The crystal structure of the ternary complex of phenylalanyl-tRNA synthetase with tRNAPhe and a phenylalanyl-adenylate analogue reveals a conformational switch of the CCA end

Biochemistry

Volumn 45, Issue 35, 2006, Pages 10572-10583

  Moor, Nina ^b   Kotik Kogan, Olga ^a   Tworowski, Dmitry ^a   Sukhanova, Maria ^b   Safro, Mark ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; CRYSTAL STRUCTURE; DATA ACQUISITION; PROTEINS; RNA; TOPOLOGY;

INTRA-RNA INTERACTIONS; PHENYLALANYL-ADENYLATE ANALOGUE; PHENYLALANYL-TRNA SYNTHETASE;

ENZYME KINETICS;

ADENOSINE PHOSPHATE; CARBON; PHENYLALANINE DERIVATIVE; PHENYLALANINE TRANSFER RNA; PHENYLALANINE TRANSFER RNA LIGASE; RIBOSE; TETRAMER;

AMINOACYLATION; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA ANALYSIS; RNA BINDING; RNA STRUCTURE; STRUCTURE ANALYSIS; THERMUS THERMOPHILUS;

ADENOSINE MONOPHOSPHATE; BINDING SITES; CRYSTALLIZATION; MODELS, MOLECULAR; PHENYLALANINE-TRNA LIGASE; PROTEIN STRUCTURE, TERTIARY; RNA, TRANSFER, PHE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 33748277245     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060491l     Document Type: Article

References (57)

1. Eriani, G., Delarue, M., Poch, O., Gangloff, J., and Moras, D. (1990) Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs, Nature 347, 203-206.
2. Cusack, S., Berthet-Colominas, C., Härtlein, M., Nassar, N., and Leberman, R. (1990) A second class of synthetase structure revealed by X-ray analysis of E. coli seryl-tRNA synthetase at 2.5 Å resolution, Nature 347, 249-255.
3. Fraser, T. H., and Rich, A. (1975) Amino acids are not all initially attached to the same position on transfer RNA molecules, Proc. Natl. Acad. Sci. U.S.A. 72, 3044-3048.
4. Sprinzl, M., and Cramer, F. (1975) Site of aminoacylation of tRNAs from E. coli with respect to the 2′- or 3′-hydroxyl group of the terminal adenosine, Proc. Natl. Acad. Sci. U.S.A. 72, 3049-3053.
5. First, E. A. (2005) Catalysis of the tRNA aminoacylation reaction, in The Aminoacyl-tRNA Synthetases (Ibba, M., Francklyn, C., and Cusack, S., Eds.) pp 328-347, Landes Bioscience, Georgetown, TX.
6. Arnez, J. G., and Moras, D. (1997) Structural and functional considerations of the aminoacylation reaction, Trends Biochem. Sci. 22, 211-216.
7. Cusack, S. (1997) Aminoacyl-tRNA synthetases, Curr. Opin. Struct. Biol. 7, 881-889.
8. Giegé, R., Sissler, M., and Florentz, C. (1998) Universal rules and idiosyncratic features in tRNA identity, Nucleic Acids Res. 26, 5017-5035.
9. Cavarelli, J., Eriani, G., Rees, B., Ruff, M., Boeglin, M., Mitschler, A., Martin, F., Gangloff, J., Thierry, J.-C., and Moras, D. (1994) The active site of yeast aspartyl-tRNA synthetase: Structural and functional aspects of the aminoacylation reaction, EMBO J. 15, 327-337.
10. Asp-complexed enzyme by structural changes in the catalytic site, hinge region, and anticodon-binding domain, J. Mol. Biol. 299, 1313-1324.
11. Asp in Escherichia coli: A snapshot of the second step, EMBO J. 18, 6532-6541.
12. Rees, B., Webster, G., Delarue, M., Boeglin, M., and Moras, D. (2000) Aspartyl-tRNA synthetase from Escherichia coli: Flexibility and adaptability to the substrates, Mol. Biol. 23, 1157-1164.
13. Asp by aspartyl-tRNA synthetase, J. Mol. Biol. 299, 1051-1060.
14. Ser and a seryl-adenylate analogue reveals a conformational switch in the active site, EMBO J. 15, 2834-2842.
15. Torres-Larios, A., Sankaranarayanan, R., Rees, B., Dock-Bregeon, A.-C., and Moras, D. (2003) Conformational movements and cooperativity upon amino acid, ATP and tRNA binding in threonyl-tRNA synthetase, J. Mol. Biol. 331, 201-211.
16. Yaremchuk, A., Tukalo, M., Grøtli, M., and Cusack, S. (2001) A succession of substrate induced conformational changes ensures the amino acid specificity of Thermus thermophilus prolyl-tRNA synthetase: Comparison with histidyl-tRNA synthetase, J. Mol. Biol. 309, 989-1002.
17. Lys transcript: Anticodon recognition and conformational changes upon binding of a lysyl-adenylate analogue, EMBO J. 15, 6321-6334.
18. Desogus, G., Todone, F., Brick, P., and Onesti, S. (2000) Active site of lysyl-tRNA synthetase: Structural studies of the adenylation reaction, Biochemistry 39, 8418-8425.
19. Berthet-Colominas, C., Seignovert, L., Hartlein, M., Grøtli, M., Cusack, S., and Leberman, R. (1998) The crystal structure of asparaginyl-tRNA synthetase from Thermus thermophilus and its complexes with ATP and asparaginyl-adenylate: The mechanism of discrimination between asparagine and aspartic acid, EMBO J. 17, 2947-2960.
20. Rath, V. L., Silvian, L. F., Beijer, B., Sproat, B. S., and Steitz, T. A. (1998) How glutaminyl-tRNA synthetase selects glutamine, Structure 6, 439-449.
21. Delagoutte, B., Moras, D., and Cavarelli, J. (2000) tRNA amino-acylation by arginyl-tRNA-synthetase: Induced conformations during substrates binding, EMBO J. 19, 5599-5610.
22. Sekine, S., Nureki, O., Dubois, D. Y., Bernier, S., Chênevert, R., Lapointe, J., Vassylyev, D. G., and Yokoyama, S. (2003) ATP binding by glutamyl-tRNA synthetase is switched to the productive mode by tRNA binding, EMBO J. 22, 676-688.
23. Mosyak, L., Reshetnikova, L., Goldgur, Y., Delarue, M., and Safro, M. (1995) Structure of phenylalanyl-tRNA synthetase from Thermus thermophilus, Nat. Struct. Biol. 2, 537-547.
24. Phe, Structure 5, 59-68.
25. Reshetnikova, L., Moor, N., Lavrik, O., and Vassylyev, D. (1999) Crystal structures of phenylalanyl-tRNA synthetase complexed with phenylalanine and a phenylalanyl-adenylate analogue, J. Mol. Biol. 287, 555-568.
26. Fishman, R., Ankilova, V., Moor, N., and Safro, M. (2001) Structure at 2.6 Å resolution of phenylalanyl-tRNA synthetase complexed with phenylalanyl-adenylate in the presence of manganese, Acta Crystallogr. D57, 1534-1544.
27. Kotik-Kogan, O., Moor, N., Tworowski, D., and Safro, M. (2005) Structural basis for discrimination of L-phenylalanine from L-tyrosine by phenylalanyl-tRNA synthetase, Structure 13, 1799-1807.
28. Safro, M., Moor, N., and Lavrik, O. (2004) Phenylalanyl-tRNA synthetase, in The Aminoacyl-tRNA synthetases (Ibba, M., Francklyn, C., and Cusack, S., Eds.) pp 250-265, Landes Bioscience, Georgetown, TX.
29. Vasil'eva, I., Ankilova, V., Lavrik, O., and Moor, N. (2002) tRNA discrimination by T. thermophilus phenylalanyl-tRNA synthetase at the binding step, J. Mol. Recognit. 15, 188-196.
30. Phe transcripts from Thermus thermophilus HB8 with homologous phenylalanyl-tRNA synthetase reveals a novel mode of interaction, Nucleic Acids Res. 23, 4598-4602.
31. Phe nucleotides contacting the subunits of Thermus thermophilus phenylalanyl-tRNA synthetase by affinity crosslinking, Biochim. Biophys. Acta 1518, 226-236.
32. Phe, Biochemistry (Moscow) 65, 1157-1166.
33. Phe acceptor end by phenylalanyl-tRNA synthetase, Biochemistry (Moscow) 69, 179-191.
34. Phe CCA end, Biochemistry 42, 10697-10708.
35. Ankilova, V., Reshetnikova, L., Chernaya, M., and Lavrik, O. (1988) Phenylalanyl-tRNA synthetase from Thermus thermophilus HB8. Purification and properties of the crystallizing enzyme, FEBS Lett. 227, 9-13.
36. Watanabe, K., Oshima, T., Iijima, K., Yamaizumi, Z., and Nishimura, S. (1980) Purification and thermal stability of several amino acid-specific tRNAs from an extreme thermophile, Thermus thermophilus HB8, J. Biochem. 87, 1-13.
37. Bischoff, R., and McLaughlin, L. W. (1985) Isolation of specific tRNAs using an ionic-hydrophobic mixed-mode chromatographic matrix, Anal. Biochem. 151, 526-533.
38. Lavrik, O., Moor, N., and Nevinskii, G. (1978) Synthesis of analogs of L-phenylalanyladenylate and study of their interactions with E. coli phenylalanyl-tRNA synthetase, Bioorg. Khim. 4, 1470-1487.
39. Phe, J. Mol. Biol. 231, 927-929.
40. Otwinowski, Z., and Minor, W. (1996) Processing of X-ray diffraction data collected processing in oscillation mode, Methods Enzymol. 276, 307-326.
41. Brunger, A., Adams, P., Clore, G., DeLano, W., Gros, P., Grosse-Kunstleve, R., Jiang, J., Kuszewski, J., Nigles, M., Pannu, N., Read, R., Rice, L., Simonson, T., and Warren, G. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
42. Jones, T., Zou, J., Cowtan, S., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
43. Berendsen, H., van der Spoel, D., and van Drunen, R. (1995) GROMACS: A message-passing parallel molecular dynamic implementation, Comput. Phys. Commun. 91, 43-56.
44. Lindahl, E., Hess, B., and van der Spoel, D. (2001) GROMACS 3.0: A package for molecular simulation and trajectory analysis, J. Mol. Model. 7, 306-317.
45. van Gunsteren, W., Billeter, S., Eising, A., Hunenberger, P., Kruger, P., Mark, A., Scott, W., and Tironi, I. (1996) Biomolecular Simulation: The GROMOS96 Manual and User Guide, Hochshulverlag AG an der ETH, Zurich, Switzerland.
46. Schüttelkopf, A. W., and van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes, Acta Crystallogr. D60, 1355-1363.
47. Phe by phenylalanyl-tRNA synthetase of Thermus thermophilus, Eur. J. Biochem. 234, 897-902.
48. Shi, H., and Moore, P. B. (2000) The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: A classic structure revisited, RNA 6, 1091-1105.
49. 2+ in 15-year old crystals. J. Mol. Biol. 301, 401-414.
50. +-C base-pair and by pseudouridine, J. Mol. Biol. 285, 115-131.
51. Asp upon binding to aspartyl-tRNA synthetase, Biochimie 78, 624-631.
52. Pro anticodon recognition by Thermus thermophilus prolyl-tRNA synthetase, Structure 6, 101-108.
53. Auffinger, P., and Westhof, E. (2001) An extended structural signature for the tRNA anticodon loop, RNA 7, 334-341.
54. Ma, J. C., and Dougherty, D. A. (1997) The cation-π interaction, Chem. Rev. 97, 1303-1324.
55. Phe do not abolish their acceptor activity, FEBS Lett. 351, 241-242.
56. Krauss, G., von der Haar, F., and Maass, G. (1979) Conformational transitions of a tRNA-aminoacyl-tRNA synthetase complex induced by tRNAs bearing different modifications in the 3′ terminus, Biochemistry 18, 4755-4761.
57. Belrhali, H., Yaremchuk, A., Tukalo, M., Larsen, K., Berthet-Colominas, C., Leberman, R., Beijer, B., Sproat, B., Als-Nielsen, J., Grübel, G., Legrand, J. F., Lehmann, M., and Cusack, S. (1994) Crystal structures at 2.5 angstrom resolution of seryl-tRNA synthetase complexed with two analogs of seryl adenylate, Science 263, 1432-1436.