What makes a protein fold amenable to functional innovation? fold polarity and stability trade-offs

Journal of Molecular Biology

Volumn 425, Issue 14, 2013, Pages 2609-2621

  Dellus Gur, Eynat ^a   Toth Petroczy, Agnes ^a   Elias, Mikael ^a   Tawfik, Dan S ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

enzyme evolution; protein disorder; protein evolution; protein folds

Indexed keywords

BETA LACTAMASE TEM 1; DIHYDROFOLATE REDUCTASE; MOLECULAR SCAFFOLD; PROTEIN VARIANT;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME KINETICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; STRUCTURE ANALYSIS;

EID: 84879549646     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.03.033     Document Type: Article

References (58)

1. E. Bornberg-Bauer, and H.S. Chan Modeling evolutionary landscapes: mutational stability, topology, and superfunnels in sequence space Proc. Natl Acad. Sci. USA 96 1999 10689 10694
2. M.A. DePristo, D.M. Weinreich, and D.L. Hartl Missense meanderings in sequence space: a biophysical view of protein evolution Nat. Rev. Genet. 6 2005 678 687
3. B.E. Shakhnovich, E. Deeds, C. Delisi, and E. Shakhnovich Protein structure and evolutionary history determine sequence space topology Genome Res. 15 2005 385 392
4. S. Bershtein, M. Segal, R. Bekerman, N. Tokuriki, and D.S. Tawfik Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein Nature 444 2006 929 932
5. J.D. Bloom, S.T. Labthavikul, C.R. Otey, and F.H. Arnold Protein stability promotes evolvability Proc. Natl Acad. Sci. USA 103 2006 5869 5874
6. 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. USA 102 2005 606 611
7. A. Wagner Robustness and Evolvability in Living Systems 2005 Princeton University Press Princeton, NJ
8. A. Wagner The Origins of Evolutionary Innovations 2011 Oxford University Press, Oxford
9. M.M. Rorick, and G.P. Wagner Protein structural modularity and robustness are associated with evolvability Genome Biol. Evol. 3 2011 456 475
10. 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
11. D.C. Marciano, J.M. Pennington, X. Wang, J. Wang, Y. Chen, and V.L. Thomas Genetic and structural characterization of an L201P global suppressor substitution in TEM-1 beta-lactamase J. Mol. Biol. 384 2008 151 164
12. N. Tokuriki, F. Stricher, L. Serrano, and D.S. Tawfik How protein stability and new functions trade off PLoS Comput Biol 4 2008 e1000002
13. M. Vihinen Relationship of protein flexibility to thermostability Protein Eng. 1 1987 477 480
14. M.T. Reetz, J.D. Carballeira, and A. Vogel Iterative saturation mutagenesis on the basis of B factors as a strategy for increasing protein thermostability Angew. Chem. Int. Ed. Engl. 45 2006 7745 7751
15. N. Tokuriki, and D.S. Tawfik Protein dynamism and evolvability Science 324 2009 203 207
16. R. Wroe, H.S. Chan, and E. Bornberg-Bauer A structural model of latent evolutionary potentials underlying neutral networks in proteins HFSP J. 1 2007 79 87
17. Y. Chen, J. Delmas, J. Sirot, B. Shoichet, and R. Bonnet Atomic resolution structures of CTX-M beta-lactamases: extended spectrum activities from increased mobility and decreased stability J. Mol. Biol. 348 2005 349 362
18. P.E. Tomatis, S.M. Fabiane, F. Simona, P. Carloni, B.J. Sutton, and A.J. Vila Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility Proc. Natl Acad. Sci. USA 105 2008 20605 20610
19. L. Maveyraud, I. Saves, O. Burlet-Schiltz, P. Swaren, J.M. Masson, and M. Delaire Structural basis of extended spectrum TEM beta-lactamases. Crystallographic, kinetic, and mass spectrometric investigations of enzyme mutants J. Biol. Chem. 271 1996 10482 10489
20. M.C. Orencia, J.S. Yoon, J.E. Ness, W.P. Stemmer, and R.C. Stevens Predicting the emergence of antibiotic resistance by directed evolution and structural analysis Nat. Struct. Biol. 8 2001 238 242
21. P.Y. De Wals, N. Doucet, and J.N. Pelletier High tolerance to simultaneous active-site mutations in TEM-1 beta-lactamase: distinct mutational paths provide more generalized beta-lactam recognition Protein Sci. 18 2009 147 160
22. 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
23. M.T. Reetz, and J.D. Carballeira Iterative saturation mutagenesis (ISM) for rapid directed evolution of functional enzymes Nat. Protoc. 2 2007 891 903
24. F.H. Arnold, P.L. Wintrode, K. Miyazaki, and A. Gershenson How enzymes adapt: lessons from directed evolution Trends Biochem. Sci. 26 2001 100 106
25. S.M. Carroll, E.A. Ortlund, and J.W. Thornton Mechanisms for the evolution of a derived function in the ancestral glucocorticoid receptor PLoS Genet. 7 2011 e1002117
26. S. Bershtein, K. Goldin, and D.S. Tawfik Intense neutral drifts yield robust and evolvable consensus proteins J. Mol. Biol. 379 2008 1029 1044
27. B. Steipe, B. Schiller, A. Pluckthun, and S. Steinbacher Sequence statistics reliably predict stabilizing mutations in a protein domain J. Mol. Biol. 240 1994 188 192
28. K. Watanabe, T. Ohkuri, S. Yokobori, and A. Yamagishi Designing thermostable proteins: ancestral mutants of 3-isopropylmalate dehydrogenase designed by using a phylogenetic tree J. Mol. Biol. 355 2006 664 674
29. J. Hecky, and K.M. Muller Structural perturbation and compensation by directed evolution at physiological temperature leads to thermostabilization of beta-lactamase Biochemistry 44 2005 12640 12654
30. Bershtein, S. (2007). Understanding the underlining mechanism of random genetic drift by experimental evolution. Ph.D. thesis, Weizmann Institute of Science.
31. I. Kather, R.P. Jakob, H. Dobbek, and F.X. Schmid Increased folding stability of TEM-1 beta-lactamase by in vitro selection J. Mol. Biol. 383 2008 238 251
32. M.L. Salverda, J.A. de Visser, and M. Barlow Natural evolution of TEM-1 beta-lactamase: experimental reconstruction and clinical relevance FEMS Microbiol. Rev. 34 2010 1015 1036
33. C. Cantu 3rd, and T. Palzkill The role of residue 238 of TEM-1 beta-lactamase in the hydrolysis of extended-spectrum antibiotics J. Biol. Chem. 273 1998 26603 26609
34. A. Petit, L. Maveyraud, F. Lenfant, J.P. Samama, R. Labia, and J.M. Masson Multiple substitutions at position 104 of beta-lactamase TEM-1: assessing the role of this residue in substrate specificity Biochem. J. 305 1995 33 40
35. S. Parthasarathy, and M.R. Murthy Analysis of temperature factor distribution in high-resolution protein structures Protein Sci. 6 1997 2561 2567
36. Z. Yuan, T.L. Bailey, and R.D. Teasdale Prediction of protein B-factor profiles Proteins 58 2005 905 912
37. J.A. Ranea, A. Sillero, J.M. Thornton, and C.A. Orengo Protein superfamily evolution and the last universal common ancestor (LUCA) J. Mol. Evol. 63 2006 513 525
38. A.M. Burroughs, K.N. Allen, D. Dunaway-Mariano, and L. Aravind Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes J. Mol. Biol. 361 2006 1003 1034
39. O. Khersonsky, and D.S. Tawfik Enzyme promiscuity: a mechanistic and evolutionary perspective Annu. Rev. Biochem. 79 2010 471 505
40. G. Amitai, R.D. Gupta, and D.S. Tawfik Latent evolutionary potentials under the neutral mutational drift of an enzyme HFSP J. 1 2007 67 78
41. M. Kirschner, and J. Gerhart Evolvability Proc. Natl Acad. Sci. USA 95 1998 8420 8427
42. E. Ferrada, and A. Wagner Protein robustness promotes evolutionary innovations on large evolutionary time-scales Proc. Biol. Sci. 275 2008 1595 1602
43. J.D. Bloom, D.A. Drummond, F.H. Arnold, and C.O. Wilke Structural determinants of the rate of protein evolution in yeast Mol. Biol. Evol. 23 2006 1751 1761
44. J.L. England, and E.I. Shakhnovich Structural determinant of protein designability Phys. Rev. Lett. 90 2003 218101
45. C. Zhang, and C. DeLisi Protein folds: molecular systematics in three dimensions Cell. Mol. Life Sci. 58 2001 72 79
46. S.H. Jeong, I.K. Bae, J.H. Lee, S.G. Sohn, G.H. Kang, and G.J. Jeon Molecular characterization of extended-spectrum beta-lactamases produced by clinical isolates of Klebsiella pneumoniae and Escherichia coli from a Korean nationwide survey J. Clin. Microbiol. 42 2004 2902 2906
47. A. Herman, and D.S. Tawfik Incorporating Synthetic Oligonucleotides via Gene Reassembly (ISOR): a versatile tool for generating targeted libraries Protein Eng. Des. Sel. 20 2007 219 226
48. J.F. Petrosino, M. Baker, and T. Palzkill Susceptibility of beta-lactamase to core amino acid substitutions Protein Eng. 12 1999 761 769
49. M.L. Salverda, E. Dellus, F.A. Gorter, A.J. Debets, J. van der Oost, and R.F. Hoekstra Initial mutations direct alternative pathways of protein evolution PLoS Genet. 7 2011 e1001321
50. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 26 1993 795 800
51. The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
52. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
53. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132
54. A.L. Cuff, I. Sillitoe, T. Lewis, A.B. Clegg, R. Rentzsch, and N. Furnham Extending CATH: increasing coverage of the protein structure universe and linking structure with function Nucleic Acids Res. 39 2011 D420 D426
55. A.S. Konagurthu, J.C. Whisstock, P.J. Stuckey, and A.M. Lesk MUSTANG: a multiple structural alignment algorithm Proteins 64 2006 559 574
56. V. Sobolev, A. Sorokine, J. Prilusky, E.E. Abola, and M. Edelman Automated analysis of interatomic contacts in proteins Bioinformatics 15 1999 327 332
57. A. Toth-Petroczy, and D.S. Tawfik Slow protein evolutionary rates are dictated by surface-core association Proc. Natl Acad. Sci. USA 108 2011 11151 11156
58. I. Mayrose, D. Graur, N. Ben-Tal, and T. Pupko Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior Mol. Biol. Evol. 21 2004 1781 1791