Directed Evolution of a Model Primordial Enzyme Provides Insights into the Development of the Genetic Code

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Müller, Manuel M ^a,d   Allison, Jane R ^a,e   Hongdilokkul, Narupat ^a   Gaillon, Laurent ^b   Kast, Peter ^a   van Gunsteren, Wilfred F ^a   Marlière, Philippe ^c   Hilvert, Donald ^a  

^a ETH ZURICH   (Switzerland)

^b DIF   (France)

^c Heurisko USA   (United States)

^d PRINCETON UNIVERSITY   (United States)

^e MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CHORISMATE MUTASE; ISOLEUCINE; LEUCINE; THREONINE; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CODON USAGE; CONTROLLED STUDY; DIRECTED MOLECULAR EVOLUTION; ENZYME ACTIVE SITE; ENZYME STABILITY; GENE MUTATION; GENETIC CODE; MOLECULAR DYNAMICS; NONHUMAN; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; CHORISMATE MUTASE; DIRECTED MOLECULAR EVOLUTION; GENETIC CODE; METHANOCOCCALES; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84873496493     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003187     Document Type: Article

References (45)

1. Joyce GF, (1989) RNA evolution and the origins of life. Nature 338: 217-224.
2. Crick FHC, (1968) The origin of the genetic code. J Mol Biol 38: 367-379.
3. Orgel LE, (1968) Evolution of the genetic apparatus. J Mol Biol 38: 381-393.
4. Narlikar GJ, Herschlag D, (2003) Mechanistic aspects of enzymatic catalysis: Lessons from comparison of RNA and protein enzymes. Annu Rev Biochem 66: 19-59.
5. Doudna JA, Lorsch JR, (2005) Ribozyme catalysis: Not different, just worse. Nat Struct Mol Biol 12: 395-402.
6. Wong JT-F, (2005) Coevolution theory of the genetic code at age thirty. BioEssays 27: 416-425.
7. Miller SL, (1953) A production of amino acids under possible primitive earth conditions. Science 117: 528-529.
8. Kvenvolden K, Lawless J, Pering K, Peterson E, Flores J, et al. (1970) Evidence for extraterrestrial amino-acids and hydrocarbons in the Murchison meteorite. Nature 228: 923-926.
9. Sicheri F, Yang DSC, (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375: 427-431.
10. Riddle DS, Santiago JV, Bray-Hall ST, Doshi N, Grantcharova VP, et al. (1997) Functional rapidly folding proteins from simplified amino acid sequences. Nat Struct Mol Biol 4: 805-809.
11. Tanaka J, Yanagawa H, Doi N, (2011) Comparison of the frequency of functional SH3 domains with different limited sets of amino acids using mRNA display. PLoS ONE 6: e18034 doi:10.1371/journal.pone.0018034.
12. Akanuma S, Kigawa T, Yokoyama S, (2002) Combinatorial mutagenesis to restrict amino acid usage in an enzyme to a reduced set. Proc Natl Acad Sci USA 99: 13549-13553.
13. MacBeath G, Kast P, Hilvert D, (1998) A small, thermostable, and monofunctional chorismate mutase from the archaeon Methanococcus jannaschii. Biochemistry 37: 10062-10073.
14. Walter KU, Vamvaca K, Hilvert D, (2005) An active enzyme constructed from a 9-amino acid alphabet. J Biol Chem 280: 37742-37746.
15. Trifonov EN, (2000) Consensus temporal order of amino acids and evolution of the triplet code. Gene 261: 139-151.
16. Kamtekar S, Schiffer J, Xiong H, Babik J, Hecht M, (1993) Protein design by binary patterning of polar and nonpolar amino acids. Science 262: 1680-1685.
17. Fisher MA, McKinley KL, Bradley LH, Viola SR, Hecht MH, (2012) De novo designed proteins from a library of artificial sequences function in Escherichia coli and enable cell growth. PLoS ONE 6: e15364 doi:10.1371/journal.pone.0015364.
18. Taylor SV, Walter KU, Kast P, Hilvert D, (2001) Searching sequence space for protein catalysts. Proc Natl Acad Sci USA 98: 10596-10601.
19. Kast P, Asif-Ullah M, Jiang N, Hilvert D, (1996) Exploring the active site of chorismate mutase by combinatorial mutagenesis and selection: The importance of electrostatic catalysis. Proc Natl Acad Sci USA 93: 5043-5048.
20. Cambray G, Mazel D, (2008) Synonymous genes explore different evolutionary landscapes. PLoS Genet 4: e1000256 doi:10.1371/journal.pgen.1000256.
21. Neuenschwander M, Butz M, Heintz C, Kast P, Hilvert D, (2007) A simple selection strategy for evolving highly efficient enzymes. Nat Biotechnol 25: 1145-1147.
22. Mutzel R, Marlière P, (2000) Method and device for selecting accelerated proliferation of living cells in suspension. pp. WO2000034433.
23. MacBeath G, Kast P, Hilvert D, (1998) Exploring sequence constraints on an interhelical turn using in vivo selection for catalytic activity. Protein Sci 7: 325-335.
24. Stewart J, Wilson DB, Ganem B, (1990) A genetically engineered monofunctional chorismate mutase. J Am Chem Soc 112: 4582-4584.
25. MacBeath G, Kast P, (1998) UGA read-through artifacts- when popular gene expression systems need a pATCH. BioTechniques 24: 789-794.
26. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinf 9: 40.
27. Lee AY, Karplus PA, Ganem B, Clardy J, (1995) Atomic structure of the buried catalytic pocket of Escherichia coli chorismate mutase. J Am Chem Soc 117: 3627-3628.
28. Dill KA, Bromberg S, Yue K, Chan HS, Ftebig KM, et al. (1995) Principles of protein folding- A perspective from simple exact models. Protein Sci 4: 561-602.
29. Wolynes PG, (1997) As simple as can be? Nat Struct Biol 4: 871-874.
30. Rogers J, Joyce GF, (1999) A ribozyme that lacks cytidine. Nature 402: 323-325.
31. Reader JS, Joyce GF, (2002) A ribozyme composed of only two different nucleotides. Nature 420: 841-844.
32. Rogers J, Joyce GF, (2001) The effect of cytidine on the structure and function of an RNA ligase ribozyme. RNA 7: 395-404.
33. Yoo TH, Link AJ, Tirrell DA, (2007) Evolution of a fluorinated green fluorescent protein. Proc Natl Acad Sci USA 104: 13887-13890.
34. Liu CC, Mack AV, Tsao M-L, Mills JH, Lee HS, et al. (2008) Protein evolution with an expanded genetic code. Proc Natl Acad Sci USA 105: 17688-17693.
35. Bacher JM, Hughes RA, Wong JT-F, Ellington AD, (2004) Evolving new genetic codes. Trends Ecol Evol 19: 69-75.
36. Lemeignan B, Sonigo P, Marlière P, (1993) Phenotypic suppression by incorporation of an alien amino acid. J Mol Biol 231: 161-166.
37. Gamper M, Kast P, (2005) Strategy for chromosomal gene targeting in RecA-deficient Escherichia coli strains. BioTechniques 38: 405-408.
38. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF, (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem 25: 1656-1676.
39. Oostenbrink C, Soares TA, van der Vegt NFA, van Gunsteren WF, (2005) Validation of the 53A6 GROMOS force field. Eur Biophys J 34: 273-284.
40. Christen M, Hünenberger PH, Bakowies D, Baron R, Bürgi R, et al. (2005) The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 26: 1719-1751.
41. Eichenberger AP, Allison JR, Dolenc J, Geerke DP, Horta BAC, et al. (2011) GROMOS++ software for the analysis of biomolecular simulation trajectories. J Chem Theory Comput 7: 3379-3390.
42. Liu DR, Cload ST, Pastor RM, Schultz PG, (1996) Analysis of active site residues in Escherichia coli chorismate mutase by site-directed mutagenesis. J Am Chem Soc 118: 1789-1790.
43. Sasso S, Ramakrishnan C, Gamper M, Hilvert D, Kast P, (2005) Characterization of the secreted chorismate mutase from the pathogen Mycobacterium tuberculosis. FEBS J 272: 375-389.
44. Mattei P, Kast P, Hilvert D, (1999) Bacillus subtilis chorismate mutase is partially diffusion-controlled. Eur J Biochem 261: 25-32.
45. Gamper M, Hilvert D, Kast P, (2000) Probing the role of the C-terminus of Bacillus subtilis chorismate mutase by a novel random protein-termination strategy. Biochemistry 39: 14087-14094.