Lateral opening of the bacterial translocon on ribosome binding and signal peptide insertion

Nature Communications

Volumn 5, Issue , 2014, Pages

  Ge, Yan ^a   Draycheva, Albena ^a   Bornemann, Thomas ^a   Rodnina, Marina V ^a   Wintermeyer, Wolfgang ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MALEIMIDE DERIVATIVE; NANODISC; PROTEINASE K; SIGNAL PEPTIDE; TRANSLOCON; FLUORESCENT DYE;

CELL ORGANELLE; ELECTRON; HYDROPHOBICITY; MEMBRANE; PEPTIDE; PHOSPHOLIPID; PLASMA; PROTEIN; TEMPERATURE EFFECT; TRANSLOCATION;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; FLUORESCENCE; HYDROPHOBICITY; LOW TEMPERATURE; METHANOCALDOCOCCUS JANNASCHII; NONHUMAN; PHASE TRANSITION; PHOSPHOLIPID BILAYER; PHOTO INDUCED ELECTRON TRANSFER; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOME; TEMPERATURE DEPENDENCE; CHEMISTRY; GENETICS; METABOLISM; METHANOCALDOCOCCUS;

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEINS; ELECTRON TRANSPORT; FLUORESCENT DYES; METHANOCALDOCOCCUS; PROTEIN SORTING SIGNALS; RIBOSOMES;

EID: 84923247437     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6263     Document Type: Article

References (33)

1. Van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36-44 (2004).
2. Breyton, C., Haase, W., Rapoport, T. A., Kuhlbrandt, W. & Collinson, I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665 (2002).
3. Egea, P. F. & Stroud, R. M. Lateral opening of a translocon upon entry of protein suggests the mechanism of insertion into membranes. Proc. Natl Acad. Sci. USA 107, 17182-17187 (2010).
4. Zimmer, J., Nam, Y. & Rapoport, T. A. Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455, 936-943 (2008).
5. Park, E. & Rapoport, T. A. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41, 21-40 (2012).
6. Hessa, T. et al. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450, 1026-1030 (2007).
7. Xie, K. et al. Features of transmembrane segments that promote the lateral release from the translocase into the lipid phase. Biochemistry 46, 15153-15161 (2007).
8. Junne, T., Kocik, L. & Spiess, M. The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration. Mol. Biol. Cell 21, 1662-1670 (2010).
9. Trueman, S. F., Mandon, E. C. & Gilmore, R. A gating motif in the translocation channel sets the hydrophobicity threshold for signal sequence function. J. Cell Biol. 199, 907-918 (2012).
10. Hizlan, D. et al. Structure of the SecY complex unlocked by a preprotein mimic. Cell Rep. 1, 21-28 (2012).
11. Taufik, I., Kedrov, A., Exterkate, M. & Driessen, A. J. Monitoring the activity of single translocons. J. Mol. Biol. 425, 4145-4153 (2013).
12. du Plessis, D. J., Berrelkamp, G., Nouwen, N. & Driessen, A. J. The lateral gate of SecYEG opens during protein translocation. J. Biol. Chem. 284, 15805-15814 (2009).
13. Frauenfeld, J. et al. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 18, 614-621 (2011).
14. Park, E. et al. Structure of the SecY channel during initiation of protein translocation. Nature 506, 102-106 (2014).
15. Gogala, M. et al. Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion. Nature 506, 107-110 (2014).
16. Bischoff, L., Wickles, S., Berninghausen, O., van der Sluis, E. O. & Beckmann, R. Visualization of a polytopic membrane protein during SecY-mediated membrane insertion. Nat. Commun. 5, 4103 (2014).
17. Rychkova, A. & Warshel, A. Exploring the nature of the translocon-assisted protein insertion. Proc. Natl Acad. Sci. USA 110, 495-500 (2013).
18. Gumbart, J., Trabuco, L. G., Schreiner, E., Villa, E. & Schulten, K. Regulation of the protein-conducting channel by a bound ribosome. Structure 17, 1453-1464 (2009).
19. Gumbart, J. C., Teo, I., Roux, B. & Schulten, K. Reconciling the roles of kinetic and thermodynamic factors in membrane-protein insertion. J. Am. Chem. Soc. 135, 2291-2297 (2013).
20. rd T. F. Hydrophobically stabilized open state for the lateral gate of the Sec translocon. Proc. Natl Acad. Sci. USA 107, 5399-5404 (2010).
21. Alami, M., Dalal, K., Lelj-Garolla, B., Sligar, S. G. & Duong, F. Nanodiscs unravel the interaction between the SecYEG channel and its cytosolic partner SecA. EMBO J. 26, 1995-2004 (2007).
22. Doose, S., Neuweiler, H. & Sauer, M. Fluorescence quenching by photoinduced electron transfer: a reporter for conformational dynamics of macromolecules. Chemphyschem 10, 1389-1398 (2009).
23. Marme, N., Knemeyer, J. P., Sauer, M. & Wolfrum, J. Inter- and intramolecular fluorescence quenching of organic dyes by tryptophan. Bioconjug. Chem. 14, 1133-1139 (2003).
24. Marty, M. T., Wilcox, K. C., Klein, W. L. & Sligar, S. G. Nanodisc-solubilized membrane protein library reflects the membrane proteome. Anal. Bioanal. Chem. 405, 4009-4016 (2013).
25. Ellis, J. P., Bakke, C. K., Kirchdoerfer, R. N., Jungbauer, L. M. & Cavagnero, S. Chain dynamics of nascent polypeptides emerging from the ribosome. ACS Chem. Biol. 3, 555-566 (2008).
26. Wu, Z. C., de Keyzer, J., Kedrov, A. & Driessen, A. J. Competitive binding of the SecA ATPase and ribosomes to the SecYEG translocon. J. Biol. Chem. 287, 7885-7895 (2012).
27. Chapman, D. Phase transitions and fluidity characteristics of lipids and cell membranes. Q. Rev. Biophys. 8, 185-235 (1975).
28. 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).
29. Holtkamp, W. et al. GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits. EMBO J. 33, 1073-1085 (2014).
30. Kusters, I. et al. Purification and functional reconstitution of the bacterial protein translocation pore, the SecYEG complex. Methods Mol. Biol. 619, 131-143 (2010).
31. Bayburt, T. H. & Sligar, S. G. Membrane protein assembly into Nanodiscs. FEBS Lett. 584, 1721-1727 (2010).
32. Ritchie, T. K. et al. Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 464, 211-231 (2009).
33. Bornemann, T., Jöckel, J., Rodnina, M. V. & Wintermeyer, W. Signal sequence-independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nat. Struct. Mol. Biol. 15, 494-499 (2008).