Real-time assembly landscape of bacterial 30S translation initiation complex

Nature Structural and Molecular Biology

Volumn 19, Issue 6, 2012, Pages 609-615

  Milón, Pohl ^a   Maracci, Cristina ^b   Filonava, Liudmila ^a   Gualerzi, Claudio O ^b   Rodnina, Marina V ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF CAMERINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; INITIATION FACTOR 3; MESSENGER RNA; TRANSFER RNA;

ARTICLE; BACTERIAL CELL; BACTERIAL KINETICS; BINDING SITE; CELL CYCLE CHECKPOINT; CELL STRUCTURE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA BINDING; TRANSLATION INITIATION;

BASE SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, MOLECULAR; PROKARYOTIC INITIATION FACTOR-2; PROKARYOTIC INITIATION FACTOR-3; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, BACTERIAL; RNA, MESSENGER; RNA, TRANSFER, MET;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84861859514     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2285     Document Type: Article

References (38)

1. Gualerzi, C.O. et al. Initiation factors in the early events of mRNA translation in bacteria. Cold Spring Harb. Symp. Quant. Biol. 66, 363-376 (2001).
2. 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).
3. Simonetti, A. et al. A structural view of translation initiation in bacteria. Cell. Mol. Life Sci. 66, 423-436 (2009).
4. Milón, P. et al. The ribosome-bound initiation factor 2 recruits initiator tRNA to the 30S initiation complex. EMBO Rep. 11, 312-316 (2010).
5. Antoun, A., Pavlov, M.Y., Lovmar, M. & Ehrenberg, M. How initiation factors tune the rate of initiation of protein synthesis in bacteria. EMBO J. 25, 2539-2550 (2006).
6. Grigoriadou, C., Marzi, S., Kirillov, S., Gualerzi, C.O. & Cooperman, B.S. A quantitative kinetic scheme for 70 S translation initiation complex formation. J. Mol. Biol. 373, 562-572 (2007).
7. Milón, P., Konevega, A.L., Gualerzi, C.O. & Rodnina, M.V. Kinetic checkpoint at a late step in translation initiation. Mol. Cell 30, 712-720 (2008).
8. 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).
9. Tomsic, J. et al. Late events of translation initiation in bacteria: a kinetic analysis. EMBO J. 19, 2127-2136 (2000).
10. Studer, S.M. & Joseph, S. Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol. Cell 22, 105-115 (2006).
11. Calogero, R.A., Pon, C.L., Canonaco, M.A. & Gualerzi, C.O. Selection of the mRNA translation initiation region by Escherichia coli ribosomes. Proc. Natl. Acad. Sci. USA 85, 6427-6431 (1988).
12. Grigoriadou, C., Marzi, S., Pan, D., Gualerzi, C.O. & Cooperman, B.S. The translational fidelity function of IF3 during transition from the 30 S initiation complex to the 70 S initiation complex. J. Mol. Biol. 373, 551-561 (2007).
13. La Teana, A., Gualerzi, C.O. & Brimacombe, R. From stand-by to decoding site. Adjustment of the mRNA on the 30S ribosomal subunit under the influence of the initiation factors. RNA 1, 772-782 (1995).
14. Milón, P. et al. Transient kinetics, fluorescence, and FRET in studies of initiation of translation in bacteria. Methods Enzymol. 430, 1-30 (2007).
15. Julián, P. et al. The cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLoS Biol. 9, e1001095 (2011).
16. Celano, B., Pawlik, R.T. & Gualerzi, C.O. Interaction of Escherichia coli translation-initiation factor IF-1 with ribosomes. Eur. J. Biochem. 178, 351-355 (1988).
17. Zucker, F.H. & Hershey, J.W. Binding of Escherichia coli protein synthesis initiation factor IF1 to 30S ribosomal subunits measured by fluorescence polarization. Biochemistry 25, 3682-3690 (1986).
18. Misselwitz, R. et al. The fMet-tRNA binding domain of translational initiation factor IF2: role and environment of its two Cys residues. FEBS Lett. 459, 332-336 (1999).
19. Weiel, J. & Hershey, J.W. The binding of fluorescein-labeled protein synthesis initiation factor 2 to Escherichia coli 30 S ribosomal subunits determined by fluorescence polarization. J. Biol. Chem. 257, 1215-1220 (1982).
20. Petrelli, D. et al. Translation initiation factor IF3: two domains, five functions, one mechanism? EMBO J. 20, 4560-4569 (2001).
21. Karimi, R., Pavlov, M.Y., Buckingham, R.H. & Ehrenberg, M. Novel roles for classical factors at the interface between translation termination and initiation. Mol. Cell 3, 601-609 (1999).
22. Peske, F., Rodnina, M.V. & Wintermeyer, W. Sequence of steps in ribosome recycling as defined by kinetic analysis. Mol. Cell 18, 403-412 (2005).
23. Antoun, A., Pavlov, M.Y., Lovmar, M. & Ehrenberg, M. How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol. Cell 23, 183-193 (2006).
24. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415 (2003).
25. Bremer, H. & Dennis, P.P. Modulation of chemical composition and other parameters of the cell by growth rate. in Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology (ed. Neidherdt, F.C.) 1527-1542 (American Society for Microbiology, Washington, DC, 1987).
26. Passalacqua, K.D. et al. Structure and complexity of a bacterial transcriptome. J. Bacteriol. 191, 3203-3211 (2009).
27. Yusupova, G., Jenner, L., Rees, B., Moras, D. & Yusupov, M. Structural basis for messenger RNA movement on the ribosome. Nature 444, 391-394 (2006).
28. Kudla, G., Murray, A.W., Tollervey, D. & Plotkin, J.B. Coding-sequence determinants of gene expression in Escherichia coli. Science 324, 255-258 (2009).
29. Carter, A.P. et al. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291, 498-501 (2001).
30. Qin, D. & Fredrick, K. Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA. Mol. Microbiol. 71, 1239-1249 (2009).
31. Kapralou, S. et al. Translation initiation factor IF1 of Bacillus stearothermophilus and Thermus thermophilus substitute for Escherichia coli IF1 in vivo and in vitro without a direct IF1-IF2 interaction. Mol. Microbiol. 70, 1368-1377 (2008).
32. Caserta, E. et al. Translation initiation factor IF2 interacts with the 30 S ribosomal subunit via two separate binding sites. J. Mol. Biol. 362, 787-799 (2006).
33. Belotserkovsky, J.M., Dabbs, E.R. & Isaksson, L.A. Mutations in 16S rRNA that suppress cold-sensitive initiation factor 1 affect ribosomal subunit association. FEBS J. 278, 3508-3517 (2011).
34. Qin, D., Abdi, N.M. & Fredrick, K. Characterization of 16S rRNA mutations that decrease the fidelity of translation initiation. RNA 13, 2348-2355 (2007).
35. Surkov, S., Nilsson, H., Rasmussen, L.C., Sperling-Petersen, H.U. & Isaksson, L.A. Translation initiation region dependency of translation initiation in Escherichia coli by IF1 and kasugamycin. FEBS J. 277, 2428-2439 (2010).
36. McCarthy, J.E. & Gualerzi, C. Translational control of prokaryotic gene expression. Trends Genet. 6, 78-85 (1990).
37. Marzi, S. et al. Structured mRNAs regulate translation initiation by binding to the platform of the ribosome. Cell 130, 1019-1031 (2007).
38. Rodnina, M.V. & Wintermeyer, W. GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs. Proc. Natl. Acad. Sci. USA 92, 1945-1949 (1995).