Visualization of distinct entities of the SecYEG translocon during translocation and integration of bacterial proteins

Molecular Biology of the Cell

Volumn 20, Issue 6, 2009, Pages 1795-1803

  Boy, Diana ^a   Koch, Hans Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MANNITOL PERMEASE; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; PROTEIN SECYEG SEC61; PROTEIN YIDC; SECRETORY PROTEIN; SECY PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; SEC61 PROTEIN; SECE PROTEIN, E COLI; SECG PROTEIN, E COLI; SECY PROTEIN, E COLI;

ARTICLE; BACTERIAL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT; CELL MEMBRANE; ENZYME SPECIFICITY; GENETICS; METABOLISM; MOLECULAR WEIGHT; PROTEIN MULTIMERIZATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

BACTERIAL PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MOLECULAR WEIGHT; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY;

EID: 65249159700     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1048     Document Type: Article

References (76)

1. Akiyama, Y., Kihara, A., Tokuda, H., and Ito, K. (1996). FtsH (HflB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins. J. Biol. Chem. 271, 31196-31201.
2. Alami, M., Dalal, K., Lelj-Garolla, B., Sligar, S. G., and Duong, F. (2007). Nanodiscs unravel the interaction between the SecYEG channel and its cyto- solic partner SecA. EMBO J. 26, 1995-2004.
3. Angelini, S., Deitermann, S., and Koch, H. G. (2005). FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep. 6, 476-481.
4. Angelini, S., Boy, D., Schiltz, E., and Koch, H. G. (2006). Membrane binding of the bacterial signal recognition particle receptor involves two distinct binding sites. J. Cell Biol. 174, 715-724.
5. Bahari, L., Parlitz, R., Eitan, A., Stjepanovic, G., Bochkareva, E. S., Sinning, I., and Bibi, E. (2007). Membrane targeting of ribosomes and their release require distinct and separable functions of FtsY. J. Biol. Chem. 282, 32168-32175.
6. Beck, K., Wu, L. F., Brunner, J., and Muller, M. (2000). Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 19, 134-143.
7. Beck, K., Eisner, G., Trescher, D., Dalbey, R., Brunner, J., and Muller, M. (2001). YidC, an assembly site for polytopic Escherichia coli membrane proteins located in immediate proximity to the SecYE translocon and lipids. EMBO Rep. 2, 709-714.
8. Beckmann, R., Spahn, C., Frank, J., and Blobel., G. (2001). The active 80S ribosome-Sec61 complex. Cold Spring Harb. Symp. Quant. Biol. 66, 543-554.
9. Beha, D., Deitermann, S., Müller, M., and Koch, H. G. (2003). Export of beta-lactamase is independent of the signal recognition particle. J. Biol. Chem. 278, 22161-22167.
10. Behrmann, M., Koch, H. G., Hengelage, T., Wieseler, B., Hoffschulte, H. K., and Müller, M. (1998). Requirements fort he translocation of elongation- arrested, ribosome-associated OmpA across the plasma membrane of E. coli. J. Biol. Chem. 273, 13898-13904.
11. Bessonneau, P., Besson, V., Collinson, I., and Duong, F. (2002). The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. EMBO J. 21, 995-1003.
12. Bostina, M., Mohsin, B., Kühlbrandt, W., and Collinson, I. (2005). Atomic model of the E. coli membrane-bound protein translocation complex SecYEG. J. Mol. Biol. 352, 1035-1043.
13. Breyton, C., Haase, W., Rapoport, T., Kühlbrandt, W., and Collinson, I. (2002). Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665.
14. Cannon, K., Or, E., Clemons, W. M., Shibata, Y., and Rapoport, T. (2005). Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J. Cell Biol. 169, 219-225.
15. Chiba, S., Akiyama, Y., and Ito, K. (2002). Membrane protein degradation by FtsH can be initiated from either end. J. Bacteriol. 184, 4775-4782.
16. Collinson, I., Breyton, C., Duong, F., Tziatzios, C., Schubert, D., Or, E., Rapoport, T., and Kuhlbrandt, W. (2001). Projection structure and oligomeric properties of a bacterial core protein translocase. EMBO J. 20, 2462-2471.
17. de Keyzer, J., van der Does, C., and Driessen, A. (2003). The bacterial trans- locase: a dynamic protein channel complex. Cell. Mol. Life Sci. 60, 2034-2052.
18. de Keyzer, J., van der Laan, M., and Driessen, A. (2007). Membrane protein insertion and secretion in bacteria. Methods Mol. Biol. 390, 17-31.
19. Duong, F., and Wickner, W. (1997). Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. 16, 2756-2768.
20. Duong, F. (2003). Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J. 22, 4375-4384.
21. Duong, F. (2007). Fraternal twins. Nature 446, 741-742.
22. Erlandson, K. J., Miller, S.B.M., Nam, Y., Osborne, A. R., Zimmer, J., and Rapoport, T. A. (2008). A role for the two-helix finger of the SecA ATPase in protein translocation. Nature 455, 984-988.
23. Goder, V., and Spiess, M. (2003). Molecular mechanism of signal sequence orientation in the endoplasmic reticulum. EMBO J. 22, 3645-3653.
24. Halic, M., and Beckmann, R. (2005). The signal recognition particle and its interactions during protein targeting. Curr. Opin. Struct. Biol. 15, 116-125.
25. Hamman, B., Chen, J., Johnson, E., and Johnson, A. (1997). The aqueous pore through the translocon has a diameter of 40-60A during cotranslational protein translocation at the ER membrane. Cell 89, 535-544.
26. Hanein, D., Matlack, K., Jungnickel, B., Plath, K., Kalies, K., Miller, K., Rap- oport, T., and Akey, C. (1996). Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 87, 721-732.
27. Harris, C., and Silhavy, T. J. (1999). Mapping an interface of SecY (PrlA) and SecE (PrlG) by using synthetic phenotypes and in vivo cross-linking. J. Bac- teriol. 181, 3438-3444.
28. Heinrich, S., and Rapoport, T. (2003). Cooperation of transmembrane segments during integration of a double-spanning protein into the ER membrane. EMBO J. 22, 3654-3663.
29. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H., and Poolman, B. (2002). Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentifugation. J. Mol. Biol. 317, 591-600.
30. Ito, K. (1984). Identification of the secY (prlA) gene product involved in protein export in Escherichia coli. Mol. Gen. Genet. 197, 204-208.
31. Junne, T., Schwede, T., Goder, V., and Spiess, M. (2006). The plug domain of yeast Sec61p is important for efficient protein translocation, but is not essential for cell viability. Mol. Biol. Cell 17, 4063-4068.
32. Kida, Y., Morimoto, F., and Sakaguchi, M. (2007). Two translocationg hydro- philic segments of a nascent chain span the ER membrane during multispan- ning protein topogenesis. J. Cell Biol. 179, 1441-1452.
33. Koch, H. G., Hengelage, T., Neumann-Haefelin, C., MacFarlane, J., Hoffschulte, H., Schimz, K., Mechler, B., and Müller, M. (1999). In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/ SecB as constituents of two independent protein-targeting pathways of E. coli. Mol. Biol. Cell 10, 2163-2173.
34. Koch, H. G., and Müller, M. (2000). Dissecting the translocase and integrase functions of the E. coli SecYEG translocon. J. Cell Biol. 150, 689 -694.
35. Koch, H. G., Moser, M., Schimz, K., and Müller, M. (2002). The integration of YidC into the cytoplasmic membrane of E. coli requires the signal recognition particle, SecA and SecYEG. J. Biol. Chem. 277, 5715-5718.
36. Koch, H. G., Moser, M., and Muller, M. (2003). Signal recognition particle- dependent protein targeting, universal to all kingdoms of life. Rev. Physiol. Biochem. Pharmacol. 146, 55-94.
37. 3-type cytochrome c oxidase complex. J. Mol. Biol. 355, 989-1004.
38. 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.
39. Maillard, A., Lalani, S., Silva, F., Belin, D., and Duong, F. (2007). Deregulation of the SecYEG translocation channel upon removal of the plug domain. J. Biol. Chem. 282, 1281-1287.
40. Manting, E., van der Does, C., Remigy, H., Engel, A., and Driessen, A. (2000). SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19, 852-861.
41. Matlack, K., Plath, K., Misselwitz, B., and Rapoport, T. A. (1997). Protein transport by purified yeast Sec complex and Kar2p without membranes. Science 277, 938-941.
42. Matsumoto, G., Yoshihisa, T., and Ito, K. (1997). SecY and SecA interact to allow SecA insertion and protein translocation across the E. coli plasma membrane. EMBO J. 16, 6384-6393.
43. McCormick, P., Miao, Y., Shao, Y., Lin, J., and Johnson, A. E. (2003). Cotrans- lational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329-341.
44. Menetret, J., Hegde, R., Heinrich, S., Chandramouli, P., Ludtke, S., Rapoport, T. A., and Akey, C. (2005). Architecture of the ribosome-channel complex derived from native membranes. J. Mol. Biol. 348, 445-457.
45. Menetret, J. F. et al. (2007). Ribosome binding of a single copy of the SecY complex: implications for protein translocation. Mol. Cell 28, 1083-1092.
46. Meyer, T., Menetret, J., Breitling, R., Miller, K., Akey, C. W., and Rapoport, T. A. (1999). The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J. Mol. Biol. 285, 1789-1800.
47. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C. L., Ban, N., Frank, J. (2005). Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438, 318-324.
48. Mitra, K., Frank, J., and Driessen, A. J. (2006). Co- and post-translational translocation through the protein-conducting channel: analogous mechanisms at work? Nat. Struct. Mol. Biol. 13, 957-964.
49. Mori, H., and Ito, K. (2003). Biochemical characterization of a mutationally altered protein translocase: proton motive force stimulation of the initiation phase of translocation. J. Bacteriol. 185, 405-412.
50. Mori, H., Tsukazaki, T., Masui, R., Kuramitsu, S., Yokoyama, S., Johnson, A., Kimura, Y., Akiyama, Y., and Ito, K. (2003). Fluorescence resonance energy transfer analysis of protein translocase. J. Biol. Chem. 278, 14257-14264.
51. Nagamori, S., Vazquez-Ibar, J., Weinglass, A., and Kaback, H. R. (2003). In vitro synthesis of lactose permease to probe the mechanism of membrane insertion and folding. J. Biol. Chem. 278, 14820-14826.
52. Neumann-Haefelin, C., Schafer, U., Miiller, M., and Koch, H. G. (2000). SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J. 19, 6419-6426.
53. Newitt, J. A., and Bernstein, H. D. (1998). A mutation in the Escherichia coli secY gene that produces distinct effects on inner membrane protein insertion and protein export. J. Biol. Chem. 273, 12451-12456.
54. Nishiyama, K., Ikegami, A., Moser, M., Schiltz, E., Tokuda, H., and Müller, M. (2006). A derivative of lipid A is involved in signal recognition particle/ SecYEG-dependent and -independent membrane integrations. J. Biol. Chem. 281, 35667-35676.
55. Nouwen, N., and Driessen, A. (2002). SecDFya C forms a heterotetrameric complex with YidC. Mol. Microbiol. 44, 1397-1405.
56. Osborne, A., 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.
57. Pogliano, K. J., and Beckwith, J. (1994). Genetic and molecular characterization of the Escherichia coli secD operon and its products. J. Bacteriol. 176, 804-814.
58. Sadlish, H., Pitonzo, D., Johnson, A. E., and Skach, W. R. (2005). Sequential triage of transmembrane segments by Sec61a during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 12, 870-878.
59. Samuelson, J., Chen, M., Jiang, F., Moller, I., Wiedmann, M., Kuhn, A., Phillips, G., and Dalbey, R. (2000). YidC mediates membrane protein insertion in bacteria. Nature 406, 637-641
60. Schagger, H. (2001). Blue native gels to isolate protein complexes from mitochondria. Methods Cell Biol. 65, 231-244.
61. Schaletzky, J., and Rapoport, T. A. (2006). Ribosome binding to and dissociation from translocation sites of the endoplasmic reticulum membrane. Mol. Biol. Cell 17, 3860-3869.
62. Scheuring, J., Braun, N., Nothdurft, L., Stumpf, M., Veenendaal, A., Kol, S., van der Does, C., Driessen, A., and Weinkauf, S. (2005). The oligomeric distribution of SecYEG is altered by SecA and translocation ligands. J. Mol. Biol. 354, 258 -271.
63. Scotti, P., Urbanus, M., Brunner, J., de Gier, J. W., von Hei ne, G., van der Does, C., Driessen, A., Oudega, B., and Luirink, J. (2000). YidC, the E. coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549.
64. Taura, T., Yoshihisa, T., and Ito, K. (1997). Protein translocation functions of E. coli SecY: in vitro characterization of cold-sensitive secY mutants. Biochimie 79, 517-521.
65. Traxler, B., and Murphy, C. (1996). Insertion of the polytopic membrane protein MalF is dependent on the bacterial secretion machinery. J. Biol. Chem. 271, 12394-12400.
66. 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.
67. Urbanus, M., Scotti, P., Froderberg, L., Saaf, A., de Gier, J. W., Brunner, J., Samuelson, J., Dalbey, R., Oudega, B., and Luirink, J. (2001). Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep. 2, 524-529.
68. van den Berg, B., Clemons, W. M., Collinson, I., Modis, Y., Hartmann, E., Harrison, S., and Rapoport, T. A. (2004). X-ray structure of a protein-conducting channel. Nature 427, 36 -44.
69. van der Does, C., den Blaauwen, T., de Wit, J., Manting, E., Groot, N., Fekkes, P., and Driessen, A. (1996). SecA is an intrinsic subunit of the E. coli preprotein translocase and exposes its carboxyl terminus to the periplasm. Mol. Micro- biol. 22, 619-629.
70. van der Does, C., de Keyzer, J., van der Laan, M., and Driessen, A. (2003). Reconstitution of purified bacterial preprotein translocase in liposomes. Methods Enzymol. 372, 86-98.
71. Weiche, B., Burk, J., Angelini, S., Schiltz, E., Thumfart, J. O., and Koch, H. G. (2008). A cleavable N-terminal membrane anchor is involved in membrane binding of the Escherichia coli SRP receptor. J. Mol. Biol. 377, 761-773.
72. Wiedemann, N., Kozjak, V., Chacinska, A., Schonfisch, B., Rospert, S., Ryan, M. T., Pfanner, N., and Meisinger, C. (2003). Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424, 565-571.
73. Wirth, A., Jung, M., Bies, C., Frien, M., Tyedmers, J., Zimmermann, R., and Wagner, R. (2003). The Sec61p complex is a dynamic precursor activated channel. Mol. Cell 12, 261-268.
74. Xie, K., Kiefer, D., Nagler, G., Dalbey, R., and Kuhn, A. (2006). Different regions of the nonconserved large periplasmic domain of E. coli YidC are involved in the SecF interaction and membrane insertase activity. Biochemistry 45, 13401-13408.
75. Yahr, T. L., and Wickner, W. T. (2000). Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J. 19, 4393-4401.
76. 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.