GTPase Mechanisms and functions of translation factors on the ribosome

Biological Chemistry

Volumn 381, Issue 5-6, 2000, Pages 377-387

  Rodnina, Marina V ^a   Stark, Holger ^b   Savelsbergh, Andreas ^a   Wieden, Hans Joachim ^a   Mohr, Dagmar ^a   Matassova, Natalia B ^a,d   Peske, Frank ^a   Daviter, Tina ^a   Gualerzi, Claudio O ^c   Wintermeyer, Wolfgang ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF CAMERINO   (Italy)

^d INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

Author keywords

Cryo electron microscopy; Initiation of translation; Motor protein; Phosphate release; Rapid kinetics; Translocation

Indexed keywords

AMINOACYL TRANSFER RNA; ELONGATION FACTOR G; ELONGATION FACTOR TU; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 2; PEPTIDYLTRANSFERASE; PHOSPHATE; RIBOSOME PROTEIN; ELONGATION FACTOR;

BINDING SITE; CODON; COMPLEX FORMATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME MECHANISM; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; RIBOSOME; RNA TRANSPORT; TRANSLATION INITIATION; METABOLISM; PROTEIN SYNTHESIS;

GTP PHOSPHOHYDROLASES; PEPTIDE ELONGATION FACTORS; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 0033624169     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.2000.050     Document Type: Review

References (73)

1. Abel, K., Yoder, M.D., Hilgenfeld, R., and Jurnak, F. (1996). An α to β conformational switch in EF-Tu. Structure 4, 1153-1159.
2. Abrahamson, J.K., Laue, T.M., Miller, D.L., and Johnson, A.E. (1985). Direct determination of the association constant between elongation factor Tu-GTP and aminoacyl-tRNA using fluorescence. Biochemistry 24, 692-700.
3. Ævarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, 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.
4. Agrawal, R.K., Penczek, P., Grassucci, R.A., and 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.
5. 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. Nature Struct. Biol. 6, 643-647.
6. Al-Karadaghi, S., Ævarsson, A., Garber, M., Zheltonosova, J., and Liljas, A. (1996). Thestructure of elongation factor G in complex with GDP: conformational flexibility and nucleotide exchange. Structure 4, 555-565.
7. 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.
8. Ban, N., Nissen, P., Hansen, J., Capel, M., Moore, P.B., and Steitz, T.A. (1999). Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit. Nature 400, 841-847.
9. Berchtold, H., Reshetnikova, L., Reiser, C.O., Schirmer, N.K., Sprinzl, M., and Hilgenfeld, R. (1993). Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365, 126-132.
10. Bourne, H.R., Sanders, D.A., and McCormick, F. (1990). The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348, 125-132.
11. Bourne, H.R., Sanders, D.A., and McCormick, F. (1991). The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127.
12. Brock, S., Szkaradkiewicz, K., and Sprinzl, M. (1998). Initiation factors of protein biosynthesis in bacteria and their structural relationship to elongation and termination factors. Mol. Microbiol. 29, 409-417.
13. Cate, J.H., Yusupov, M.M., Yusupova, G.Z., Earnest, T.N., and Noller, H.F. (1999). X-ray crystal structures of 70S ribosome functional complexes. Science 285, 2095-2104.
14. iα1 and the mechanism of GTP hydrolysis. Science 265, 1405-1412.
15. 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.
16. Czworkowski, J., and Moore, P.B. (1997). The conformational properties of elongation factor G and the mechanism of translocation. Biochemistry 36, 10327-10334.
17. Dell, V.A., Miller, D.L., and Johnson, A.E. (1990). Effects of nucleotide-and aurodox-induced changes in elongation factor Tu conformation upon its interactions with aminoacyl transfer RNA. A fluorescence study. Biochemistry 29, 1757-1763.
18. Eccleston, J.F., Dix, D.B., and Thompson, R.C. (1985). The rate of cleavage of GTP on the binding of Phe-tRNA-elongation factor Tu-GTP to poly(U)-programmed ribosomes of Escherichia coli. J. Biol. Chem. 260, 16237-16241.
19. Fourmy, D., Recht, M.I., Blanchard, S.C., and Puglisi, J.D. (1996). Structure of the A site of Escherichia coli 16S RNA complexed with an aminoglycoside antibiotic. Science 274, 1367-1371.
20. Fourmy, D., Yoshizawa, S., and Puglisi, J.D. (1998). Paromomycin binding induces a local conformational change in the A-site of 16 S rRNA. J. Mol. Biol. 277, 333-345.
21. Goldberg, J. (1999). Structural and functional analysis of the ARF1 -ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 96, 893-902.
22. Gualerzi, C.O., Brandi, L., Caserta, E., La Teana, A., Spurio, R., Tomšic, J., and Pon, C.L. (2000). Translation initiation in bacteria. In: The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions, R.A. Garrett, S.R. Douthwaite, A. Liljas, A.-T. Matheson, P.B. Moore and H.F. Noller, eds. (Washington, D.C., USA: ASM Press), pp. 477-494.
23. Hilgenfeld, R. (1995). How do the GTPases really work? Nature Struct. Biol. 2, 3-6.
24. Ito, K., Ebihara, K., Uno, M., and Nakamura, Y. (1996). Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: tRNA-protein mimicry hypothesis. Proc. Natl. Acad. Sci. USA 93, 5443-5448.
25. Kaziro, Y. (1978). The role of guanosine 5′-triphosphate in polypeptide chain elongation. Biochim. Biophys. Acta 505, 95-127.
26. Kjeldgaard, M., and Nyborg, J. (1992). Refined structure of elongation factor EF-Tu from Escherichia coli. J. Mol. Biol. 223, 721-742.
27. Kjeldgaard, M., Nissen, P., Thirup, S., and Nyborg, J. (1993). The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1, 35-50.
28. Liljas, A. (1996). Protein synthesis: imprinting through molecular mimicry. Curr. Biol. 6, 247-263.
29. Lodmell, J.S., and Dahlberg, A.E. (1997). A conformational switch in Escherichia coli 16S ribosomal RNA during decoding of messenger RNA. Science 277, 1262-1267.
30. Moazed, D., Robertson, J.M., and Noller, H.F. (1988). Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334, 362-364.
31. Moore, P.B. (1995). Molecular mimicry in protein synthesis? Science 270, 1453-1454.
32. Nakamura, Y., Ito, K., and lsaksson, L.A. (1996). Emerging understanding of translation termination. Cell 87, 147-150.
33. Phe, EF-Tu, and a GTP analog. Science 270, 1464-1472.
34. Nissen, P., Thirup, S., Kjeldgaard, M., and Nyborg, J. (1999). The crystal structure of Cys-tRNACys-EF-Tu-GDPNP reveals general and specific features in the ternary complex and in tRNA. Structure 7, 143-156.
35. Nixon, A.E., Brune, M., Lowe, P.N., and Webb, M.R. (1995). Kinetics of inorganic phosphate release during the interaction of p21ras with the GTPase-activating proteins, p120-GAP and neurofibromin. Biochemistry 34, 15592-15598.
36. Nyborg, J., Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., Clark, B.F., and Reshetnikova, L. (1997). Macromolecular mimicry in protein biosynthesis. Fold. Des. 2, 7-11.
37. O'Connor, M., Brunelli, C.A., Firpo, M.A., Gregory, S.T., Lieberman, K.R., Lodmell, J.S., Moine, H., Van Ryk, D.I., and Dahlberg, A.E. (1995). Genetic probes of ribosomal RNA function. Biochem. Cell Biol. 73, 859-868.
38. Ott, G., Faulhammer, H.G., and Sprinzl, M. (1989). Interaction of elongation factor Tu from Escherichia coli with aminoacyl-tRNA carrying a fluorescent reporter group on the 3' terminus. Eur. J. Biochem. 184, 345-352.
39. Pape, T., Wintermeyer, W., and Rodnina, M.V. (1998). Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. EMBO J. 17, 7490-7497.
40. Pape, T., Wintermeyer, W., and Rodnina, M.V. (1999). Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J. 18, 3800-3807.
41. Pape, T., Wintermeyer, W., and Rodnina, M.V. (2000). Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome. Nature Struct. Biol. 7, 104-107.
42. Parmeggiani, A., and Sander, G. (1981). Properties and regulation of the GTPase activities of elongation factors Tu and G, and of initiation factor 2. Mol. Cell Biochem. 35, 129-158.
43. Piepenburg, O., Pape, T., Pleiss, J.A., Wintermeyer, W., Uhlenbeck, O., and Rodnina, M.V. (2000). Intact aminoacyl-tRNA is required to trigger GTP hydrolysis by elongation factor Tu on the ribosome. Biochemistry 39, 1734-1738.
44. Polekhina, G., Thirup, S., Kjeldgaard, M., Nissen, P., Lippmann, C., and Nyborg, J. (1996). Helix unwinding in the effector region of elongation factor EF-Tu-GDP. Structure 4, 1141-1151.
45. Powers, T., and Noller, H.F. (1993). Evidence for functional interaction between elongation factor Tu and 16S ribosomal RNA. Proc. Natl. Acad. Sci. USA. 90, 1364-1368.
46. Rittinger, K., Walker, P.A., Eccleston, J.F., Nurmahomed, K., Owen, D., Laue, E., Gamblin, S.J., and Smerdon, S.J. (1997a). Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP. Nature 388, 693-697.
47. Rittinger, K., Walker, P.A., Eccleston, J.F., Smerdon, S.J., and Gamblin, S.J. (1997b). Structure at 1.65 Å of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389, 758-762.
48. Rodnina, M.V., Fricke, R., and Wintermeyer, W. (1994). Transient conformational states of aminoacyl-tRNA during ribosome binding catalyzed by elongation factor Tu. Biochemistry 33, 12267-12275.
49. Rodnina, M.V., Fricke, R., Kuhn, L., and Wintermeyer, W. (1995a). Codon-dependent conformational change of elongation factor Tu preceding GTP hydrolysis on the ribosome. EMBO J. 14, 2613-2619.
50. Rodnina, M.V., Pape, T., Fricke, R., and Wintermeyer, W. (1995b). Elongation factor Tu, a GTPase triggered by codon recognition on the ribosome: mechanism and GTP consumption. Biochem. Cell Biol. 73, 1221-1227.
51. Rodnina, M.V., Pape, T., Fricke, R., Kuhn, L., and Wintermeyer, W. (1996). Initial binding of the elongation factor Tu-GTP·aminoacyl-tRNA complex preceding codon recognition on the ribosome. J. Biol. Chem. 271, 646-652.
52. 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.
53. Rodnina, M.V., Savelsbergh, A., Matassova, N.B., Katunin, V.I., Semenkov, Y.P., and Wintermeyer, W. (1999a). Thiostrepton inhibits turnover but not GTP hydrolysis by elongation factor G on the ribosome. Proc. Natl. Acad. Sci. USA 96, 9586-9590.
54. Rodnina, M.V., Savelsbergh, A., and Wintermeyer, W. (1999b). Dynamics of translation on the ribosome: molecular mechanics of translocation. FEMS Microbiol. Rev. 23, 317-333.
55. 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.
56. Scheffzek, K., Ahmadian, M.R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997). The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338.
57. 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.
58. -4. Nature 372, 276-279.
59. Spurio, R., Brandi, L.E.C., Pon, C., Gualerzi, C.O., Misselwitz, R., Krafft, C., Welfle, K., and Welfle, H. (2000). The C-terminal subdomain (IF2 C-2) contains the entire fMet-tRNA binding site of initiation factor IF2. J. Biol. Chem. 275, 2447-2454.
60. Stark, H., Orlova, E.V., Rinke-Appel, J., Jünke, N., Mueller, F., Rodnina, M.V., Wintermeyer, W., Brimacombe, R., and van Heel, M. (1997a). Arrangement of tRNAs in pre-and post-translocational ribosomes revealed by electron cryomicroscopy. Cell 88, 19-28.
61. Stark, H., Rodnina, M.V., Rinke-Appel, J., Brimacombe, R., Wintermeyer, W., and van Heel, M. (1997b). Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389, 403-406.
62. 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 changes of the ribosome during translocation. Cell 100, 301-309.
63. Stöffler, G., Cundliffe, E., Stöffler-Meilicke, M., and Dabbs, E.R. (1980). Mutants of Escherichia coli lacking ribosomal protein L11. J. Biol. Chem. 255, 10517-10522.
64. Tapprich, W.E., and Dahlberg, A.E. (1990). A single base mutation at position 2661 in E. coli 23S ribosomal RNA affects the binding of ternary complex to the ribosome. EMBO J. 9, 2649-2655.
65. iα1: stabilization of the transition state for GTP hydrolysis. Cell 89, 251-261.
66. Ting, T.D., and Ho, Y.K. (1991). Molecular mechanism of GTP hydrolysis by bovine transducin: pre-steady-state kinetic analyses. Biochemistry 30, 8996-9007.
67. Tomšic, J., Vitali, L.A., Daviter, T., Savelsbergh, A., Spurio, R., Striebeck, P., Wintermeyer, W., Rodnina, M.V., and Gualerzi, C.O. (2000). Late events of translation initiation in bacteria: a kinetic analysis. EMBO J., in press.
68. Traut, R.R., Dey, D., Bochkariov, D.E., Oleinikov, A.V., Jokhadze, G.G., Hamman, B., and Jameson, D. (1995). Location and domain structure of Escherichia coli ribosomal protein L7/L12: site specific cysteine cross-linking and attachment of fluorescent probes. Biochem. Cell Biol. 73, 949-958.
69. Vale, R.D. (1996). Switches, latches and amplifiers: common themes of G proteins and molecular motors. J. Cell Biol. 135, 291-302.
70. Wahl, M.C., Bourenkov, G.P., Bartunik, H.D., and Huber, R. (2000). Flexibility, conformational diversity, and two dimerization modes in complexes of ribosomal protein L12. EMBO J. 19, 174-186.
71. Wittinghofer, F. (1998). Ras signalling - caught in the act of the switch-on. Nature 394, 317.
72. Yarus, M., and Smith, D. (1995). tRNA on the ribosome: a waggle theory. In: tRNA: Structure, Biosynthesis, and Function, D. Söll and U. RajBhandary, eds. (Washington, D.C., USA: American Society for Microbiology), pp. 443-468.
73. Zeidler, W., Egle, C., Ribeiro, S., Wagner, A., Katunin, V., Kreutzer, R., Rodnina, M., Wintermeyer, W., and Sprinzl, M. (1995). Site-directed mutagenesis of Thermus thermophilus elongation factor Tu. Replacement of His85, Asp81 and Arg300. Eur. J. Biochem. 229, 596-604.