Chaperonin overexpression promotes genetic variation and enzyme evolution

Nature

Volumn 459, Issue 7247, 2009, Pages 668-673

  Tokuriki, Nobuhiko ^a   Tawfik, Dan S ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CARBONATE DEHYDRATASE II; CHAPERONIN; ENZYME VARIANT; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PHOSPHOTRIESTERASE; TRIOSEPHOSPHATE ISOMERASE; ESTERASE;

BACTERIUM; ENZYME ACTIVITY; EVOLUTION; GENE EXPRESSION; GENETIC VARIATION; HEAT SHOCK; MUTATION; PROTEIN;

ARTICLE; CONTROLLED STUDY; ENERGY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE MUTATION; GENETIC VARIABILITY; HUMAN; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; PSEUDOMONAS;

ESCHERICHIA COLI;

CHAPERONINS; ESCHERICHIA COLI; ESTERASES; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENETIC VARIATION; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GROEL PROTEIN; GROES PROTEIN; HUMANS; MUTATION; PROTEIN STABILITY; PSEUDOMONAS; SUBSTRATE SPECIFICITY;

EID: 66649132872     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08009     Document Type: Article

References (48)

1. DePristo, M. A., Weinreich, D. M. & Hartl, D. L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nature Rev. Genet. 6, 678-687 (2005).
2. Wilke, C. O., Bloom, J. D., Drummond, D. A. & Raval, A. Predicting the tolerance of proteins to random amino acid substitution. Biophys. J. 89, 3714-3720 (2005).
3. Zeldovich, K. B., Chen, P. & Shakhnovich, E. I. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc. Natl Acad. Sci. USA 104, 16152-16157 (2007).
4. Wang, X., Minasov, G. & Shoichet, B. K. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol. 320, 85-95 (2002).
5. Tokuriki, N., Stricher, F., Serrano, L. & Tawfik, D. S. How protein stability and new functions trade off. PLOS Comput. Biol. 4, e1000002 (2008).
6. Wagner, A. Robustness and Evolvability in Living Systems. (Princeton Univ. Press, 2005).
7. Martin, J. & Hartl, F. U. Chaperone-assisted protein folding. Curr. Opin. Struct. Biol. 7, 41-52 (1997).
8. Thirumalai, D. & Lorimer, G. H. Chaperonin-mediated protein folding. Annu. Rev. Biophys. Biomol. Struct. 30, 245-269 (2001).
9. Fares, M. A., Moya, A. & Barrio, E. GroEL and the maintenance of bacterial endosymbiosis. Trends Genet. 20, 413-416 (2004).
10. Rutherford, S. L. Between genotype and phenotype: protein chaperones and evolvability. Nature Rev. Genet. 4, 263-274 (2003).
11. Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342 (1998).
12. Queitsch, C., Sangster, T. A. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618-624 (2002).
13. Sangster, T. A., Lindquist, S. & Queitsch, C. Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays 26, 348-362 (2004).
14. Van Dyk, T. K., Gatenby, A. A. & LaRossa, R. A. Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature 342, 451-453 (1989).
15. Fares, M. A., Ruiz-González, M. X., Moya, A., Elena, S. F. & Barrio, E. Endosymbiotic bacteria: GroEL buffers against deleterious mutations. Nature 417, 398 (2002).
16. Maisnier-Patin, S. et al. Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nature Genet. 37, 1376-1379 (2005).
17. Cowen, L. E. & Lindquist, S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309, 2185-2189 (2005).
18. Sangster, T. A. & Queitsch, C. The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr. Opin. Plant Biol. 8, 86-92 (2005).
19. Bobula, J. et al. Why molecular chaperones buffer mutational damage: a case study with a yeast Hsp40/70 system. Genetics 174, 937-944 (2006).
20. Kerner, M. J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
21. Persson, M., Carlsson, U. & Bergenhem, N. C. GroEL reversibly binds to, and causes rapid inactivation of, human carbonic anhydrase II at high temperatures. Biochim. Biophys. Acta 1298, 191-198 (1996).
22. Chapman, E. et al. Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL. Proc. Natl Acad. Sci. USA 103, 15800-15805 (2006).
23. Bershtein, S., Golding, K. & Tawfik, D. Intense drifts yield robust and evolvable consensus proteins. J. Mol. Biol. 379, 1029-1044 (2008).
24. Tokuriki, N., Stricher, F., Schymkowitz, J., Serrano, L. & Tawfik, D. S. The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369, 1318-1332 (2007).
25. Sasidharan, R. & Chothia, C. The selection of acceptable protein mutations. Proc. Natl Acad. Sci. USA 104, 10080-10085 (2007).
26. Amitai, G., Gupta, R. A. & Tawfik, D. S. Latent evolutionary potentials under the neutral mutational drift of an enzyme. HFSP Journal 1, 67-78 (2007).
27. McLoughlin, S. Y. & Copley, S. D. A compromise required by gene sharing enables survival: implications for evolution of new enzyme activities. Proc. Natl Acad. Sci. USA 105, 13497-13502 (2008).
28. Roodveldt, C. & Tawfik, D. S. Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily. Biochemistry 44, 12728-12736 (2005).
29. Le Rouzic, A. & Carlborg, O. Evolutionary potential of hidden genetic variation. Trends Ecol. Evol. 23, 33-37 (2007).
30. Fontana, W. & Schuster, P. Continuity in evolution: on the nature of transitions. Science 280, 1451-1455 (1998).
31. Bershtein, S., Segal, M., Bekerman, R., Tokuriki, N. & Tawfik, D. S. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444, 929-932 (2006).
32. Yue, P., Li, Z. & Moult, J. Loss of protein structure stability as a major causative factor in monogenic disease. J. Mol. Biol. 353, 459-473 (2005).
33. Lindner, A. B., Madden, R., Demarez, A., Stewart, E. J. & Taddei, F. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl Acad. Sci. USA 105, 3076-3081 (2008).
34. Noivirt-Brik, O., Unger, R. & Horovitz, A. Low folding propensity and high translation efficiency distinguish in vivo substrates of GroEL from other Escherichia coli proteins. Bioinformatics 23, 3276-3279 (2007).
35. Radman, M., Matic, I. & Taddei, F. Evolution of evolvability. Ann. NY Acad. Sci. 870, 146-155 (1999).
36. Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700-702 (1997).
37. Kerner, M. J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
38. Roodveldt, C. & Tawfik, D. S. Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily. Biochemistry 44, 12728-12736 (2005).
39. Roodveldt, C. & Tawfik, D. S. Directed evolution of phosphotriesterase from Pseudomonas diminuta for heterologous expression in Escherichia coli results in stabilization of the metal-free state. Protein Eng. Des. Sel. 18, 51-58 (2005).
40. Aharoni, A. et al. Directed evolution of mammalian paraoxonases PON1 and PON3 for bacterial expression and catalytic specialization. Proc. Natl Acad. Sci. USA 101, 482-487 (2004).
41. Kitagawa, M. et al. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-120RF archive): unique resources for biological research. DNA Res. 12, 291-299 (2005).
42. Gould, S. M. & Tawfik, D. S. Directed evolution of the promiscuous esterase activity of carbonic anhydrase II. Biochemistry 44, 5444-5452 (2005).
43. Nishihara, K., Kanemori, M., Kitagawa, M., Yanagi, H. & Yura, T. Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl. Environ. Microbiol. 64, 1694-1699 (1998).
44. Misset, O. & Opperdoes, F. R. Simultaneous purification of hexokinase, class-1 fructose-bisphosphate aldolase, triosephosphate isomerase and phosphoglycerate kinase from Trypanosoma brucei. Eur. J. Biochem. 144, 475-483 (1984).
45. Yifrach, O. & Horovitz, A. Transient kinetic analysis of adenosine 5′-triphosphate binding-induced conformational changes in the allosteric chaperonin GroEL. Biochemistry 37, 7083-7088 (1998).
46. Guerois, R., Nielsen, J. E. & Serrano, L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320, 369-387 (2002).
47. Schymkowitz, J. et al. The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-W388 (2005).
48. Tokuriki, N., Stricher, F., Schymkowitz, J., Serrano, L. & Tawfik, D. S. The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369, 1318-1332 (2007).