SecYEG assembles into a tetramer to form the active protein translocation channel

EMBO Journal

Volumn 19, Issue 5, 2000, Pages 852-861

  Manting, Erik H ^a   Van Der Does, Chris ^a   Remigy, Hervé ^b   Engel, Andreas ^b   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Preprotein translocation; SecA; SecY; Translocase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN; DIMER; MEMBRANE PROTEIN; TETRAMER;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ESCHERICHIA COLI; MEMBRANE CHANNEL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN QUATERNARY STRUCTURE; PROTEIN TRANSPORT; STOICHIOMETRY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0034161573     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.5.852     Document Type: Article

References (60)

1. Akita, M., Shinkai, A., Matsuyama, S. and Mizushima, S. (1991) SecA, an essential component of the secretory machinery of Escherichia coli, exists as homodimer. Biochem. Biophys. Res. Commun., 174, 211-216.
2. Arkowitz, R.A. and Wickner, W. (1994) SecD and SecF are required for the proton electrochemical gradient stimulation of preprotein translocation. EMBO J., 13, 954-963.
3. Baba, T., Taura, T., Shimioke, T., Akiyama, Y., Yoshihisa, T. and Ito, K. (1994) A cytoplasmic domain is important for the formation of a SecY-SecE translocator complex. Proc. Natl Acad. Sci. USA, 91, 4539-4543.
4. Bassilana, M. and Wickner, W. (1993) Purified Escherichia coli preprotein translocase catalyses multiple cycles of precursor protein translocation. Biochemistry, 32, 2626-2630.
5. Beckmann, R., Bubeck, D., Grassucci, R., Penczek, P., Verschoor, A., Blobel, G. and Frank, J. (1997) Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex. Science, 278, 2123-2126.
6. Bevington, P.R. (1969) Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York, NY.
7. Brundage, L.A., Hendrick, J.P., Schiebel, E., Driessen, A.J.M. and Wickner, W. (1990) The purified Escherichia coli integral membrane protein SecY/E is sufficient for the reconstitution of SecA-dependent precursor protein translocation. Cell, 62, 649-657.
8. Cabelli, R.J., Chen, L., Tai, P.C. and Oliver, D.B. (1988) SecA protein is required for secretory protein translocation into E.coli membrane vesicles. Cell, 55, 683-692.
9. Chen, X., Xu, H. and Tai, P. (1996) A significant fraction of SecA is permanently embedded in the membrane. J. Biol. Chem., 271, 29698-29706.
10. Crooke, E., Guthrie, B., Lecker, S., Lill, R. and Wickner, W. (1988) ProOmpA is stabilized for membrane translocation by either purified E.coli trigger factor or canine signal recognition particle. Cell, 54, 1003-1011.
11. den Blaauwen, T., Fekkes, P., de Wit, J.G., Kuiper, W. and Driessen, A.J.M. (1996) Domain interactions of the peripheral preprotein translocase subunit SecA. Biochemistry, 35, 11994-12004.
12. den Blaauwen, T., de Wit, J.G., Gosker, H., van der Does, C., Breukink, E.-J., de Leij, L. and Driessen, A.J.M. (1997) Inhibition of preprotein translocation and reversion of the membrane inserted state of SecA by a carboxyl terminus binding mAb. Biochemistry, 36, 9159-9168.
13. Douville, K., Price, A., Eichler, J., Economou, T. and Wickner, W. (1995) SecYEG and SecA are the stoichiometric components of preprotein translocase. J. Biol. Chem., 270, 20106-20111.
14. 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.
15. Duong, F. and Wickner, W. (1998) Sec-dependent membrane protein biogenesis: SecYEG, preprotein hydrophobicity and translocation kinetics control the stop-transfer function. EMBO J., 17, 696-705.
16. Driessen, A.J.M. (1992) Precursor protein translocation by the Escherichia coli translocase is directed by the proton motive force. EMBO J., 11, 847-853.
17. Driessen, A.J.M. (1993) SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer. Biochemistry, 32, 13190-13197.
18. Driessen, A.J.M., Fekkes, P. and van der Wolk, J.P.W. (1998) The Sec system. Curr. Opin. Microbiol., 1, 216-222.
19. Economou, A. (1998) Bacterial preprotein translocase: mechanism and conformational dynamics of a processive enzyme. Mol. Microbiol., 27, 511-518.
20. Economou, A. and Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell, 78, 835-843.
21. Eichler, J. and Wickner, W. (1997) Both an N-terminal 65-kDa domain and a C-terminal 30-kDa domain of SecA cycle into the membrane at SecYEG during translocation. Proc. Natl Acad. Sci. USA, 94, 5574-5581.
22. Eichler, J., Brunner, J. and Wickner, W. (1997) The protease-protected 30 kDa domain of SecA is largely inaccessible to the membrane lipid phase. EMBO J., 16, 2188-2196.
23. Flower, A.M., Osborne, R.S. and Silhavy, T.J. (1995) The allele-specific synthetic lethality of prlA-prlG double mutants predicts interactive domains of SecY and SecE. EMBO J., 14, 884-893.
24. Frank, J., Bretaudiere, J.-P., Carazo, J.-M., Verschoor, A. and Wagenknecht, T. (1988) Classification of images of biomolecular assemblies. A study of ribosomes and ribosomal subunits of Escherichia coli. J. Microsc., 150, 99-115.
25. Geller, B.L. (1990) Electrochemical potential releases a membrane-bound secretion intermediate of maltose-binding protein in Escherichia coli. J. Bacteriol., 172, 4870-4876.
26. Hamman, B.D., Chen, J.-C., Johnson, E.E. and Johnson, A.E. (1997) 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.
27. Hamman, B.D., Hendershot, L.M. and Johnson, A.E. (1998) BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell, 92, 747-758.
28. Hanada, M., Nishiyama, K., Mizushima, S. and Tokuda, H. (1994) Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE and SecG (p12). J. Biol. Chem., 269, 23625-23631.
29. Hanein, D., Matlack, K.E.S., Jungnickel, B., Plath, K., Kalies, K.-U., Miller, K.R., Rapoport, T.A. and Akey, C.W. (1996) Oligomeric rings of the Sec61 complex induced by ligands required for protein translocation. Cell, 87, 721-732.
30. Hartl, F.-U., Lecker, S., Schiebel, E., Hendrick, J.P. and Wickner, W. (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E.coli plasma membrane. Cell, 63, 269-279.
31. Hartmann, E., Sommer, T., Prehn, S., Görlich, D., Jentsch, S. and Rapoport, T.A. (1994) Evolutionary conservation of the components of the protein translocation complex. Nature, 367, 654-657.
32. Hendrick, J.P. and Wickner, W. (1991) SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J. Biol. Chem., 266, 24596-24600.
33. Joly, J.C. and Wickner, W. (1993) The SecA and SecY subunits of translocase are the nearest neighbors of a translocating preprotein, shielding it from phospholipids. EMBO J., 12, 255-263.
34. Joly, J.C., Leonard, M. and Wickner, W. (1994) Subunit dynamics in Escherichia coli preprotein translocase. Proc. Natl Acad. Sci. USA, 91, 4703-4707.
35. Kim, Y.J., Rajapandi, T. and Oliver, D.B. (1994) SecA protein is exposed to the periplasmic surface of the E.coli inner membrane in its active state. Cell, 78, 845-853.
36. Lill, R., Dowham, W. and Wickner, W. (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY and the leader and mature domains of precursor proteins. Cell, 60, 271-280.
37. Manting, E.H., van der Does, C. and Driessen, A.J.M. (1997) In vivo crosslinking of the SecA and SecY subunits of the Escherichia coli preprotein translocase. J. Bacteriol., 179, 5699-5704.
38. Matsuyama, S., Akimura, J. and Mizushima, S. (1990) SecE-dependent overproduction of SecY in Escherichia coli. FEBS Lett., 269, 96-100.
39. Matsuyama, S., Fujita, Y. and Mizushima, S. (1993) SecD is involved in the release of translocated secretory proteins from the cytoplasmic membrane of Escherichia coli. EMBO J., 12, 265-270.
40. Meyer, T.H., Ménétret, J.-F., Breitling, R., Miller, K.R., 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.
41. Müller, S.A. and Engel, A. (1998) Mass measurement in the scanning transmission electron microscope: a powerful tool for studying membrane proteins. J. Struct. Biol., 121, 219-230.
42. Müller, S.A., Goldie, K.N., Bürki, R., Häring, R. and Engel, A. (1992) Factors influencing the precision of quantitative scanning transmission electron microscopy. Ultramicroscopy, 46, 317-334.
43. Nishiyama, K.-i., Mizushima, S. and Tokuda, H. (1993) A novel membrane protein involved in protein translocation across the cytoplasmic membrane of Escherichia coli. EMBO J., 12, 3409-3415.
44. Nishiyama, K.-i., Suzuki, T. and Tokuda, H. (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell, 85, 71-81.
45. Nishiyama, K.-i., Fukuda, A., Morita, K. and Tokuda, H. (1999) Membrane-deinsertion of SecA underlying proton motive force-dependent stimulation of protein translocation. EMBO J., 18, 1049-1058.
46. 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.
47. Price, A., Economou, A., Duong, F. and Wickner, W. (1996) Separable ATPase and membrane insertion domains of the SecA subunit of preprotein translocase. J. Biol. Chem., 271, 31580-31584.
48. Ramamurthy, V. and Oliver, D.B. (1997) Topology of the integral membrane form of Escherichia coli SecA protein reveals multiple periplasmically exposed regions and modulation by ATP binding. J. Biol. Chem., 272, 23239-23246.
49. Sagara, K., Matsuyama, S. and Mizushima, S. (1994) SecF stabilizes SecD and SecY, components of the protein translocation machinery of the Escherichia coli cytoplasmic membrane. J. Bacteriol., 176, 4111-4116.
50. Saxton, W.O., Pitt, T.J. and Horner, M. (1979) Digital image processing: the Semper system. Ultramicroscopy, 4, 343-354.
51. + and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell, 64, 927-939.
52. Snyders, S., Ramamurhty, V. and Oliver, D.B. (1997) Identification of a region of interaction between Escherichia coli SecA and SecY proteins. J. Biol. Chem., 272, 11302-11306.
53. Swaving, J., van Wely, K.H.M. and Driessen, A.J.M. (1999) Host specificity is determined by the core subunits of preprotein translocase. J. Bacteriol., 181, 7021-7027.
54. Tani, K., Tokuda, H. and Mizushima, S. (1990) Translocation of proOmpA possessing an intramolecular disulphide bridge into membrane vesicles of Escherichia coli. Effect of membrane energization. J. Biol. Chem., 265, 17341-17347.
55. van der Does, C., den Blaauwen, T., de Wit, J.G., Manting, E.H., Groot, N., Fekkes, P. and Driessen, A.J.M. (1996) SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxy-terminus to the periplasm. Mol. Microbiol., 22, 619-629.
56. van der Does, C., Manting, E.H., Kaufmann, A., Lutz, M. and Driessen, A.J.M. (1998) Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry, 37, 201-210.
57. van der Wolk, J.P.W., de Wit, J.G. and Driessen, A.J.M. (1997) The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J., 16, 7297-7304.
58. van Voorst, F., van der Does, C., Brunner, J., Driessen, A.J.M. and de Kruijff, B. (1998) Translocase-bound SecA is largely shielded from the phospholipid acyl chains. Biochemistry, 37, 12261-12268.
59. van Wely, K.H.M., Swaving, J., Broekhuizen, C.P., Rose, M., Quax, W.J. and Driessen, A.J.M. (1999) Functional identification of the product of the Bacillus subtilis yvalL gene as a SecG homologue. J. Bacteriol., 181, 1786-1791.
60. Weiss, J.B., Ray, P.H. and Bassford, P.J., Jr (1988) Purified secB protein of Escherichia coli retards folding and promotes membrane translocation of the maltose-binding protein in vitro. Proc. Natl Acad. Sci. USA, 85, 8978-8982.