Structural basis of tRNA agmatinylation essential for AUA codon decoding

Nature Structural and Molecular Biology

Volumn 18, Issue 11, 2011, Pages 1275-1280

  Osawa, Takuo ^a   Kimura, Satoshi ^b   Terasaka, Naohiro ^b   Inanaga, Hideko ^a   Suzuki, Tsutomu ^b   Numata, Tomoyuki ^a,c  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AGMATINE; STRUCTURAL PROTEIN; TRANSFER RNA;

ARCHAEOGLOBUS FULGIDUS; ARTICLE; BINDING SITE; CODON; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA TRANSLATION;

ADENOSINE TRIPHOSPHATE; ANTICODON; ARCHAEAL PROTEINS; ARCHAEOGLOBUS FULGIDUS; CRYSTALLOGRAPHY, X-RAY; CYTIDINE; ISOLEUCINE-TRNA LIGASE; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; RNA, ARCHAEAL; RNA, TRANSFER, ILE;

ARCHAEA; ARCHAEOGLOBUS FULGIDUS;

EID: 80555131000     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2144     Document Type: Article

References (40)

1. Björk, G.R. Biosynthesis and function of modified nucleosides. in tRNA: Structure, Biosynthesis, and Function (eds. Söll, D. & RajBhandary, U.L.) 165-205 (American Society for Microbiology, Washington, DC, 1995).
2. Yokoyama, S. & Nishimura, S. Modified nucleosides and codon recognition. in tRNA: Structure, Biosynthesis, and Function (eds. Söll, D. & RajBhandary, U.L.) 207-224 (American Society for Microbiology, Washington, DC, 1995).
3. Suzuki, T. Biosynthesis and function of tRNA wobble modifications. in Topics in Current Genetics: Fine-Tuning of RNA Functions by Modification and Editing (ed. Grosjean, H.) 24-69 (Springer, New York, 2005).
4. Muramatsu, T. et al. Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 336, 179-181 (1988). (Pubitemid 18266147)
5. Sylvers, L.A., Rogers, K.C., Shimizu, M., Ohtsuka, E. & Söll, D. A 2-thiouridine derivative in tRNAGlu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase. Biochemistry 32, 3836-3841 (1993). (Pubitemid 23126971)
6. Senger, B., Auxilien, S., Englisch, U., Cramer, F. & Fasiolo, F. The modified wobble base inosine in yeast tRNAIle is a positive determinant for aminoacylation by isoleucyl-tRNA synthetase. Biochemistry 36, 8269-8275 (1997). (Pubitemid 27297536)
7. Ikeuchi, Y. et al. Agmatine-conjugated cytidine in a tRNA anticodon is essential for AUA decoding in archaea. Nat. Chem. Biol. 6, 277-282 (2010).
8. Mandal, D. et al. Agmatidine, a modified cytidine in the anticodon of archaeal tRNAIle, base pairs with adenosine but not with guanosine. Proc. Natl. Acad. Sci. USA 107, 2872-2877 (2010).
9. Köhrer, C. et al. Identification and characterization of a tRNA decoding the rare AUA codon in Haloarcula marismortui. RNA 14, 117-126 (2008).
10. Muramatsu, T. et al. A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli. J. Biol. Chem. 263, 9261-9267 (1988).
11. Terasaka, N., Kimura, S., Osawa, T., Numata, T. & Suzuki, T. Biogenesis of 2-agmatinylcytidine catalyzed by the dual protein and RNA kinase TiaS. Nat. Struct. Mol. Biol. 18, doi:10.1038/nsmb.2121 (published online 16 October 2011).
12. Soma, A. et al. An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol. Cell 12, 689-698 (2003). (Pubitemid 37222489)
13. Ikeuchi, Y. et al. Molecular mechanism of lysidine synthesis that determines tRNA identity and codon recognition. Mol. Cell 19, 235-246 (2005). (Pubitemid 41019670)
14. Nakanishi, K. et al. Structural basis for lysidine formation by ATP pyrophosphatase accompanied by a lysine-specific loop and a tRNA-recognition domain. Proc. Natl. Acad. Sci. USA 102, 7487-7492 (2005). (Pubitemid 40740998)
15. Nakanishi, K. et al. Structural basis for translational fidelity ensured by transfer RNA lysidine synthetase. Nature 461, 1144-1148 (2009).
16. Kuratani, M. et al. Structural basis of the initial binding of tRNAIle lysidine synthetase TilS with ATP and L-lysine. Structure 15, 1642-1653 (2007). (Pubitemid 350213407)
17. Suzuki, T. & Miyauchi, K. Discovery and characterization of tRNAIle lysidine synthetase (TilS). FEBS Lett. 584, 272-277 (2010).
18. Bork, P. & Koonin, E.V. A P-loop-like motif in a widespread ATP pyrophosphatase domain: implications for the evolution of sequence motifs and enzyme activity. Proteins 20, 347-355 (1994).
19. Carter, A.P. et al. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340-348 (2000).
20. Schmitt, E. et al. Crystal structure of aspartyl-tRNA synthetase from Pyrococcus kodakaraensis KOD: archaeon specificity and catalytic mechanism of adenylate formation. EMBO J. 17, 5227-5237 (1998). (Pubitemid 28408488)
21. Krishna, S.S., Majumdar, I. & Grishin, N.V. Structural classification of zinc fingers. Nucleic Acids Res. 31, 532-550 (2003). (Pubitemid 36175942)
22. Shi, H. & Moore, P.B. The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: a classic structure revisited. RNA 6, 1091-1105 (2000). (Pubitemid 30620393)
23. Cusack, S., Yaremchuk, A., Krikliviy, I. & Tukalo, M. tRNAPro anticodon recognition by Thermus thermophilus prolyl-tRNA synthetase. Structure 6, 101-108 (1998). (Pubitemid 28084403)
24. Silvian, L.F., Wang, J. & Steitz, T.A. Insights into editing from an Ile-tRNA synthetase structure with tRNAIle and mupirocin. Science 285, 1074-1077 (1999).
25. Eiler, S., Dock-Bregeon, A., Moulinier, L., Thierry, J.C. & Moras, D. Synthesis of aspartyl-tRNAAsp in Escherichia coli-a snapshot of the second step. EMBO J. 18, 6532-6541 (1999). (Pubitemid 29533257)
26. Fukai, S. et al. Mechanism of molecular interactions for tRNAVal recognition by valyl-tRNA synthetase. RNA 9, 100-111 (2003). (Pubitemid 36206306)
27. Nakanishi, K., Ogiso, Y., Nakama, T., Fukai, S. & Nureki, O. Structural basis for anticodon recognition by methionyl-tRNA synthetase. Nat. Struct. Mol. Biol. 12, 931-932 (2005). (Pubitemid 41486718)
28. Hoang, C. & Ferre-D'Amare, A.R. Cocrystal structure of a tRNA Ψ55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell 107, 929-939 (2001). (Pubitemid 34084983)
29. Lee, T.T., Agarwalla, S. & Stroud, R.M. A unique RNA fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function. Cell 120, 599-611 (2005). (Pubitemid 40343073)
30. Numata, T., Ikeuchi, Y., Fukai, S., Suzuki, T. & Nureki, O. Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442, 419-424 (2006). (Pubitemid 44264786)
31. Fukuda, W., Morimoto, N., Imanaka, T. & Fujiwara, S. Agmatine is essential for the cell growth of Thermococcus kodakaraensis. FEMS Microbiol. Lett. 287, 113-120 (2008).
32. Morimoto, N. et al. Dual biosynthesis pathway for longer-chain polyamines in the hyperthermophilic archaeon Thermococcus kodakarensis. J. Bacteriol. 192, 4991-5001 (2010).
33. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
34. Weeks, C.M. & Miller, R. The design and implementation of SnB version 2.0. J. Appl. Crystallogr. 32, 120-124 (1999). (Pubitemid 129699323)
35. de La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997). (Pubitemid 27085618)
36. Abrahams, J.P. & Leslie, A.G.W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 52, 30-42 (1996).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
38. Brünger, A.T. et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
39. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).
40. Vagin, A. & Teplyakov, A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56, 1622-1624 (2000). (Pubitemid 32040020)