The periplasmic chaperone PpiD interacts with secretory proteins exiting from the SecYEG translocon

Biochemistry

Volumn 47, Issue 20, 2008, Pages 5649-5656

  Antonoaea, Raluca ^a,c   Fürst, Michaela ^a   Nishiyama, Ken Ichi ^a,b   Müller, Matthias ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF TOKYO   (Japan)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; ESCHERICHIA COLI; POLYPEPTIDES;

MEMBRANE PROTEINS; PERIPLASMIC CHAPERONE; RIBOSOMES; SEC TRANSLOCON;

PROTEINS;

MEMBRANE PROTEIN; MOLECULAR MOTOR; PERIPLASMIC PROTEIN; POLYPEPTIDE; PROTEIN SECA; SECRETORY PROTEIN; SECYEG PROTEIN; TRANSLOCON;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN TRANSPORT; RIBOSOME;

CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN TRANSPORT;

ESCHERICHIA COLI;

EID: 43949125856     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800233w     Document Type: Article

References (39)

1. van den Berg, B., Clemons, W. M., Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004) X-ray structure of a protein-conducting channel. Nature 427, 36-44.
2. Maillard, A. P., Lalani, S., Silva, F., Belin, D., and Duong, F. (2007) Deregulation of the SecYEG translocation channel upon removal of the plug domain. J. Biol. Chem. 282, 1281-1287.
3. Li, W., Schulman, S., Boyd, D., Erlandson, K., Beckwith, J., and Rapoport, T. A. (2007) The plug domain of the SecY protein stabilizes the closed state of the translocation channel and maintains a membrane seal. Mol. Cell 26, 511-521.
4. Tam, P. C., Maillard, A. P., Chan, K. K., and Duong, F. (2005) Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J. 24, 3380-3388.
5. Qi, H. Y., and Bernstein, H. D. (1999) SecA is required for the insertion of inner membrane proteins targeted by the Escherichia coli signal recognition particle. J. Biol. Chem. 274, 8993-8997.
6. Tian, H., Boyd, D., and Beckwith, J. (2000) A mutant hunt for defects in membrane protein assembly yields mutations affecting the bacterial signal recognition particle and Sec machinery. Proc. Natl. Acad. Sci. U.S.A. 97, 4730-4735.
7. Neumann-Haefelin, C., Schäfer, U., Müller, M., and Koch, H. G. (2000) SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J. 19, 6419-6426.
8. van der Laan, M., Nouwen, N., and Driessen, A. J. (2004) SecYEG proteoliposomes catalyze the Δψ-dependent membrane insertion of FtsQ. J. Biol. Chem. 279, 1659-1664.
9. Deitermann, S., Sprie, G. S., and Koch, H. G. (2005) A dual function for SecA in the assembly of single spanning membrane proteins in Escherichia coli. J. Biol. Chem. 280, 39077-39085.
10. Scotti, P. A., Valent, Q. A., Manting, E. H., Urbanus, M. L., Driessen, A. J., Oudega, B., and Luirink, J. (1999) SecA is not required for signal recognition particle-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J. Biol. Chem. 274, 29883-29888.
11. Casadaban, M. J., and Cohen, S. N. (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: In vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. U.S.A. 76, 4530-4533.
12. Behrmann, M., Koch, H. G., Hengelage, T., Wieseler, B., Hoffschulte, H. K., and Müller, M. (1998) Requirements for the translocation of elongation-arrested, ribosome-associated OmpA across the plasma membrane of Escherichia coli. J. Biol. Chem. 273, 13898-13904.
13. Studier, F. W., Rosenberg, A. H., Dunn, J. J., and Dubendorff, J. W. ( 1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60-89.
14. Matsumoto, G., Yoshihisa, T., and 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.
15. Nishiyama, K., Suzuki, T., and Tokuda, H. (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85, 71-81.
16. Eisner, G., Koch, H. G., Beck, K., Brunner, J., and Müller, M. (2003) Ligand crowding at a nascent signal sequence. J. Cell Biol. 163, 35-44.
17. Schäfer, U., Beck, K., and Müller, M. (1999) Skp, a molecular chaperone of Gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J. Biol. Chem. 274, 24567-24574.
18. Müller, M., Fisher, R. P., Rienhöfer-Schweer, A., and Hoffschulte, H. K. (1987) DCCD inhibits protein translocation into plasma membrane vesicles from Escherichia coli at two different steps. EMBO J. 6, 3855-3861.
19. Beck, K., Wu, L. F., Brunner, J., and Müller, 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.
20. Josefsson, L. G., and Randall, L. L. (1981) Different exported proteins in E. coli show differences in the temporal mode of processing in vivo. Cell 25, 151-157.
21. 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. A translocation intermediate accumulates transiently in the absence of the proton motive force. J. Biol. Chem. 264, 18582-18588.
22. Schiebel, E., Driessen, A. J., Haiti, F. U., and Wickner, W. (1991) Δμ H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64, 927-939.
23. 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.
24. Cheng, Z., Jiang, Y., Mandon, E. C., and Gilmore, R. (2005) Identification of cytoplasmic residues of Sec61p involved in ribosome binding and cotranslational translocation. J. Cell Biol. 168, 67-77.
25. Mori, H., and Ito, K. (2001) An essential amino acid residue in the protein translocation channel revealed by targeted random mutagenesis of SecY. Proc. Natl. Acad. Sci. U.S.A. 98, 5128-5133.
26. Zito, C. R., and Oliver, D. (2003) Two-stage binding of SecA to the bacterial translocon regulates ribosome-translocon interaction. J. Biol. Chem. 278, 40640-40646.
27. 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.
28. Beckmann, R., Spann, C. M., Eswar, N., Helmers, J., Penczek, P. A., Sali, A., Frank, J., and Blobel, G. (2001) Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372.
29. Yahr, T. L., and Wickner, W. T. (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J. 19, 4393-4401.
30. Manting, E. H., van Der Does, C., Remigy, H., Engel, A., and Driessen, A. J. (2000) SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19, 852-861.
31. Duong, F. (2003) Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J. 22, 4375-4384.
32. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C. L., III, Ban, N., and Frank, J. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438, 318-324.
33. Dartigalongue, C., and Raina, S. (1998) A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17, 3968-3980.
34. Lazar, S. W., and Kolter, R. (1996) SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 178, 1770-1773.
35. Rouviere, P. E., and Gross, C. A. (1996) SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 10, 3170-3182.
36. Mogensen, J. E., and Otzen, D. E. (2005) Interactions between folding factors and bacterial outer membrane proteins. Mol. Microbiol. 57, 326-346.
37. Justice, S. S., Hunstad, D. A., Harper, J. R., Duguay, A. R., Pinkner, J. S., Bann, J., Frieden, C., Silhavy, T. J., and Hultgren, S. J. (2005) Periplasmic peptidyl prolyl cis-trans isomerases are not essential for viability, but SurA is required for pilus biogenesis in Escherichia coli. J. Bacteriol. 187, 7680-7686.
38. Ullers, R. S., Ang, D., Schwager, F., Georgopoulos, C., and Genevaux, P. (2007) Trigger Factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 104, 3101-3106.
39. Sugiyama, J. E., Mahmoodian, S., and Jacobson, G. R. (1991) Membrane topology analysis of Escherichia coli mannitol permease by using a nested-deletion method to create mtlA-phoA fusions. Proc. Natl. Acad. Sci. U.S.A. 88, 9603-9607.