Importance of single molecular determinants in the fidelity of expanded genetic codes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 4, 2011, Pages 1320-1325

  Antonczak, Alicja K ^a   Simova, Zuzana ^a   Yonemoto, Isaac T ^e   Bochtler, Matthias ^a,b,c   Piasecka, Anna ^d   Czapińska, Honorata ^a,c   Brancale, Andrea ^b   Tippmann, Eric M ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^d UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

^e NONE   (United States)

Author keywords

Directed evolution; Protein engineering

Indexed keywords

5 HYDROXYTRYPTOPHAN; AMINO ACID TRANSFER RNA LIGASE; TRYPTOPHAN; TYROSINE;

ARTICLE; ENZYME STRUCTURE; GEOBACILLUS STEAROTHERMOPHILUS; METHANOCALDOCOCCUS JANNASCHII; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

AMINO ACIDS; AMINO ACYL-TRNA SYNTHETASES; ANTICODON; BASE SEQUENCE; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; GENETIC CODE; HYDROGEN BONDING; METHANOCOCCALES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA, TRANSFER, TYR; SUBSTRATE SPECIFICITY; TYROSINE;

MAMMALIA; METHANOCALDOCOCCUS JANNASCHII;

EID: 79952140370     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012276108     Document Type: Article

References (69)

1. Budisa N (2006) Engineering the Genetic Code (Wiley, Weinheim, Germany).
2. Delarue M, Moras D (1993) The aminoacyl-tRNA synthetase family: Modules at work. Bioessays 15:675-687.
3. Carter CW, Jr (1993) Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu Rev Biochem 62:715-748.
4. Ibba M, Soll D (2000) Aminoacyl-tRNA synthesis. Annu Rev Biochem 69:617-650.
5. Silvian LF, Wang J, Steitz TA (1999) Insights into editing from an ile-tRNA synthetase structure with tRNAile and mupirocin. Science 285:1074-1077.
6. Mursinna RS, Lincecum TL, Jr, Martinis SA (2001) A conserved threonine within Escherichia colileucyl-tRNA synthetase prevents hydrolytic editing of leucyl-tRNALeu. Biochemistry 40:5376-5381. (Pubitemid 32458237)
7. Yarus M, Berg P (1967) Recognition of tRNA by aminoacyl tRNA synthetases. J Mol Biol 28:479-490.
8. Fersht AR, Mulvey RS, Koch GLE (1975) Ligand binding and enzymic catalysis coupled through subunits in tyrosyl-tRNA synthetase. Biochemistry 14:13-18.
9. Fersht AR, et al. (1985) Hydrogen bonding and biological specificity analysed by protein engineering. Nature 314:235-238. (Pubitemid 15076511)
10. Xie J, Schultz PG (2006) A chemical toolkit for proteins - An expanded genetic code. Nat Rev Mol Cell Biol 7:775-782. (Pubitemid 44450461)
11. Hino N, et al. (2005) Protein photo-cross-linking in mammalian cells by site-specific incorporation of a photoreactive amino acid. Nat Methods 2:201-206. (Pubitemid 41122127)
12. Kiga D, et al. (2002) An engineered Escherichia coli tyrosyl-tRNA synthetase for site-specific incorporation of an unnatural amino acid into proteins in eukaryotic translation and its application in a wheat germ cell-free system. Proc Natl Acad Sci USA 99:9715-9720. (Pubitemid 34831113)
13. Lepthien S, Hoesl MG, Merkel L, Budisa N (2008) Azatryptophans endow proteins with intrinsic blue fluorescence. Proc Natl Acad Sci USA 105:16095-16100.
14. Bae JH, et al. (2003) Expansion of the genetic code enables design of a novel "gold" class of green fluorescent proteins. J Mol Biol 328:1071-1081.
15. Praetorius-Ibba M, et al. (2000) Ancient adaptation of the active site of tryptophanyl-tRNA synthetase for tryptophan binding. Biochemistry 39:13136-13143.
16. Doublie S, Bricogne G, Gilmore C, Carter CW, Jr (1995) Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase. Structure 3:17-31.
17. Yang XL, et al. (2003) Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc Natl Acad Sci USA 100:15376-15380.
18. Landes C, et al. (1995) A structure-based multiple sequence alignment of all class I aminoacyl-tRNA synthetases. Biochimie 77:194-203.
19. Kwon I, Kirshenbaum K, Tirrell DA (2003) Breaking the degeneracy of the genetic code. J Am Chem Soc 125:7512-7513. (Pubitemid 36750261)
20. Magliery TJ, Anderson JC, Schultz PG (2001) Expanding the genetic code: Selection of efficient suppressors of four-base codons and identification of "shifty" four-base codons with a library approach in Escherichia coli. J Mol Biol 307:755-769.
21. Wan W, et al. (2010) A facile system for genetic incorporation of two different noncanonical amino acids into one protein in Escherichia coli. Angew Chem Int Ed Engl 49:3211-3214.
22. Sakamoto K, et al. (2002) Site-specific incorporation of an unnatural amino acid into proteins in mammalian cells. Nucleic Acids Res 30:4692-4699. (Pubitemid 35331751)
23. Young TS, Ahmad I, Brock A, Schultz PG (2009) Expanding the genetic repertoire of the methylotrophic yeast Pichia pastoris. Biochemistry 48:2643-2653.
24. Wang L, Brock A, Herberich B, Schultz PG (2001) Expanding the genetic code of Escherichia coli. Science 292:498-500. (Pubitemid 32335951)
25. Zhang ZW, et al. (2004) Selective incorporation of 5-hydroxytryptophan into proteins in mammalian cells. Proc Natl Acad Sci USA 101:8882-8887.
26. Lee HS, Spraggon G, Schultz PG, Wang F (2009) Genetic incorporation of a metal-ion chelating amino acid into proteins as a biophysical probe. J Am Chem Soc 131:2481-2483.
27. Tippmann EM, Liu W, Surnmerer D, Mack AV, Schultz PG (2007) A genetically encoded diazirine photocrosslinker in Escherichia coli. Chembiochem 8:2210-2214.
28. Wang L, Zhang Z, Brock A, Schultz PG (2003) Addition of the keto functional group to the genetic code of Escherichia coli. Proc Natl Acad Sci USA 100:56-61. (Pubitemid 36078029)
29. Santoro SW, Wang L, Herberich B, King DS, Schultz PG (2002) An efficient system for the evolution of aminoacyl-tRNA synthetase specificity. Nat Biotechnol 20:1044-1048.
30. Melançon Cr, Schultz P (2009) One plasmid selection system for the rapid evolution of aminoacyl-tRNA synthetases. Bioorg Med Chem Lett 19:3845-3847.
31. Zhang Z, et al. (2009) A new strategy for the synthesis of glycoproteins. Science 326:1187.
32. Xu R, et al. (2009) Site-specific incorporation of the mucin-type N-acetylgalactosamine-alpha-O-threonine into protein in Escherichia coli. J Am Chem Soc 131:13883.
33. Alfonta L, Zhang Z, Uryu S, Loo J, Schultz P (2003) Site-specific incorporation of a redox-active amino acid into proteins. J Am Chem Soc 125:14662-14663. (Pubitemid 37475531)
34. de Prat Gay G, Duckworth HW, Fersht AR (1993) Modification of the amino acid specificity of tyrosyl-tRNA synthetase by protein engineering. FEBS Lett 318:167-171.
35. Fersht AR (1987) Dissection of the structure and activity of the tyrosyl-tRNA synthetase by site-directed mutagenesis. Biochemistry 26:8031-8037.
36. Bhat TN, Blow DM, Brick P, Nyborg J (1982) Tyrosyl-tRNA synthetase forms a mononucleotide-binding fold. J Mol Biol 158:699-709. (Pubitemid 12044692)
37. Kobayashi T, et al. (2003) Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion. Nat Struct Biol 10:425-432. (Pubitemid 36637639)
38. Seyedsayamdost MR, Xie J, Chan CTY, Schultz PG, Stubbe J (2007) Site-specific insertion of 3-aminotyrosine into subunit α2 of E. coli ribonucleotide reductase: Direct evidence for involvement of Y730 and Y731 in radical propagation. J Am Chem Soc 129:15060-15071. (Pubitemid 350230727)
39. Zhang Z, et al. (2004) A new strategy for the synthesis of glycoproteins. Science 303:371-373. (Pubitemid 38095776)
40. Xu R, et al. (2004) Site-specific incorporation of the mucin-type N-acetylgalactosamine- α-O-threonine into protein in Escherichia coli. J Am Chem Soc 126:15654-15655. (Pubitemid 39602420)
41. Antonczak AK, Simova Z, Tippmann EM (2009) A critical examination of Escherichia coli esterase activity. J Biol Chem 284:28795-28800.
42. Yonemoto IT, Tippmann EM (2010) The juggernauts of biology. Bioessays 32:314-321.
43. Igarashi K, Hotta K, Kasuya F, Abe K, Sakoda S (2003) Determination of cabergoline and L-dopa in human plasma using liquid chromatography-tandem mass spectrometry. J Chromatogr B 792:55-61. (Pubitemid 36773801)
44. Bourcier S, et al. (2006) Detection of 28 neurotransmitters and related compounds in biological fluids by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 20:1405-1421.
45. Xie J, et al. (2004) The site-specific incorporation of p-iodo-L-phenylalanine into proteins for structure determination. Nat Biotechnol 22:1297-1301. (Pubitemid 39336783)
46. Brustad E, et al. (2008) A genetically encoded boronate-containing amino acid. Angew Chem Int Edit 47:8220-8223.
47. Jia J, et al. (2002) Two essential regions for tRNA recognition in Bacillus subtilis tryptophanyl-tRNA synthetase. Biochem J 365:749-756. (Pubitemid 34864457)
48. Xue H, Shen W, Giegé R, Wong J (1993) Identity elements of tRNA(Trp). Identification and evolutionary conservation. J Biol Chem 268:9316-9322. (Pubitemid 23145977)
49. Budisa N, et al. (2002) Global replacement of tryptophan with aminotryptophans generates non-invasive protein-based optical pH sensors. Angew Chem Int Edit 41:4066-4069. (Pubitemid 35396626)
50. Lepthien S, Wiltschi B, Bolic B, Budisa N (2006) In vivo engineering of proteins with nitrogen-containing tryptophan analogs. Appl Microbiol Biotechnol 73:740-754.
51. Wong CY, Eftink MR (1997) Biosynthetic incorporation of tryptophan analogues into staphylococcal nuclease: Effect of 5-hydroxytryptophan and 7-azatryptophan on structure and stability. Protein Sci 6:689-697.
52. Azim MK, Budisa N (2008) Docking of tryptophan analogs to trytophanyl-tRNA synthetase: implications for non-canonical amino acid incorporations. Biol Chem 389:1173-1182.
53. Retailleau P, Weinreb V, Hu M, Carter CW, Jr (2007) Crystal structure of tryptophanyl-tRNA synthetase complexed with adenosine-5′ tetraphosphate: Evidence for distributed use of catalytic binding energy in amino acid activation by class I aminoacyl-tRNA synthetases. J Mol Biol 369:108-128.
54. Barlati S, Ciferri O (1970) Incorporation of 5-methyl- and 5-hydroxy-tryptophan into the protein of Bacillus subtilis. J Bacteriol 101:166-172.
55. Kwon I, Tirrell DA (2007) Site-specific incorporation of tryptophan analogues into recombinant proteins in bacterial cells. J Am Chem Soc 129:10431-10437. (Pubitemid 47330261)
56. Kwon I, Wang P, Tirrell DA (2006) Design of a bacterial host for site-specific incorporation of p-bromophenylalanine into recombinant proteins. J Am Chem Soc 128:11778-11783. (Pubitemid 44360212)
57. Laowanapiban P, et al. (2009) Independent saturation of three TrpRS subsites generates a partially assembled state similar to those observed in molecular simulations. Proc Natl Acad Sci USA 106:1790-1795.
58. Buddha MR, Crane BR (2005) Structure and activity of an aminoacyl-tRNA synthetase that charges tRNA with nitro-tryptophan. Nat Struct Mol Biol 12:274-275. (Pubitemid 43079370)
59. Sever S, Rogers K, Rogers MJ, Carter C, Soll D (1996) Escherichia colitryptophanyl-tRNA synthetase mutants selected for tryptophan auxotrophy implicate the dimer interface in optimizing amino acid binding. Biochemistry 35:32-40. (Pubitemid 26036403)
60. Buddha MR, Tao T, Parry RJ, Crane BR (2004) Regioselective nitration of tryptophan by a complex between bacterial nitric-oxide synthase and tryptophanyl-tRNA synthetase. J Biol Chem 279:49567-49570. (Pubitemid 39577757)
61. Zhou Q, et al. (2010) Orthogonal use of a human tRNA synthetase active site to achieve multifunctionality. Nat Struct Mol Biol 17:57-61.
62. Young TS, Ahmad I, Yin JA, Schultz PG (2010) An enhanced system for unnatural amino acid mutagenesis in E. coli. J Mol Biol 395:361-374.
63. Iraha F, et al. (2010) Functional replacement of the endogenous tyrosyl-tRNA synthetase-tRNATyr pair by the archaeal tyrosine pair in Escherichia coli for genetic code expansion. Nucleic Acids Res 38:3682-3691.
64. Liu W, Brock A, Chen S, Schultz PG (2007) Genetic incorporation of unnatural amino acids into proteins in mammalian cells. Nat Methods 4:239-244. (Pubitemid 46358874)
65. James NG, Byrne SL, Mason AB (2009) Incorporation of 5-hydroxytryptophan into transferrin and its receptor allows assignment of the pH induced changes in intrinsic fluorescence when iron is released. Biochem Biophys Acta 1794:532-540.
66. Majerfeld I, Barlati S, Ciferri O (1970) Tryptophanless death in Bacillus subtilis. J Bacteriol 101:350-354.
67. Wells JA, Fairbrother WJ, Otlewski J, Laskowski M, Jr, Burnier J (1994) A reinvestigation of a synthetic peptide (TrPepz) designed to mimic trypsin. Proc Natl Acad Sci USA 91:4110-4114. (Pubitemid 24143382)
68. Miyake-Stoner SJ, et al. (2010) Generating permissive site-specific unnatural aminoacyl- tRNA synthetases. Biochemistry 49:1667-1677.
69. Buurma NJ, Haq I (2007) Advances in the analysis of isothermal titration calorimetry data for ligand-DNA interactions. Methods 42:162-172. (Pubitemid 46654816)