Projection structure and oligomeric properties of a bacterial core protein translocase

EMBO Journal

Volumn 20, Issue 10, 2001, Pages 2462-2471

  Collinson, Ian ^a   Breyton, Cécile ^b   Duong, Franck ^d   Tziatzios, Christos ^c   Schubert, Dieter ^c   Or, Eran ^a   Rapoport, Tom ^a   Kühlbrandt, Werner ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Electron crystallography; Oligomerization; SecYEG; Translocation; Two dimensional crystallization

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN;

ARTICLE; ELECTRON MICROSCOPY; ENZYME SUBSTRATE; ESCHERICHIA COLI; MEMBRANE CHANNEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT;

BACTERIAL PROTEINS; CRYSTALLIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; OLIGOPEPTIDES; PEPTIDYL TRANSFERASES; PRECIPITIN TESTS; SOLUTIONS;

EID: 0035873223     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/20.10.2462     Document Type: Article

References (59)

1. Akimaru, J., Matsuyama, S., Tokuda, H. and Mizushima, S. (1991) Reconstitution of a protein translocation system containing purified SecY, SecE and SecA from Escherichia coli. Proc. Natl Acad. Sci. USA, 88, 6545-6549.
2. +-ATPaSe in the open conformation. Nature, 392, 840-843.
3. Bassilana, M. and Wickner, W. (1993) Purified Escherichia coli preprotein translocase catalyzes multiple cycles of precursor protein translocation. Biochemistry, 32, 2626-2630.
4. 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.
5. Bieker, K.L., Phillips, G.J. and Silhavy, T.J. (1990) The sec and prl genes of Escherichia coli. J. Bioenerg. Biomembr., 22, 291-310.
6. Brundage, L., Hendrick, J., Schiebel, E., Driessen, A. and 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.
7. 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.
8. Collaborative Computational Project No. 4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D, 50, 760-763.
9. 1-ATPaSe. Biochemistry, 33, 7971-7978.
10. Crowther, R., Henderson, R. and Smith, J. (1996) MRC image processing programs. J. Struct. Biol., 116, 9-16.
11. 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.
12. Driessen, A., Fekkes, P. and van der Wolk, J. (1998) The Sec system. Curr. Opin. Microbiol., 1, 216-222.
13. Duong, F. and Wickner, W. (1997a) Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J., 16, 2756-2768.
14. Duong, F. and Wickner, W. (1997b)The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J., 16, 4871-4879.
15. Duong, F. and Wickner, W. (1999) The PrlA and PrlG phenotypes are caused by a loosened association among the translocase SecYEG subunits. EMBO J., 18, 3263-3270.
16. Duong, F., Eichler, J., Price, A., Leonard, M. and Wickner, W. (1997) Biogenesis of the gram-negative bacterial envelope. Cell, 91, 567-573.
17. Durchschlag, H. (1986) Specific volumes of biological macromolecules and some other molecules of biological interest. In Hinz, H.-J. (ed), Thermodynamic Data for Biochemistry and Biotechnology. Springer-Verlag, Berlin, pp. 45-128.
18. Economou, A. and Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell, 78, 835-843.
19. Economou, A., Pogliano, J., Beckwith, J., Oliver, D. and 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.
20. Grigorieff, N., Ceska, T., Downing, K., Baldwin, J. and Henderson, R. (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol., 259, 393-421.
21. Hanein, D., Matlack, K., Jungnickel, B., Plath, K., Kalies, K., Miller, K., Rapoport, T. and Akey, C. (1996) Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell, 87, 721-732.
22. Henderson, R., Baldwin, J., Downing, K. and Zemlin, F. (1986) Structure of purple membrane from Halobacterium halobium. Recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy, 19, 147-178.
23. Henderson, R., Baldwin, J., Ceska, T., Zemlin, F., Beckmann, E. and Downing, K. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol., 213, 899-929.
24. Jungnickel, B., Rapoport, T. and Hartmann, E. (1994) Protein translocation: common themes from bacteria to man. FEBS Lett., 346, 73-77.
25. Krebs, A., Villa, C., Edwards, P.C. and Schertler, G.F. (1998) Characterisation of an improved two-dimensional p22121 crystal from bovine rhodopsin. J. Mol. Biol., 282, 991-1003.
26. Kühlbrandt, W. (1992) Two-dimensional crystallization of membrane proteins. Q. Rev. Biophys., 25, 1-49.
27. Kühlbrandt, W., Wang, D. and Fujiyoshi, Y. (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature, 367, 614-621.
28. Kumamoto, C. and Beckwith, J. (1983) Mutations in a new gene, secB, cause defective protein localization in Escherichia coli. J. Bacteriol., 154, 253-260.
29. Kunkele, K. et al. (1998) The preprotein translocation channel of the outer membrane of mitochondria. Cell, 93, 1009-1019.
30. Laemmli, U. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
31. Lill, R., Cunningham, K., Brundage, L., Ito, K., Oliver, D. and Wickner, W. (1989) SecA protein hydrolyzes ATP and is an essential component of the protein translocalion ATPase of Escherichia coli. EMBO J., 8, 961-966.
32. Lill, R., Dowhan, 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.
33. Mant, A., Schmidt, I., Herrmann, R., Robinson, C. and Klosgen, R. (1995) Sec-dependent thylakoid protein translocation. ΔpH requirement is dictated by passenger protein and ATP concentration. J. Biol. Chem., 270, 23275-23281.
34. Manting, E., van, D.D.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.
35. Ménetret, J., Neuhof, A., Morgan, D., Plath, K., Radermacher, M., Rapoport, T. and Akey, C. (2000) The structure of ribosome-channel complexes engaged in protein translocation. Mol. Cell, 6, 1219-1232.
36. Meyer, T., Ménetret, J., Breitling, R., Miller, K., Akey, C. and Rapoport, T. (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.
37. Miroux, B. and Walker, J. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol., 260, 289-298.
38. Misselwitz, B., Staeck, O., Matlack, K. and Rapoport, T. (1999) Interaction of BiP with the J-domain of the Sec63p component of the endoplasmic reticulum protein translocation complex. J. Biol. Chem., 274, 20110-20115.
39. Murata, K., Mitsuoka, K., Hirai, T., Walz, T., Agre, P., Heymann, J.B., Engel, A. and Fujiyoshi, Y. (2000) Structural determinants of water permeation through aquaporin-1. Nature, 407, 599-605.
40. Nishiyama, K., Hanada, M. and Tokuda, H. (1994) Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J., 13, 3272-3277.
41. Oliver, D. and Beckwith, J. (1982) Identification of a new gene (secA) and gene product involved in the secretion of envelope proteins in Escherichia coli. J. Bacteriol., 150, 686-691.
42. Pohlschroder, M., Prinz, W., Hartmann, E. and Beckwith, J. (1997) Protein translocation in the three domains of life: variations on a theme. Cell, 91, 563-566.
43. Prinz, A., Behrens, C., Rapoport, T., Hartmann, E. and Kalies, K. (2000) Evolutionarily conserved binding of ribosomes to the translocation channel via the large ribosomal RNA. EMBO J., 19, 1900-1906.
44. Prinz, W., Spiess, C., Ehrmann, M., Schierle, C. and Beckwith, J. (1996) Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase. EMBO J., 15, 5209-5217.
45. Rapoport, T., Jungnickel, B. and Kutay, U. (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Anna. Rev. Biochem., 65, 271-303.
46. Rhee, K., Morris, E., Barber, J. and Kuhlbrandt, W. (1998) Three-dimensional structure of the plant photosystem II reaction centre at 8 A resolution. Nature, 396, 283-286.
47. Schatz, P., Riggs, P., Jacq, A., Fath, M. and Beckwith, J. (1989) The secE gene encodes an integral membrane protein required for protein export in Escherichia coli. Cenes Dev. 3, 1035-1044.
48. Schubert, D. and Schuck, P. (1991) Analytical ultracentrifugation as a tool for studying membrane proteins. Prog. Colloid Polym. Sci., 86, 12-22.
49. Schuck, P. (1994) Simultaneous radial and wavelength analysis with the Optima XL-A analytical ultracentrifuge. Prog. Colloid Polym. Sci., 94, 1-13.
50. Schuck, P., Legrum, B., Passow, H. and Schubert, D. (1995) The influence of two anion-transport inhibitors, 4,4′-diisothiocyanatodihydrostilbene-2,2′-disulfonate and 4,4′-dibenzoylstilbene-2,2′-disulfonate, on the self-association of erythrocyte band 3 protein. Eur. J. Biochem., 230, 806-812.
51. Shilton, B., Svergun, D., Volkov, V., Koch, M., Cusack, S. and Economou, A. (1998) Escherichia coli SecA shape and dimensions. FEBS Lett., 436, 277-282.
52. Unger, V., Kumar, N., Gilula, N. and Yeager, M. (1997a) Projection structure of a gap junction membrane channel at 7 Å resolution. Nature Struct. Biol., 4, 39-43.
53. Unger, V.M., Hargrave, PA., Baldwin, J.M. and Schertler, G.F. (1997b) Arrangement of rhodopsin transmembrane α-helices. Nature, 389, 203-206.
54. Unger, V., Kumar, N., Gilula, N. and Yeager, M. (1999) Three-dimensional structure of a recombinant gap junction membrane channel. Science, 283, 1176-1180.
55. Valpuesta, J., Carrascosa, J. and Henderson, R. (1994) Analysis of electron microscope images and electron diffraction patterns of thin crystals of M-X29 connectors in ice. J. Mol. Biol., 240, 281-287.
56. van der Does, C., Swaving, J., van, K.W. and Driessen, A. (2000) Non-bilayer lipids stimulate the activity of the reconstituted bacterial protein translocase. J. Biol. Chem., 275, 2472-2478.
57. van der Wolk, J., Fekkes, P., Boorsma, A., Huie, J., Silhavy, T. and Driessen, A. (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.
58. Williams, K. (2000) Three-dimensional structure of the ion-coupled transport protein NhaA. Nature, 403, 112-115.
59. Yahr, T. and Wickner, W. (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J., 19, 4393-4401.