The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex

Journal of Molecular Biology

Volumn 285, Issue 4, 1999, Pages 1789-1800

  Meyer, Thomas H ^a   Ménétret, Jean François ^b   Breitling, Reinhard ^c   Miller, Kenneth R ^d   Akey, Christopher W ^b   Rapoport, Tom A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d BROWN UNIVERSITY   (United States)

Author keywords

Channel; Sec61p complex; SecYEG complex; Translocation

Indexed keywords

PROTEIN SUBUNIT;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL TRANSLOCATION; CELL MEMBRANE; COMPLEX FORMATION; ELECTRON MICROSCOPY; EUKARYOTE; LIPID BILAYER; MEMBRANE CHANNEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 0345196631     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2413     Document Type: Article

References (43)

1. Akey C. W. Structural plasticity of the nuclear pore complex. J. Mol. Biol. 248:1995;273-293.
2. Akimaru J., Matsuyama S., Tokuda H., Mizushima S. Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA fromEscherichia coli. Proc. Natl Acad. Sci. USA. 88:1991;6545-6549.
3. Akiyama Y., Ito K. Topology analysis of the SecY protein, an integral membrane protein involved in protein export inEscherichia coli. EMBO J. 6:1987;3465-3470.
4. Bassilana M., Wickner W. Purified Escherichia coli preprotein translocase catalyzes multiple cycles of precursor protein translocation. Biochemistry. 32:1993;2626-2630.
5. Beckmann R., Bubeck D., Grassucci R., Penczek P., Verschoor A., Blobel G., Frank J. Alignment of conduits for the nascent polypeptide chain in the ribosome- Sec61 complex. Science. 278:1997;2123-2126.
6. Brundage L., Hendrick J. P., Schiebel E., Driessen A. J., Wickner W. The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell. 62:1990;649-657.
7. Cunningham K., Lill R., Crooke E., Rice M., Moore K., Wickner W., Oliver D. SecA protein, a peripheral protein of the Escherichia coli plasma membrane, is essential for the functional binding and translocation of proOmpA. EMBO J. 8:1989;955-959.
8. Deshaies R. J., Schekman R. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J. Cell Biol. 105:1987;633-645.
9. Douville K., Price A., Eichler J., Economou A., Wickner W. SecYEG and SecA are the stoichiometric components of preprotein translocase. J. Biol. Chem. 270:1995;20106-20111.
10. Dubochet J., Adrian M., Chang J. J., Homo J. C., Lepault J., McDowall A. W., Schultz P. Cryo-electron microscopy of vitrified specimens. Quart. Rev. Biophys. 21:1988;129-228.
11. Duong F., Wickner W. Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. 16:1997;2756-2768.
12. Economou A., Pogliano J. A., Beckwith J., Oliver D. B., Wickner W. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell. 83:1995;1171-1181.
13. Esnault Y., Feldheim D., Blondel M. O., Schekman R., Kepes F. SSS1 encodes a stabilizing component of the Sec61 subcomplex of the yeast protein translocation apparatus. J. Biol. Chem. 269:1994;27478-27485.
14. Frank J., Bretaudiere J. P., Carazo J. M., Verschoor A., Wagenknecht T. Classification of images of biomolecular assemblies: a study of ribosomes and ribosomal subunits ofEscherichia coli. J. Microsc. 150:1988;99-115.
15. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116:1996;190-199.
16. Gardel C., Johnson K., Jacq A., Beckwith J. The secD locus of E. coli codes for two membrane proteins required for protein export. EMBO J. 9:1990;3209-3216.
17. Görlich D., Rapoport T. A. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell. 75:1993;615-630.
18. Görlich D., Prehn S., Hartmann E., Kalies K. U., Rapoport T. A. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell. 71:1992;489-503.
19. Hamman B. D., Hendershot L. M., Johnson A. E. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell. 92:1998;747-758.
20. Hanada M., Nishiyama K., Mizushima S., Tokuda H. 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.
21. Hanein D., Matlack K. E., Jungnickel B., Plath K., Kalies K. U., Miller K. R., Rapoport T. A., Akey C. W. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell. 87:1996;721-732.
22. Hartl F. U., Lecker S., Schiebel E., Hendrick J. P., Wickner W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell. 63:1990;269-279.
23. Hartmann E., Sommer T., Prehn S., Görlich D., Jentsch S., Rapoport T. A. Evolutionary conservation of components of the protein translocation complex. Nature. 367:1994;654-657.
24. Ito K. Identification of the secY (prlA) gene product involved in protein export in Escherichia coli. Mol. Gen. Genet. 197:1984;204-208.
25. Joly J. C., Wickner W. 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.
26. Joly J. C., Leonard M. R., Wickner W. T. Subunit dynamics in Escherichia coli preprotein translocase. Proc. Natl Acad. Sci. USA. 91:1994;4703-4707.
27. Kalies K. U., Görlich D., Rapoport T. A. Binding of ribosomes to the rough endoplasmic reticulum mediated by the Sec61p-complex. J. Cell Biol. 126:1994;925-934.
28. Kalies K. U., Rapoport T. A., Hartmann E. The beta subunit of the Sec61 complex facilitates cotranslational protein transport and interacts with the signal peptidase during translocation. J. Cell Biol. 141:1998;887-894.
29. Klose M., Schimz K. L., van der Wolk J., Driessen A. J., Freudl R. Lysine 106 of the putative catalytic ATP-binding site of the Bacillus subtilis SecA protein is required for functional complementation of Escherichia coli secA mutants in vivo. J. Biol. Chem. 268:1993;4504-4510.
30. Kocsis E., Cerritelli M. E., Trus B. L., Cheng N., Steven A. C. Improved methods for determination of rotational symmetries in macromolecules. Ultramicroscopy. 60:1995;219-228.
31. Lill R., Cunningham K., Brundage L. A., Ito K., Oliver D., Wickner W. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase ofEscherichia coli. EMBO J. 8:1989;961-966.
32. Lill R., Dowhan W., Wickner W. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell. 60:1990;271-280.
33. Mothes W., Prehn S., Rapoport T. A. Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO J. 13:1994;3973-3982.
34. Murphy C. K., Beckwith J. Residues essential for the function of SecE, a membrane component of the Escherichia coli secretion apparatus, are located in a conserved cytoplasmic region. Proc. Natl Acad. Sci. USA. 91:1994;2557-2561.
35. Nishiyama K., Hanada M., Tokuda H. 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. 13:1994;3272-3277.
36. Panzner S., Dreier L., Hartmann E., Kostka S., Rapoport T. A. Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell. 81:1995;561-570.
37. Pohlschröder M., Prinz W. A., Hartmann E., Beckwith J. Protein translocation in the three domains of life: variations on a theme. Cell. 91:1997;563-536.
38. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
39. Schatz P. J., Riggs P. D., Jacq A., Fath M. J., Beckwith J. The SecE gene encodes an integral membrane protein required for protein export inEscherichia coli. Genes Dev. 3:1989;1035-1044.
40. Schatz P. J., Bieker K. L., Ottemann K. M., Silhavy T. J., Beckwith J. One of three transmembrane stretches is sufficient for the functioning of the SecE protein, a membrane component of theE. coli secretion machinery. EMBO J. 10:1991;1749-1757.
41. Trieu-Cuot P., Courvalin P. Nucleotide sequence of the Streptococcus faecalis plasmid gene encoding the 3′5″-aminoglycoside phosphotransferase type III. Gene. 23:1983;331-341.
42. Yang Q., Rout M. P., Akey C. W. Three-dimensional architecture of the yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell. 1:1998;223-234.
43. Yansura D. G., Henner D. J. Use of the Escherichia coli lac repressor and operator to control gene expression inBacillus subtilis. Proc. Natl Acad. Sci. USA. 81:1984;439-443.