Molecular mechanisms underlying the early stage of protein translocation through the Sec translocon

Biochemistry

Volumn 49, Issue 5, 2010, Pages 945-950

  Mori, Takaharu ^a,b   Ishitani, Ryuichiro ^c   Tsukazaki, Tomoya ^c   Nureki, Osamu ^c   Sugita, Yuji ^a,b  

^a RIKEN   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSED FORM; CONFORMATIONAL CHANGE; CONFORMATIONAL TRANSITIONS; CROSS-MEMBRANES; CYTOSOLIC; EXPLICIT SOLVENTS; FAB FRAGMENTS; GATE REGION; LIPID MOLECULES; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; POSITIVELY CHARGED; PROTEIN TRANSLOCATION; PROTEIN-CONDUCTING CHANNELS; RESTING STATE; SIGNAL PEPTIDE; THERMUS THERMOPHILUS; TRANSITIONAL STATE; TRANSLOCON;

BACTERIOLOGY; COMPLEXATION; CONFORMATIONS; MOLECULAR DYNAMICS; PHOSPHOLIPIDS;

PROTEINS;

IMMUNOGLOBULIN F(AB) FRAGMENT; PROTEIN SECA; SEC TRANSLOCON; SECY PROTEIN; SECYE BETA PROTEIN; SECYE PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; METHANOCOCCUS JANNASCHII; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; THERMUS THERMOPHILUS;

ADENOSINE TRIPHOSPHATASES; ARCHAEAL PROTEINS; BACTERIAL PROTEINS; MEMBRANE TRANSPORT PROTEINS; METHANOCOCCUS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN TRANSPORT; THERMUS THERMOPHILUS;

EUKARYOTA; METHANOCALDOCOCCUS JANNASCHII; THERMUS THERMOPHILUS;

EID: 75749143418     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901594w     Document Type: Article

References (34)

1. Van den Berg, B., Clemons, W. M., Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004) X-ray structure of a protein-conducting channel. Nature 427, 36-44.
2. Rapoport, T. A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669.
3. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C. L., III, Ban, N., and Frank, J. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438, 318-324.
4. Menetret, J. F., Schaletzky, J., Clemons, W. M., Jr., Osborne, A. R., Skanland, S. S., Denison, C., Gygi, S. P., Kirkpatrick,D. S., Park, E., Ludtke, S. J., Rapoport, T. A., and Akey, C. W. (2007) Ribosome binding of a single copy of the SecY complex: Implications for protein translocation. Mol. Cell 28, 1083-1092.
5. Douville, K., Price, A., Eichler, J., Economou, A., and Wickner, W. (1995) SecYEG and SecA are the stoichiometric components of preprotein translocase. J. Biol. Chem. 270, 20106-20111.
6. Hunt, J. F., Weinkauf, S., Henry, L., Fak, J. J., McNicholas, P., Oliver, D. B., and Deisenhofer, J. (2002) Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297, 2018-2026.
7. Osborne, A. R., Clemons, W. M., Jr., and Rapoport, T. A. (2004) A large conformational change of the translocation ATPase SecA. Proc. Natl. Acad. Sci. U.S.A. 101, 10937-10942.
8. Vrontou, E., and Economou, A. (2004) Structure and function of SecA, the preprotein translocase nanomotor. Biochim. Biophys. Acta 1694, 67-80.
9. Mori, H., and Ito, K. (2001) The Sec protein-translocation pathway. Trends Microbiol. 9, 494-500.
10. Veenendaal, A. K., van der Does, C., and Driessen, A. J. (2004) The protein-conducting channel SecYEG. Biochim. Biophys. Acta 1694, 81-95.
11. Papanikou, E., Karamanou, S., and Economou, A. (2007) Bacterial protein secretion through the translocase nanomachine. Nat. Rev. Microbiol. 5, 839-851.
12. Li, W., Schulman, S., Boyd, D., Erlandson, K., Beckwith, J., and Rapoport, T. A. (2007) The plug domain of the SecY protein stabilizes the closed state of the translocation channel and maintains a membrane seal. Mol. Cell 26, 511-521.
13. Zimmer, J., Nam, Y., and Rapoport, T. A. (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455, 936-943.
14. Tsukazaki, T., Mori, H., Fukai, S., Ishitani, R., Mori, T., Dohmae, N., Perederina, A., Sugita, Y., Vassylyev, D. G., Ito, K., and Nureki, O. (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455, 988-991.
15. Haider, S., Hall, B. A., and Sansom, M. S. (2006) Simulations of a protein translocation pore: SecY. Biochemistry 45, 13018-13024.
16. Tian, P., and Andricioaei, I. (2006) Size, motion, and function of the SecY translocon revealed by molecular dynamics simulations with virtual probes. Biophys. J. 90, 2718-2730.
17. Gumbart, J., and Schulten, K. (2007) Structural determinants of lateral gate opening in the protein translocon. Biochemistry 46, 11147-11157.
18. Tam, P. C., Maillard, A. P., Chan, K. K., and Duong, F. (2005) Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J. 24, 3380-3388.
19. Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., Phillips, J., Shinozaki,A., Varadarajan, K., and Schulten, K. (1999) NAMD2: Greater scalability for parallel molecular dynamics. J. Comput. Phys. 151, 283-312.
20. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., III, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616.
21. Mackerell, A. D., Jr., Feig, M., and Brooks, C. L., III (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415.
22. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: An N.log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
23. Hubbard, S. J., and Thornton, J. M. (1993) NACCESS, Department of Biochemistry and Molecular Biology, University College London, London.
24. Petrek, M., Kosinova, P., Koca, J., and Otyepka,M. (2007) MOLE:A Voronoi diagram-based explorer of molecular channels, pores, and tunnels. Structure 15, 1357-1363.
25. Hayward, S., Kitao, A., and Berendsen, H. J. (1997) Model-free methods of analyzing domain motions in proteins from simulation: a comparison of normal mode analysis and molecular dynamics simulation of lysozyme. Proteins 27, 425-437.
26. Mori, H., and Ito, K. (2001) An essential amino acid residue in the protein translocation channel revealed by targeted random mutagenesis of SecY. Proc. Natl. Acad. Sci. U.S.A. 98, 5128-5133.
27. de Keyzer, J., Regeling, A., and Driessen, A. J. (2007) Arginine 357 of SecY is needed for SecA-dependent initiation of preprotein translocation. FEBS Lett. 581, 1859-1864.
28. Cheng, Z., Jiang, Y., Mandon, E. C., and Gilmore, R. (2005) Identification of cytoplasmic residues of Sec61p involved in ribosome binding and cotranslational translocation. J. Cell Biol. 168, 67-77.
29. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807.
30. van Dalen, A., and de Kruijff, B. (2004) The role of lipids in membrane insertion and translocation of bacterial proteins. Biochim. Biophys. Acta 1694, 97-109.
31. McKnight, C. J., Briggs, M. S., and Gierasch, L. M. (1989) Functional and nonfunctional LamB signal sequences can be distinguished by their biophysical properties. J. Biol. Chem. 264, 17293-17297.
32. Keller, R. C., Killian, J. A., and de Kruijff, B. (1992) Anionic phospholipids are essential for α-helix formation of the signal peptide of prePhoE upon interaction with phospholipid vesicles. Biochemistry 31, 1672-1677.
33. Breyton, C., Haase, W., Rapoport, T. A., Kuhlbrandt, W., and Collinson, I. (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665.
34. Osborne, A. R., and Rapoport, T. A. (2007) Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 129, 97-110.