Cryo-EM structure of the ribosome-SecYE complex in the membrane environment

Nature Structural and Molecular Biology

Volumn 18, Issue 5, 2011, Pages 614-621

  Frauenfeld, Jens ^a,b   Gumbart, James ^c   Sluis, Eli O Van Der ^a,b   Funes, Soledad ^d   Gartmann, Marco ^a,b   Beatrix, Birgitta ^a,b   Mielke, Thorsten ^e   Berninghausen, Otto ^a,b   Becker, Thomas ^a,b   Schulten, Klaus ^c   Beckmann, Roland ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

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

^d INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; ION CHANNEL; LIPID; MEMBRANE PROTEIN; PEPTIDYLTRANSFERASE; POLYPEPTIDE; PROTEIN CONDUCTING CHANNEL; PROTEIN SECYE; RIBOSOME RNA; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE TRANSPORT; CHANNEL GATING; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; LIPID BILAYER; MOLECULAR DYNAMICS; PRIORITY JOURNAL; RIBOSOME; SIGNAL TRANSDUCTION; SIMULATION;

EID: 85027919032     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2026     Document Type: Article

References (59)

1. Rapoport, T.A. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669 (2007). (Pubitemid 350207698)
2. Halic, M. & Beckmann, R. The signal recognition particle and its interactions during protein targeting. Curr. Opin. Struct. Biol. 15, 116-125 (2005). (Pubitemid 40249518)
3. Van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36-44 (2004). (Pubitemid 38094813)
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. 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).
8. Osborne, A.R. & Rapoport, T.A. Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 129, 97-110 (2007). (Pubitemid 46507582)
9. Mitra, K. et al. Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438, 318-324 (2005). (Pubitemid 41643943)
10. Menetret, J.-F. et al. Ribosome binding of a single copy of the SecY complex: implications for protein translocation. Mol. Cell 28, 1083-1092 (2007). (Pubitemid 350297028)
11. Menetret, J.-F. et al. Single copies of Sec61 and TRAP associate with a nontranslating mammalian ribosome. Structure 16, 1126-1137 (2008). (Pubitemid 351899291)
12. Kalies, K.U., Stokes, V. & Hartmann, E. A single Sec61 complex functions as a protein-conducting channel. Biochim. Biophys. Acta 1783, 2375-2383 (2008).
13. Becker, T. et al. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
14. 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).
15. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001). (Pubitemid 33049979)
16. Beckmann, R. et al. Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex. Science 278, 2123-2126 (1997). (Pubitemid 28028322)
17. Menetret, J.-F. et al. Architecture of the ribosome-channel complex derived from native membranes. J. Mol. Biol. 348, 445-457 (2005). (Pubitemid 40462108)
18. Morgan, D.G., Menetret, J.F., Neuhof, A., Rapoport, T.A. & Akey, C.W. Structure of the mammalian ribosome-channel complex at 17A resolution. J. Mol. Biol. 324, 871-886 (2002). (Pubitemid 36044119)
19. Menetret, J.-F. et al. The structure of ribosome-channel complexes engaged in protein translocation. Mol. Cell 6, 1219-1232 (2000).
20. Matlack, K.E., Plath, K., Misselwitz, B. & Rapoport, T.A. Protein transport by purified yeast Sec complex and Kar2p without membranes. Science 277, 938-941 (1997). (Pubitemid 27366676)
21. Raunser, S. & Walz, T. Electron crystallography as a technique to study the structure on membrane proteins in a lipidic environment. Annu. Rev. Biophys. 38, 89-105 (2009).
22. Wang, L. & Sigworth, F.J. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature 461, 292-295 (2009).
23. 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). (Pubitemid 46625796)
24. Shih, A.Y. et al. Molecular modeling of the structural properties and formation of high-density lipoprotein particles. in Current Topics in Membranes: Computational Modeling of Membrane Bilayers (ed. Feller, S.) 313-342 (Elsevier, 2008).
25. Halic, M. et al. Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 444, 507-511 (2006). (Pubitemid 44809070)
26. Urbanus, M.L. et al. Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep. 2, 524-529 (2001). (Pubitemid 32611350)
27. Hamman, B.D., Chen, J.C., Johnson, E.E. & Johnson, A.E. The aqueous pore through the translocon has a diameter of 40-60 Å during cotranslational protein translocation at the ER membrane. Cell 89, 535-544 (1997). (Pubitemid 27511764)
28. 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). (Pubitemid 351615021)
29. Cockburn, J.J. et al. Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432, 122-125 (2004). (Pubitemid 39490839)
30. Laurinmaki, P.A., Huiskonen, J.T., Bamford, D.H. & Butcher, S.J. Membrane proteins modulate the bilayer curvature in the bacterial virus Bam35. Structure 13, 1819-1828 (2005). (Pubitemid 41772950)
31. Tilley, S.J., Orlova, E.V., Gilbert, R.J., Andrew, P.W. & Saibil, H.R. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121, 247-256 (2005). (Pubitemid 40546392)
32. Wu, Z. et al. The refined structure of nascent HDL reveals a key functional domain for particle maturation and dysfunction. Nat. Struct. Mol. Biol. 14, 861-868 (2007). (Pubitemid 47373831)
33. Borhani, D.W., Rogers, D.P., Engler, J.A. & Brouillette, C.G. Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl. Acad. Sci. USA 94, 12291-12296 (1997). (Pubitemid 27492521)
34. 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).
35. Collinson, I. The structure of the bacterial protein translocation complex SecYEG. Biochem. Soc. Trans. 33, 1225-1230 (2005). (Pubitemid 41779655)
36. Chiba, K., Mori, H. & Ito, K. Roles of the C-terminal end of SecY in protein translocation and viability of Escherichia coli. J. Bacteriol. 184, 2243-2250 (2002). (Pubitemid 34259674)
37. Murphy, C.K. & Beckwith, J. Residues essential for the function of SecE, a membrane component of the Escherichia coli secretion apparatus, are located in a conserved cytoplasmic region. Proc. Natl. Acad. Sci. USA 91, 2557-2561 (1994). (Pubitemid 24139386)
38. Houben, E.N., Zarivach, R., Oudega, B. & Luirink, J. Early encounters of a nascent membrane protein: specificity and timing of contacts inside and outside the ribosome. J. Cell Biol. 170, 27-35 (2005). (Pubitemid 40994093)
39. Bornemann, T., Jockel, 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). (Pubitemid 351653581)
40. Gumbart, J. & Schulten, K. Structural determinants of lateral gate opening in the protein translocon. Biochemistry 46, 11147-11157 (2007). (Pubitemid 47502781)
41. Scotti, P.A. et al. The Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549 (2000). (Pubitemid 30093727)
42. van der Laan, M., Houben, E.N., Nouwen, N., Luirink, J. & Driessen, A.J. Reconstitution of Sec-dependent membrane protein insertion: nascent FtsQ interacts with YidC in a SecYEG-dependent manner. EMBO Rep. 2, 519-523 (2001). (Pubitemid 32611349)
43. Michanek, A., Kristen, N., Hook, F., Nylander, T. & Sparr, E. RNA and DNA interactions with zwitterionic and charged lipid membranes-a DSC and QCM-D study. Biochim. Biophys. Acta 4, 829-838 (1798).
44. Khvorova, A., Kwak, Y.G., Tamkun, M., Majerfeld, I. & Yarus, M. RNAs that bind and change the permeability of phospholipid membranes. Proc. Natl. Acad. Sci. USA 96, 10649-10654 (1999). (Pubitemid 29442198)
45. Janas, T. & Yarus, M. Specific RNA binding to ordered phospholipid bilayers. Nucleic Acids Res. 34, 2128-2136 (2006). (Pubitemid 44314210)
46. Marty, R., N'Soukpoe-Kossi, C.N., Charbonneau, D.M., Kreplak, L. & Tajmir-Riahi, H.A. Structural characterization of cationic lipid-tRNA complexes. Nucleic Acids Res. 37, 5197-5207 (2009).
47. Jaud, S. et al. Insertion of short transmembrane helices by the Sec61 translocon. Proc. Natl. Acad. Sci. USA 106, 11588-11593 (2009).
48. von Heijne, G. The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J. 5, 3021-3027 (1986).
49. van der Does, C., de Keyzer, J., van der Laan, M. & Driessen, A.J. Reconstitution of purified bacterial preprotein translocase in liposomes. Methods Enzymol. 372, 86-98 (2003). (Pubitemid 37337802)
50. Denisov, I.G., Grinkova, Y.V., Lazarides, A.A. & Sligar, S.G. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J. Am. Chem. Soc. 126, 3477-3487 (2004). (Pubitemid 38366738)
51. 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).
52. 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). (Pubitemid 26093143)
53. Chen, J.Z. & Grigorieff, N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol. 157, 168-173 (2007). (Pubitemid 44895517)
54. Berk, V., Zhang, W., Pai, R.D. & Cate, J.H. Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl. Acad. Sci. USA 103, 15830-15834 (2006). (Pubitemid 44657552)
55. Seidelt, B. et al. Structural insight into nascent polypeptide chain-mediated translational stalling. Science 326, 1412-1415 (2009).
56. Söding, J., Biegert, A. & Lupas, A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-8 (2005). (Pubitemid 44529917)
57. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
58. Bostina, M., Mohsin, B., Kühlbrandt, W. & Collinson, I. Atomic model of the E. coli membrane-bound protein translocation complex SecYEG. J. Mol. Biol. 352, 1035-1043 (2005). (Pubitemid 41316713)
59. Breyton, C., Haase, W., Rapoport, T.A., Kühlbrandt, W. & Collinson, I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665 (2002).