EttA regulates translation by binding the ribosomal e site and restricting ribosome-tRNA dynamics

Nature Structural and Molecular Biology

Volumn 21, Issue 2, 2014, Pages 152-159

  Chen, Bo ^a   Boël, Grégory ^a   Hashem, Yaser ^a   Ning, Wei ^a   Fei, Jingyi ^a,b   Wang, Chi ^a   Gonzalez, Ruben L ^a   Hunt, John F ^a   Frank, Joachim ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-BINDING CASSETTE TRANSPORTERS; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RIBOSOMES; RNA, TRANSFER;

EID: 84893807276     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2741     Document Type: Article

References (70)

1. Wilson, D.N. & Nierhaus, K.H. The weird and wonderful world of bacterial ribosome regulation. Crit. Rev. Biochem. Mol. Biol. 42, 187-219 (2007).
2. Schmeing, T.M. & Ramakrishnan, V. What recent ribosome structures have revealed about the mechanism of translation. Nature 461, 1234-1242 (2009).
3. Steitz, T.A. A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 9, 242-253 (2008).
4. Boël, G. et al. The ABC-F protein EttA gates ribosome entry into the translation elongation cycle. Nat. Struct. Mol. Biol. doi:10.1038/nsmb.2740 (5 January 2014).
5. Agrawal, R.K., Heagle, A.B., Penczek, P., Grassucci, R.A. & Frank, J. EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat. Struct. Biol. 6, 643-647 (1999).
6. Valle, M. et al. Locking and unlocking of ribosomal motions. Cell 114, 123-134 (2003).
7. Blanchard, S.C., Kim, H.D., Gonzalez, R.L., Puglisi, J.D. & Chu, S. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA 101, 12893-12898 (2004).
8. Cornish, P.V., Ermolenko, D.N., Noller, H.F. & Ha, T. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30, 578-588 (2008).
9. Cornish, P.V. et al. Following movement of the L1 stalk between three functional states in single ribosomes. Proc. Natl. Acad. Sci. USA 106, 2571-2576 (2009).
10. 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).
11. Fei, J., Kosuri, P., MacDougall, D.D. & Gonzalez, R.L. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell 30, 348-359 (2008).
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. Kim, H.D., Puglisi, J.D. & Chu, S. Fluctuations of transfer RNAs between classical and hybrid states. Biophys. J. 93, 3575-3582 (2007).
14. Frank, J. & Agrawal, R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318-322 (2000).
15. Agrawal, R.K. et al. Visualization of tRNA movements on the Escherichia coli 70S ribosome during the elongation cycle. J. Cell Biol. 150, 447-460 (2000).
16. Spirin, A.S. in Prog. Nucleic Acid Res. Mol. Biol. Vol. 32 (eds. Waldo, E.C. & Kivie, M.) 75-114 (Academic Press, 1985).
17. Gao, Y.-G. et al. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694-699 (2009).
18. Pisarev, A.V. et al. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell 37, 196-210 (2010).
19. Khoshnevis, S. et al. The iron-sulphur protein RNase L inhibitor functions in translation termination. EMBO Rep. 11, 214-219 (2010).
20. Barthelme, D. et al. Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proc. Natl. Acad. Sci. USA 108, 3228-3233 (2011).
21. Becker, T. et al. Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature 482, 501-506 (2012).
22. Karcher, A., Schele, A. & Hopfner, K.-P. X-ray structure of the complete ABC enzyme ABCE1 from Pyrococcus abyssi. J. Biol. Chem. 283, 7962-7971 (2008).
23. Grassucci, R.A., Taylor, D. & Frank, J. Visualization of macromolecular complexes using cryo-electron microscopy with FEI Tecnai transmission electron microscopes. Nat. Protoc. 3, 330-339 (2008).
24. Frank, J. Three-dimensional electron microscopy of macromolecular assemblies: visualization of biological molecules in their native state (Oxford Univ. Press, 2006).
25. Fei, J. et al. A highly purifed, fuorescently labeled in vitro translation system for single-molecule studies of protein synthesis. Methods Enzymol. 472, 221-259 (2010).
26. Grajevskaja, R.A., Ivanov, Y.V. & Saminsky, E.M. 70-S ribosomes of Escherichia coli have an additional site for deacylated tRNA binding. Eur. J. Biochem. 128, 47-52 (1982).
27. Valle, M. et al. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat. Struct. Biol. 10, 899-906 (2003).
28. Agirrezabala, X. et al. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ratcheting ribosome. Mol. Cell 32, 190-197 (2008).
29. Trabuco, L.G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible ftting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673-683 (2008).
30. Atwell, S. et al. Structures of a minimal human CFTR frst nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng. Des. Sel. 23, 375-384 (2010).
31. Karpowich, N. et al. Crystal structures of the MJ1267 ATP binding cassette reveal an induced-ft effect at the ATPase cctive site of an ABC transporter. Structure 9, 571-586 (2001).
32. Agirrezabala, X. et al. Structural characterization of mRNA-tRNA translocation intermediates. Proc. Natl. Acad. Sci. USA 109, 6094-6099 (2012).
33. Steinberg, S., Misch, A. & Sprinzl, M. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 21, 3011-3015 (1993).
34. Finn, R.D. et al. The Pfam protein families database. Nucleic Acids Res. 38, D211-D222 (2010).
35. Laursen, B.S., Sorensen, H.P., Mortensen, K.K. & Sperling-Petersen, H.U. Initiation of protein synthesis in bacteria. Microbiol. Mol. Biol. Rev. 69, 101-123 (2005).
36. fMet to initiate protein synthesis. Nucleic Acids Res. 36, 4894-4901 (2008).
37. Voorhees, R.M., Weixlbaumer, A., Loakes, D., Kelley, A.C. & Ramakrishnan, V. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16, 528-533 (2009).
38. Marshall, R.A., Aitken, C.E. & Puglisi, J.D. GTP hydrolysis by IF2 guides progression of the ribosome into elongation. Mol. Cell 35, 37-47 (2009).
39. Sternberg, S.H., Fei, J., Prywes, N., McGrath, K.A. & Gonzalez, R.L. Translation factors direct intrinsic ribosome dynamics during translation termination and ribosome recycling. Nat. Struct. Mol. Biol. 16, 861-868 (2009).
40. Smith, P.C. et al. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10, 139-149 (2002).
41. Davidson, A.L., Dassa, E., Orelle, C. & Chen, J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364 (2008).
42. Dawson, R.J. & Locher, K.P. Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (2006).
43. Oldham, M.L. & Chen, J. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332, 1202 (2011).
44. Andersen, C.B.F. et al. Structure of eEF3 and the mechanism of transfer RNA release from the E-site. Nature 443, 663-668 (2006).
45. Hopfner, K.-P. et al. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800 (2000).
46. Vergani, P., Lockless, S.W., Nairn, A.C. & Gadsby, D.C. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433, 876-880 (2005).
47. Doerfel, L.K. et al. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339, 85-88 (2013).
48. Buckstein, M.H., He, J. & Rubin, H. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J. Bacteriol. 190, 718-726 (2008).
49. Chapman, A.G., Fall, L. & Atkinson, D.E. Adenylate energy charge in Escherichia coli during growth and starvation. J. Bacteriol. 108, 1072-1086 (1971).
50. Blaha, G., Stanley, R.E. & Steitz, T.A. Formation of the frst peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325, 966-970 (2009).
51. Fei, J., Richard, A.C., Bronson, J.E. & Gonzalez, R.L. Transfer RNA-mediated regulation of ribosome dynamics during protein synthesis. Nat. Struct. Mol. Biol. 18, 1043-1051 (2011).
52. Youngman, E.M., Brunelle, J.L., Kochaniak, A.B. & Green, R. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117, 589-599 (2004).
53. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
54. Shaikh, T.R. et al. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 3, 1941-1974 (2008).
55. Rath, B.K. & Frank, J. Fast automatic particle picking from cryo-electron micrographs using a locally normalized cross-correlation function: a case study. J. Struct. Biol. 145, 84-90 (2004).
56. Gabashvili, I.S. et al. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100, 537-549 (2000).
57. Scheres, S.H.W. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406-418 (2012).
58. Scheres, S.H.W. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
59. Scheres, S.H. & Chen, S. Prevention of overftting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012).
60. Lewis, H.A. et al. Structure and dynamics of NBD1 from CFTR characterized using crystallography and hydrogen/deuterium exchange mass spectrometry. J. Mol. Biol. 396, 406-430 (2010).
61. Kelley, L.A. & Sternberg, M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
62. Pettersen, E.F. et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
63. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).
64. Dunkle, J.A. et al. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981-984 (2011).
65. Villa, E. et al. Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis. Proc. Natl. Acad. Sci. USA 106, 1063-1068 (2009).
66. Phillips, J.C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
67. Brooks, B.R. et al. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217 (1983).
68. MacKerell, A.D. et al. in The Encyclopedia of Computational Chemistry, Vol. 1 (eds. Schleyer, P.v.R. et al.) 271-277 (John Wiley & Sons, 1998).
69. Ledoux, S. & Uhlenbeck, O.C. [3′-32P]-labeling tRNA with nucleotidyltransferase for assaying aminoacylation and peptide bond formation. Methods 44, 74-80 (2008).
70. Ala identity by inorganic pyrophosphatase. Proc. Natl. Acad. Sci. USA 99, 5965-5970 (2002).