The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling

EMBO Journal

Volumn 16, Issue 16, 1997, Pages 4871-4879

  Duong, Franck ^a   Wickner, William ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Membrane proteins; Preprotein translocase; Proton motive force; Sec proteins; SecDFyajC

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL ENZYME; CARRIER PROTEIN; MEMBRANE ENZYME; PROTEIN PRECURSOR;

ARTICLE; CONTROLLED STUDY; ENZYME STABILITY; ESCHERICHIA COLI; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; PROTON MOTIVE FORCE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; APROTININ; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN PRECURSORS; PROTON-MOTIVE FORCE; PROTONS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0030745847     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.16.4871     Document Type: Article

References (45)

1. Akimaru, J., Matsuyama, S.-i, 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. 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. Bassilana, M. and Wickner, W. (1993) Purified Escherichia coli preprotein translocase catalyzes multiples cycles of precursor protein translocation. Biochemistry, 32, 2626-2630.
4. Brundage, L., Hendrick, J.P., Schiebel, E., Driessen, A.J.M. 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.
5. Brundage, L., Fimmel, C.J., Mizushima, S. and Wickner, W. (1992) SecY, SecE and band 1 form the membrane-embedded domain of Escherichia coli preprotein translocase. J. Biol. Chem., 267, 4166-4170.
6. Carlson, J., Drevin, H. and Axen, R. (1978) Protein thiolation and reversible protein-protein conjugation. Biochem. J., 173, 723-737.
7. Chen, L. and Tai, P.C. (1985) ATP is essential for protein translocation into Escherichia coli membrane vesicles. Proc. Natl Acad. Sci. USA, 82, 4384-4388.
8. Chen, X., Xu, H. and Tai, P.C. (1996) A significant fraction of functional SecA is permanently embedded in the membrane. J. Biol. Chem., 271, 29698-29706.
9. Crooke, E., Brundage, L., Rice, M. and Wickner, W. (1988) ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes. EMBO J., 7, 1831-1835.
10. Cunningham, K., Lill, R., Crooke, E., Rice, M., Moore, K., Wickner, W. and Oliver, D. (1989) Isolation of SecA protein, a peripheral protein of the E.coli plasma membrane that is essential for the functional binding and translocation of proOmpA. EMBO J., 8, 955-959.
11. Douville, K., Leonard, M., Brundage, L., Nishiyama, K.-i., Tokuda, H., Mizushima, S. and Wickner, W. (1994) Band 1 subunit of Esherichia coli preprotein translocase and integral membrane export factor P12 are the same protein. J. Biol. Chem., 269, 18705-18707.
12. 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.
13. Driessen, A.J.M. (1992) Precusor protein translocation by the Escherichia coli translocase is directed by the protonmotive force. EMBO J., 11, 847-853.
14. 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.
15. 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.
16. Economou, A. and Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell, 78, 835-843.
17. Economou, A., Pogliano, J.A., Beckwith, J., Oliver, D.B. 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.
18. 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.
19. 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.
20. Gardel, C., Johnson, K., Jacq, A. and Beckwith, J. (1990) The secD locus of E.coli codes for two membrane proteins required for protein export. EMBO J., 9, 3209-3216.
21. Geller, B.L., Movva, N.R. and Wickner, W. (1986) Both ATP and the electrochemical potential are required for optimal assembly of proOmpA into Escherichia coli inner membrane vesicles. Proc. Natl Acad. Sci. USA, 83, 4219-4222.
22. 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.
23. 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.
24. Joly, J.C., Leonard, M.R. and Wickner, W. (1994) Subunit dynamics in Escherichia coli preprotein translocase. Proc. Natl Acad. Sci. USA, 91, 4703-4707.
25. Kawasaki, S., Mizushima, S. and Tokuda, H. (1993) Membrane vesicles containing overproduced SecY and SecE exhibit high translocation ATPase activity and countermovement of protons in a SecA-and presecretory protein-dependent manner. J. Biol. Chem., 268, 8193-8198.
26. Kim, Y.J., Rajapandi, T. and 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.
27. Kleerebezem, M. and Tommassen, J. (1993) Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol. Microbiol., 7, 947-956.
28. Lill, R., Cunningham, K., Brundage, L., Ito, K., Oliver, D. and Wickner, W. (1989) The SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of E.coli. EMBO J., 8, 961-966.
29. 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, 259-269.
30. 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.
31. 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.
32. Osborne, R.S. and Silhavy, T.J. (1993) PrIA suppressor mutations cluster in regions corresponding to three distinct topological domains. EMBO J., 12, 3391-33987
33. Pogliano, J.A. and Beckwith, J. (1994a) SecD and SecF facilitate protein export in Escherichia coli. EMBO J., 13, 554-561.
34. Pogliano, K.J. and Beckwith, J. (1994b) Genetic and molecular characterization of the Escherichia coli secD operon and its products. J. Bacteriol., 176, 804-814.
35. 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., 272, 31580-31584.
36. Sato, K., Mori, H., Yoshida, M., Tagaya, M. and Mizushima, S. (1997) Short hydrophobic segments in the mature domain of proOmpA determine its stepwise movement during translocation across the cytoplasmic membrane of Escherichia coli. J. Biol. Chem., 272, 5880-5886.
37. Schatz, P.J. and Beckwith, J. (1990) Genetic analysis of protein export in Escherichia coli. Annu. Rev. Genet., 24, 215-248.
38. Schiebel, E. and Wickner, W. (1992) Preprotein translocation creates a halide anion permeability in the Escherichia coli plasma membrane. J. Biol. Chem., 267, 7505-7510.
39. μH+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell, 64, 927-939.
40. Shiozuka, K., Tani, K., Mizushima, S. and Tokuda, H. (1990) The proton motive force lowers the level of ATP required for the in vitro translocation of a secretory protein in Escherichia coli. J. Biol. Chem., 265, 18843-18847.
41. Tani, K., Shiozuka, K., Tokuda, H. and Mizushima, S. (1989) In vitro analysis of the process of translocation of OmpA across the Escherichia coli cytoplasmic membrane. J. Biol. Chem., 264, 18582-18588.
42. Uchida, K., Mori, H. and Mizushima, S. (1995) Stepwise movement of preproteins in the process of translocation across the cytoplasmic membrane of Escherichia coli. J. Biol. Chem., 270, 30862-30868.
43. 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.
44. Wickner, W. and Rice Leonard, M.R. (1996) Escherichia coli preprotein translocase. J. Biol. Chem., 271, 29514-29516.
45. Yamada, H., Matsuyama, S.-i., Tokuda, H. and Mizushima, S. (1989) A high concentration of SecA allows proton motive force-independent translocation of a model secretory protein into Escherichia coli membrane vesicles. J. Biol. Chem., 264, 18577-18581.