Phage Shock Protein PspA of Escherichia coli Relieves Saturation of Protein Export via the Tat Pathway

Journal of Bacteriology

Volumn 186, Issue 2, 2004, Pages 366-373

  DeLisa, Matthew P ^a,b   Lee, Philip ^c   Palmer, Tracy ^c   Georgiou, George ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GENE PRODUCT; HYBRID PROTEIN; PHAGE SHOCK PROTEIN; PROTEIN PSPA; PROTEIN TORA; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENOME; NONHUMAN; PHYLOGENY; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 0346655242     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.2.366-373.2004     Document Type: Article

References (48)

1. Adams, H., W. Teertstra, J. Demmers, R. Boesten, and J. Tommassen. 2003. Interactions between phage-shock proteins in Escherichia coli. J. Bacteriol. 185:1174-1180.
2. Alami, M., D. Trescher, L. F. Wu, and M. Muller. 2002. Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J. Biol. Chem. 277:20499-20503.
3. Alder, N. N., and S. M. Theg. 2003. Energetics of protein transport across biological membranes, a study of the thylakoid ΔpH-dependent/cpTat pathway. Cell 112:231-242.
4. Barrett, C. M., N. Ray, J. D. Thomas, C. Robinson, and A. Bolhuis. 2003. Quantitative export of a reporter protein, GFP, by the twin-arginine translocation pathway in Escherichia coli. Biochem. Biophys. Res. Commun. 304:279-284.
5. Berks, B. C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:393-404.
6. Berks, B. C., T. Palmer, and F. Sargent. 2003. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47:187-254.
7. Berks, B. C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274.
8. Bogsch, E. G., F. Sargent, N. R. Stanley, B. C. Berks, C. Robinson, and T. Palmer. 1998. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273:18003-18006.
9. Brissette, J. L., M. Russel, L. Weiner, and P. Model. 1990. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 87:862-866.
10. Buchanan, G., E. Leeuw, N. R. Stanley, M. Wexler, B. C. Berks, F. Sargent, and T. Palmer. 2002. Functional complexity of the twin-arginine translocase TatC component revealed by site-directed mutagenesis. Mol. Microbiol. 43:1457-1470.
11. Chanal, A., C. L. Santini, and L. F. Wu. 2003. Specific inhibition of the translocation of a subset of Escherichia coli TAT substrates by the TorA signal peptide. J. Mol. Biol. 327:563-570.
12. Chen, G., A. Hayhurst, J. G. Thomas, B. R. Harvey, B. L. Iverson, and G. Georgiou. 2001. Isolation of high-affinity ligand-binding proteins by periplasmic expression with cytometric screening (PECS). Nat. Biotechnol. 19:537-542.
13. Cristobal, S., J. W. de Gier, H. Nielsen, and G. von Heijne. 1999. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 18:2982-2990.
14. Daugherty, P. S., G. Chen, B. L. Iverson, and G. Georgiou. 2000. Quantitative analysis of the effect of the mutation frequency on the affinity maturation of single chain Fv antibodies. Proc. Natl. Acad. Sci. USA 97:2029-2034.
15. DeLisa, M. P., P. Samuelson, T. Palmer, and G. Georgiou. 2002. Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J. Biol. Chem. 277:29825-29831.
16. DeLisa, M. P., D. Tullman, and G. Georgiou. 2003. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl. Acad. Sci. USA 100:6115-6120.
17. Derman, A. I., J. W. Puziss, P. J. Bassford, Jr., and J. Beckwith. 1993. A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J. 12:879-888.
18. Driessen, A. J., P. Fekkes, and J. P. van der Wolk. 1998. The Sec system. Curr. Opin. Microbiol. 1:216-222.
19. Elderkin, S., S. Jones, J. Schumacher, D. Studholme, and M. Buck. 2002. Mechanism of action of the Escherichia coli phage shock protein PspA in repression of the AAA family transcription factor PspF. J. Mol. Biol. 320:23-37.
20. Jovanovic, G., L. Weiner, and P. Model. 1996. Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J. Bacteriol. 178:1936-1945.
21. Kleerebezem, M., W. Crielaard, and J. Tommassen. 1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 5:162-171.
22. Kleerebezem, M., and J. Tommassen. 1993. Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol. Microbiol. 7:947-956.
23. Kroll, D., K. Meierhoff, N. Bechtold, M. Kinoshita, S. Westphal, U. C. Vothknecht, J. Soll, and P. Westhoff. 2001. VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc. Natl. Acad. Sci. USA 98:4238-4242.
24. Mikhaleva, N. I., C. L. Santini, G. Giordano, M. A. Nesmeyanova, and L. F. Wu. 1999. Requirement for phospholipids of the translocation of the trimethylamine N-oxide reductase through the Tat pathway in Escherichia coli. FEBS Lett. 463:331-335.
25. Model, P., G. Jovanovic, and J. Dworkin. 1997. The Escherichia coli phage-shock-protein (psp) operon. Mol. Microbiol. 24:255-261.
26. Mori, H., and K. Cline. 2002. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J. Cell Biol. 157:205-210.
27. Musser, S. M., and S. M. Theg. 2000. Characterization of the early steps of OE17 precursor transport by the thylakoid ΔpH/Tat machinery. Eur. J. Biochem. 267:2588-2598.
28. Musser, S. M., and S. M. Theg. 2000. Proton transfer limits protein translocation rate by the thylakoid ΔpH/Tat machinery. Biochemistry 39:8228-8233.
29. Oresnik, I. J., C. L. Ladner, and R. J. Turner. 2001. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 40:323-331.
30. Papish, A. L., C. L. Ladner, and R. J. Turner. 2003. The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase. J. Biol. Chem. 278:32501-32506.
31. Randall, L. L., and S. J. Hardy. 1986. Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell 46:921-928.
32. Ray, N., J. Oates, R. J. Turner, and C. Robinson. 2003. DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett. 534:156-160.
33. Rodrigue, A., A. Chanal, K. Beck, M. Muller, and L. F. Wu. 1999. Cotranslocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem. 274:13223-13228.
34. Sanders, C., N. Wethkamp, and H. Lill. 2001. Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41:241-246.
35. Sargent, F., B. C. Berks, and T. Palmer. 2002. Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch. Microbiol. 178:77-84.
36. Sargent, F., E. G. Bogsch, N. R. Stanley, M. Wexler, C. Robinson, B. C. Berks, and T. Palmer. 1998. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17:3640-3650.
37. Sargent, F., U. Gohlke, E. De Leeuw, N. R. Stanley, T. Palmer, H. R. Saibil, and B. C. Berks. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268:3361-3367.
38. Sargent, F., N. R. Stanley, B. C. Berks, and T. Palmer. 1999. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274:36073-36082.
39. Stanley, N. R., T. Palmer, and B. C. Berks. 2000. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596.
40. Stanley, N. R., F. Sargent, G. Buchanan, J. Shi, V. Stewart, T. Palmer, and B. C. Berks. 2002. Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol. Microbiol. 43:1005-1021.
41. Thomas, J. D., R. A. Daniel, J. Errington, and C. Robinson. 2001. Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol. Microbiol. 39:47-53.
42. Van Der Laan, M., M. L. Urbanus, C. M. Ten Hagen-Jongman, N. Nouwen, B. Oudega, N. Harms, A. J. Driessen, and J. Luirink. 2003. A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc. Natl. Acad. Sci. USA 100:5801-5806.
43. Weiner, L., J. L. Brissette, and P. Model. 1991. Stress-induced expression of the Escherichia coli phage shock protein operon is dependent on sigma 54 and modulated by positive and negative feedback mechanisms. Genes Dev. 5:1912-1923.
44. Westphal, S., L. Heins, J. Soll, and U. C. Vothknecht. 2001. Vippl deletion mutant of Synechocytis: a connection between bacterial phage shock and thylakoid biogenesis? Proc. Natl. Acad. Sci. USA 98:4243-4248.
45. Wexler, M., F. Sargent, R. L. Jack, N. R. Stanley, E. G. Bogsch, C. Robinson, B. C. Berks, and T. Palmer. 2000. TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in see-independent protein export. J. Biol. Chem. 275:16717-16722.
46. Wu, L. F., B. Ize, A. Chanal, Y. Quentin, and G. Fichant. 2000. Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J. Mol. Microbiol. Biotechnol. 2:179-189.
47. Yahr, T. L., and W. T. Wickner. 2001. Functional reconstitution of bacterial Tat translocation in vitro. EMBO J. 20:2472-2479.
48. Yen, M. R., Y. H. Tseng, E. H. Nguyen, L. F. Wu, and M. H. Saier, Jr. 2002. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177:441-450.