The oligomeric distribution of SecYEG is altered by SecA and translocation ligands

Journal of Molecular Biology

Volumn 354, Issue 2, 2005, Pages 258-271

  Scheuring, Johannes ^a   Braun, Nathalie ^a   Nothdurft, Lars ^a,c   Stumpf, Matthias ^a,d   Veenendaal, Andreas K J ^b   Kol, Stefan ^b   Van Der Does, Chris ^b,e   Driessen, Arnold J M ^b   Weinkauf, Sevil ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c SAS Hagmann   (Germany)

^d Tietz Video and Image Processing Systems GmbH   (Germany)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

Electron microscopy; Oligomerization; Preprotein translocation; SecYEG; Translocase

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DIMER; MONOMER; OLIGOMER; PROTEIN PRECURSOR; PROTEIN SECA; SECYEG PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; FREEZE FRACTURE; MEMBRANE; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; PROTEOLIPOSOME; STIMULATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 27644518797     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.09.058     Document Type: Article

References (54)

1. E.H. Manting, and A.J.M. Driessen Escherichia coli translocase: the unraveling of a molecular machine Mol. Microbiol. 37 2000 226 238
2. A.J.M. Driessen, E.H. Manting, and C. van der Does The structural basis of protein targeting and translocation in bacteria Nature Struct. Biol. 8 2001 492 498
3. H. Mori, and K. Ito The Sec protein-translocation pathway Trends Microbiol. 9 2001 494 500
4. J. de Keyzer, C. van der Does, and A.J.M. Driessen The bacterial translocase: a dynamic protein channel complex Cell Mol. Life Sci. 60 2003 2034 2052
5. A. Economou, and W. Wickner SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion Cell 78 1994 835 843
6. H+ and ATP function at different steps of the catalytic cycle of preprotein translocase Cell 64 1991 927 939
7. J.P. van der Wolk, J.G. de Wit, and A.J.M. Driessen The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events EMBO J. 16 1997 7297 7304
8. J.C. Joly, and W. Wickner The SecA and SecY subunits of translocase are the nearest neighbors of a translocating preprotein, shielding it from phospholipids EMBO J. 12 1993 255 263
9. J. Eichler, and W. Wickner 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 1997 5574 5581
10. F. Duong, and W. Wickner Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme EMBO J. 16 1997 2756 2768
11. F. Duong, and W. Wickner The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling EMBO J. 16 1997 4871 4879
12. P.A. Scotti, M.L. Urbanus, J. Brunner, J.W.L. de Gier, G. von Heinje, and C. van der Does YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the sec translocase EMBO J. 19 2000 542 549
13. J.C. Samuelson, M. Chen, F. Jiang, I. Moller, M. Wiedmann, and A. Kuhn YidC mediates membrane protein insertion in bacteria Nature 405 2000 637 641
14. 0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis J. Cell Biol. 165 2004 213 222
15. N. Nouwen, and A.J.M. Driessen SecDFyajC forms a heterotetrameric complex with YidC Mol. Microbiol. 44 2002 1397 1405
16. R.L. Woodbury, S.J. Hardy, and L.L. Randall Complex behavior in solution of homodimeric SecA Protein Sci. 11 2002 875 882
17. H. Ding, J.F. Hunt, I. Mukerji, and D. Oliver Bacillus subtilis SecA ATPase exists as an antiparallel dimer in solution Biochemistry 42 2003 8729 8738
18. A.J.M. Driessen SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer Biochemistry 32 1993 13190 13197
19. E. Or, D. Boyd, S. Gon, J. Beckwith, and T. Rapoport The bacterial ATPase SecA functions as a monomer in protein translocation J. Biol. Chem. 280 2005 9097 9105
20. J. Benach, Y.T. Chou, J.J. Fak, A. Itkin, D.D. Nicolae, and P.C. Smith Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA J. Biol. Chem. 278 2003 3628 3638
21. P. Bessonneau, V. Besson, I. Collinson, and F. Duong The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure EMBO J. 21 2002 995 1003
22. I. Collinson, C. Breyton, F. Duong, C. Tziatzios, D. Schubert, and E. Or Projection structure and oligomeric properties of a bacterial core protein translocase EMBO J. 20 2001 2462 2471
23. E.H. Manting, C. van der Does, H. Remigy, A. Engel, and A.J.M. Driessen SecYEG assembles into a tetramer to form the active protein translocation channel EMBO J. 19 2000 852 861
24. T.H. Meyer, J.F. Ménétret, R. Breitling, K.R. Miller, C.W. Akey, and T.A. Rapoport The bacterial SecY/E complex forms channel-like structures similar to those of eucaryotic Sec61p complex J. Mol. Biol. 285 1999 1789 1800
25. E. Hartmann, T. Sommer, S. Prehn, D. Görlich, S. Jentsch, and T.A. Rapoport Evolutionary conservation of the components of the protein translocation complex Nature 367 1994 654 657
26. D. Hanein, K.E.S. Matlack, B. Jungnickel, K. Plath, K.U. Kalies, and K.R. Miller Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation Cell 87 1996 721 732
27. H. Mori, T. Tsukazaki, R. Masui, S. Kuramitsu, S. Yokoyama, and A.E. Johnson Fluorescence resonance energy transfer analysis of protein translocase. SecYE from Thermus thermophilus HB8 forms a constitutive oligomer in membranes J. Biol. Chem. 278 2003 14257 14264
28. C. Breyton, W. Haase, T.A. Rapoport, W. Kühlbrandt, and I. Collinson Three-dimensional structure of the bacterial protein-translocation complex SecYEG Nature 418 2002 662 665
29. R. Beckmann, C.M.T. Spahn, N. Eswar, J. Helmers, P.A. Penczek, and A. Sali Architecture of the protein-conducting channel associated with the translating 80S ribosome Cell 107 2001 361 372
30. B. van den Berg, W.M. Clemons Jr, I. Collinson, Y. Modis, E. Hartmann, S.C. Harrison, and T.A. Rapoport X-ray structure of a protein-conducting channel Nature 427 2004 36 44
31. T.L. Yahr, and W. Wickner Evaluating the oligomeric state of SecYEG in preprotein translocase EMBO J. 19 2000 4393 4401
32. F. Duong Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase EMBO J. 22 2003 4375 4384
33. C. Tziatzios, D. Schubert, M. Lotz, D. Gundogan, H. Betz, and H. Schägger The bacterial protein translocation complex: SecYEG dimers associate with one or two SecA molecules J. Mol. Biol. 340 2004 513 524
34. R. Beckmann, D. Bubeck, R. Grassucci, P. Penczek, A. Verschoor, G. Blobel, and J. Frank Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex Science 278 1997 2123 2126
35. B.D. Hamman, J.C. Chen, E.E. Johnson, and A.E. Johnson The aqueous pore through the translocon has a diameter of 40-60 Å during the cotranslational protein translocation at the ER membrane Cell 89 1997 535 544
36. H.-W. Wang, Y. Chen, H. Yang, X. Chen, M.-X. Duan, P.C. Tai, and S.-F. Sui Ring-like pore structures of SecA: implication for bacterial protein-conducting channels Proc. Natl Acad. Sci. USA 100 2003 4221 4226
37. M. Hanada, K. Nishiyama, S. Mizushima, and H. Tokuda Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE and SecG (p12) J. Biol. Chem. 269 1994 23625 23631
38. M. Bassilana, and W. Wickner Purified Escherichia coli preprotein translocase catalyses multiple cycles of precursor protein translocation Biochemistry 32 1993 2626 2630
39. M. van der Laan, N. Nouwen, and A.J.M. Driessen SecYEG proteoliposomes catalyze the Δψ-dependent membrane insertion of FtsQ J. Biol. Chem. 279 2004 1659 1664
40. J.C. Joly, M.R. Leonard, and W.T. Wickner Subunit dynamics in Escherichia coli preprotein translocase Proc. Natl Acad. Sci. USA 91 1994 4703 4707
41. B.D. Hamman, L.M. Hendershot, and A.E. Johnson BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon before and early in translocation Cell 92 1998 747 758
42. A. Kaufmann, E.H. Manting, A. Veenendaal, A.J.M. Driessen, and C. van der Does Cysteine-directed cross-linking demonstrates that helix 3 of SecE is close to helix 2 of SecY and helix 3 of a neighboring SecE Biochemistry 38 1999 9115 9121
43. A.K.J. Veenendaal, C. van der Does, and A.J.M. Driessen Mapping the sites of interaction between SecY and SecE by cysteine scanning mutagenesis J. Biol. Chem. 276 2001 32559 32566
44. R.J. Cabelli, L. Chen, P.C. Tai, and D.B. Oliver SecA protein is required for secretory protein translocation into E. coli membrane vesicles Cell 55 1988 683 692
45. J.B. Weiss, P.H. Ray, and P.J. Bassford Jr 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 1988 8978 8982
46. E. Crooke, S. Guthrie, S. Lecker, R. Lill, and W. Wickner ProOmpA is stabilized for membrane translocation by either purified E. coli trigger factor or canine signal recognition particle Cell 54 1988 1003 1011
47. C. van der Does, E.H. Manting, A. Kaufmann, M. Lutz, and A.J.M. Driessen Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state Biochemistry 37 1998 201 210
48. C. van der Does, J. Swaving, W. van Klompenburg, and A.J.M. Driessen Non-bilayer lipids stimulate the activity of the reconstituted bacterial preprotein translocase J. Biol. Chem. 275 2000 2472 2478
49. P.A. Lanzetta, L.J. Alvarez, P.S. Reinach, and O.A. Candia An improved assay for nanomole amounts of inorganic phosphate Anal. Biochem. 100 1979 95 97
50. R. Lill, W. Dowhan, and W. Wickner The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor protein Cell 60 1990 271 280
51. W.O. Saxton, T.J. Pitt, and M. Horner Digital image processing: the SEMPER system Ultramicroscopy 4 1979 343 354
52. M. van Heel, and W. Keegstra Imagic: a fast, flexible and friendly image analysis software system Ultramicroscopy 7 1981 113 130
53. M. van Heel, G. Harauz, E.V. Orlova, R. Schmidt, and M. Schatz A new generation of IMAGIC image processing system J. Struct. Biol. 116 1996 17 24
54. M. van Heel, and J. Frank Use of multivariate statistics in analysing the images of biological macromolecules Ultramicroscopy 6 1981 187 194