Mechanism of elongation factor-G-mediated fusidic acid resistance and fitness compensation in Staphylococcus aureus

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30257-30267

  Koripella, Ravi Kiran ^a   Chen, Yang ^a   Peisker, Kristin ^a   Koh, Cha San ^a   Selmer, Maria ^a   Sanyal, Suparna ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; CONFORMATIONAL DYNAMICS; DOUBLE MUTANTS; FAST KINETICS; FUSIDIC ACID; GTP HYDROLYSIS; HYDROPHOBIC CORE; INTER-DOMAIN; KEY RESIDUES; PATHOGENIC BACTERIUM; S. AUREUS; STAPHYLOCOCCUS AUREUS; WILD TYPES;

ACID RESISTANCE; ANTIBIOTICS; BACTERIA; DROPS; HYDROLYSIS; MACROMOLECULES;

HEALTH;

ELONGATION FACTOR G; FUSIDIC ACID; GUANOSINE TRIPHOSPHATE; ISOLEUCINE; LEUCINE; METHIONINE; MUTANT PROTEIN; PEPTIDE TRANSFER RIBONUCLEIC ACID; PHENYLALANINE; TRANSFER RNA; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; FITNESS COMPENSATION; HYDROPHOBICITY; KINETICS; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RIBOSOME; RNA TRANSPORT; SENSITIVITY ANALYSIS; STAPHYLOCOCCUS AUREUS; WILD TYPE;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; FUSIDIC ACID; GUANOSINE TRIPHOSPHATE; MUTATION, MISSENSE; PEPTIDE ELONGATION FACTOR G; RIBOSOMES; RNA, BACTERIAL; RNA, TRANSFER; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 84865777571     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.378521     Document Type: Article

References (51)

1. Björkman, J., and Andersson, D. I. (2000) The cost of antibiotic resistance from a bacterial perspective. Drug Resist. Updat. 3, 237-245
2. Johanson, U., Aevarsson, A., Liljas, A., and Hughes, D. (1996) The dynamic structure of EF-G studied by fusidic acid resistance and internal revertants. J. Mol. Biol. 258, 420-432
3. Levin, B. R., Perrot, V., and Walker, N. (2000) Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154, 985-997
4. Nagaev, I., Björkman, J., Andersson, D. I., and Hughes, D. (2001) Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol. Microbiol. 40, 433-439
5. Brown, E. M., and Thomas, P. (2002) Fusidic acid resistance in Staphylococcus aureus isolates. Lancet 359, 803
6. Bodley, J. W., Zieve, F. J., Lin, L., and Zieve, S. T. (1969) Formation of the ribosome-G factor-GDP complex in the presence of fusidic acid. Biochem. Biophys. Res. Commun. 37, 437-443
7. Savelsbergh, A., Rodnina, M. V., and Wintermeyer, W. (2009) Distinct functions of elongation factor G in ribosome recycling and translocation. RNA 15, 772-780
8. Willie, G. R., Richman, N., Godtfredsen, W. P., and Bodley, J. W. (1975) Some characteristics of and structural requirements for the interaction of 24,25-dihydrofusidic acid with ribosome-elongation factor g complexes. Biochemistry 14, 1713-1718
9. Pavlov, M. Y., Antoun, A., Lovmar, M., and Ehrenberg, M. (2008) Complementary roles of initiation factor 1 and ribosome recycling factor in 70S ribosome splitting. EMBO J. 27, 1706-1717
10. Savelsbergh, A., Mohr, D., Kothe, U., Wintermeyer, W., and Rodnina, M. V. (2005) Control of phosphate release from elongation factor G by ribosomal protein L7/12. EMBO J. 24, 4316-4323
11. Guo, X., Peisker, K., Bäckbro, K., Chen, Y., Koripella, R. K., Mandava, C. S., Sanyal, S., and Selmer, M. (2012) Structure and function of FusB. An elongation factor G-binding fusidic acid resistance protein active in ribosomal translocation and recycling. Open Biol. 2, 120016
12. Agrawal, R. K., Heagle, A. B., Penczek, P., Grassucci, R. A., and Frank, J. (1999) EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat. Struct. Biol. 6, 643-647
13. Gao, Y. G., Selmer, M., Dunham, C. M., Weixlbaumer, A., Kelley, A. C., and Ramakrishnan, V. (2009) The structure of the ribosome with elongation factor Gtrapped in the posttranslocational state. Science 326, 694-699
14. Mohr, D., Wintermeyer, W., and Rodnina, M. V. (2002) GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41, 12520-12528
15. Stark, H., Rodnina, M. V., Wieden, H. J., van Heel, M., and Wintermeyer, W. (2000) Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100, 301-309
16. Connell, S. R., Takemoto, C., Wilson, D. N., Wang, H., Murayama, K., Terada, T., Shirouzu, M., Rost, M., Schüler, M., Giesebrecht, J., Dabrowski, M., Mielke, T., Fucini, P., Yokoyama, S., and Spahn, C. M. (2007) Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol. Cell 25, 751-764
17. Rodnina, M. V., Savelsbergh, A., Katunin, V. I., and Wintermeyer, W. (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37-41
18. Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M., and Frank, J. (2003) Locking and unlocking of ribosomal motions. Cell 114, 123-134
19. Ticu, C., Murataliev, M., Nechifor, R., and Wilson, K. S. (2011) A central interdomain protein joint in elongation factor G regulates antibiotic sensitivity, GTP hydrolysis, and ribosome translocation. J. Biol. Chem. 286, 21697-21705
20. Laurberg, M., Kristensen, O., Martemyanov, K., Gudkov, A. T., Nagaev, I., Hughes, D., and Liljas, A. (2000) Structure of a mutant EF-G reveals domain III and possibly the fusidic acid binding site. J. Mol. Biol. 303, 593-603
21. Martemyanov, K. A., Liljas, A., Yarunin, A. S., and Gudkov, A. T. (2001) Mutations in the G-domain of elongation factorGfrom Thermus thermophilus affect both its interaction with GTP and fusidic acid. J. Biol. Chem. 276, 28774-28778
22. Chen, Y., Koripella, R. K., Sanyal, S., and Selmer, M. (2010) Staphylococcus aureus elongation factor G. Structure and analysis of a target for fusidic acid. FEBS J. 277, 3789-3803
23. Huang, C., Mandava, C. S., and Sanyal, S. (2010) The ribosomal stalk plays a key role in IF2-mediated association of the ribosomal subunits. J. Mol. Biol. 399, 145-153
24. Mandava, C. S., Peisker, K., Ederth, J., Kumar, R., Ge, X., Szaflarski, W., and Sanyal, S. (2012) Bacterial ribosome requires multiple L12 dimers for efficient initiation and elongation of protein synthesis involving IF2 and EF-G. Nucleic Acids Res. 40, 2054-2064
25. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800
26. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
27. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
28. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
29. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
30. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
31. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680
32. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119
33. Khade, P. K., and Joseph, S. (2011) Messenger RNA interactions in the decoding center control the rate of translocation. Nat. Struct. Mol. Biol. 18, 1300-1302
34. Munro, J. B., Wasserman, M. R., Altman, R. B., Wang, L., and Blanchard, S. C. (2010) Correlated conformational events in EF-G and the ribosome regulate translocation. Nat. Struct. Mol. Biol. 17, 1470-1477
35. Rodnina, M. V., and Wintermeyer, W. (2011) The ribosome as a molecular machine. The mechanism of tRNA-mRNA movement in translocation. Biochem. Soc. Trans. 39, 658-662
36. Karimi, R., Pavlov, M. Y., Buckingham, R. H., and Ehrenberg, M. (1999) Novel roles for classical factors at the interface between translation termination and initiation. Mol. Cell 3, 601-609
37. Peske, F., Rodnina, M. V., and Wintermeyer, W. (2005) Sequence of steps in ribosome recycling as defined by kinetic analysis. Mol. Cell 18, 403-412
38. Zavialov, A. V., Hauryliuk, V. V., and Ehrenberg, M. (2005) Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G. Mol. Cell 18, 675-686
39. Savelsbergh, A., Mohr, D., Wilden, B., Wintermeyer, W., and Rodnina, M. V. (2000) Stimulation of the GTPase activity of translation elongation factor G by ribosomal protein L7/12. J. Biol. Chem. 275, 890-894
40. AEvarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., al-Karadaghi, S., Svensson, L. A., and Liljas, A. (1994) Three-dimensional structure of the ribosomal translocase. Elongation factor G from Thermus thermophilus. EMBO J. 13, 3669-3677
41. Czworkowski, J., Wang, J., Steitz, T. A., and Moore, P. B. (1994) The crystal structure of elongation factor G complexed with GDP, at 2.7 A resolution. EMBO J. 13, 3661-3668
42. Hansson, S., Singh, R., Gudkov, A. T., Liljas, A., and Logan, D. T. (2005) Crystal structure of a mutant elongation factor G trapped with a GTP analogue. FEBS Lett. 579, 4492-4497
43. Hansson, S., Singh, R., Gudkov, A. T., Liljas, A., and Logan, D. T. (2005) Structural insights into fusidic acid resistance and sensitivity in EF-G. J. Mol. Biol. 348, 939-949
44. Johanson, U., and Hughes, D. (1994) Fusidic acid-resistant mutants define three regions in elongation factor G of Salmonella typhimurium. Gene 143, 55-59
45. Norström, T., Lannergård, J., and Hughes, D. (2007) Genetic and phenotypic identification of fusidic acid-resistant mutants with the small-colony- variant phenotype in Staphylococcus aureus. Antimicrob. Agents Chemother. 51, 4438-4446
46. Ratje, A. H., Loerke, J., Mikolajka, A., Brünner, M., Hildebrand, P. W., Starosta, A. L., Dönhöfer, A., Connell, S. R., Fucini, P., Mielke, T., Whitford, P. C., Onuchic, J. N., Yu, Y., Sanbonmatsu, K. Y., Hartmann, R. K., Penczek, P. A., Wilson, D. N., and Spahn, C. M. (2010) Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468, 713-716
47. Frank, J., and Agrawal, R. K. (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318-322
48. Li, M., Li, F., Shen, R., and Guo, X. (2011) Molecular dynamics study of the structures and properties of RDX/GAP propellant. J. Hazard Mater. 186, 2031-2036
49. Chen, C., Stevens, B., Kaur, J., Cabral, D., Liu, H., Wang, Y., Zhang, H., Rosenblum, G., Smilansky, Z., Goldman, Y. E., and Cooperman, B. S. (2011) Single-molecule fluorescence measurements of ribosomal translocation dynamics. Mol. Cell 42, 367-377
50. Frank, J., and Gonzalez, R. L., Jr. (2010) Structure and dynamics of a processive Brownian motor. The translating ribosome. Annu. Rev. Biochem. 79, 381-412
51. Johansson, M., Ieong, K. W., Trobro, S., Strazewski, P., Åqvist, J., Pavlov, M. Y., and Ehrenberg, M. (2011) pH-sensitivity of the ribosomal peptidyl transfer reaction dependent on the identity of the A-site aminoacyl-tRNA. Proc. Natl. Acad. Sci. U.S.A. 108, 79-84