Assembly of the translocase motor onto the preprotein-conducting channel

Molecular Microbiology

Volumn 70, Issue 2, 2008, Pages 311-322

  Karamanou, Spyridoula ^a   Bariami, Vassiliki ^a,b   Papanikou, Efrosyni ^a,b,d   Kalodimos, Charalampos G ^c   Economou, Anastassios ^a,b  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c RUTGERS UNIVERSITY   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; POLYPEPTIDE; PROTEIN SECA; PROTEIN SECYEG; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CYTOPLASM; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; TEMPERATURE SENSITIVITY; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

EID: 52649178409     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06402.x     Document Type: Article

References (66)

1. Baba, T., Jacq, A., Brickman, E., Beckwith, J., Taura, T., Ueguchi, C., et al. (1990) Characterization of cold-sensitive secY mutants of Escherichia coli. J Bacteriol 172 : 7005 7010.
2. Beck, K., Wu, L.F., Brunner, J. 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.
3. Bessonneau, P., Besson, V., Collinson, I. Duong, F. (2002) The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. EMBO J 21 : 995 1003.
4. den Blaauwen, T., Fekkes, P., de Wit, J.G., Kuiper, W. Driessen, A.J. (1996) Domain interactions of the peripheral preprotein translocase subunit SecA. Biochemistry 35 : 11994 12004.
5. den Blaauwen, T., de Wit, J.G., Gosker, H., van der Does, C., Breukink, E.J., de Leij, L. Driessen, A.J. (1997a) Inhibition of preprotein translocation and reversion of the membrane inserted state of SecA by a carboxyl terminus binding mAb. Biochemistry 36 : 9159 9168.
6. den Blaauwen, T., Terpetschnig, E., Lakowicz, J.R. Driessen, A.J. (1997b) Interaction of SecB with soluble SecA. FEBS Lett 416 : 35 38.
7. Breukink, E., Nouwen, N., van Raalte, A., Mizushima, S., Tommassen, J. de Kruijff, B. (1995) The C terminus of SecA is involved in both lipid binding and SecB binding. J Biol Chem 270 : 7902 7907.
8. Breyton, C., Haase, W., Rapoport, T.A., Kuhlbrandt, W. Collinson, I. (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418 : 662 665.
9. Brundage, L., Hendrick, J.P., Schiebel, E., Driessen, A.J. Wickner, W. (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62 : 649 657.
10. Chen, X., Xu, H. Tai, P.C. (1996) A significant fraction of functional SecA is permanently embedded in the membrane. SecA cycling on and off the membrane is not essential during protein translocation. J Biol Chem 271 : 29698 29706.
11. Chiba, K., Mori, H. Ito, K. (2002) Roles of the C-terminal end of SecY in protein translocation and viability of Escherichia coli. J Bacteriol 184 : 2243 2250.
12. Dapic, V. Oliver, D. (2000) Distinct membrane binding properties of N- and C-terminal domains of Escherichia coli SecA ATPase. J Biol Chem 275 : 25000 25007.
13. Derman, A.I., Puziss, J.W., Bassford, P.J., Jr, Beckwith, J. (1993) A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J 12 : 879 888.
14. van der Does, C., den Blaauwen, T., de Wit, J.G., Manting, E.H., Groot, N.A., Fekkes, P. Driessen, A.J. (1996) SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxyl terminus to the periplasm. Mol Microbiol 22 : 619 629.
15. van der Does, C., Manting, E.H., Kaufmann, A., Lutz, M. Driessen, A.J. (1998) Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry 37 : 201 210.
16. Duong, F. (2003) Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J 22 : 4375 4384.
17. Economou, A. Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78 : 835 843.
18. Economou, A., Pogliano, J.A., Beckwith, J., Oliver, D.B. Wickner, W. (1995) SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 83 : 1171 1181.
19. Eichler, J. 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.
20. Eichler, J. Wickner, W. (1998) The SecA subunit of Escherichia coli preprotein translocase is exposed to the periplasm. J Bacteriol 180 : 5776 5779.
21. Eichler, J., Brunner, J. Wickner, W. (1997) The protease-protected 30 kDa domain of SecA is largely inaccessible to the membrane lipid phase. EMBO J 16 : 2188 2196.
22. Gelis, I., Bonvin, A.M., Keramisanou, D., Koukaki, M., Gouridis, G., Karamanou, S., et al. (2007) Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131 : 756 769.
23. Hartl, F.U., Lecker, S., Schiebel, E., Hendrick, J.P. 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.
24. Hunt, J.F., Weinkauf, S., Henry, L., Fak, J.J., McNicholas, P., Oliver, D.B. Deisenhofer, J. (2002) Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297 : 2018 2026.
25. Jilaveanu, L.B., Zito, C.R. Oliver, D. (2005) Dimeric SecA is essential for protein translocation. Proc Natl Acad Sci USA 102 : 7511 7516.
26. Joly, J.C. 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.
27. Karamanou, S., Vrontou, E., Sianidis, G., Baud, C., Roos, T., Kuhn, A., et al. (1999) A molecular switch in SecA protein couples ATP hydrolysis to protein translocation. Mol Microbiol 34 : 1133 1145.
28. Karamanou, S., Sianidis, G., Gouridis, G., Pozidis, C., Papanikolau, Y., Papanikou, E. Economou, A. (2005) Escherichia coli SecA truncated at its termini is functional and dimeric. FEBS Lett 579 : 1267 1271.
29. Karamanou, S., Gouridis, G., Papanikou, E., Sianidis, G., Gelis, I., Keramisanou, D., et al. (2007) Preprotein-controlled catalysis in the helicase motor of SecA. EMBO J 26 : 2904 2914.
30. Keramisanou, D., Biris, N., Gelis, I., Sianidis, G., Karamanou, S., Economou, A. Kalodimos, C.G. (2006) Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nat Struct Mol Biol 13 : 594 602.
31. de Keyzer, J., van der Sluis, E.O., Spelbrink, R.E., Nijstad, N., de Kruijff, B., Nouwen, N., et al. (2005) Covalently dimerized SecA is functional in protein translocation. J Biol Chem 280 : 35255 35260.
32. Kim, Y.J., Rajapandi, T. Oliver, D. (1994) SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state. Cell 78 : 845 853.
33. Manting, E.H., Kaufmann, A., van der Does, C. Driessen, A.J. (1999) A single amino acid substitution in SecY stabilizes the interaction with SecA. J Biol Chem 274 : 23868 23874.
34. Manting, E.H., van Der Does, C., Remigy, H., Engel, A. Driessen, A.J. (2000) SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J 19 : 852 861.
35. Matsumoto, G., Yoshihisa, T. Ito, K. (1997) SecY and SecA interact to allow SecA insertion and protein translocation across the Escherichia coli plasma membrane. EMBO J 16 : 6384 6393.
36. Matsumoto, G., Nakatogawa, H., Mori, H. Ito, K. (2000) Genetic dissection of SecA: suppressor mutations against the secY205 translocase defect. Genes Cells 5 : 991 999.
37. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C.L., et al. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438 : 318 324.
38. Mori, H. Ito, K. (2001) An essential amino acid residue in the protein translocation channel revealed by targeted random mutagenesis of SecY. Proc Natl Acad Sci USA 98 : 5128 5133.
39. Mori, H. Ito, K. (2006) Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc Natl Acad Sci USA 103 : 16159 16164.
40. Natale, P., Swaving, J., van der Does, C., de Keyzer, J. Driessen, A.J. (2004) Binding of SecA to the SecYEG complex accelerates the rate of nucleotide exchange on SecA. J Biol Chem 279 : 13769 13777.
41. Nishiyama, K., Suzuki, T. Tokuda, H. (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85 : 71 81.
42. Or, E., Navon, A. Rapoport, T. (2002) Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J 21 : 4470 4479.
43. Osborne, A.R. 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.
44. Papanikou, E., Karamanou, S., Baud, C., Sianidis, G., Frank, M. Economou, A. (2004) Helicase Motif III in SecA is essential for coupling preprotein binding to translocation ATPase. EMBO Rep 5 : 807 811.
45. Papanikou, E., Karamanou, S., Baud, C., Frank, M., Sianidis, G., Keramisanou, D., et al. (2005) Identification of the preprotein binding domain of SecA. J Biol Chem 280 : 43209 43217.
46. Papanikou, E., Karamanou, S. Economou, A. (2007) Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 5 : 839 851.
47. Ramamurthy, V. Oliver, D. (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.
48. Randall, L.L., Crane, J.M., Lilly, A.A., Liu, G., Mao, C., Patel, C.N. Hardy, S.J. (2005) Asymmetric binding between SecA and SecB two symmetric proteins: implications for function in export. J Mol Biol 348 : 479 489.
49. Rapoport, T.A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450 : 663 669.
50. Reineke, U., Volkmer-Engert, R. Schneider-Mergener, J. (2001) Applications of peptide arrays prepared by the SPOT-technology. Curr Opin Biotechnol 12 : 59 64.
51. Robson, A., Booth, A.E., Gold, V.A., Clarke, A.R. Collinson, I. (2007) A large conformational change couples the ATP binding site of SecA to the SecY protein channel. J Mol Biol 374 : 965 976.
52. Scheuring, J., Braun, N., Nothdurft, L., Stumpf, M., Veenendaal, A.K., Kol, S., et al. (2005) The oligomeric distribution of SecYEG is altered by SecA and translocation ligands. J Mol Biol 354 : 258 271.
53. Schiebel, E., Driessen, A.J., Hartl, F.U. Wickner, W. (1991) Delta mu H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64 : 927 939.
54. Schmidt, M., Dina, H., Ramamurthy, V., Mukerji, I. Oliver, D. (2000) Nucleotide binding activity of SecA homodimer is conformationally regulated by temperature and altered by prlD and azi mutations. J Biol Chem 275 : 15540 15448.
55. Sianidis, G., Karamanou, S., Vrontou, E., Boulias, K., Repanas, K., Kyrpides, N., et al. (2001) Cross-talk between catalytic and regulatory elements in a DEAD motor domain is essential for SecA function. EMBO J 20 : 961 970.
56. van der Sluis, E.O., Nouwen, N., Koch, J., de Keyzer, J., van der Does, C., Tampe, R. Driessen, A.J. (2006) Identification of two interaction sites in SecY that are important for the functional interaction with SecA. J Mol Biol 361 : 839 849.
57. Smith, M.A., Clemons, W.M., Jr, DeMars, C.J. Flower, A.M. (2005) Modeling the effects of prl mutations on the Escherichia coli SecY complex. J Bacteriol 187 : 6454 6465.
58. Song, M. Kim, H. (1997) Stability and solvent accessibility of SecA protein of Escherichia coli. J Biochem (Tokyo) 122 : 1010 1018.
59. Tam, P.C., Maillard, A.P., Chan, K.K. Duong, F. (2005) Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J 24 : 3380 3388.
60. Taura, T., Akiyama, Y. Ito, K. (1994) Genetic analysis of SecY: additional export-defective mutations and factors affecting their phenotypes. Mol Gen Genet 243 : 261 269.
61. Tziatzios, C., Schubert, D., Lotz, M., Gundogan, D., Betz, H., Schagger, H., et al. (2004) The bacterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules. J Mol Biol 340 : 513 524.
62. Van den Berg, B., Clemons, W.M., Jr, Collinson, I., Modis, Y., Hartmann, E., Harrison, S.C. Rapoport, T.A. (2004) X-ray structure of a protein-conducting channel. Nature 427 : 36 44.
63. van Voorst, F., van der Does, C., Brunner, J., Driessen, A.J. de Kruijff, B. (1998) Translocase-bound SecA is largely shielded from the phospholipid acyl chains. Biochemistry 37 : 12261 12268.
64. Vrontou, E., Karamanou, S., Baud, C., Sianidis, G. Economou, A. (2004) Global co-ordination of protein translocation by the SecA IRA1 switch. J Biol Chem 279 : 22490 22497.
65. van der Wolk, J.P., Fekkes, P., Boorsma, A., Huie, J.L., Silhavy, T.J. Driessen, A.J. (1998) PrlA4 prevents the rejection of signal sequence defective preproteins by stabilizing the SecA-SecY interaction during the initiation of translocation. EMBO J 17 : 3631 3639.
66. Yahr, T.L. Wickner, W.T. (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J 19 : 4393 4401.