Structure of the SecY channel during initiation of protein translocation

Nature

Volumn 506, Issue 7486, 2014, Pages 102-106

  Park, Eunyong ^a   Ménétret, Jean François ^b   Gumbart, James C ^c   Ludtke, Steven J ^d   Li, Weikai ^a   Whynot, Andrew ^a   Rapoport, Tom A ^a   Akey, Christopher W ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893726448     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12720     Document Type: Article

References (39)

1. Park, E. & Rapoport, T. A. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41, 21-40 (2012).
2. Shao, S. & Hegde, R. S. Membrane protein insertion atthe endoplasmic reticulum. Annu. Rev. Cell Dev. Biol. 27, 25-56 (2011)
3. Vanden Berg, B. et al. X-ray structureofaprotein-conducting channel. Nature 427, 36-44 (2004).
4. Tsukazaki, T. et al. Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455, 988-991 (2008).
5. 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).
6. Armache, J. P. et al. Promiscuous behaviour of archaeal ribosomal proteins: implications for eukaryoticribosome evolution. Nucleic Acids Res. 41, 1284-1293 (2013).
7. 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).
8. 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).
9. Ménétret, J. F. et al. Single copies of Sec61 and TRAP associate with a nontranslating mammalian ribosome. Structure 16, 1126-1137 (2008).
10. Becker, T. et al. Structure ofmonomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
11. Frauenfeld, J. et al. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nature Struct. Mol. Biol. 18, 614-621 (2011).
12. Berk, V., Zhang, W., Pai, R. D. & Cate, J. H. D. Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl Acad. Sci. USA 103, 15830-15834 (2006).
13. 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).
14. Park, E. & Rapoport, T. A. Preserving the membrane barrier for small molecules during bacterial protein translocation. Nature 473, 239-242 (2011).
15. Park, E. & Rapoport, T. A. Bacterial protein translocation requires only one copy of the SecY complex in vivo. J. Cell Biol. 198, 881-893 (2012).
16. Schierle, C. F. et al. The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J. Bacteriol. 185, 5706-5713 (2003).
17. Nakatogawa, H. & Ito, K. The ribosomal exit tunnel functions as a discriminating gate. Cell 108, 629-636 (2002).
18. Zhang, Y. et al. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 12, 913-923 (2003).
19. Muto, H., Nakatogawa, H. & Ito, K. Genetically encoded but nonpolypeptide prolyl-tRNA functions in the A site for SecM-mediated ribosomal stall. Mol. Cell 22, 545-552 (2006).
20. Sengupta, J., Agrawal, R. K. & Frank, J. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc. Natl Acad. Sci. USA 98, 11991-11996 (2001).
21. 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).
22. 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).
23. Knyazev, D. G. et al. The bacterial translocon SecYEG opens upon ribosome binding. J. Biol. Chem. 288, 17941-17946 (2013).
24. Shaw, A. S., Rottier, P. J. & Rose, J. K. Evidence for the loop model of signal-sequence insertion into the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 85, 7592-7596 (1988).
25. Hizlan, D. et al. Structure of the SecY complex unlocked by a preprotein mimic. Cell Rep 1, 21-28 (2012).
26. Matlack, K. E., Misselwitz, B., Plath, K. & Rapoport, T. A. BiP acts as a molecular ratchet during posttranslational transport of prepro-a factor across the ER membrane. Cell 97, 553-564 (1999).
27. Nicchitta, C. V. & Blobel, G. Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation. Cell 73, 989-998 (1993).
28. Tsukazaki, T. et al. Structure and function of a membrane component SecDF that enhances protein export. Nature 474, 235-238 (2011).
29. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
30. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
31. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000).
32. 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).
33. Nath, A., Atkins, W. M. & Sligar, S. G. Applications of phospholipid bilayer nanodiscsinthe studyofmembranes andmembrane proteins. Biochemistry 46, 2059-2069 (2007).
34. 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).
35. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
36. Jenner, L. B., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural aspects of messenger RNA readingframe maintenancebythe ribosome. Nature Struct. Mol. Biol. 17, 555-560 (2010).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
38. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
39. DiMaio, F., Tyka, M. D., Baker, M. L., Chiu, W. & Baker, D. Refinement of protein structures into low-resolution density maps using Rosetta. J. Mol. Biol. 392, 181-190 (2009).