Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion

Nature Structural Biology

Volumn 10, Issue 6, 2003, Pages 425-432

  Kobayashi, Takatsugu ^a   Nurekil, Osamu ^a,b,c,d   Ishitani, Ryuichiro ^a   Yaremchuk, Anna ^e,f   Tukalo, Michael ^e,f   Cusack, Stephen ^e   Sakamoto, Kensaku ^a,b   Yokoyama, Shigeyuki ^a,b,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN YOKOHAMA INSTITUTE   (Japan)

^c RIKEN HARIMA INSTITUTE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^f INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA; TYROSINE TRANSFER RNA LIGASE;

ANTICODON; ARCHAEBACTERIUM; ARTICLE; BASE PAIRING; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GENETIC CODE; GEOBACILLUS STEAROTHERMOPHILUS; METHANOCOCCUS JANNASCHII; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; ANTICODON; BASE PAIRING; CRYSTALLOGRAPHY, X-RAY; GENETIC CODE; METHANOCOCCUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; RNA, TRANSFER, TYR; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; THERMUS THERMOPHILUS; TYROSINE; TYROSINE-TRNA LIGASE;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; GEOBACILLUS STEAROTHERMOPHILUS; METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; THERMUS; THERMUS THERMOPHILUS;

EID: 0037512360     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb934     Document Type: Article

References (49)

1. Koide, H. et al. Biosynthesis of a protein containing a nonprotein amino acid by Escherichia coli: L-2-aminohexanoic acid at position 21 in human epidermal growth factor. Proc. Natl. Acad. Sci. USA 85, 6237-6241 (1988).
2. Nowak, M. W. et al. Nicotinic receptor binding site probed with unnatural amino acid incorporation in intact cells. Science 268, 439-442 (1995).
3. Short, G.F.Ill et al. Probing the S1/S1′ substrate binding pocket geometry of HIV-1 protease with modified aspartic acid analogues. Biochemistry 39, 8768-8781 (2000).
4. Chin, J.W. et al. Addition of p-azido-L-phenylalanine to the genetic code of Escherichia coli. J. Am. Chem. Soc. 124, 9026-9027 (2002).
5. Chin, J.W., Martin, A.B., King, D.S., Wang, L. & Schultz, P.G. Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. USA 99, 11020-11024 (2002).
6. Hendrickson, W.A., Horton, J.R. & LeMaster, D.M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9, 1665-1672 (1990).
7. Yabuki, T. et al. Dual amino acid-selective and site-directed stable-isotope labeling of the human c-Ha-Ras protein by cell-free synthesis. J. Biomol. NMR 11, 295-306 (1998).
8. Lu, W., Gong, D., Bar-Sagi, D. & Cole, P.A. Site-specific incorporation of a phosphotyrosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol. Cell 8, 759-769 (2001).
9. Wang, L. & Schultz, P.G. Expanding the genetic code. Chem. Commun. (Camb.) 1, 1-11 (2002).
10. Furter, R. Expansion of the genetic code: site-directed p-fluoro-phenylalanine incorporation in Escherichia coli. Protein Sci. 7, 419-426 (1998).
11. Wang, L., Brock, A., Herberich, B. & Schultz, P.G. Expanding the genetic code of Escherichia coli. Science 292, 498-500 (2001).
12. Wang, L., Brock, A. & Schultz, P.G. Adding L-3-(2-naphthyl)alanine to the genetic code of E. coli. J. Am. Chem. Soc. 124, 1836-1837 (2002).
13. Santoro, S.W., Wang, L., Herberich, B., King, D.S. & Schultz, P.G. An efficient system for the evolution of aminoacyl-tRNA synthetase specificity. Nat. Biotechnol. 20, 1044-1048 (2002).
14. Wang, L., Zhang, Z., Brock, A. & Schultz, P.G. Addition of the keto functional group to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. USA 100, 56-61 (2003).
15. Kiga, D. et al. An engineered Escherichia coli tyrosyl-tRNA synthetase for sitespecific 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 (2002).
16. Sakamoto, K. et al. Site-specific incorporation of an unnatural amino acid into proteins in mammalian cells. Nucleic Acids Res. 30, 4692-4699 (2002).
17. Chow, C.M. & RajBhandary, U.L. Saccharomyces cerevisiae cytoplasmic tyrosyl-tRNA synthetase gene. Isolation by complementation of a mutant Escherichia coli suppressor tRNA defective in aminoacylation and sequence analysis. J. Biol. Chem. 268, 12855-12863 (1993).
18. Quinn, C.L., Tao, N. & Schimmel, P. Species-specific microhelix aminoacylation by a eukaryotic pathogen tRNA synthetase dependent on a single base pair. Biochemistry 34, 12489-12495 (1995).
19. Tyr are conserved but expressed differently. Eur. J. Biochem. 268, 761-767 (2001).
20. Wang, L., Magliery, T.J., Liu, D.R. & Schultz, P.G. A new functional suppressor tRNA/aminoacyl-tRNA synthetase pair for the in vivo incorporation of unnatural amino acids into proteins. J. Am. Chem. Soc. 122, 5010-5011 (2000).
21. Giegé, R., Sissler, M. & Florentz, C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 26, 5017-5035 (1998).
22. Marck, C. & Grosjean, H. tRNomics: analysis of tRNA genes from 50 genomes of eukarya, archaea, and bacteria reveals anticodon-sparing strategies and domainspecific features. RNA 8, 1189-1232 (2002).
23. Ser in vitro. Nucleic Acids Res. 18, 6815-6819 (1990).
24. Lee, C.P. & RajBhandary, U.L. Mutants of Escherichia coli initiator tRNA that are aminoacylated with tyrosine by yeast extracts. Proc. Natl. Acad. Sci. USA 88, 11378-11382 (1991).
25. Fechter, P., Rudinger-Thirion, J., Théobald-Dietrich, A. & Giegé, R. Identity of tRNA for yeast tyrosyl-tRNA synthetase: tyrosylation is more sensitive to identity nucleotides than to structural features. Biochemistry 39, 1725-1733 (2000).
26. Brick, P., Bhat, T.N. & Blow, D.M. Structure of tyrosyl-tRNA synthetase refined at 2.3 Å resolution. Interaction of the enzyme with the tyrosyl adenylate intermediate. J. Mol. Biol. 208, 83-98 (1989).
27. Qiu, X. et al. Crystal structure of Staphylococcus aureus tyrosyl-tRNA synthetase in complex with a class of potent and specific inhibitors. Protein Sci. 10, 2008-2016 (2001).
28. Yaremchuk, A., Kriklivyi, I., Tukalo, M. & Cusack, S. Class I tyrosyl-tRNA synthetase has a class II mode of cognate tRNA recognition. EMBO J. 21, 3829-3840 (2002).
29. Yang, X.L., Skene, R.J., McRee, D.E. & Schimmel, P. Crystal structure of a human aminoacyl-tRNA synthetase cytokine. Proc. Natl. Acad. Sci. USA 99, 15369-15374 (2002).
30. Steer, B.A. & Schimmel, P. Major anticodon-binding region missing from an archaebacterial tRNA synthetase. J. Biol. Chem. 274, 35601-35606 (1999).
31. Eriani, G., Delarue, M., Poch, O., Gangloff, J. & Moras, D. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347, 203-206 (1990).
32. Starzyk, R.M., Webster, T.A. & Schimmel, P. Evidence for dispensable sequences inserted into a nucleotide fold. Science 237, 1614-1618 (1987).
33. Asp. Science 252, 1682-1689 (1991).
34. Gln and ATP at 2.8 Å resolution. Science 246, 1135-1142 (1989).
35. Wakasugi, K., Quinn, C.L., Tao, N. & Schimmel, P. Genetic code in evolution: switching species-specific aminoacylation with a peptide transplant. EMBO J. 17, 297-305 (1998).
36. Steer, B.A. & Schimmel, P. Domain-domain communication in a miniature archaebacterial tRNA synthetase. Proc. Natl. Acad. Sci. USA 96, 13644-13649 (1999).
37. Tyr gene are both transcribed in a HeLa cell extract but spliced along different pathways. EMBO J. 6, 35-41 (1987).
38. Brick, P. & Blow, D.M. Crystal structure of a deletion mutant of a tyrosyl-tRNA synthetase complexed with tyrosine. J. Mol. Biol. 194, 287-297 (1987).
39. Zhang, D., Vaidehi, N., Goddard, W.A. III, Danzer, J.F. & Debe, D. Structure-based design of mutant Methanococcus jannaschii tyrosyl-tRNA synthetase for incorporation of O-methyl-L-tyrosine. Proc. Natl. Acad. Sci. USA 99, 6579-6584 (2002).
40. Fechter, P., Rudinger, J., Giegé, R. & Théobald-Dietrich, A. Ribozyme processed tRNA transcripts with unfriendly internal promoter for T7 RNA polymerase: production and activity. FEBS Lett. 436, 99-103 (1998).
41. 15N heteronuclear NMR studies of Escherichia coli thionedoxin in samples isotopically labeled by residue type. Biochemistry 24, 7263-7268 (1985).
42. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collection in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
43. Weeks, C.M. & Miller, R. Optimizing Shake-and-Bake for proteins. Acta Crystallogr. D 55, 492-500 (1999).
44. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
45. Terwilliger, T.C. Maximum-likelihood density modification. Acta Crystallogr. D 56, 965-972 (2000).
46. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
47. Brunger, A. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
48. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (1997).
49. Gouet, P., Courcelle, E., Stuart, D.I. & Métoz, F. ESPript: multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).