MRNA translocation occurs during the second step of ribosomal intersubunit rotation

Nature Structural and Molecular Biology

Volumn 18, Issue 4, 2011, Pages 457-463

  Ermolenko, Dmitri N ^a,b   Noller, Harry F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ARTICLE; CELL MOTION; CELL TRANSPORT; COMPARATIVE STUDY; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; FLUORESCENCE; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA TRANSPORT;

BIOLOGICAL TRANSPORT; CRYOELECTRON MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; RIBOSOMES; RNA, MESSENGER;

EID: 79953777970     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2011     Document Type: Article

References (51)

1. Cate, J.H., Yusupov, M.M., Yusupova, G.Z., Earnest, T.N. & Noller, H.F. X-ray crystal structures of 70S ribosome functional complexes. Science 285, 2095-2104 (1999). (Pubitemid 29451422)
2. Korostelev, A., Trakhanov, S., Laurberg, M. & Noller, H.F. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126, 1065-1077 (2006). (Pubitemid 44380300)
3. Selmer, M. et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935-1942 (2006). (Pubitemid 44497996)
4. Yusupov, M.M. et al. Crystal structure of the ribosome at 5.5 Å resolution. Science 292, 883-896 (2001). (Pubitemid 32422479)
5. Yusupova, G.Z., Yusupov, M.M., Cate, J.H. & Noller, H.F. The path of messenger RNA through the ribosome. Cell 106, 233-241 (2001). (Pubitemid 32772633)
6. Moazed, D. & Noller, H.F. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342, 142-148 (1989). (Pubitemid 19277015)
7. Spiegel, P.C., Ermolenko, D.N. & Noller, H.F. Elongation factor G stabilizes the hybrid-state conformation of the 70S ribosome. RNA 13, 1473-1482 (2007). (Pubitemid 47347418)
8. Pan, D., Kirillov, S.V. & Cooperman, B.S. Kinetically competent intermediates in the translocation step of protein synthesis. Mol. Cell 25, 519-529 (2007). (Pubitemid 46274443)
9. Frank, J. & Agrawal, R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318-322 (2000). (Pubitemid 30604411)
10. Gao, H. et al. Study of the structural dynamics of the E. coli 70S ribosome using real-space refnement. Cell 113, 789-801 (2003). (Pubitemid 36724942)
11. Valle, M. et al. Locking and unlocking of ribosomal motions. Cell 114, 123-134 (2003). (Pubitemid 36859846)
12. Frank, J., Gao, H., Sengupta, J., Gao, N. & Taylor, D.J. The process of mRNA-tRNA translocation. Proc. Natl. Acad. Sci. USA 104, 19671-19678 (2007).
13. Horan, L.H. & Noller, H.F. Intersubunit movement is required for ribosomal translocation. Proc. Natl. Acad. Sci. USA 104, 4881-4885 (2007). (Pubitemid 47186145)
14. Ermolenko, D.N. et al. The antibiotic viomycin traps the ribosome in an intermediate state of translocation. Nat Struct. Mol. Biol. 14, 493-497 (2007). (Pubitemid 46871807)
15. Agirrezabala, X. et al. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 32, 190-197 (2008).
16. Julián, P. et al. Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc Natl. Acad. Sci. USA 105, 16924-16927 (2008).
17. Cornish, P.V., Ermolenko, D.N., Noller, H.F. & Ha, T. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30, 578-588 (2008). (Pubitemid 351760964)
18. Blanchard, S.C., Kim, H.D., Gonzalez, R.L. Jr., Puglisi, J.D. & Chu, S. tRNA dynamics on the ribosome during translation. Proc Natl. Acad. Sci. USA 101, 12893-12898 (2004). (Pubitemid 39167554)
19. Ermolenko, D.N. et al. Observation of intersubunit movement of the ribosome in solution using FRET. J. Mol. Biol. 370, 530-540 (2007). (Pubitemid 46898430)
20. Fei, J. et al. Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc Natl. Acad. Sci. USA 106, 15702-15707 (2009).
21. Fei, J., Kosuri, P., MacDougall, D.D. & Gonzalez, R.L. Jr. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell 30, 348-359 (2008). (Pubitemid 351615315)
22. Munro, J.B., Altman, R.B., O'Connor, N. & Blanchard, S.C. Identifcation of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25, 505-517 (2007). (Pubitemid 46274447)
23. Lill, R. et al. Specifc recognition of the 3'-terminal adenosine of tRNAPhe in the exit site of Escherichia coli ribosomes. J. Mol. Biol. 203, 699-705 (1988).
24. Studer, S.M., Feinberg, J.S. & Joseph, S. Rapid kinetic analysis of EF-G-dependent mRNA translocation in the ribosome. J. Mol. Biol. 327, 369-381 (2003). (Pubitemid 36298708)
25. Munro, J.B. et al. Spontaneous formation of the unlocked state of the ribosome is a multistep process. Proc Natl. Acad. Sci. USA 107, 709-714 (2010).
26. Peske, F., Savelsbergh, A., Katunin, V.I., Rodnina, M.V. & Wintermeyer, W. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J. Mol. Biol. 343, 1183-1194 (2004). (Pubitemid 39387819)
27. Shi, X., Chiu, K., Ghosh, S. & Joseph, S. Bases in 16S rRNA important for subunit association, tRNA binding, and translocation. Biochemistry 48, 6772-6782 (2009).
28. Dorner, S., Brunelle, J.L., Sharma, D. & Green, R. The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nat Struct. Mol. Biol. 13, 234-241 (2006). (Pubitemid 43348509)
29. Borovinskaya, M.A., Shoji, S., Fredrick, K. & Cate, J.H. Structural basis for hygromycin B inhibition of protein biosynthesis. RNA 14, 1590-1599 (2008).
30. Borovinskaya, M.A., Shoji, S., Holton, J.M., Fredrick, K. & Cate, J.H. A steric block in translation caused by the antibiotic spectinomycin. ACS Chem. Biol. 2, 545-552 (2007). (Pubitemid 350011325)
31. Zavialov, A.V., Hauryliuk, V.V. & Ehrenberg, M. Guanine-nucleotide exchange on ribosome-bound elongation factor G initiates the translocation of tRNAs. J. Biol. 4, 9 (2005).
32. Belitsina, N.V., Glukhova, M.A. & Spirin, A.S. Elongation factor G-promoted translocation and polypeptide elongation in ribosomes without GTP cleavage: use of columns with matrix-bound polyuridylic acid. Methods Enzymol. 60, 761-779 (1979).
33. Bodley, J.W., Zieve, F.J., Lin, L. & Zieve, S.T. Formation of the ribosome-G factor-GDP complex in the presence of fusidic acid. Biochem. Biophys. Res. Commun. 37, 437-443 (1969).
34. Inoue-Yokosawa, N., Ishikawa, C & Kaziro, Y. The role of guanosine triphosphate in translocation reaction catalyzed by elongation factor G. J. Biol. Chem. 249, 4321-4323 (1974).
35. Ticu, C., Nechifor, R., Nguyen, B., Desrosiers, M. & Wilson, K.S. Conformational changes in switch I of EF-G drive its directional cycling on and off the ribosome. EMBO J. 28, 2053-2065 (2009).
36. Savelsbergh, A., Rodnina, M.V. & Wintermeyer, W. Distinct functions of elongation factor G in ribosome recycling and translocation. RNA 15, 772-780 (2009).
37. Rodnina, M.V., Savelsbergh, A., Katunin, V.I. & Wintermeyer, W. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37-41 (1997). (Pubitemid 27024544)
38. Savelsbergh, A. et al. An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell 11, 1517-1523 (2003). (Pubitemid 36776538)
39. Schuwirth, B.S. et al. Structures of the bacterial ribosome at 3.5 A resolution. Science 310, 827-834 (2005). (Pubitemid 41567336)
40. Ali, I.K., Lancaster, L., Feinberg, J., Joseph, S. & Noller, H.F. Deletion of a conserved, central ribosomal intersubunit RNA bridge. Mol. Cell 23, 865-874 (2006). (Pubitemid 44363047)
41. Feinberg, J.S. & Joseph, S. Ribose 2'-hydroxyl groups in the 5'strand of the acceptor arm of P-site tRNA are not essential for EF-G catalyzed translocation. RNA 12, 580-588 (2006).
42. Feldman, M.B., Terry, D.S., Altman, R.B. & Blanchard, S.C. Aminoglycoside activity observed on single pre-translocation ribosome complexes. Nat Chem. Biol. 6, 54-62 (2010).
43. Katunin, V.I., Savelsbergh, A., Rodnina, M.V. & Wintermeyer, W. Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome. Biochemistry 41, 12806-12812 (2002). (Pubitemid 35192509)
44. Robertson, J.M., Paulsen, H. & Wintermeyer, W. Pre-steady-state kinetics of ribosomal translocation. J. Mol. Biol. 192, 351-360 (1986). (Pubitemid 17203062)
45. Gao, Y.G. et al. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694-699 (2009).
46. Martemyanov, K.A., Yarunin, A.S., Liljas, A. & Gudkov, A.T. An intact conformation at the tip of elongation factor G domain IV is functionally important. FEBS Lett 434, 205-208 (1998). (Pubitemid 28404689)
47. Peske, F., Matassova, N.B., Savelsbergh, A., Rodnina, M.V. & Wintermeyer, W. Conformationally restricted elongation factor G retains GTPase activity but is inactive in translocation on the ribosome. Mol. Cell 6, 501-505 (2000).
48. Wilson, K.S. & Noller, H.F. Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing. Cell 92, 131-139 (1998). (Pubitemid 28053304)
49. Culver, G.M. & Noller, H.F. Effcient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins. RNA 5, 832-843 (1999). (Pubitemid 29283784)
50. Hickerson, R., Majumdar, Z.K., Baucom, A., Clegg, R.M. & Noller, H.F. Measurement of internal movements within the 30 S ribosomal subunit using Forster resonance energy transfer. J. Mol. Biol. 354, 459-472 (2005). (Pubitemid 41579858)
51. Lieberman, K.R. et al. The 23 S rRNA environment of ribosomal protein L9 in the 50 S ribosomal subunit. J. Mol. Biol. 297, 1129-1143 (2000).