Kinetics and thermodynamics of RRF, EF-G, and thiostrepton interaction on the Escherichia coli ribosome

Biochemistry

Volumn 43, Issue 40, 2004, Pages 12728-12740

  Seo, Hyuk Soo ^a   Kiel, Michael ^a   Pan, Dongli ^a   Raj, V Samuel ^a   Kaji, Akira ^a   Cooperman, Barry S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ESCHERICHIA COLI; PROTEINS; REACTION KINETICS; SYNTHESIS (CHEMICAL); THERMODYNAMICS;

ELONGATION; RIBOSOME RECYCLING FACTOR (RRF);

BIOCHEMISTRY;

BACTERIAL PROTEIN; ELONGATION FACTOR G; RIBOSOME RECYCLING FACTOR; THIOSTREPTON; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; DISSOCIATION; ESCHERICHIA COLI; ISOMERIZATION; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; QUANTITATIVE ANALYSIS; RIBOSOME; THERMODYNAMICS;

COUMARINS; ESCHERICHIA COLI; KINETICS; NUCLEOTIDES; PEPTIDE ELONGATION FACTOR G; PROTEIN BINDING; PROTEINS; RIBOSOMAL PROTEINS; RIBOSOMES; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS; THIOSTREPTON;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 4944227490     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048927p     Document Type: Article

References (47)

1. Bashan, A., Agmon, I., Zarivach, R., Schluenzen, F., Harms, J., Berisio, R., Bartels, H., Franceschi, F., Auerbach, T., Hansen, H. A., Kossoy, E., Kessler, M., and Yonath, A. (2003) Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression, Mol. Cell 11, 91-102.
2. Frank, J. (2003) Electron microscopy of functional ribosome complexes, Biopolymers 68, 223-233.
3. Moore, P. B., and Steitz, T. A. (2003) The structural basis of large ribosomal subunit function, Annu. Rev. Biochem. 72, 813-850.
4. Ramakrishnan, V. (2002) Ribosome structure and the mechanism of translation, Cell 108, 557-572.
5. Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H., and Noller, H. F. (2001) Crystal structure of the ribosome at 5.5 Å resolution, Science 292, 883-896.
6. Rodnina, M. V., Daviter, T., Gromadski, K., and Wintermeyer, W. (2002) Structural dynamics of ribosomal RNA during decoding on the ribosome, Biochimie 84, 745-754.
7. Cassataro, J., Delpino, M. V., Velikovsky, C. A., Bruno, L., Fossati, C. A., and Baldi, P. C. (2002) Diagnostic usefulness of antibodies against ribosome recycling factor from Brucella melitensis in human or canine brucellosis, Clin. Diagn. Lab. Immunol. 9, 366-369.
8. Cassataro, J., Velikovsky, C. A., Giambartolomei, G. H., Estein, S., Bruno, L., Cloeckaert, A., Bowden, R. A., Spitz, M., and Fossati, C. A. (2002) Immunogenicity of the Brucella melitensis recombinant ribosome recycling factor-homologous protein and its cDNA, Vaccine 20, 1660-1669.
9. Hirokawa, G., Kiel, M. C., Muto, A., Kawai, G., Igarashi, K., Kaji, H., and Kaji, A. (2002) Binding of ribosome recycling factor to ribosomes, comparison with tRNA, J. Biol. Chem. 277, 35847-35852.
10. Hirokawa, G., Kiel, M. C., Muto, A., Selmer, M., Raj, V. S., Liljas, A., Igarashi, K., Kaji, H., and Kaji, A. (2002) Post-termination complex disassembly by ribosome recycling factor, a functional tRNA mimic, EMBO J. 21, 2272-2281.
11. Ito, K., Fujiwara, T., Toyoda, T., and Nakamura, Y. (2002) Elongation factor G participates in ribosome disassembly by interacting with ribosome recycling factor at their tRNA-mimicry domains, Mol. Cell 9, 1263-1272.
12. Janosi, L., Mottagui-Tabar, S., Isaksson, L. A., Sekine, Y., Ohtsubo, E., Zhang, S., Goon, S., Nelken, S., Shuda, M., and Kaji, A. (1998) Evidence for in vivo ribosome recycling, the fourth step in protein biosynthesis, EMBO J. 17, 1141-1151.
13. Janosi, L., Mori, H., Sekine, Y., Abragan, J., Janosi, R., Hirokawa, G., and Kaji, A. (2000) Mutations influencing the frr gene coding for ribosome recycling factor (RRF), J. Mol. Biol. 295, 815-829.
14. 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.
15. Kiel, M. C., Raj, V. S., Kaji, H., and Kaji, A. (2003) Release of ribosome-bound ribosome recycling factor by elongation factor G, J. Biol. Chem. 278, 48041-48050.
16. Rao, A. R., and Varshney, U. (2001) Specific interaction between the ribosome recycling factor and the elongation factor G from Mycobacterium tuberculosis mediates peptidyl-tRNA release and ribosome recycling in Escherichia coli, EMBO J. 20, 2977-2986.
17. Vizcaino, N., Cloeckaert, A., Dubray, G., and Zygmunt, M. S. (1996) Cloning, nucleotide sequence, and expression of the gene coding for a ribosome releasing factor-homologous protein of Brucella melitensis, Infect. Immun. 64, 4834-4837.
18. Hirashima, A., and Kaji, A. (1972) Factor-dependent release of ribosomes from messenger RNA. Requirement for two heat-stable factors, J. Mol. Biol. 65, 43-58.
19. Kaji, A., Kiel, M. C., Hirokawa, G., Muto, A., Inokuchi, Y., and Kaji, H. (2001) The fourth step of protein synthesis, disassembly of the post-termination complex is catalyzed by elongation factor G and ribosome recycling factor, RRF, a near perfect mimic of tRNA, in Cold Spring Harbor Symposia on Quantitative Biology, The Ribosome, pp 515-529, Cold Spring Harbor Laboratory Press, Plainview, NY.
20. Rodnina, M. V., and Wintermeyer, W. (1995) GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs, Proc. Natl. Acad. Sci. U.S.A. 92, 1945-1949.
21. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
22. Wilson, K. S., and Noller, H. F. (1998) Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing, Cell 92, 131-139.
23. Rohrbach, M. S., Bodley, J. W., and Mann, K. G. (1975) Chemical and physical studies on the structure of Escherichia coli elongation factor G, J. Biol. Chem. 250, 6831-6836.
24. Deng, H. Y., Odom, O. W., and Hardesty, B. (1986) Localization of L11 on the Escherichia coli ribosome by singlet-singlet energy transfer, Eur. J. Biochem. 156, 497-503.
25. Lakowicz, J. R. (1999) Principles of fluorescence spectroscopy, 2nd ed., Kluwer Academic/Plenum Press, New York.
26. Fersht, A. (1999) Structure and mechanism in protein science, a guide to enzyme catalysis and protein folding, W. H. Freeman & Company, New York.
27. Ellman, G. L. (1958) A colorimetric method for determining low concentrations of mercaptans, Arch. Biochem. Biophys. 74, 443-450.
28. Nakano, H., Yoshida, T., Uchiyama, S., Kawachi, M., Matsuo, H., Kato, T., Ohshima, A., Yamaichi, Y., Honda, T., Kato, H., Yamagata, Y., Ohkubo, T., and Kobayashi, Y. (2003) Structure and binding mode of a ribosome recycling factor (RRF) from mesophilic bacterium, J. Biol. Chem. 278, 3427-3436.
29. Baca, O. G., Rohrbach, M. S., and Bodley, J. W. (1976) Equilibrium measurements of the interactions of guanine nucleotides with Escherichia coli elongation factor G and the ribosome, Biochemistry 15, 4570-4574.
30. Rodnina, M. V., Savelsbergh, A., Matassova, N. B., Katunin, V. I., Semenkov, Y. P., and Wintermeyer, W. (1999) Thiostrepton inhibits the turnover but not the GTPase of elongation factor G on the ribosome, Proc. Natl. Acad. Sci. U.S.A. 96, 9586-9590.
31. Agrawal, A. K., Sharma, M. R., Kiel, M. C., Hirokawa, G., Booth, T. M., Spahn, C. M. T., Grassucci, R. A., Kaji, A., and Frank, J. (2004) Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications. Proc. Natl. Acad. Sci. U.S.A. 101, 8900-8905.
32. Cameron, D. M., Thompson, J., Gregory, S. T., March, P. E., and Dahlberg, A. E. (2004) Thiostrepton-resistant mutants of Thermus thermophilus, Nucleic Acids Res. 32, 3220-3227.
33. Selmer, M., Al-Karadaghi, S., Hirokawa, G., Kaji, A., and Liljas, A. (1999) Crystal structure of Thermotoga maritima ribosome recycling factor, a tRNA mimic, Science 286, 2349-2352.
34. 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.
35. 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 Å resolution, EMBO J. 13, 3661-3668.
36. Gordon, J. (1970) Regulation of the in vivo synthesis of the polypeptide chain elongation factors in Escherichia coli, Biochemistry 9, 912-917.
37. Lambert, J. M., Boileau, G., Howe, J. G., and Traut, R. R. (1983) Levels of ribosomal protein S1 and elongation factor G in the growth cycle of Escherichia coli, J. Bacteriol. 154, 1323-1328.
38. Caldas, T., Laalami, S., and Richarme, G. (2000) Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2, J. Biol. Chem. 275, 855-860.
39. Andersen, L. D., Moreno, J. M., Clark, B. F., Mortensen, K. K., and Sperling-Petersen, H. U. (1999) Immunochemical determination of cellular content of translation release factor RF4 in Escherichia coli, IUBMB Life 48, 283-286.
40. 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.
41. Frank, J., and Agrawal, R. K. (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation, Nature 406, 318-322.
42. Savelsbergh, A., Katunin, V. I., Mohr, D., Peske, F., Rodnina, M. V., and Wintermeyer, W. (2003) An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation, Mol. Cell 11, 1517-1523.
43. Bremer, H., and Dennis, P. P. (1996) Modulation of chemical composition and other parameters of the cell by growth rate, in Escherichia coli and Salmonella (Neidhart, F. C., Ed.) 2nd ed., Vol. 2, pp 1553-1569, ASM Press, Washington, DC.
44. Pavlov, M. Y., Freistroffer, D. V., MacDougall, J., Buckingham, R. H., and Ehrenberg, M. (1997) Fast recycling of Escherichia coli ribosomes requires both ribosome recycling factor (RRF) and release factor RF3, EMBO J. 16, 4134-4141.
45. Lancaster, L., Kiel, M. C., Kaji, A., and Noller, H. F. (2002) Orientation of ribosome recycling factor in the ribosome from directed hydroxyl radical probing, Cell 111, 129-140.
46. Noller, H. F., Yusupov, M. M., Yusupova, G. Z., Baucom, A., and Cate, J. H. (2002) Translocation of tRNA during protein synthesis, FEBS Lett. 514, 11-16.
47. Cameron, D. M., Thompson, J., March, P. E., and Dahlberg, A. E. (2002) Initiation factor IF2, thiostrepton and micrococcin prevent the binding of elongation factor G to the Escherichia coli ribosome, J. Mol. Biol. 319, 27-35.