Progression of the Ribosome Recycling Factor through the Ribosome Dissociates the Two Ribosomal Subunits

Molecular Cell

Volumn 27, Issue 2, 2007, Pages 250-261

  Barat, Chandana ^a   Datta, Partha P ^a   Raj, V Samuel ^b   Sharma, Manjuli R ^a   Kaji, Hideko ^c   Kaji, Akira ^b   Agrawal, Rajendra K ^a,d  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

RNA

Indexed keywords

ELONGATION FACTOR G; GUANOSINE TRIPHOSPHATE; RIBOSOME RECYCLING FACTOR;

ARTICLE; DEACETYLATION; ELECTRON MICROSCOPY; ESCHERICHIA COLI; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RIBOSOME;

BINDING SITES; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MACROMOLECULAR SUBSTANCES; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PEPTIDE ELONGATION FACTOR G; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, BACTERIAL; RNA, TRANSFER;

ESCHERICHIA COLI;

EID: 34447331273     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.06.005     Document Type: Article

References (52)

1. Agrawal R.K., Penczek P., Grassucci R.A., and Frank J. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl. Acad. Sci. USA 95 (1998) 6134-6138
2. Agrawal R.K., Heagle A.B., Penczek P., Grassucci R.A., and Frank J. EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat. Struct. Biol. 6 (1999) 643-647
3. Agrawal R.K., Penczek P., Grassucci R.A., Burkhardt N., Nierhaus K.H., and Frank J. Effect of buffer conditions on the position of tRNA on the 70S ribosome as visualized by cryo-electron microscopy. J. Biol. Chem. 274 (1999) 8723-8729
4. Agrawal R.K., Sharma M.R., Kiel M.C., Hirokawa G., Booth T.M., Spahn C.M., Grassucci R.A., Kaji A., and Frank J. Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications. Proc. Natl. Acad. Sci. USA 101 (2004) 8900-8905
5. Bottcher B., Wynne S.A., and Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386 (1997) 88-91
6. Carson M. Ribbons 2.0. J. Appl. Cryst. 24 (1991) 103-106
7. Dallas A., and Noller H.F. Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol. Cell 8 (2001) 855-864
8. Datta P.P., Sharma M.R., Qi L., Frank J., and Agrawal R.K. Interaction of the G′ domain of elongation factor G and the C-terminal domain of ribosomal protein L7/L12 during translocation as revealed by cryo-EM. Mol. Cell 20 (2005) 723-731
9. Frank J., and Agrawal R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406 (2000) 318-322
10. Frank J., and Agrawal R.K. Ratchet-like movements between the two ribosomal subunits: their implications in elongation factor recognition and tRNA translocation. Cold Spring Harb. Symp. Quant. Biol. 66 (2001) 67-75
11. Frank J., Penczek P., Agrawal R.K., Grassucci R.A., and Heagle A.B. Three-dimensional cryoelectron microscopy of ribosomes. Methods Enzymol. 317 (2000) 276-291
12. Gabashvili I.S., Agrawal R.K., Spahn C.M., Grassucci R.A., Svergun D.I., Frank J., and Penczek P. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100 (2000) 537-549
13. Gao N., Zavialov A.V., Li W., Sengupta J., Valle M., Gursky R.P., Ehrenberg M., and Frank J. Mechanism for the disassembly of the posttermination complex inferred from cryo-EM studies. Mol. Cell 18 (2005) 663-674
14. Hainfeld J.F. A small gold-conjugated antibody label: improved resolution for electron microscopy. Science 236 (1987) 450-453
15. Hirashima A., and Kaji A. Factor-dependent release of ribosomes from messenger RNA. Requirement for two heat-stable factors. J. Mol. Biol. 65 (1972) 43-58
16. Hirashima A., and Kaji A. Role of elongation factor G and a protein factor on the release of ribosomes from messenger ribonucleic acid. J. Biol. Chem. 248 (1973) 7580-7587
17. Hirokawa G., Kiel M.C., Muto A., Kawai G., Igarashi K., Kaji H., and Kaji A. Binding of ribosome recycling factor to ribosomes-comparison with tRNA. J. Biol. Chem. 277 (2002) 35847-35852
18. Hirokawa G., Kiel M.C., Muto A., Selmer M., Raj V.S., Liljas A., Igarashi K., Kaji H., and Kaji A. Post-termination complex disassembly by ribosome recycling factor, a functional tRNA mimic. EMBO J. 21 (2002) 2272-2281
19. Hirokawa G., Nijman R.M., Raj V.S., Kaji H., Igarashi K., and Kaji A. The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits. RNA 11 (2005) 1317-1328
20. Hirokawa G., Demeshkina N., Iwakura N., Kaji H., and Kaji A. The ribosome-recycling step: consensus or controversy?. Trends Biochem. Sci. 31 (2006) 143-149
21. Ichikawa S., and Kaji A. Molecular cloning and expression of ribosome releasing factor. J. Biol. Chem. 264 (1989) 20054-20059
22. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
23. Kaji A., Kiel M.C., Hirokawa G., Muto A.R., Inokuchi Y., and Kaji H. The fourth step of protein synthesis: disassembly of the posttermination complex is catalyzed by elongation factor G and ribosome recycling factor, a near-perfect mimic of tRNA. Cold Spring Harb. Symp. Quant. Biol. 66 (2001) 515-529
24. Karimi R., Pavlov M.Y., Buckingham R.H., and Ehrenberg M. Novel roles for classical factors at the interface between translation termination and initiation. Mol. Cell 3 (1999) 601-609
25. Kiel M.C., Raj V.S., Kaji H., and Kaji A. Release of ribosome-bound ribosome recycling factor by elongation factor G. J. Biol. Chem. 278 (2003) 48041-48050
26. Kikkawa M., Okada Y., and Hirokawa N. 15 Å resolution model of the monomeric kinesin motor, KIF1A. Cell 100 (2000) 241-252
27. Kim K.K., Min K., and Suh S.W. Crystal structure of the ribosome recycling factor from Escherichia coli. EMBO J. 19 (2000) 2362-2370
28. Lancaster L., Kiel M.C., Kaji A., and Noller H.F. Orientation of ribosome recycling factor in the ribosome from directed hydroxyl radical probing. Cell 111 (2002) 129-140
29. Met and fitting of L1 protein. J. Mol. Biol. 280 (1998) 103-116
30. Nakano H., Yoshida T., Uchiyama S., Kawachi M., Matsuo H., Kato T., Ohshima A., Yamaichi Y., Honda T., Kato H., et al. Structure and binding mode of a ribosome recycling factor (RRF) from mesophilic bacterium. J. Biol. Chem. 278 (2003) 3427-3436
31. Orlova E.V., Dube P., Harris J.R., Beckman E., Zemlin F., Markl J., and van Heel M. Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å resolution by electron cryomicroscopy and angular reconstitution. J. Mol. Biol. 271 (1997) 417-437
32. Penczek P.A., Grassucci R.A., and Frank J. The ribosome at improved resolution: new techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles. Ultramicroscopy 53 (1994) 251-270
33. Penczek P.A., Zhu J., Schroder R., and Frank J. Three-dimensional reconstruction with contrast transfer function compensation from defocus series. Scanning Microsc. 11 (1997) 147-154
34. Peske F., Rodnina M.V., and Wintermeyer W. Sequence of steps in ribosome recycling as defined by kinetic analysis. Mol. Cell 18 (2005) 403-412
35. Raj V.S., Kaji H., and Kaji A. Interaction of RRF and EF-G from E. coli and T. thermophilus with ribosomes from both origins-insight into the mechanism of the ribosome recycling step. RNA 11 (2005) 275-284
36. Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell 108 (2002) 557-572
37. Rao A.R., and Varshney U. 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 (2001) 2977-2986
38. Safer D. Undecagold cluster labeling of proteins at reactive cysteine residues. J. Struct. Biol. 127 (1999) 101-105
39. Saikrishnan K., Kalapala S.K., Varshney U., and Vijayan M. X-ray structural studies of Mycobacterium tuberculosis RRF and a comparative study of RRFs of known structure. Molecular plasticity and biological implications. J. Mol. Biol. 345 (2005) 29-38
40. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (2005) 827-834
41. Selmer M., Al-Karadaghi S., Hirokawa G., Kaji A., and Liljas A. Crystal structure of Thermotoga maritima ribosome recycling factor: a tRNA mimic. Science 286 (1999) 2349-2352
42. Selmer M., Dunham C.M., Murphy IV F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., and Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942
43. Seo H.S., Kiel M., Pan D., Raj V.S., Kaji A., and Cooperman B.S. Kinetics and thermodynamics of RRF, EF-G, and thiostrepton interaction on the Escherichia coli ribosome. Biochemistry 43 (2004) 12728-12740
44. Singh N.S., Das G., Seshadri A., Sangeetha R., and Varshney U. Evidence for a role of initiation factor 3 in recycling of ribosomal complexes stalled on mRNAs in Escherichia coli. Nucleic Acids Res. 33 (2005) 5591-5601
45. Toyoda T., Tin O.F., Ito K., Fujiwara T., Kumasaka T., Yamamoto M., Garber M.B., and Nakamura Y. Crystal structure combined with genetic analysis of the Thermus thermophilus ribosome recycling factor shows that a flexible hinge may act as a functional switch. RNA 6 (2000) 1432-1444
46. Valle M., Sengupta J., Swami N.K., Grassucci R.A., Burkhardt N., Nierhaus K.H., Agrawal R.K., and Frank J. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 21 (2002) 3557-3567
47. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., and Frank J. Locking and unlocking of ribosomal motions. Cell 114 (2003) 123-134
48. Wagenknecht T., Grassucci R., and Frank J. Electron microscopy and computer image averaging of ice-embedded large ribosomal subunits from Escherichia coli. J. Mol. Biol. 199 (1988) 137-147
49. Wilson D.N., Schluenzen F., Harms J.M., Yoshida T., Ohkubo T., Albrecht R., Buerger J., Kobayashi Y., and Fucini P. X-ray crystallography study on ribosome recycling: the mechanism of binding and action of RRF on the 50S ribosomal subunit. EMBO J. 24 (2005) 251-260
50. Yoshida T., Uchiyama S., Nakano H., Kashimori H., Kijima H., Ohshima T., Saihara Y., Ishino T., Shimahara H., Yoshida T., et al. Solution structure of the ribosome recycling factor from Aquifex aeolicus. Biochemistry 40 (2001) 2387-2396
51. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., and Noller H.F. Crystal structure of the ribosome at 5.5 Å resolution. Science 292 (2001) 883-896
52. Zavialov A.V., Hauryliuk V.V., and Ehrenberg M. Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G. Mol. Cell 18 (2005) 675-686