. Dym, and S.H. Peck A de novo protein binding pair by computational design and directed evolution Mol Cell 42 2011 250 260
28. B.S. Der, D.R. Edwards, and B. Kuhlman Catalysis by a de novo zinc-mediated protein interface: implications for natural enzyme evolution and rational enzyme engineering Biochemistry 51 2012 3933 3940
29. N. Tokuriki, C.J. Jackson, L. Afriat-Jurnou, K.T. Wyganowski, R. Tang, and D.S. Tawfik Diminishing returns and tradeoffs constrain the laboratory optimization of an enzyme Nat Commun 3 2012 1257
30. J.J. Havranek, and P.B. Harbury Automated design of specificity in molecular recognition Nat Struct Biol 10 2003 45 52
31. G. Grigoryan, A.W. Reinke, and A.E. Keating Design of protein-interaction specificity gives selective bZIP-binding peptides Nature 458 2009 859 864
32. J. Ashworth, G.K. Taylor, J.J. Havranek, S.A. Quadri, B.L. Stoddard, and D. Baker Computational reprogramming of homing endonuclease specificity at multiple adjacent base pairs Nucleic Acids Res 38 2010 5601 5608
33. E.L. Humphris, and T. Kortemme Design of multi-specificity in protein interfaces PLoS Comput Biol 3 2007 1591 1604
34. E. Procko, R. Hedman, K. Hamilton, J. Seetharaman, S. Fleishman, and M. Su Computational design of a protein-based enzyme inhibitor J Mol Biol 425 2013 3563 3575
35. S.J. Fleishman, T.A. Whitehead, D.C. Ekiert, C. Dreyfus, J.E. Corn, and E.-M. Strauch Computational design of proteins targeting the conserved stem region of influenza hemagglutinin Science 332 2011 816 821
36. E.-M. Strauch, S.J. Fleishman, and D. Baker Computational design of a pH-sensitive IgG binding protein Proc Natl Acad Sci U S A 111 2014 675 680
37. C.E. Tinberg, S.D. Khare, J. Dou, L. Doyle, J.W. Nelson, and A. Schena Computational design of ligand-binding proteins with high affinity and selectivity Nature 501 2013 212 216
38. S.J. Fleishman, S.D. Khare, N. Koga, and D. Baker Restricted sidechain plasticity in the structures of native proteins and complexes Protein Sci 20 2011 753 757
39. J. Kuriyan, B. Konforti, and D. Wemmer The molecules of life 2012 Garland Science New York
40. K. a Krohn, and J.M. Link Interpreting enzyme and receptor kinetics: keeping it simple, but not too simple Nucl Med Biol 30 2003 819 826
41. A. Hirschi, M. Cecchini, R.C. Steinhardt, M.R. Schamber, F.A. Dick, and S.M. Rubin An overlapping kinase and phosphatase docking site regulates activity of the retinoblastoma protein Nat Struct Mol Biol 17 2010 1051 1057
42. E. Dekel, and U. Alon Optimality and evolutionary tuning of the expression level of a protein Nature 436 2005 588 592
43. P. Beltrao, P. Bork, N.J. Krogan, and V. van Noort Evolution and functional cross-talk of protein post-translational modifications Mol Syst Biol 9 2013 714
44. Y. Diekmann, and J.B. Pereira-Leal Evolution of intracellular compartmentalization Biochem J 449 2013 319 331
45. A. Ciechanover Proteolysis: from the lysosome to ubiquitin and the proteasome Nat Rev Mol Cell Biol 6 2005 79 87
46. W. Li, A.H. Keeble, C. Giffard, R. James, G.R. Moore, and C. Kleanthous Highly discriminating protein-protein interaction specificities in the context of a conserved binding energy hotspot J Mol Biol 337 2004 743 759
47. A.R. Fersht Structure and mechanism in protein science 1999 Freeman New York
48. S. Bershtein, W. Mu, A.W.R. Serohijos, J. Zhou, and E.I. Shakhnovich Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness Mol Cell 49 2013 133 144
49. A.W. Serohijos, and E.I. Shakhnovich Merging molecular mechanism and evolution: theory and computation at the interface of biophysics and evolutionary population genetics Curr Opin Struct Biol 26 2014 84 91
50. D.J. Scott, L. Kummer, D. Tremmel, and A. Plückthun Stabilizing membrane proteins through protein engineering Curr Opin Chem Biol 17 2013 427 435
51. A. Wörn, and A. Plückthun Stability engineering of antibody single-chain Fv fragments J Mol Biol 305 2001 989 1010
52. L.A. Zadeh Fuzzy sets Inf Control 8 1965 338 353
53. A.E. Hassanien, E.T. Al-Shammari, and N.I. Ghali Computational intelligence techniques in bioinformatics Comput Biol Chem 47 2013 37 47
54. A. Leaver-Fay, R. Jacak, P.B. Stranges, and B. Kuhlman A generic program for multistate protein design PLoS One 6 2011 e20937
55. B.D. Allen, and S.L. Mayo An efficient algorithm for multistate protein design based on FASTER J Comput Chem 31 2009 904 916
56. L.A. Joachimiak, T. Kortemme, B.L. Stoddard, and D. Baker Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein-protein interface J Mol Biol 361 2006 195 208
57. D.W. Sammond, Z.M. Eletr, C. Purbeck, and B. Kuhlman Computational design of second-site suppressor mutations at protein-protein interfaces Proteins 78 2010 1055 1065
58. T. Kortemme, L.A. Joachimiak, A.N. Bullock, A.D. Schuler, B.L. Stoddard, and D. Baker Computational redesign of protein-protein interaction specificity Nat Struct Mol Biol 11 2004 371 379
59. C. Yanover, M. Fromer, and J.M. Shifman Dead-end elimination for multistate protein design J Comput Chem 28 2007 2122 2129
60. J.J. Havranek Specificity in computational protein design J Biol Chem 285 2010 31095 31099
61. M.E. Pacold, S. Suire, O. Perisic, S. Lara-Gonzalez, C.T. Davis, and E.H. Walker Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma Cell 103 2000 931 943
62. K. Scheffzek The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338
63. P.A. Boriack-sjodin, S.M. Margarit, D. Bar-sagi, and J. Kuriyan The structural basis of the activation of Ras by Sos Nature 394 1998 337 343
64. K. Scheffzek, P. Grünewald, S. Wohlgemuth, W. Kabsch, H. Tu, and M. Wigler The Ras-Byr2RBD complex: structural basis for Ras effector recognition in yeast Structure 9 2001 1043 1050
65. C.M. Rosseland, L. Wierød, L.I. Flinder, M.P. Oksvold, E. Skarpen, and H.S. Huitfeldt Distinct functions of H-Ras and K-Ras in proliferation and survival of primary hepatocytes due to selective activation of ERK and PI3K J Cell Physiol 215 2008 818 826
66. L. Xue The Ras/phosphatidylinositol 3-kinase and Ras/ERK pathways function as independent survival modules each of which inhibits a distinct apoptotic signaling pathway in sympathetic neurons J Biol Chem 275 2000 8817 8824
67. J.M. Shifman, and S.L. Mayo Modulating calmodulin binding specificity through computational protein design J Mol Biol 323 2002 417 423
68. G.E. Crooks, G. Hon, J. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res 14 2004 1188 1190
69. G. Papadakos, J.a Wojdyla, and C. Kleanthous Nuclease colicins and their immunity proteins Q Rev Biophys 45 2012 57 103
70. J.A. Wojdyla, S.J. Fleishman, D. Baker, and C. Kleanthous Structure of the ultra-high-affinity colicin E2 DNase-Im2 complex J Mol Biol 417 2012 79 94
71. A.H.A. Keeble, L.L. a Joachimiak, M.M.J. Maté, N. Meenan, N. Kirkpatrick, and D. Baker Experimental and computational analyses of the energetic basis for dual recognition of immunity proteins by colicin endonucleases J Mol Biol 379 2008 745 759
72. A.H. Keeble, N. Kirkpatrick, S. Shimizu, and C. Kleanthous Calorimetric dissection of colicin DNase-immunity protein complex specificity Biochemistry 45 2006 3243 3254
73. U.C. Kühlmann, a J. Pommer, G.R. Moore, R. James, and C. Kleanthous Specificity in protein-protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes J Mol Biol 301 2000 1163 1178
74. N. a G. Meenan, A. Sharma, S.J. Fleishman, C.J. Macdonald, B. Morel, and R. Boetzel The structural and energetic basis for high selectivity in a high-affinity protein-protein interaction Proc Natl Acad Sci USA 107 2010 10080 10085
75. N. Ollikainen, C. a Smith, J.S. Fraser, and T. Kortemme Flexible backbone sampling methods to model and design protein alternative conformations 1st edit 523 2013 Elsevier Inc
76. S. Knowling, A.I. Bartlett, and S.E. Radford Dissecting key residues in folding and stability of the bacterial immunity protein 7 Protein Eng Des Sel 24 2011 517 523
77. S.J. Gould, and R.C. Lewontin The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme Proc R Soc B Biol Sci 205 1979 581 598
78. J.E. Dueber, B.J. Yeh, R.P. Bhattacharyya, and W.a Lim Rewiring cell signaling: the logic and plasticity of eukaryotic protein circuitry Curr Opin Struct Biol 14 2004 690 699
79. S.-Y. Rhee, M.J. Gonzales, R. Kantor, B.J. Betts, J. Ravela, and R.W. Shafer Human immunodeficiency virus reverse transcriptase and protease sequence database Nucleic Acids Res 31 2003 298 303
80. R. Fisher, G.U. van Zyl, S. a a Travers, S.L. Kosakovsky Pond, S. Engelbrech, and B. Murrell Deep sequencing reveals minor protease resistance mutations in patients failing a protease inhibitor regimen J Virol 86 2012 6231 6237
81. T. a Whitehead, A. Chevalier, Y. Song, C. Dreyfus, S.J. Fleishman, and C. De Mattos Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing Nat Biotechnol 30 2012 543 548
82. D.M. Fowler, C.L. Araya, S.J. Fleishman, E.H. Kellogg, J.J. Stephany, and D. Baker High-resolution mapping of protein sequence-function relationships Nat Methods 7 2010 741 746
83. G. Pál, J.-L.K. Kouadio, D.R. Artis, A. a Kossiakoff, and S.S. Sidhu Comprehensive and quantitative mapping of energy landscapes for protein-protein interactions by rapid combinatorial scanning J Biol Chem 281 2006 22378 22385
84. D.M. Fowler, and S. Fields Deep mutational scanning: a new style of protein science Nat Methods 11 2014 801 807
85. O. Shoval, H. Sheftel, G. Shinar, Y. Hart, O. Ramote, and a Mayo Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space Science 336 2012 1157 1160
86. R. Das, and D. Baker Macromolecular modeling with rosetta Annu Rev Biochem 77 2008 363 382
87. S.J. Fleishman, A. Leaver-Fay, J.E. Corn, E.-M. Strauch, S.D. Khare, and N. Koga RosettaScripts: a scripting language interface to the Rosetta macromolecular modeling suite PLoS One 6 2011 e20161