Enhanced amino acid selection in fully evolved tryptophanyl-trna synthetase, relative to its urzyme, requires domain motion sensed by the D1 switch, a remote dynamic packing motif

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 4367-4376

  Weinreb, Violetta ^a   Li, Li ^a   Chandrasekaran, Srinivas Niranj ^a   Koehl, Patrice ^b   Delarue, Marc ^c   Carter Jr , Charles W ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of California Davis   (United States)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERY; AMINOACYL TRNA SYNTHESIS; CONFORMATIONAL CHANGE; COOPERATIVITY; ENZYME MECHANISMS; MINIMUM ACTION PATH; MUTAGENESIS SITE SPECIFIC; POCKET VOLUME; THERMODYNAMICS; TRANSITION STATE;

AMINO ACID MOTIFS; AMINO ACYL-TRNA SYNTHETASES; BACTERIAL PROTEINS; CATALYSIS; GEOBACILLUS STEAROTHERMOPHILUS; PROTEIN STRUCTURE, TERTIARY; TRYPTOPHAN-TRNA LIGASE;

EID: 84894199948     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538660     Document Type: Article

References (33)

1. Perutz, M. F., Wilkinson, A. J., Paoli, M., and Dodson, G. G. (1998) The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27, 1-34
2. Perutz, M. F. (1970) Stereochemistry of cooperative effects of hemoglobin. Nature 228, 726-739
3. Weinreb, V., and Carter, C. W., Jr. (2008) Mg2-free B. stearothermophilus tryptophanyl-tRNA synthetase activates tryptophan with a major fraction of the overall rate enhancement. J. Am. Chem. Soc. 130, 1488-1494
4. Weinreb, V., Li, L., Campbell, C. L., Kaguni, L. S., and Carter, C. W., Jr. (2009) Mg2-assisted catalysis by B. stearothermophilus TrpRS is promoted by allosteric effects. Structure 17, 952-964
5. Weinreb, V., Li, L., and Carter, C. W., Jr. (2012) A master switch couples Mg2-assisted catalysis to domain motion in B. stearothermophilus tryptophanyl-tRNA synthetase. Structure 20, 128-138
6. Cammer, S., and Carter, C. W., Jr. (2010) Six rossmannoid folds, including the class I aminoacyl-tRNA synthetases, share a partial core with the anticodon-binding domain of a class II aminoacyl-tRNA synthetase. Bioinformatics 26, 709-714
7. Kapustina, M., Weinreb, V., Li, L., Kuhlman, B., and Carter, C. W., Jr. (2007) A conformational transition state accompanies tryptophan activation by B. stearothermphilus tryptophanyl-tRNA synthetase. Structure 15, 1272-1284
8. Li, L., and Carter, C. W., Jr. (2013) Full implementation of the genetic code by tryptophanyl-tRNA synthetase requires cooperativity between recently acquired structural modules. J. Biol. Chem. 288, 34736-34745
9. Praetorius-Ibba, M., Stange-Thomann, N., Kitabatake, M., Ali, K., Söll, I., Carter, C. W., Jr., Ibba, M., and Söll, D. (2000) Ancient adaptation of the active site of tryptophanyl-tRNA synthetase for tryptophan binding. Biochemistry 39, 13136-13143
10. Franklin, J., Koehl, P., Doniach, S., and Delarue, M. (2007) MinActionPath. Maximum likelihood trajectory for large-scale structural transitions in a coarse-grained locally harmonic energy landscape. Nucleic Acids Res. 35, W477-W482
11. Francklyn, C. S., First, E. A., Perona, J. J., and Hou, Y.-M. (2008) Methods for kinetic and thermodynamic analysis of aminoacyl-tRNA synthetases. Methods 44, 100-118
12. Retailleau, P., Hu, M., Vachette, P., and Carter, C. W., Jr. (2003) Interconversion ofATPbinding and conformational free energies by tryptophanyltRNA synthetase. Structures of ATP bound to open and closed, pre-transition conformations. J. Mol. Biol. 325, 39-63
13. Horovitz, A., and Fersht, A. R. (1990) Strategy for analyzing the co-operativity of intramolecular interactions in peptides and proteins. J. Mol. Biol. 214, 613-617
14. Carter, C. W., Jr. (1990) Efficient factorial designs and the analysis of macromolecular crystal growth conditions. Methods 1, 12-24
15. Weinkam, P., Pons, J., and Sali, A. (2012) Structure-based model of allostery predicts coupling between distant sites. Proc. Natl. Acad. Sci. U.S.A. 109, 4875-4880
16. Laowanapiban, P., Kapustina, M., Vonrhein, C., Delarue, M., Koehl, P., and Carter, C. W., Jr. (2009) Independent saturation of three TrpRS subsites generates a partially assembled state similar to those observed in molecular simulations. Proc Natl. Acad. Sci. U.S.A. 106, 1790-1795
17. Pham, Y., Kuhlman, B., Butterfoss, G. L., Hu, H., Weinreb, V., and Carter, C. W., Jr. (2010) Tryptophanyl-tRNA synthetase Urzyme. A model to recapitulate molecular evolution and investigate intramolecular complementation. J. Biol. Chem. 285, 38590-38601
18. Pham, Y., Li, L., Kim, A., Erdogan, O., Weinreb, V., Butterfoss, G. L., Kuhlman, B., and Carter, C. W., Jr. (2007) A minimal TrpRS catalytic domain supports sense/antisense ancestry of class I and II aminoacyltRNA synthetases. Mol. Cell 25, 851-862
19. Sadovsky, E., and Yifrach, O. (2007) Principles underlying energetic coupling along an allosteric communication trajectory of a voltage-activated K channel. Proc. Natl. Acad. Sci. U.S.A. 104, 19813-19818
20. Durrant, J. D., de Oliveira, C. A., and McCammon, J. A. (2011) POVME. An algorithm for measuring binding-pocket volumes. J. Mol. Graph. Model 29, 773-776
21. Prevost, M. S., Sauguet, L., Nury, H., Van Renterghem, C., Huon, C., Poitevin, F., Baaden, M., Delarue, M., and Corringer, P.-J. (2012) A locally closed conformation of a bacterial pentameric proton-gated ion channel. Nat. Struct. Mol. Biol. 19, 642-649
22. Lam, S. S., and Schimmel, P. R. (1975) Equilibrium measurements of cognate and noncognate interactions between aminoacyl transfer RNA synthetases and transfer RNA. Biochemistry 14, 2775-2780
23. Ebel, J. P., Giegé, R., Bonnet, J., Kern, D., Befort, N., Bollack, C., Fasiolo, F., Gangloff, J., and Dirheimer, G. (1973) Factors determining the specificity of the tRNA aminoacylation reaction non-absolute specificity of tRNAaminoacyl-tRNA synthetase recognition and particular importance of the maximal velocity. Biochimie 55, 547-557
24. Rogers, M. J., Adachi, T., Inokuchi, H., and Söll, D. (1992) Switching tRNAGln identity from glutamine to tryptophan. Proc. Natl. Acad. Sci. U.S.A. 89, 3463-3467
25. Rogers, M. J., Weygand-Durasevi, I., Schwob, E., Sherman, J. M., Rogers, K. C., Adachi, T., Inokuchi, H., and Söll, D. (1993) Selectivity and specificity in the recognition of tRNA by E. coli by glutaminyl-tRNA synthetase. Biochimie 75, 1083-1090
26. Bullock, T. L., Uter, N., Nissan, T. A., and Perona, J. J. (2003) Amino acid discrimination by a class I aminoacyl-tRNA synthetase specified by negative determinants. J. Mol. Biol. 328, 395-408
27. Bullock, T. L., Rodríguez-Hernández, A., Corigliano, E. M., and Perona, J. J. (2008) A rationally engineered misacylating aminoacyl-tRNA synthetase. Proc. Natl. Acad. Sci. U.S.A. 105, 7428-7433
28. Corigliano, E. M., and Perona, J. J. (2009) Architectural underpinnings of the genetic code for glutamine. Biochemistry 28, 676-687
29. Ibba, M., Kast, P., and Hennecke, H. (1994) Substrate specificity is determined by amino acid binding pocket size in Escherichia coli phenylalanyltRNA synthetase. Biochemistry 33, 7107-7112
30. Chin, J. W., Cropp, T. A., Anderson, J. C., Mukherji, M., Zhang, Z., and Schultz, P. G. (2003) An expanded eukaryotic genetic code. Science 301, 964-967
31. Liu, C. C., and Schultz, P. G. (2010) Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79, 413-444
32. Wang, L., Brock, A., Herberich, B., and Schultz, P. G. (2001) Expanding the genetic code of Escherichia coli. Science 292 498-500
33. del Sol, A., Fujihashi, H., Amoros, D., and Nussinov, R. (2006) Residues crucial for maintaining short paths in network communication mediate signaling in proteins. Mol. Syst. Biol. 2, 2006.0019