Rational design of an orthogonal tryptophanyl nonsense suppressor tRNA

Nucleic Acids Research

Volumn 38, Issue 19, 2010, Pages 6813-6830

  Hughes, Randall A ^a   Ellington, Andrew D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; CYTOSINE; GUANINE; LYSINE TRANSFER RNA LIGASE; TRANSFER RNA; TRYPTOPHAN TRANSFER RNA; TYROSINE TRANSFER RNA LIGASE;

AMINO ACID SEQUENCE; ARTICLE; CODON; ENZYME STRUCTURE; ESCHERICHIA COLI; GENETIC CODE; METHANOCOCCUS JANNASCHII; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN MODIFICATION; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; CODON, NONSENSE; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; RNA, TRANSFER, TRP; SACCHAROMYCES CEREVISIAE; SUPPRESSION, GENETIC; TRANSFER RNA AMINOACYLATION; TRYPTOPHAN-TRNA LIGASE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; METHANOCALDOCOCCUS JANNASCHII; SACCHAROMYCES CEREVISIAE;

EID: 78049389374     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq521     Document Type: Article

References (72)

1. Kiga,D., Sakamoto,K., Kodama,K., Kigawa,T., Matsuda,T., Yabuki,T., Shirouzu,M., Harada,Y., Nakayama,H., Takio,K. 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.
2. Xie,J. and Schultz,P.G. (2006) A chemical toolkit for proteins-an expanded genetic code. Nat. Rev. Mol. Cell Biol., 7, 775-782.
3. Wang,L., Brock,A., Herberich,B. and Schultz,P.G. (2001) Expanding the genetic code of Escherichia coli. Science, 292, 498-500.
4. Anderson,J.C., Wu,N., Santoro,S.W., Lakshman,V., King,D.S. and Schultz,P.G. (2004) An expanded genetic code with a functional quadruplet. Proc. Natl Acad. Sci. USA, 101, 7566-7571.
5. Pastrnak,M., Mageliery,T.M. and Schultz,P.G. (2000) A new orthogonal suppressor tRNA/Aminoacyl-tRNA synthetase pair for evolving an organism with an expanded genetic code. Helv. Chim. Acta, 83, 2277-2286.
6. Liu,D.R. and Schultz,P.G. (1999) Progress toward the evolution of an organism with an expanded genetic code. Proc. Natl Acad. Sci. USA, 96, 4780-4785.
7. Kwon,I., Wang,P. and Tirrell,D.A. (2006) Design of a bacterial host for site-specific incorporation of p-bromophenylalanine into recombinant proteins. J. Am. Chem. Soc., 128, 11778-11783.
8. Santoro,S.W., Anderson,J.C., Lakshman,V. and Schultz,P.G. (2003) An archaebacteria-derived glutamyl-tRNA synthetase and tRNA pair for unnatural amino acid mutagenesis of proteins in Escherichia coli. Nucleic Acids Res., 31, 6700-6709.
9. Anderson,J.C. and Schultz,P.G. (2003) Adaptation of an orthogonal archaeal leucyl-tRNA and synthetase pair for four-base, amber, and opal suppression. Biochemistry, 42, 9598-9608.
10. Nguyen,D.P., Garcia Alai,M.M., Kapadnis,P.B., Neumann,H. and Chin,J.W. (2009) Genetically encoding N(epsilon)-methyl-L-lysine in recombinant histones. J. Am. Chem. Soc., 131, 14194-14195.
11. Landes,C., Perona,J.J., Brunie,S., Rould,M.A., Zelwer,C., Steitz,T.A. and Risler,J.L. (1995) A structure-based multiple sequence alignment of all class I aminoacyl-tRNA synthetases. Biochimie, 77, 194-203.
12. Yang,X.L., Otero,F.J., Skene,R.J., McRee,D.E., Schimmel,P. and Ribas de Pouplana,L. (2003) Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc. Natl Acad. Sci. USA, 100, 15376-15380.
13. Praetorius-Ibba,M., Stange-Thomann,N., Kitabatake,M., Ali,K., Soll,I., Carter,C.W. Jr, Ibba,M. and Soll,D. (2000) Ancient adaptation of the active site of tryptophanyl-tRNA synthetase for tryptophan binding. Biochemistry, 39, 13136-13143.
14. Ribas de Pouplana,L., Frugier,M., Quinn,C.L. and Schimmel,P. (1996) Evidence that two present-day components needed for the genetic code appeared after nucleated cells separated from eubacteria. Proc. Natl Acad. Sci. USA, 93, 166-170.
15. Doublie,S., Bricogne,G., Gilmore,C. and Carter,C.W. Jr (1995) Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase. Structure, 3, 17-31.
16. Budisa,N. (2006) Engineering the Genetic Code. Wiley-VCH, Weinheim.
17. Budisa,N., Rubini,M., Bae,J.H., Weyher,E., Wenger,W., Golbik,R., Huber,R. and Moroder,L. (2002) Global replacement of tryptophan with aminotryptophans generates non-invasive protein-based optical pH sensors. Angew. Chem. Int. Ed. Engl., 41, 4066-4069.
18. Wong,J.T. (1983) Membership mutation of the genetic code: loss of fitness by tryptophan. Proc. Natl Acad. Sci. USA, 80, 6303-6306.
19. Bacher,J.M., Bull,J.J. and Ellington,A.D. (2003) Evolution of phage with chemically ambiguous proteomes. BMC Evol. Biol., 3, 24.
20. Bacher,J.M. and Ellington,A.D. (2001) Selection and characterization of Escherichia coli variants capable of growth on an otherwise toxic tryptophan analogue. J. Bacteriol., 183, 5414-5425.
21. Zhang,Z., Alfonta,L., Tian,F., Bursulaya,B., Uryu,S., King,D.S. and Schultz,P.G. (2004) Selective incorporation of 5-hydroxytryptophan into proteins in mammalian cells. Proc. Natl Acad. Sci. USA, 101, 8882-8887.
22. Himeno,H., Hasegawa,T., Asahara,H., Tamura,K. and Shimizu,M. (1991) Identity determinants of E. coli tryptophan tRNA. Nucleic Acids Res., 19, 6379-6382.
23. Yesland,K.D. and Johnson,J.D. (1993) Anticodon bases C34 and C35 are major, positive, identity elements in Saccharomyces cerevisiae tRNA(Trp). Nucleic Acids Res., 21, 5079-5084.
24. Yaniv,M., Folk,W.R., Berg,P. and Soll,L. (1974) A single mutational modification of a tryptophan-specific transfer RNA permits aminoacylation by glutamine and translation of the codon UAG. J. Mol. Biol., 86, 245-260.
25. Yesland,K.D., Nelson,A.W., Six Feathers,D.M. and Johnson,J.D. (1993) Identity of Saccharomyces cerevisiae tRNA(Trp) is not changed by an anticodon mutation that creates an amber suppressor. J. Biol. Chem., 268, 217-220.
26. Atkin,A.L., Riazi,M.A., Greer,C.L., Roy,K.L. and Bell,J.B. (1993) The functional analysis of nonsense suppressors derived from in vitro engineered Saccharomyces cerevisiae tRNA(Trp) genes. Gene, 134, 57-65.
27. John,T.R., Ghosh,M. and Johnson,J.D. (1997) Identification and expression of the Saccharomyces cerevisiae cytoplasmic tryptophanyl-tRNA synthetase gene. Yeast, 13, 37-41.
28. de Boer,H.A., Comstock,L.J. and Vasser,M. (1983) The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc. Natl Acad. Sci. USA, 80, 21-25.
29. Balbas,P., Soberon,X., Merino,E., Zurita,M., Lomeli,H., Valle,F., Flores,N. and Bolivar,F. (1986) Plasmid vector pBR322 and its special-purpose derivatives-a review. Gene, 50, 3-40.
30. Duester,G., Campen,R.K. and Holmes,W.M. (1981) Nucleotide sequence of an Escherichia coli tRNA (Leu 1) operon and identification of the transcription promoter signal. Nucleic Acids Res., 9, 2121-2139.
31. Bauer,B.F., Kar,E.G., Elford,R.M. and Holmes,W.M. (1988) Sequence determinants for promoter strength in the leuV operon of Escherichia coli. Gene, 63, 123-134.
32. Ross,W., Salomon,J., Holmes,W.M. and Gourse,R.L. (1999) Activation of Escherichia coli leuV transcription by FIS. J. Bacteriol., 181, 3864-3868.
33. Hsu,L.M., Klee,H.J., Zagorski,J. and Fournier,M.J. (1984) Structure of an Escherichia coli tRNA operon containing linked genes for arginine, histidine, leucine, and proline tRNAs. J. Bacteriol., 158, 934-942.
34. Smith,M.C., Furman,T.C., Ingolia,T.D. and Pidgeon,C. (1988) Chelating peptide-immobilized metal ion affinity chromatography. A new concept in affinity chromatography for recombinant proteins. J. Biol. Chem., 263, 7211-7215.
35. Stemmer,W.P., Crameri,A., Ha,K.D., Brennan,T.M. and Heyneker,H.L. (1995) Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides. Gene, 164, 49-53.
36. Hoover,D.M. and Lubkowski,J. (2002) DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res., 30, e43.
37. Reim,D.F. and Speicher,D.W. (2001) N-terminal sequence analysis of proteins and peptides. Curr. Protoc. Protein Sci., Chapter 11, Unit 11 10.
38. McClain,W.H., Foss,K., Jenkins,R.A. and Schneider,J. (1990) Nucleotides that determine Escherichia coli tRNA(Arg) and tRNA(Lys) acceptor identities revealed by analyses of mutant opal and amber suppressor tRNAs. Proc. Natl Acad. Sci. USA, 87, 9260-9264.
39. Tamura,K., Himeno,H., Asahara,H., Hasegawa,T. and Shimizu,M. (1992) In vitro study of E. coli tRNA(Arg) and tRNA(Lys) identity elements. Nucleic Acids Res., 20, 2335-2339.
40. Xu,F., Chen,X., Xin,L., Chen,L., Jin,Y. and Wang,D. (2001) Species-specific differences in the operational RNA code for aminoacylation of tRNA(Trp). Nucleic Acids Res., 29, 4125-4133.
41. Cusack,S., Yaremchuk,A. and Tukalo,M. (1996) The crystal structures of T. thermophilus lysyl-tRNA synthetase complexed with E. coli tRNA(Lys) and a T. thermophilus tRNA(Lys) transcript: anticodon recognition and conformational changes upon binding of a lysyl-adenylate analogue. EMBO J., 15, 6321-6334.
42. Furter,R. (1998) Expansion of the genetic code: site-directed p-fluoro-phenylalanine incorporation in Escherichia coli. Protein Sci., 7, 419-426.
43. Fukunaga,J., Yokogawa,T., Ohno,S. and Nishikawa,K. (2006) Misacylation of yeast amber suppressor tRNA(Tyr) by E. coli lysyl-tRNA synthetase and its effective repression by genetic engineering of the tRNA sequence. J. Biochem., 139, 689-696.
44. Fukunaga,J., Ohno,S., Nishikawa,K. and Yokogawa,T. (2006) A base pair at the bottom of the anticodon stem is reciprocally preferred for discrimination of cognate tRNAs by Escherichia coli lysyl- and glutaminyl-tRNA synthetases. Nucleic Acids Res., 34, 3181-3188.
45. Brevet,A., Chen,J., Commans,S., Lazennec,C., Blanquet,S. and Plateau,P. (2003) Anticodon recognition in evolution: switching tRNA specificity of an aminoacyl-tRNA synthetase by site-directed peptide transplantation. J. Biol. Chem., 278, 30927-30935.
46. Commans,S., Lazard,M., Delort,F., Blanquet,S. and Plateau,P. (1998) tRNA anticodon recognition and specification within subclass IIb aminoacyl-tRNA synthetases. J. Mol. Biol., 278, 801-813.
47. Commans,S., Plateau,P., Blanquet,S. and Dardel,F. (1995) Solution structure of the anticodon-binding domain of Escherichia coli lysyl-tRNA synthetase and studies of its interaction with tRNA(Lys). J. Mol. Biol., 253, 100-113.
48. Onesti,S., Desogus,G., Brevet,A., Chen,J., Plateau,P., Blanquet,S. and Brick,P. (2000) Structural studies of lysyl-tRNA synthetase: conformational changes induced by substrate binding. Biochemistry, 39, 12853-12861.
49. Saruwatari,Y., Wada,T., Takita,T. and Inouye,K. (2008) Substrate-induced conformational changes of the truncated catalytic domain of Geobacillus stearothermophilus lysyl-tRNA synthetase as examined by fluorescence. Biochim. Biophys. Acta, 1784, 1633-1640.
50. Buttcher,V., Senger,B., Schumacher,S., Reinbolt,J. and Fasiolo,F. (1994) Modulation of the suppression efficiency and amino acid identity of an artificial yeast amber isoleucine transfer RNA in Escherichia coli by a G-U pair in the anticodon stem. Biochem. Biophys. Res. Commun., 200, 370-377.
51. Guo,Q., Gong,Q., Tong,K.L., Vestergaard,B., Costa,A., Desgres,J., Wong,M., Grosjean,H., Zhu,G., Wong,J.T. et al. (2002) Recognition by tryptophanyl-tRNA synthetases of discriminator base on tRNATrp from three biological domains. J. Biol. Chem., 277, 14343-14349.
52. Bacher,J.M., Hughes,R.A., Tze-Fei Wong,J. and Ellington,A.D. (2004) Evolving new genetic codes. Trends Ecol. Evol., 19, 69-75.
53. Wang,Q., Parrish,A.R. and Wang,L. (2009) Expanding the genetic code for biological studies. Chem. Biol., 16, 323-336.
54. Xie,J. and Schultz,P.G. (2005) An expanding genetic code. Methods, 36, 227-238.
55. Taira,H., Matsushita,Y., Kojima,K. and Hohsaka,T. (2006) Development of amber suppressor tRNAs appropriate for incorporation of nonnatural amino acids. Nucleic Acids Symp. Ser., 233-234.
56. Taira,H., Matsushita,Y., Kojima,K., Shiraga,K. and Hohsaka,T. (2008) Comprehensive screening of amber suppressor tRNAs suitable for incorporation of non-natural amino acids in a cell-free translation system. Biochem. Biophys. Res. Commun., 374, 304-308.
57. Normanly,J., Kleina,L.G., Masson,J.M., Abelson,J. and Miller,J.H. (1990) Construction of Escherichia coli amber suppressor tRNA genes. III. Determination of tRNA specificity. J. Mol. Biol., 213, 719-726.
58. Guigou,L. and Mirande,M. (2005) Determinants in tRNA for activation of arginyl-tRNA synthetase: evidence that tRNA flexibility is required for the induced-fit mechanism. Biochemistry, 44, 16540-16548.
59. Schultz,D.W. and Yarus,M. (1994) Transfer RNA mutation and the malleability of the genetic code. J. Mol. Biol., 235, 1377-1380.
60. Schultz,D.W. and Yarus,M. (1996) On malleability in the genetic code. J. Mol. Evol., 42, 597-601.
61. Yarus,M. and Schultz,D.W. (1997) Further comments on codon reassignment. Response. J. Mol. Evol., 45, 3-6.
62. Wang,L. and Schultz,P.G. (2001) A general approach for the generation of orthogonal tRNAs. Chem. Biol., 8, 883-890.
63. Alexander,R.W., Eargle,J. and Luthey-Schulten,Z. (2010) Experimental and computational determination of tRNA dynamics. FEBS Lett., 584, 376-386.
64. Giege,R., Sissler,M. and Florentz,C. (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res., 26, 5017-5035.
65. Sanderson,L.E. and Uhlenbeck,O.C. (2007) Exploring the specificity of bacterial elongation factor Tu for different tRNAs. Biochemistry, 46, 6194-6200.
66. Hirsh,D. (1971) Tryptophan transfer RNA as the UGA suppressor. J. Mol. Biol., 58, 439-458.
67. Cochella,L. and Green,R. (2005) An active role for tRNA in decoding beyond codon: anticodon pairing. Science, 308, 1178-1180.
68. Shimizu,Y., Inoue,A., Tomari,Y., Suzuki,T., Yokogawa,T., Nishikawa,K. and Ueda,T. (2001) Cell-free translation reconstituted with purified components. Nat. Biotechnol., 19, 751-755.
69. Forster,A.C., Tan,Z., Nalam,M.N., Lin,H., Qu,H., Cornish,V.W. and Blacklow,S.C. (2003) Programming peptidomimetic syntheses by translating genetic codes designed de novo. Proc. Natl Acad. Sci. USA, 100, 6353-6357.
70. Forster,A.C., Cornish,V.W. and Blacklow,S.C. (2004) Pure translation display. Anal Biochem., 333, 358-364.
71. Josephson,K., Hartman,M.C. and Szostak,J.W. (2005) Ribosomal synthesis of unnatural peptides. J. Am. Chem. Soc., 127, 11727-11735.
72. Hartman,M.C., Josephson,K., Lin,C.W. and Szostak,J.W. (2007) An expanded set of amino acid analogs for the ribosomal translation of unnatural peptides. PLoS ONE, 2, e972.