Shape-selective RNA recognition by cysteinyl-tRNA synthetase

Nature Structural and Molecular Biology

Volumn 11, Issue 11, 2004, Pages 1134-1141

  Hauenstein, Scott ^a   Zhang, Chun Mei ^b   Hou, Ya Ming ^b   Perona, John J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; BACTERIAL ENZYME; CYSTEINE TRANSFER RNA; ELONGATION FACTOR TU; SUGAR PHOSPHATE;

AMINOACYLATION; ANTICODON; ARTICLE; BASE PAIRING; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HYDROGEN BOND; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS;

AMINO ACYL-TRNA SYNTHETASES; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; HYDROGEN BONDING; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; NUCLEIC ACID CONFORMATION; PHOSPHATES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA; RNA, TRANSFER; TIME FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 7544240563     PISSN: 15459993     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsmb849     Document Type: Article

References (63)

1. Seeman, N.C., Rosenberg, J.M. & Rich, A. Sequence-specific recognition of double helical nucleic acids by proteins. Proc. Natl. Acad. Sci. USA 73, 804-808 (1976).
2. Rhodes, D., Schwabe, J.W., Chapman, L. & Fairall, L. Towards an understanding of protein-DNA recognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 501-509 (1996).
3. Gromiha, M., Siebers, J.G., Selvaraj, S., Kono, H. & Sarai, A. Intermolecular and intramolecular readout mechanisms in protein-DNA recognition. J. Mol. Biol. 337, 285-294 (2004).
4. Otwinowski, Z. et al. Crystal structure of trp repressor/operator complex at atomic resolution. Nature 335, 321-329 (1988).
5. Lesser, D.R., Kurpiewski, M.R., Waters, T., Connolly, B.A. & Jen-Jacobsen, L. Facilitated distortion of the DNA site enhances EcoRI endonuclease-DNA recognition. Proc. Natl. Acad. Sci. USA 90, 7548-7452 (1993).
6. Martin, A.M., Sam, M.D., Reich, N.O. & Perona, J.J. Structural and energetic origins of indirect readout in site-specific DNA cleavage by a restriction endonuclease. Nat. Struct. Biol. 6, 269-277 (1999).
7. Lynch, T.W., Read, E.K., Mattis, A.N., Gardner, J.F. & Rice, P.A. Integration host factor: putting a twist on protein-DNA recognition. J. Mol. Biol. 330, 493-502 (2003).
8. Ibba, M. & Soll, D. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617-650 (2000).
9. Nissan, T.A. & Perona, J.J. Alternative designs for construction of the class II transfer RNA tertiary core. RNA 6, 1585-1596 (2000).
10. Avalos, J., Corrochano, L.M. & Brenner, S. Cysteinyl-tRNA synthetase is a direct descendent of the first aminoacyl-tRNA synthetase. FEBS Lett. 286, 176-180 (1991).
11. Eriani, G., Dirheimer, G. & Gangloff, J. Cysteinyl-tRNA synthetase: determination of the last E. coli aminoacyl-tRNA synthetase primary structure. Nucleic Acids Res. 19, 265-269 (1991).
12. Hou, Y.M., Shiba, K., Mottes, C. & Schimmel, P. Sequence determination and modeling of structural motifs for the smallest monomeric aminoacyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 88, 976-980 (1991).
13. Newberry, K.J., Hou, Y.M. & Perona, J.J. Structural origins of amino acid selection without editing by cysteinyl-tRNA synthetase. EMBO J. 21, 2778-2787 (2002).
14. Levitt, M. Detailed molecular model for transfer ribonucleic acid. Nature 224, 759-763 (1969).
15. Nissen, P., Thirup, S., Kjeldgaard, M. & Nyborg, J. The crystal structure of Cys-tRNACys-Ef-TU-GDPNP reveals general and specific features in the ternary complex and in tRNA. Structure Fold Des. 7, 143-156 (1999).
16. Hamann, C.S. & Hou, Y.M. An RNA structural determinant for tRNA recognition. Biochemistry 36, 7967-7972 (1997).
17. Hou, Y.M., Westof, E. & Giege, R. An unusual RNA tertiary interaction has a role for the specific aminoacylation of a transfer RNA. Proc. Natl. Acad. Sci. USA 90, 6776-6780 (1993).
18. Hou, Y.M., Sterner, T. & Bhalla, R. Evidence for a conserved relationship between an acceptor stem and a tRNA for aminoacylation. RNA 1, 707-712 (1995).
19. Lipman, R.S. & Hou, Y.M. Aminoacylation of tRNA in the evolution of an aminoacyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 95, 13495-13500 (1998).
20. Cavarelli, J., Delagoutte, B., Eriani, G., Gangloff, J. & Moras, D. L-arginine recognition by yeast arginyl-tRNA synthetase. EMBO J. 17, 5438-5448 (1998).
21. Cusack, S., Yaremchuk, A. & Tukalo, M. The 2 Å crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue. EMBO J. 19, 2351-2361 (2000).
22. Fukai, S. et al. Structural basis for double-sieve discrimination of L-valine from L-isoleucine and L-threonine by the complex of tRNA(Val) and valyl-tRNA synthetase. Cell 103, 793-803 (2000).
23. Silvian, L.F., Wang, J. & Steitz, T.A. Insights into editing from an ile-tRNA structure with tRNAIIe and mupirocin. Science 285, 1074-1077 (1999).
24. Sugiura, I. et al. The 2.0 Å crystal structure of Thermus thermophilus methionyl-tRNA synthetase reveals two RNA-binding modules. Structure Fold Des. 8, 197-208 (2000).
25. Nakama, T., Nureki, O. & Yokoyama, S. Structural basis for the recognition of isoleucyl-adenylate and an antibiotic, mupirocin, by isoleucyl-tRNA synthetase. J. Biol. Chem. 276, 47387-47393 (2001).
26. Fukai, S. et al. Mechanism of molecular interactions for tRNA(Val) recognition by valyl-tRNA synthetase. RNA 9, 100-111 (2003).
27. Sherlin, L.D. & Perona, J.J. tRNA-dependent active site assembly in a class I aminoacyl-tRNA synthetase. Structure 11, 591-603 (2003).
28. Williamson, J.R. Induced fit in RNA-protein recognition. Nat. Struct. Biol. 7, 834-837 (2000).
29. Komatsoulis, G.A. & Abelson, J. Recognition of tRNA(Cys) by Escherichia coli cysteinyl-tRNA synthetase. Biochemistry 32, 7435-7444 (1993).
30. Burkard, M.E., Kierzek, R. & Turner, D.H. Thermodynamics of unpaired terminal nucleotides on short RNA helixes correlates with stacking at helix termini in larger RNAs. J. Mol. Biol. 290, 967-982 (1999).
31. Ming, X., Smith, K., Suga, H. & Hou, Y.M. Recognition of tRNA backbone for aminoacylation with cysteine: evolution from Escherichia coli to human. J. Mol. Biol. 318, 1207-1220 (2002).
32. Hamann, C.S. & Hou, Y.M. Probing a tRNA core that contributes to aminoacylation. J. Mol. Biol. 295, 777-789 (2000).
33. Hamann, C.S. & Hou, Y.M. A strategy of tRNA recognition that includes determinants of RNA structure. Bioorg. Med. Chem. 5, 1011-1019 (1997).
34. Hou, Y.M. Structural elements that contribute to an unusual tertiary interaction in a transfer RNA. Biochemistry 33, 4677-4681 (1994).
35. Christian, T., Lipman, R.S., Evilia, C. & Hou, Y.M. Alternative design of a tRNA core for aminoacylation. J. Mol. Biol. 303, 503-514 (2000).
36. Delagoutte, B., Moras, D. & Cavarelli, J. tRNA aminoacylation by arginyl-tRNA synthetase: induced conformations during substrates binding. EMBO J. 19, 5599-5610 (2000).
37. Fersht, A.R. & Dingwall, C. Cysteinyl-tRNA synthetase from Escherichia coli does not need an editing mechanism to reject serine and alanine. High energy of small groups in specific molecular interactions. Biochemistry 18, 1245-1249 (1979).
38. Zhang, C.M., Christian, T., Newberry, K.J., Perona, J.J. & Hou, Y.M. Zinc-mediated amino acid discrimination in cysteinyl-tRNA synthetase. J. Mol. Biol. 327, 911-917 (2003).
39. Zhang, C.M., Perona, J.J. & Hou, Y.M. Amino acid discrimination by a highly differentiated metal center of an aminoacyl-tRNA synthetase. Biochemistry 42, 10931-10937 (2003).
40. 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).
41. Sekine, S. et al. ATP binding by glutamyl-tRNA synthetase is switched to the productive mode by tRNA binding. EMBO J. 22, 676-688 (2003).
42. Rould, M.A., Perona, J.J., Soll, D. & Steitz, T.A. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 Å resolution. Science 246, 1135-1142 (1989).
43. Yang, X.L. et al. Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc. Natl. Acad. Sci. USA 100, 15376-15380 (2003).
44. Perona, J.J., Swanson, R.N., Rould, M.A., Steitz, T.A. & Soll, D. Structural basis for misaminoacylation by mutant E. coli glutaminyl-tRNA synthetase enzymes. Science 246, 1152-1154 (1989).
45. Doublie, S., Bricogne, G., Gilmore, C. & Carter, C.W. Jr. Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase. Structures, 17-31 (1995).
46. Pallanck, L., Li, S. & Schulman, L.H. The anticodon and discriminator base are major determinants of cysteine tRNA identity in vivo. J. Biol. Chem. 267, 7221-7223 (1992).
47. Hamann, C.S. & Hou, Y.M. Enzymatic aminoacylation of tRNA acceptor stem helices with cysteine is dependent on a single nucleotide. Biochemistry 34, 6527-6532 (1995).
48. Biou, V., Yaremchuk, A., Tukalo, M. & Cusack, S. The 2.9 Å crystal structure T. thermophilus seryl-tRNA synthetase complexed with tRNA(Ser). Science 263, 1404-1410 (1994).
49. Sekine, S. et al. Major identity determinants in the "augmented D helix" of tRNA(Gln) from Escherichia coli. J. Mol. Biol. 256, 685-700 (1996).
50. Shimada, A., Nureki, O., Goto, M., Takahashi, S. & Yokoyama, S. Structural and mutational studies of the recognition of the arginine tRNA-specific major identity element, A20, by arginyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 98, 13537-13542 (2001).
51. Sherlin, L.D. et al. Influence of transfer RNA tertiary structure on aminoacylation efficiency by glutaminyl and cysteinyl-tRNA synthetases. J. Mol. Biol. 299, 431-446 (2000).
52. Giege, R., Sissler, M. & Florentz, C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 26, 5017-5035 (1998).
53. Grodberg, J.D., Jr. OmpT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170, 1245-1258 (1988).
54. Lyakhov, D. et al. Site-specific mutagenesis of the Lys-172 residue in phage T7 RNA polymerase: characterization of the transcriptional properties of mutant proteins. Mol. Biol. 26, 679-687 (1992).
55. Newberry, K.J., Kohn, J., Hou, Y.M. & Perona, J.J. Crystallization and preliminary diffraction analysis of Escherichia coli cysteinyl-tRNA synthetase. Acta Crystallogr. D 55, 1046-1047 (1999).
56. Sherlin, L.D. et al. Chemical and enzymatic synthesis of tRNAs for high-throughput crystallization. RNA 7, 1671-1678 (2001).
57. Bullock, T.L., Uter, N., Nissan, T.A. & Perona, J.J. Amino acid discrimination by a class I aminoacyl-tRNA synthetase specified by negative determinants. J. Mol. Biol. 328, 395-408 (2003).
58. Chen, Z. & Ruffner, D.E. Modified crush-and-soak method for recovering oligodeoxynucleotides from polyacrylamide gel. Biotechniques 21, 820-822 (1996).
59. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
60. Brunger, A.T. et al. Crystallography & NMR system. A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
61. 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).
62. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta. Crystallogr. D 50, 760-763 (1994).
63. Fersht, A.R. et al. Active site titration and aminoacyl adenylate binding stoichiometry of aminoacyl-tRNA synthetases. Biochemistry 14, 1-4 (1975).