Intense Neutral Drifts Yield Robust and Evolvable Consensus Proteins

Journal of Molecular Biology

Volumn 379, Issue 5, 2008, Pages 1029-1044

  Bershtein, Shimon ^a   Goldin, Korina ^a   Tawfik, Dan S ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

consensus ancestor sequence; mutational robustness; neutral drift; protein evolution; protein evolvability

Indexed keywords

BETA LACTAMASE TEM 1; CEFOTAXIME;

ARTICLE; ENZYME ACTIVITY; GENE LIBRARY; GENETIC VARIABILITY; MUTATION; PRIORITY JOURNAL; PROTEIN FAMILY;

EID: 44349161622     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.04.024     Document Type: Article

References (57)

1. Camps M., Herman A., Loh E., and Loeb L.A. Genetic constraints on protein evolution. Crit. Rev. Biochem. Mol. Biol. 42 (2007) 313-326
2. Tokuriki N., Stricher F., Schymkowitz J., Serrano L., and Tawfik D.S. The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369 (2007) 1318-1332
3. Yue P., Li Z., and Moult J. Loss of protein structure stability as a major causative factor in monogenic disease. J. Mol. Biol. 353 (2005) 459-473
4. Tokuriki, N., Stritcher, F., Serrano, L. & Tawfik, D. S. How protein stability and new functions tradeoff. PLoS Comput. Biol. In press. doi:10.1371/journal.pcbi.1000002.
5. Wang X., Minasov G., and Shoichet B.K. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol. 320 (2002) 85-95
6. DePristo M.A., Weinreich D.M., and Hartl D.L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat. Rev. Genet. 6 (2005) 678-687
7. Drake J.W., Charlesworth B., Charlesworth D., and Crow J.F. Rates of spontaneous mutation. Genetics 148 (1998) 1667-1686
8. van Nimwegen E. Epidemiology. Influenza escapes immunity along neutral networks. Science 314 (2006) 1884-1886
9. Vignuzzi M., Stone J.K., Arnold J.J., Cameron C.E., and Andino R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439 (2006) 344-348
10. Bornberg-Bauer E., and Chan H.S. Modeling evolutionary landscapes: mutational stability, topology, and superfunnels in sequence space. Proc. Natl. Acad. Sci. USA 96 (1999) 10689-10694
11. Wagner A. Robustness and Evolvability in Living Systems (2005), Princeton University Press, Princeton, NJ
12. Wilke C.O., Wang J.L., Ofria C., Lenski R.E., and Adami C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412 (2001) 331-333
13. Amitai G., Devi-Gupta R., and Tawfik D.S. Latent evolutionary potentials under the neutral mutational drift of an enzyme. HFSP J. 1 (2007) 79-87
14. Bershtein S., Segal M., Bekerman R., Tokuriki N., and Tawfik D.S. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444 (2006) 929-932
15. Bloom J.D., Romero P.A., Lu Z., and Arnold F.H. Neutral genetic drift can alter promiscuous protein functions, potentially aiding functional evolution. Biol. Direct 2 (2007) 17
16. Bloom J.D., Lu Z., Chen D., Raval A., Venturelli O.S., and Arnold F.H. Evolution favors protein mutational robustness in sufficiently large populations. BMC Biol. 5 (2007) 29
17. Bloom J.D., Silberg J.J., Wilke C.O., Drummond D.A., Adami C., and Arnold F.H. Thermodynamic prediction of protein neutrality. Proc. Natl. Acad. Sci. USA 102 (2005) 606-611
18. Forster R., Adami C., and Wilke C.O. Selection for mutational robustness in finite populations. J. Theor. Biol. 243 (2006) 181-190
19. van Nimwegen E., Crutchfield J.P., and Huynen M. Neutral evolution of mutational robustness. Proc. Natl. Acad. Sci. USA 96 (1999) 9716-9720
20. Hall B.G., and Barlow M. Evolution of the serine beta-lactamases: past, present and future. Drug Resist. Update 7 (2004) 111-123
21. Kimura M. The Neutral Theory of Molecular Evolution (1983), Cambridge University Press, Cambridge
22. Godoy-Ruiz R., Ariza F., Rodriguez-Larrea D., Perez-Jimenez R., Ibarra-Molero B., and Sanchez-Ruiz J.M. Natural selection for kinetic stability is a likely origin of correlations between mutational effects on protein energetics and frequencies of amino acid occurrences in sequence alignments. J. Mol. Biol. 362 (2006) 966-978
23. Steipe B., Schiller B., Pluckthun A., and Steinbacher S. Sequence statistics reliably predict stabilizing mutations in a protein domain. J. Mol. Biol. 240 (1994) 188-192
24. Lehmann M., and Wyss M. Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr. Opin. Biotechnol. 12 (2001) 371-375
25. Lehmann M., Kostrewa D., Wyss M., Brugger R., D'Arcy A., Pasamontes L., and van Loon A.P. From DNA sequence to improved functionality: using protein sequence comparisons to rapidly design a thermostable consensus phytase. Protein Eng. 13 (2000) 49-57
26. Forrer P., Binz H.K., Stumpp M.T., and Pluckthun A. Consensus design of repeat proteins. ChemBioChem 5 (2004) 183-189
27. Nikolova P.V., Henckel J., Lane D.P., and Fersht A.R. Semirational design of active tumor suppressor p53 DNA binding domain with enhanced stability. Proc. Natl. Acad. Sci. USA 95 (1998) 14675-14680
28. Wang Q., Buckle A.M., Foster N.W., Johnson C.M., and Fersht A.R. Design of highly stable functional GroEL minichaperones. Protein Sci. 8 (1999) 2186-2193
29. Gaucher E.A., Govindarajan S., and Ganesh O.K. Palaeotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451 (2008) 704-707
30. Miyazaki J., Nakaya S., Suzuki T., Tamakoshi M., Oshima T., and Yamagishi A. Ancestral residues stabilizing 3-isopropylmalate dehydrogenase of an extreme thermophile: experimental evidence supporting the thermophilic common ancestor hypothesis. J. Biochem. (Tokyo) 129 (2001) 777-782
31. Watanabe K., Ohkuri T., Yokobori S., and Yamagishi A. Designing thermostable proteins: ancestral mutants of 3-isopropylmalate dehydrogenase designed by using a phylogenetic tree. J. Mol. Biol. 355 (2006) 664-674
32. Polizzi K.M., Chaparro-Riggers J.F., Vazquez-Figueroa E., and Bommarius A.S. Structure-guided consensus approach to create a more thermostable penicillin G acylase. Biotechnol. J. 1 (2006) 531-536
33. Sideraki V., Huang W., Palzkill T., and Gilbert H.F. A secondary drug resistance mutation of TEM-1 beta-lactamase that suppresses misfolding and aggregation. Proc. Natl. Acad. Sci. USA 98 (2001) 283-288
34. Hecky J., and Muller K.M. Structural perturbation and compensation by directed evolution at physiological temperature leads to thermostabilization of beta-lactamase. Biochemistry 44 (2005) 12640-12654
35. Guerois R., Nielsen J.E., and Serrano L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320 (2002) 369-387
36. Baker D., and Agard D.A. Kinetics versus thermodynamics in protein folding. Biochemistry 33 (1994) 7505-7509
37. Watters A.L., Deka P., Corrent C., Callender D., Varani G., Sosnick T., and Baker D. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell 128 (2007) 613-624
38. Georgiou G., Valax P., Ostermeier M., and Horowitz P.M. Folding and aggregation of TEM beta-lactamase: analogies with the formation of inclusion bodies in Escherichia coli. Protein Sci. 3 (1994) 1953-1960
39. Vanhove M., Raquet X., and Frere J.M. Investigation of the folding pathway of the TEM-1 beta-lactamase. Proteins 22 (1995) 110-118
40. Vanhove M., Guillaume G., Ledent P., Richards J.H., Pain R.H., and Frere J.M. Kinetic and thermodynamic consequences of the removal of the Cys-77-Cys-123 disulphide bond for the folding of TEM-1 beta-lactamase. Biochem. J. 321 Pt. 2 (1997) 413-417
41. Bloom J.D., Labthavikul S.T., Otey C.R., and Arnold F.H. Protein stability promotes evolvability. Proc. Natl. Acad. Sci. USA 103 (2006) 5869-5874
42. Schuster P., Fontana W., Stadler P.F., and Hofacker I.L. From sequences to shapes and back: a case study in RNA secondary structures. Proc. Biol. Sci. 255 (1994) 279-284
43. Govindarajan S., and Goldstein R.A. Evolution of model proteins on a foldability landscape. Proteins 29 (1997) 461-466
44. Maxwell K.L., and Davidson A.R. Mutagenesis of a buried polar interaction in an SH3 domain: sequence conservation provides the best prediction of stability effects. Biochemistry 37 (1998) 16172-16182
45. Ohage E.C., Graml W., Walter M.M., Steinbacher S., and Steipe B. Beta-turn propensities as paradigms for the analysis of structural motifs to engineer protein stability. Protein Sci. 6 (1997) 233-241
46. Giver L., Gershenson A., Freskgard P.O., and Arnold F.H. Directed evolution of a thermostable esterase. Proc. Natl. Acad. Sci. USA 95 (1998) 12809-12813
47. Williams P.D., Pollock D.D., Blackburne B.P., and Goldstein R.A. Assessing the accuracy of ancestral protein reconstruction methods. PLoS Comput. Biol. 2 (2006) e69
48. Kirschner M., and Gerhart J. Evolvability. Proc. Natl. Acad. Sci. USA 95 (1998) 8420-8427
49. Ancel L.W., and Fontana W. Plasticity, evolvability, and modularity in RNA. J. Exp. Zool. 288 (2000) 242-283
50. James L.C., and Tawfik D.S. Conformational diversity and protein evolution-a 60-year-old hypothesis revisited. Trends Biochem. Sci. 28 (2003) 361-368
51. Di Giulio M. The universal ancestor was a thermophile or a hyperthermophile. Gene 281 (2001) 11-17
52. Fox R.J., Davis S.C., Mundorff E.C., Newman L.M., Gavrilovic V., Ma S.K., et al. Improving catalytic function by ProSAR-driven enzyme evolution. Nat. Biotechnol. 25 (2007) 338-344
53. Herman A., and Tawfik D.S. Incorporating synthetic oligonucleotides via gene reassembly (ISOR): a versatile tool for generating targeted libraries. Protein Eng. Des. Sel. 20 (2007) 219-226
54. Zaccolo M., Williams D.M., Brown D.M., and Gherardi E. An approach to random mutagenesis of DNA using mixtures of triphosphate derivatives of nucleoside analogues. J. Mol. Biol. 255 (1996) 589-603
55. Khersonsky O., and Tawfik D.S. The histidine 115-histidine 134 dyad mediates the lactonase activity of mammalian serum paraoxonases. J. Biol. Chem. 281 (2006) 7649-7656
56. Sosa-Peinado A., Mustafi D., and Makinen M.W. Overexpression and biosynthetic deuterium enrichment of TEM-1 beta-lactamase for structural characterization by magnetic resonance methods. Protein Expression Purif. 19 (2000) 235-245
57. Fersht A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. In: Freeman W.H. (Ed) (1998), Macmillan, New York