Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion

Nature

Volumn 506, Issue 7486, 2014, Pages 107-110

  Gogala, Marko ^a   Becker, Thomas ^a   Beatrix, Birgitta ^a   Armache, Jean Paul ^a   Barrio Garcia, Clara ^a   Berninghausen, Otto ^a   Beckmann, Roland ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893630228     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12950     Document Type: Article

References (45)

1. Park, E. & Rapoport, T. A. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41, 21-40 (2012)
2. van den Berg, B. et al. X-ray structure ofa protein-conducting channel. Nature 427, 36-44 (2004).
3. Park, E. & Rapoport, T. A. Preserving the membrane barrier for small molecules during bacterial protein translocation. Nature 473, 239-242 (2011).
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. Tsukazaki, T. et al. Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455, 988-991 (2008).
6. 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).
7. Becker, T. et al. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
8. Frauenfeld, J. et al. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nature Struct. Mol. Biol. 18, 614-621 (2011).
9. Erickson, A. H. & Blobel, G. Cell-free translationofmessenger RNAinawheat germ system. Methods Enzymol. 96, 38-50 (1983).
10. Sääf, A., Wallin, E. & von Heijne, G. Stop-transfer function ofpseudo-random amino acid segments during translocation across prokaryotic and eukaryotic membranes. Eur. J. Biochem. 251, 821-829 (1998).
11. Bhushan, S. et al. Structural basis for translational stalling by human cytomegalovirus and fungal arginine attenuator peptide. Mol. Cell 40, 138-146 (2010).
12. Degnin, C. R., Schleiss, M. R., Cao, J. & Geballe, A. P. Translational inhibition mediatedbyashortupstream open reading frameinthe human cytomegalovirus gpUL4 (gp48) transcript. J. Virol. 67, 5514-5521 (1993).
13. Ménétret, J.-F. et al. Single copies of Sec61 and TRAP associate with a nontranslating mammalian ribosome. Structure 16, 1126-1137 (2008).
14. Ménétret, J.-F. et al. Ribosome binding of a single copy of the SecY complex: implications for protein translocation. Mol. Cell 28, 1083-1092 (2007).
15. Simon, S. M. & Blobel, G. A protein-conducting channel in the endoplasmic reticulum. Cell 65, 371-380 (1991)
16. 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).
17. Lycklama A, Nijeholt, J. A., Bulacu M., Marrink, S. J. & Driessen, A. J. Immobilization of the plug domain inside the SecY channel allows unrestricted protein translocation. J. Biol. Chem. 285, 23747-23754 (2010).
18. Cannon, K. S., Or, E., Clemons, W. M. Jr, Shibata, Y. & Rapoport, T. A. Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J. Cell Biol. 169, 219-225 (2005).
19. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J. & Rapoport, T. A. Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807 (1998).
20. Hizlan, D. et al. Structureofthe SecY complex unlockedby apreprotein mimic. Cell Rep. 1, 21-28 (2012).
21. Sadlish, H., Pitonzo, D., Johnson, A. E. & Skach, W. R. Sequential triage of transmembrane segments by Sec61a during biogenesis of a native multispanning membrane protein. Nature Struct. Mol. Biol. 12, 870-878 (2005).
22. Pitonzo, D., Yang, Z., Matsumura, Y., Johnson, A. E. & Skach, W. R. Sequence-specific retention andregulatedintegrationofanascentmembraneproteinbythe endoplasmic reticulum Sec61 translocon. Mol. Biol. Cell 20, 685-698 (2009).
23. Hou, B., Lin, P. J. & Johnson, A. E. Membrane protein TMsegments are retained at the translocon during integration until the nascent chain cues FRET-detected release into bulk lipid. Mol. Cell 48, 398-408 (2012).
24. Heinrich, S. U. & Rapoport, T. A. Cooperationoftransmembrane segments during the integration of a double-spanning protein into the ER membrane. EMBO J. 22, 3654-3663 (2003).
25. Martoglio, B., Hofmann, M. W., Brunner, J. & Dobberstein, B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell 81, 207-214 (1995).
26. Hessa, T. et al. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377-381 (2005).
27. Hessa, T. et al. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450, 1026-1030 (2007).
28. Heinrich, S. U., Mothes, W., Brunner, J. & Rapoport, T. A. The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233-244 (2000).
29. Lycklamaa Nijeholt, J. A., Wu, Z. C. & Driessen, A. J. Conformational dynamicsofthe plug domain of the SecYEG protein-conducting channel. J. Biol. Chem. 286, 43881-43890 (2011).
30. Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808-814 (2004).
31. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
32. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
33. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
34. Walter, P., Ibrahimi, I. & Blobel, G. Translocationofproteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 545-550 (1981).
35. Görlich, D. & Rapoport, T. A. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75, 615-630 (1993).
36. Martoglio, B. H. S. and Dobberstein, B. in Cell Biology: A Laboratory Handbook 2nd edn (ed J. E. Celis) Vol. 1, 265-273 (1997).
37. Wagenknecht, T., Grassucci, R. & Frank, J. Electron microscopy and computer image averaging of ice-embedded large ribosomal subunits from Escherichia coli. J. Mol. Biol. 199, 137-147 (1988).
38. Chen, J. Z. & Grigorieff, N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol. 157, 168-173 (2007).
39. Norousi, R. et al. Automatic post-picking using MAPPOS improves particle image detection from cryo-EM micrographs. J. Struct. Biol. 182, 59-66 (2013).
40. Söding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248 (2005).
41. Eswar, N., Eramian, D., Webb, B., Shen, M. Y. & Sali, A. Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159 (2008).
42. Armache, J. P. et al. Cryo-EM structure and rRNA modelofatranslating eukaryotic 80S ribosome at 5. 5A resolution. Proc. Natl Acad. Sci. USA 107, 19748-19753 (2010).
43. Armache, J. P. et al. Localization of eukaryote-specific ribosomal proteins in a5. 5 A cryo-EM map of the 80S eukaryotic ribosome. Proc. Natl Acad. Sci. USA 107, 19754-19759 (2010).
44. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3. 0A resolution. Science 334, 1524-1529 (2011).
45. Trabuco, L. G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673-683 (2008).