A bacterial elongation factor G homologue exclusively functions in ribosome recycling in the spirochaete Borrelia burgdorferi

Molecular Microbiology

Volumn 75, Issue 6, 2010, Pages 1445-1454

  Suematsu, Takuma ^a   Yokobori, Shin Ichi ^b   Morita, Hiroyuki ^c   Yoshinari, Shigeo ^a   Ueda, Takuya ^c   Kita, Kiyoshi ^a   Takeuchi, Nono ^c   Watanabe, Yoh Ichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR G; ELONGATION FACTOR G1; ELONGATION FACTOR G2; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 3; RIBOSOME RECYCLING FACTOR; TRANSFER RNA; UNCLASSIFIED DRUG; BACTERIAL DNA; RIBOSOME PROTEIN;

ARTICLE; BORRELIA BURGDORFERI; DISSOCIATION; HUMAN; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; RECYCLING; RIBOSOME; RNA TRANSLATION; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; SPIROCHAETA;

BORRELIA BURGDORFERI; CLUSTER ANALYSIS; DNA, BACTERIAL; GUANOSINE TRIPHOSPHATE; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE ELONGATION FACTOR G; PHYLOGENY; PROKARYOTIC INITIATION FACTOR-3; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77949404662     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07067.x     Document Type: Article

References (53)

1. Barat, C., Datta, P.P., Raj, V.S., Sharma, M.R., Kaji, H., Kaji, A., and Agrawal, R.K. (2007) Progression of the ribosome recycling factor through the ribosome dissociates the two ribosomal subunits. Mol Cell 27: 250-261.
2. Bhargava, K., Templeton, P., and Spremulli, L. (2004) Expression and characterization of isoform 1 of human mitochondrial elongation factor G. Protein Expr Purif 37: 368-376.
3. 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.
4. Burgdorfer, W., Barbour, A.G., Hayes, S.F., Benach, J.L., Grunwaldt, E., and Davis, J.P. (1982) Lyme disease-a tickborne spirochetosis? Science 216: 1317-1319.
5. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
6. Connell, S.R., Takemoto, C., Wilson, D.N., Wang, H., Murayama, K., Terada, T., et al. (2007) Structural basis for interaction of the ribosome with the switch regions of GTPbound elongation factors. Mol Cell 25: 751-764.
7. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
8. Frank, J., Gao, H., Sengupta, J., Gao, N., and Taylor, D.J. (2007) The process of mRNA-tRNA translocation. Proc Natl Acad Sci USA 104: 19671-19678.
9. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
10. Gao, N., Zavialov, A.V., Ehrenberg, M., and Frank, J. (2007) Specific interaction between EF-G and RRF and its implication for GTP-dependent ribosome splitting into subunits. J Mol Biol 374: 1345-1358.
11. 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 G trapped in the posttranslocational state. Science 326: 694-699.
12. Girbes, T., Cabrer, B., and Modolell, J. (1979) Preparation and assay of purified Escherichia coli polysomes devoid of free ribosomal subunits and endogenous GTPase activities. Methods Enzymol 59: 353-362.
13. Grunberg-Manago, M., Dessen, P., Pantaloni, D., Godefroy-Colburn, T., Wolfe, A.D., and Dondon, J. (1975) Lightscattering studies showing the effect of initiation factors on the reversible dissociation of Escherichia coli ribosomes. J Mol Biol 94: 461-478.
14. Hammarsund, M., Wilson, W., Corcoran, M., Merup, M., Einhorn, S., Grander, D., and Sangfelt, O. (2001) Identification and characterization of two novel human mitochondrial elongation factor genes, hEFG2 and hEFG1, phylogenetically conserved through evolution. Hum Genet 109: 542-550.
15. Hayashi, K., and Kojima, C. (2008) pCold-GST vector: a novel cold-shock vector containing GST tag for soluble protein production. Protein Expr Purif 62: 120-127.
16. 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.
17. Hirashima, A., and 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.
18. Hirokawa, G., Kiel, M.C., Muto, A., Selmer, M., Raj, V.S., Liljas, A., et al. (2002) Post-termination complex disassembly by ribosome recycling factor, a functional tRNA mimic. EMBO J 21: 2272-2281.
19. Hirokawa, G., Nijman, R.M., Raj, V.S., Kaji, H., Igarashi, K., and Kaji, A. (2005) The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits. RNA 11: 1317-1328.
20. Hirokawa, G., Iwakura, N., Kaji, A., and Kaji, H. (2008) The role of GTP in transient splitting of 70S ribosomes by RRF (ribosome recycling factor) and EF-G (elongation factor G). Nucleic Acids Res 36: 6676-6687.
21. Hunfeld, K.P., Weigand, J., Wichelhaus, T.A., Kekoukh, E., Kraiczy, P., and Brade, V. (2001) In vitro activity of mezlocillin, meropenem, aztreonam, vancomycin, teicoplanin, ribostamycin and fusidic acid against Borrelia burgdorferi. Int J Antimicrob Agents 17: 203-208.
22. 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 tRNAmimicry domains. Mol Cell 9: 1263-1272.
23. Jobb, G., von Haeseler, A., and Strimmer, K. (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4: 18.
24. 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.
25. Kaempfer, R. (1972) Initiation factor IF-3: a specific inhibitor of ribosomal subunit association. J Mol Biol 71: 583-598.
26. 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.
27. Katunin, V.I., Savelsbergh, A., Rodnina, M.V., and Wintermeyer, W. (2002) Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome. Biochemistry 41: 12806-12812.
28. Komoda, T., Sato, N., Phelps, S., Namba, N., Joseph, S., and Suzuki, T. (2006) The a-site finger in 23 S rRNA acts as a functional attenuator for translocation. J Biol Chem 281: 32303-32309.
29. Le, S.Q., and Gascuel, O. (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307-1320.
30. Lee-Huang, S., Lee, H., and Ochoa, S. (1974) Inhibition of polypeptide chain initiation in Escherichia coli by elongation factor G. Proc Natl Acad Sci USA 71: 2928-2931.
31. Margus, T., Remm, M., and Tenson, T. (2007) Phylogenetic distribution of translational GTPases in bacteria. BMC Genomics 8: 15.
32. Moazed, D., and Noller, H.F. (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature 342: 142-148.
33. Nishizuka, Y., and Lipmann, F. (1966) The interrelationship between guanosine triphosphatase and amino acid polymerization. Arch Biochem Biophys 116: 344-351.
34. Nyborg, J., Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., and Clark, B.F. (1996) Structure of the ternary complex of EF-Tu: macromolecular mimicry in translation. Trends Biochem Sci 21: 81-82.
35. 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.
36. 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.
37. Rodnina, M., Savelsbergh, A., Katunin, V., and Wintermeyer, W. (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385: 37-41.
38. Ronquist, F., and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
39. Savelsbergh, A., Matassova, N.B., Rodnina, M.V., and Wintermeyer, W. (2000) Role of domains 4 and 5 in elongation factorGfunctions on the ribosome. J Mol Biol 300: 951-961.
40. 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.
41. 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.
42. Savelsbergh, A., Rodnina, M.V., and Wintermeyer, W. (2009) Distinct functions of elongation factor G in ribosome recycling and translocation. RNA 15: 772-780.
43. Seo, H.S., Abedin, S., Kamp, D., Wilson, D.N., Nierhaus, K.H., and Cooperman, B.S. (2006) EF-G-dependent GTPase on the ribosome. conformational change and fusidic acid inhibition. Biochemistry 45: 2504-2514.
44. Seshadri, A., and Varshney, U. (2006) Mechanism of recycling of post-termination ribosomal complexes in eubacteria: a new role of initiation factor 3. J Biosci 31: 281-289.
45. Seshadri, A., Samhita, L., Gaur, R., Malshetty, V., and Varshney, U. (2009) Analysis of the fusA2 locus encoding EFG2 in Mycobacterium smegmatis. Tuberculosis (Edinb) 89: 453-464.
46. Shimizu, Y., Inoue, A., Tomari, Y., Suzuki, T., Yokogawa, T., Nishikawa, K., and Ueda, T. (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19: 751-755.
47. Singh, N.S., Das, G., Seshadri, A., Sangeetha, R., and Varshney, U. (2005) Evidence for a role of initiation factor 3 in recycling of ribosomal complexes stalled on mRNAs in Escherichia coli. Nucleic Acids Res 33: 5591-5601.
48. Tanaka, N., Kinoshita, T., and Masukawa, H. (1968) Mechanism of protein synthesis inhibition by fusidic acid and related antibiotics. Biochem Biophys Res Commun 30: 278-283.
49. Terasaki, M., Suzuki, T., Hanada, T., and Watanabe, K. (2004) Functional compatibility of elongation factors between mammalian mitochondrial and bacterial ribosomes: characterization of GTPase activity and translation elongation by hybrid ribosomes bearing heterologous L7/12 proteins. J Mol Biol 336: 331-342.
50. Tsuboi, M., Morita, H., Nozaki, Y., Akama, K., Ueda, T., Ito, K., et al. (2009) EF-G2mt is an exclusive recycling factor in mammalian mitochondrial protein synthesis. Mol Cell 35: 502-510.
51. Yang, Z. (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39: 306-314.
52. Zavialov, A.V., Hauryliuk, V.V., and Ehrenberg, M. (2005a) Guanine-nucleotide exchange on ribosome-bound elongation factor G initiates the translocation of tRNAs. J Biol 4: 9.
53. Zavialov, A.V., Hauryliuk, V.V., and Ehrenberg, M. (2005b) Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G. Mol Cell 18: 675-686.