Staphylococcus aureus elongation factor G - Structure and analysis of a target for fusidic acid

FEBS Journal

Volumn 277, Issue 18, 2010, Pages 3789-3803

  Chen, Yang ^a   Koripella, Ravi Kiran ^a   Sanyal, Suparna ^a   Selmer, Maria ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

antibiotic resistance; crystallography; elongation factor G (EF G); fusidic acid; switch region

Indexed keywords

BACTERIAL PROTEIN; ELONGATION FACTOR G; FUSIDIC ACID;

ARTICLE; CRYSTAL STRUCTURE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE; RIBOSOME; STAPHYLOCOCCUS AUREUS; THERMUS THERMOPHILUS;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS; THERMUS THERMOPHILUS;

EID: 77956316251     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07780.x     Document Type: Article

References (49)

1. Schmeing TM Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature 461, 1234 1242.
2. Steitz TA (2008) A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol 9, 242 253.
3. Shoji S, Walker SE Fredrick K (2009) Ribosomal translocation: one step closer to the molecular mechanism. ACS Chem Biol 4, 93 107.
4. Wintermeyer W, Savelsbergh A, Semenkov YP, Katunin VI Rodnina MV (2001) Mechanism of elongation factor G function in tRNA translocation on the ribosome. Cold Spring Harb Symp Quant Biol 66, 449 458.
5. Hirashima A Kaji A (1973) Role of elongation factor G and a protein factor on the release of ribosomes from messenger ribonucleic acid. J Biol Chem 248, 7580 7587.
6. Peske F, Rodnina MV Wintermeyer W (2005) Sequence of steps in ribosome recycling as defined by kinetic analysis. Mol Cell 18, 403 412.
7. Zavialov AV, Hauryliuk VV Ehrenberg M (2005) Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G. Mol Cell 18, 675 686.
8. Mohr D, Wintermeyer W Rodnina MV (2002) GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41, 12520 12528.
9. Helgstrand M, Mandava CS, Mulder FA, Liljas A, Sanyal S Akke M (2007) The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J Mol Biol 365, 468 479.
10. Rodnina MV, Savelsbergh A, Katunin VI Wintermeyer W (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37 41.
11. Savelsbergh A, Rodnina MV Wintermeyer W (2009) Distinct functions of elongation factor G in ribosome recycling and translocation. RNA 15, 772 780.
12. Czworkowski J, Wang J, Steitz TA Moore PB (1994) The crystal structure of elongation factor G complexed with GDP, at 2.7 angstrom resolution. EMBO J 13, 3661 3668.
13. Aevarsson A, Brazhnikov E, Garber M, Zheltonosova J, Chirgadze Y, Al-Karadaghi S, Svensson LA Liljas A (1994) Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J 13, 3669 3677.
14. Hansson S, Singh R, Gudkov AT, Liljas A Logan DT (2005) Structural insights into fusidic acid resistance and sensitivity in EF-G. J Mol Biol 348, 939 949.
15. Hansson S, Singh R, Gudkov AT, Liljas A Logan DT (2005) Crystal structure of a mutant elongation factor G trapped with a GTP analogue. FEBS Lett 579, 4492 4497.
16. Laurberg M, Kristensen O, Martemyanov K, Gudkov AT, Nagaev I, Hughes D 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.
17. Vetter IR Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294, 1299 1304.
18. Connell SR, Takemoto C, Wilson DN, Wang H, Murayama K, Terada T, Shirouzu M, Rost M, Schuler M, Giesebrecht J et al. (2007) Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol Cell 25, 751 764.
19. Agrawal RK, Penczek P, Grassucci RA Frank J (1998) Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc Natl Acad Sci USA 95, 6134 6138.
20. Stark H, Rodnina MV, Wieden HJ, van Heel M Wintermeyer W (2000) Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100, 301 309.
21. Agrawal RK, Linde J, Sengupta J, Nierhaus KH Frank J (2001) Localization of L11 protein on the ribosome and elucidation of its involvement in EF-G-dependent translocation. J Mol Biol 311, 777 787.
22. Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC Ramakrishnan V (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694 699.
23. Czworkowski J Moore PB (1997) The conformational properties of elongation factor G and the mechanism of translocation. Biochemistry 36, 10327 10334.
24. Hauryliuk V, Mitkevich VA, Eliseeva NA, Petrushanko IY, Ehrenberg M Makarov AA (2008) The pretranslocation ribosome is targeted by GTP-bound EF-G in partially activated form. Proc Natl Acad Sci USA 105, 15678 15683.
25. Bodley JW, Zieve FJ, Lin L Zieve ST (1969) Formation of the ribosome-G factor-GDP complex in the presence of fusidic acid. Biochem Biophys Res Commun 37, 437 443.
26. Lannergard J, Norstrom T Hughes D (2009) Genetic determinants of resistance to fusidic acid among clinical bacteremia isolates of Staphylococcus aureus. Antimicrob Agents Chemother 53, 2059 2065.
27. Norstrom T, Lannergard J 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.
28. Ticu C, Nechifor R, Nguyen B, Desrosiers M Wilson KS (2009) Conformational changes in switch I of EF-G drive its directional cycling on and off the ribosome. EMBO J 28, 2053 2065.
29. Jorgensen R, Ortiz PA, Carr-Schmid A, Nissen P, Kinzy TG Andersen GR (2003) Two crystal structures demonstrate large conformational changes in the eukaryotic ribosomal translocase. Nat Struct Biol 10, 379 385.
30. Al Karadaghi S, Aevarsson A, Garber M, Zheltonosova J Liljas A (1996) The structure of elongation factor G in complex with GDP: conformational flexibility and nucleotide exchange. Structure 4, 555 565.
31. Polekhina G, Thirup S, Kjeldgaard M, Nissen P, Lippmann C Nyborg J (1996) Helix unwinding in the effector region of elongation factor EF-Tu-GDP. Structure 4, 1141 1151.
32. Kjeldgaard M, Nissen P, Thirup S Nyborg J (1993) The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1, 35 50.
33. Liljas A, Kristensen O, Laurberg M, Al-Karadaghi S, Gudkov A, Martemyanov K, Hughes D Nagaev I (2000) The states, conformational dynamics, and fusidic acid-resistant mutants of elongation factor G. In The Ribosome: Structure, Function, Antibiotics and Cellular Interactions (Garrett RA, Douthwaite SR, Liljas A, Matheson AT, Moore PB Noller HF eds pp. 359 365. ASM Press, Washington, DC.
34. Johanson U Hughes D (1994) Fusidic acid-resistant mutants define three regions in elongation factor G of Salmonella typhimurium. Gene 143, 55 59.
35. Nagaev I, Bjorkman J, Andersson DI Hughes D (2001) Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol Microbiol 40, 433 439.
36. Martemyanov KA, Liljas A, Yarunin AS Gudkov AT (2001) Mutations in the G-domain of elongation factor G from Thermus thermophilus affect both its interaction with GTP and fusidic acid. J Biol Chem 276, 28774 28778.
37. Li JJ, Venkataramana M, Wang AQ, Sanyal S, Janson JC Su ZG (2005) A mild hydrophobic interaction chromatography involving polyethylene glycol immobilized to agarose media refolding recombinant Staphylococcus aureus elongation factor G. Protein Expr Purif 40, 327 335.
38. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26, 795 800.
39. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658 674.
40. Emsley P Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126 2132.
41. Perrakis A, Morris R Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6, 458 463.
42. Brunger AT (2007) Version 1.2 of the Crystallography and NMR system. Nat Protoc 2, 2728 2733.
43. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54, 905 921.
44. Murshudov GN, Vagin AA Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240 255.
45. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760 763.
46. Kleywegt GJ (1999) Experimental assessment of differences between related protein crystal structures. Acta Crystallogr D Biol Crystallogr 55, 1878 1884.
47. Jones TA, Zou J-Y, Cowan SW 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.
48. Diederichs K Karplus PA (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 4, 269 275.
49. Richter Dahlfors AA Kurland CG (1990) Novel mutants of elongation factor G. J Mol Biol 215, 549 557.