Specific inhibition of the translocation of a subset of Escherichia coli TAT substrates by the TorA signal peptide

Journal of Molecular Biology

Volumn 327, Issue 3, 2003, Pages 563-570

  Chanal, Angélique ^a   Santini, Claire Lise ^a   Wu, Long Fei ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Competition; SufI; TAT system; TorA; Twin arginine signal peptide

Indexed keywords

ARGININE DERIVATIVE; BACTERIAL PROTEIN; DIMETHYL SULFOXIDE REDUCTASE; FORMATE DEHYDROGENASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; HYDROGENASE; ISOENZYME; LIGAND; NITRATE; OXIDOREDUCTASE; PROTEIN SUFL; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; TRIMETHYLAMINE OXIDE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CELL FRACTIONATION; CONTROLLED STUDY; ELECTROPHORESIS; ENZYME ASSAY; ESCHERICHIA COLI; GENE DELETION; GENE TRANSLOCATION; IMMUNOBLOTTING; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

ESCHERICHIA COLI;

EID: 0037470623     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00170-0     Document Type: Article

References (48)

1. Pugsley A.P. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:1993;50-108.
2. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 271:1996;1519-1526.
3. Driessen A.J. SecB, a molecular chaperone with two faces. Trends Microbiol. 9:2001;193-196.
4. Phillips G.J., Silhavy T.J. Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature. 344:1990;882-884.
5. Wild J., Altman E., Yura T., Gross C.A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 6:1992;1165-1172.
6. Wild J., Rossmeissl P., Walter W.A., Gross C.A. Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J. Bacteriol. 178:1996;3608-3613.
7. Berks B.C., Sargent F., Palmer T. The Tat protein export pathway. Mol. Microbiol. 35:2000;260-274.
8. Wu L.-F., Ize B., Chanal A., Quentin Y., Fichant G. Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J. Mol. Microbiol. Biotechnol. 2:2000;179-189.
9. Rodrigue A., Boxer D.H., Mandrand-Berthelot M.A., Wu L.-F. Requirement for nickel of the transmembrane translocation of NiFe- hydrogenase 2 in Escherichia coli. FEBS Letters. 392:1996;81-86.
10. Santini C.L., Ize B., Chanal A., Müller M., Giordano G., Wu L.-F. A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17:1998;101-112.
11. Oresnik I.J., Ladner C.L., Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 40:2001;323-331.
12. Weiner J.H., Bilous P.T., Shaw G.M., Lubitz S.P., Frost L., Thomas G.H., et al. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell. 93:1998;93-101.
13. Stanley N.R., Palmer T., Berks B.C. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:2000;11591-11596.
14. Kato J., Nishimura Y., Yamada M., Suzuki H., Hirota Y. Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli. J. Bacteriol. 170:1988;3967-3977.
15. Ingledew W.J., Poole R.K. The respiratory chains of Escherichia coli. Microbiol. Rev. 48:1984;222-271.
16. Silvestro A., Pommier J., Pascal M.C., Giordano G. The inducible trimethylamine N-oxide reductase of Escherichia coli K-12: its localization and inducers. Biochim. Biophys. Acta. 994:1989;208-216.
17. Berks B.C. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:1996;393-404.
18. Yahr T.L., Wickner W.T. Functional reconstitution of bacterial Tat translocation in vitro. EMBO J. 20:2001;2472-2479.
19. Sargent F., Stanley N.R., Berks B.C., Palmer T. Sec-independent protein translocation in Escherichia coli: a distinct and pivotal role for the tatB protein. J. Biol. Chem. 274:1999;36073-36082.
20. Alami M., Trescher D., Wu L.-F., Muller M. Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J. Biol. Chem. 277:2002;20499-20503.
21. Sargent F., Bogsch E.G., Stanley N.R., Wexler M., Robinson C., Berks B.C., Palmer T. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17:1998;3640-3650.
22. Bogsch E., Sargent F., Stanley N.R., Berks B.C., Robinson C., Palmer T. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273:1998;18003-18006.
23. Cristobal S., de Gier J.-W., Nielsen H., von Heijne G. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 18:1999;2982-2990.
24. Santini C.-L., Bernadac A., Zhang M., Chanal A., Ize B., Blanco C., Wu L.-F. Translocation of jellyfish green fluorescent protein via the Tat system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J. Biol. Chem. 276:2001;8159-8164.
25. Bolhuis A., Mathers J.E., Thomas J.D., Barrett C.M., Robinson C. TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J. Biol. Chem. 276:2001;20213-20219.
26. Ize B., Gérard F., Zhang M., Chanal A., Voulhoux R., Palmer T., et al. In vivo dissection of the Tat translocation pathway in Escherichia coli. J. Mol. Biol. 317:2002;327-335.
27. Czjzek M., Dos Santos J.P., Pommier J., Giordano G., Mejean V., Haser R. Crystal structure of oxidized trimethylamine N-oxide reductase from Shewanella massilia at 2.5 Å resolution. J. Mol. Biol. 284:1998;435-447.
28. Allen S.C., Barrett C.M., Ray N., Robinson C. Essential cytoplasmic domains in the Escherichia coli TatC protein. J. Biol. Chem. 277:2002;10362-10366.
29. Rodrigue A., Chanal A., Beck K., Muller M., Wu L.-F. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J. Biol. Chem. 274:1999;13223-13228.
30. Stanley N.R., Sargent F., Buchanan G., Shi J., Stewart V., Palmer T., Berks B.C. Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol. Microbiol. 43:2002;1005-10021.
31. Thomas J.D., Daniel R.A., Errington J., Robinson C. Export of active green fluorescent protein to the perilasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol. Microbiol. 39:2001;47-53.
32. Ray N., Oates J., Turner R.J., Robinson C. 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 Letters. 534:2003;156-160.
33. Sambasivarao D., Turner R.J., Simala-Grant J.L., Shaw G., Hu J., Weiner J.H. Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 275:2000;22526-22531.
34. Manting E.H., Driessen A.J. Escherichia coli translocase: the unravelling of a molecular machine. Mol. Microbiol. 37:2000;226-238.
35. Mori H., Ito K. The Sec protein-translocation pathway. Trends Microbiol. 9:2001;494-500.
36. Wexler M., Sargent F., Jack R.L., Stanley N.R., Bogsch E.G., Robinson C., et al. TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export. J. Biol. Chem. 275:2000;16717-16722.
37. Bassford P.J. Jr, Silhavy T.J., Beckwith J.R. Use of gene fusion to study secretion of maltose-binding protein into Escherichia coli periplasm. J. Bacteriol. 139:1979;19-31.
38. Tommassen J., Leunissen J., van Damme-Jongsten M., Overduin P. Failure of E. coli K-12 to transport PhoE-LacZ hybrid proteins out of the cytoplasm. EMBO J. 4:1985;1041-1047.
39. Ito K., Akiyama Y., Yura T., Shiba K. Diverse effects of the MalE-LacZ hybrid protein on Escherichia coli cell physiology. J. Bacteriol. 167:1986;201-204.
40. Tjalsma H., Bolhuis A., Jongbloed J.D., Bron S., van Dijl J.M. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 64:2000;515-547.
41. Mori H., Cline K. A signal peptide that directs non-Sec transport in bacteria also directs efficient and exclusive transport on the thylakoid ΔpH pathway. J. Biol. Chem. 273:1998;11405-11408.
42. Wexler M., Bogsch E.G., Klösgen R.B., Palmer T., Robinson C., Berks B.C. Targeting signals for a bacterial Sec-independent export system direct plant thylakoid import by the delta pH pathway. FEBS Letters. 431:1998;339-342.
43. Halbig D., Hou B., Freudl R., Sprenger G.A., Klösgen R.B. Bacterial proteins carrying twin-R signal peptides are specifically targeted by the delta pH-dependent transport machinery of the thylakoid membrane system. FEBS Letters. 447:1999;95-98.
44. Blaudeck N., Sprenger G.A., Freudl R., Wiegert T. Specificity of signal peptide recognition in tat-dependent bacterial protein translocation. J. Bacteriol. 183:2001;604-610.
45. Pop O., Martin U., Abel C., Muller J.P. The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system. J. Biol. Chem. 277:2002;3268-3273.
46. Voordouw G. A universal system for the transport of redox proteins: early roots and latest developments. Biophys. Chem. 86:2000;131-140.
47. Maneewannakul S., Maneewannakul K., Ippen-Ihler K. The pKSM710 vector cassette provides tightly regulated lac and T7lac promoters and strategies for manipulating N-terminal protein sequences. Plasmid. 31:1994;300-307.
48. Takagi M., Tsuchiya T., Ishimoto M. Proton translocation coupled to trimethylamine N-oxide reduction in anaerobically grown Escherichia coli. J. Bacteriol. 148:1981;762-768.