The Twin-arginine Leader-binding Protein, DmsD, Interacts with the TatB and TatC Subunits of the Escherichia coli Twin-arginine Translocase

The twin-arginine translocase (Tat) pathway is involved in the targeting and translocation of fully folded proteins to the inner membrane and periplasm of bacteria. Proteins that use this pathway contain a characteristic twin-arginine signal sequence, which interacts with the receptor complex formed by the TatBC subunits. Recently, the DmsD protein was discovered, which binds to the twin-arginine signal sequences of the anaerobic respiratory enzymes dimethylsulfoxide reductase (DmsABC) and trimethylamine N-oxide (TMAO) reductase. In this work, the targeting of DmsD within Escherichia coli was investigated. Using cell fractionation and Western blot analysis, DmsD is found to be associated with the inner membrane of wild-type E. coli and a dmsABC mutant E. coli under anaerobic conditions. In contrast, DmsD is predominantly found in the cytoplasmic fraction of a ΔtatABCDE strain, which suggests that DmsD interacts with the membrane-associated Tat complex. Under aerobic conditions DmsD was also found primarily in the cytoplasmic fraction of wild-type E. coli, suggesting that physiological conditions have a significant effect upon the targeting of DmsD to the inner membrane. Size exclusion chromatography data and membrane washing studies indicate that DmsD is interacting tightly with an integral membrane protein and not with the lipid component of the E. coli inner membrane. Additional investigation into the nature of this interaction revealed that the TatB and TatC subunits of the translocase are important for the interaction of DmsD with the E. coli inner membrane. The twin-arginine translocase (Tat) pathway is involved in the targeting and translocation of fully folded proteins to the inner membrane and periplasm of bacteria. Proteins that use this pathway contain a characteristic twin-arginine signal sequence, which interacts with the receptor complex formed by the TatBC subunits. Recently, the DmsD protein was discovered, which binds to the twin-arginine signal sequences of the anaerobic respiratory enzymes dimethylsulfoxide reductase (DmsABC) and trimethylamine N-oxide (TMAO) reductase. In this work, the targeting of DmsD within Escherichia coli was investigated. Using cell fractionation and Western blot analysis, DmsD is found to be associated with the inner membrane of wild-type E. coli and a dmsABC mutant E. coli under anaerobic conditions. In contrast, DmsD is predominantly found in the cytoplasmic fraction of a ΔtatABCDE strain, which suggests that DmsD interacts with the membrane-associated Tat complex. Under aerobic conditions DmsD was also found primarily in the cytoplasmic fraction of wild-type E. coli, suggesting that physiological conditions have a significant effect upon the targeting of DmsD to the inner membrane. Size exclusion chromatography data and membrane washing studies indicate that DmsD is interacting tightly with an integral membrane protein and not with the lipid component of the E. coli inner membrane. Additional investigation into the nature of this interaction revealed that the TatB and TatC subunits of the translocase are important for the interaction of DmsD with the E. coli inner membrane. In prokaryotes, proteins can be transported across the cytoplasmic membrane in various manners. A common method for protein translocation is the general secretory (Sec) 1The abbreviations used are: Sec, general secretory; Tat, twin arginine translocase; TMAO, trimethylamine N-oxide; HRP, horseradish peroxidase; LB, Luria-Bertani; IPTG, isopropyl 1-thio-β-d-galactopyranoside; WT, wild type; SEC, size exclusion chromatography; SRP, signal recognition particle. pathway, which threads proteins across the membrane in an unfolded state (1Pugsley A.P. Possot O. Mol. Microbiol. 1993; 10: 665-674Crossref PubMed Scopus (49) Google Scholar, 2Manting E.H. Driessen A.J. Mol. Microbiol. 2000; 37: 226-238Crossref PubMed Scopus (210) Google Scholar). In contrast, the discovery of a Sec-independent pathway reveals that fully folded proteins can also be translocated across the membrane (3Santini C.-L. Ize B. Chanal A. Muller M. Giordano G. Wu L.-F. EMBO J. 1998; 17: 101-112Crossref PubMed Scopus (290) Google Scholar, 4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar). This pathway is now referred to as the twin-arginine translocase (Tat) protein-export pathway. Proteins that use the Tat system, including many respiratory enzymes that bind redox-active cofactors, contain a characteristic twin-arginine motif SRRXFLK in their signal peptides (6Berks B.C. Mol. Microbiol. 1996; 22: 393-404Crossref PubMed Scopus (561) Google Scholar). This conserved twin-arginine signal sequence targets precursor proteins to the membrane-bound Tat complex (7Berks B.C. Sargent F. Palmer T. Mol. Microbiol. 2000; 35: 260-274Crossref PubMed Scopus (472) Google Scholar). The E. coli Tat pathway is composed of tatA, tatB, tatC, and tatE, whose gene products encode integral membrane proteins (4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar, 8de Leeuw E. Porcelli I. Sargent F. Palmer T. Berks B.C. FEBS Lett. 2001; 506: 143-148Crossref PubMed Scopus (71) Google Scholar). The tatA, tatB, and tatC genes form an operon with a fourth gene, tatD, which is not required for protein translocation (9Wexler M. Sargent F. Jack R.L. Stanley N.R. Bogsch E.G. Robinson C. Berks B.C. Palmer T. J. Biol. Chem. 2000; 275: 16717-16722Abstract Full Text Full Text PDF PubMed Scopus (223) Google Scholar). TatA, TatB, and TatC are all required for protein translocation (4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar, 10Sargent F. Stanley N.R. Berks B.C. Palmer T. J. Biol. Chem. 1999; 274: 36073-36082Abstract Full Text Full Text PDF PubMed Scopus (249) Google Scholar, 11Bogsch E.G. Sargent F. Stanley N.R. Berks B.C. Robinson C. Palmer T. J. Biol. Chem. 1998; 273: 18003-18006Abstract Full Text Full Text PDF PubMed Scopus (329) Google Scholar) and are estimated to be in the cell at a molar ratio of 40:2:1 (12Sargent F. Gohlke U. De Leeuw E. Stanley N.R. Palmer T. Saibil H.R. Berks B.C. Eur. J. Biochem. 2001; 268: 3361-3367Crossref PubMed Scopus (128) Google Scholar). However, complexes with varying ratios of the three integral membrane proteins have been isolated and characterized (13Bolhuis A. Bogsch E.G. Robinson C. FEBS Lett. 2000; 472: 88-92Crossref PubMed Scopus (63) Google Scholar, 14Bolhuis A. Mathers J.E. Thomas J.D. Barrett C.M. Robinson C. J. Biol. Chem. 2001; 276: 20213-20219Abstract Full Text Full Text PDF PubMed Scopus (222) Google Scholar, 15de Leeuw E. Granjon T. Porcelli I. Alami M. Carr S.B. Muller M. Sargent F. Palmer T. Berks B.C. J. Mol. Biol. 2002; 322: 1135-1146Crossref PubMed Scopus (91) Google Scholar, 16Porcelli I. de Leeuw E. Wallis R. van den Brink-van der Laan E. de Kruijff B. Wallace B.A. Palmer T. Berks B.C. Biochemistry. 2002; 41: 13690-13697Crossref PubMed Scopus (96) Google Scholar). TatA and TatE are homologous proteins with overlapping functions in the Tat pathway, and recent studies have suggested that tatE may be a cryptic gene duplication of tatA (4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar, 17Jack R.L. Sargent F. Berks B.C. Sawers G. Palmer T. J. Bacteriol. 2001; 183: 1801-1804Crossref PubMed Scopus (115) Google Scholar). It has also been suggested that TatA might form the transport channel (7Berks B.C. Sargent F. Palmer T. Mol. Microbiol. 2000; 35: 260-274Crossref PubMed Scopus (472) Google Scholar, 18Palmer T. Berks B.C. Microbiology. 2003; 149: 547-556Crossref PubMed Scopus (81) Google Scholar, 19Sargent F. Berks B.C. Palmer T. Arch. Microbiol. 2002; 178: 77-84Crossref PubMed Scopus (81) Google Scholar). Though TatB is sequence related to TatA and TatE (4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar), it has a distinct role in the translocation of proteins (12Sargent F. Gohlke U. De Leeuw E. Stanley N.R. Palmer T. Saibil H.R. Berks B.C. Eur. J. Biochem. 2001; 268: 3361-3367Crossref PubMed Scopus (128) Google Scholar). The tatC gene product is predicted to be a polytopic membrane protein with four (20Gouffi K. Santini C.L. Wu L.F. FEBS Lett. 2002; 525: 65-70Crossref PubMed Scopus (42) Google Scholar) or six (19Sargent F. Berks B.C. Palmer T. Arch. Microbiol. 2002; 178: 77-84Crossref PubMed Scopus (81) Google Scholar) transmembrane helices and is considered capable of forming a specific binding site for the twin-arginine signal sequence (7Berks B.C. Sargent F. Palmer T. Mol. Microbiol. 2000; 35: 260-274Crossref PubMed Scopus (472) Google Scholar, 18Palmer T. Berks B.C. Microbiology. 2003; 149: 547-556Crossref PubMed Scopus (81) Google Scholar). Studies involving the thylakoid Tat system have shown that TatBC homologues form a complex that recognizes precursor proteins (21Cline K. Mori H. J. Cell Biol. 2001; 154: 719-729Crossref PubMed Scopus (244) Google Scholar) while in the bacterial system TatB and TatC have also been shown to form a functional and structural unit, which acts as a receptor complex for the twin-arginine leader sequence of Tat-bound proteins (10Sargent F. Stanley N.R. Berks B.C. Palmer T. J. Biol. Chem. 1999; 274: 36073-36082Abstract Full Text Full Text PDF PubMed Scopus (249) Google Scholar, 14Bolhuis A. Mathers J.E. Thomas J.D. Barrett C.M. Robinson C. J. Biol. Chem. 2001; 276: 20213-20219Abstract Full Text Full Text PDF PubMed Scopus (222) Google Scholar, 19Sargent F. Berks B.C. Palmer T. Arch. Microbiol. 2002; 178: 77-84Crossref PubMed Scopus (81) Google Scholar). Recently, a protein that specifically binds the twin-arginine signal sequence of the E. coli dimethylsulfoxide (Me2SO) reductase (DmsA subunit) was discovered (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar). This 204-residue protein, DmsD, has homology to the TorD family of molecular chaperones (19Sargent F. Berks B.C. Palmer T. Arch. Microbiol. 2002; 178: 77-84Crossref PubMed Scopus (81) Google Scholar). Sequence analysis predicts that members of this family comprise at least two distinct structural domains (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar, 23Tranier S. Iobbi-Nivol C. Birck C. Ilbert M. Mortier-Barriere I. Mejean V. Samama J.P. Structure. 2003; 11: 165-174Abstract Full Text Full Text PDF PubMed Scopus (58) Google Scholar). DmsD has also been shown to interact with the precursor form of trimethylamine N-oxide (TMAO) reductase (TorA) (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar), a DmsA homologue that also binds a molybdopterin cofactor. However, DmsD is unable to interact with the fully folded mature forms of DmsA and TorA, suggesting that it interacts with the twin-arginine signal sequence (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar). Recent speculation proposes that DmsD might also have the ability to interact with the cofactorless (unfolded) mature portions of the two redox enzymes (18Palmer T. Berks B.C. Microbiology. 2003; 149: 547-556Crossref PubMed Scopus (81) Google Scholar, 19Sargent F. Berks B.C. Palmer T. Arch. Microbiol. 2002; 178: 77-84Crossref PubMed Scopus (81) Google Scholar). An understanding of the role of DmsD in the Tat system is still in a preliminary stage. Previously, it was proposed that specific leader binding proteins might exist to escort twin-arginine containing proteins to the Tat translocase (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar). In this study, the targeting of DmsD to the E. coli inner membrane was investigated. It was shown that under anaerobic conditions, DmsD is associated with the inner membrane in wild type (WT) and dmsABC mutant strains of E. coli. However, in the absence of the Tat translocase complex, DmsD is found primarily in the cytoplasmic fraction. DmsD was also predominantly in the fraction of E. coli under aerobic conditions, that the the targeting of investigation of the nature of the interaction of DmsD with the membrane under anaerobic conditions, it was shown that DmsD interacts tightly with an integral membrane investigation suggests that the TatB and TatC subunits are important for the interaction of DmsD with the membrane-associated Tat this that the twin-arginine leader binding protein, DmsD, interacts with the TatBC twin-arginine signal sequence receptor complex the E. coli inner membrane. and coli strains and by and J. of and by F. Sargent of was with a DmsD with an (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar). by a strains and or coli T. Studies the G. Shaw G. J. J.H. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google G. Shaw G. J. J.H. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google G. Shaw G. J. J.H. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google G. Shaw G. J. J.H. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google J.H. Biochem. PubMed Scopus Google U. S. A. PubMed Scopus Google F. Stanley N.R. Berks B.C. Palmer T. J. Biol. Chem. 1999; 274: 36073-36082Abstract Full Text Full Text PDF PubMed Scopus (249) Google F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google F. Stanley N.R. Berks B.C. Palmer T. J. Biol. Chem. 1999; 274: 36073-36082Abstract Full Text Full Text PDF PubMed Scopus (249) Google M. Sargent F. Jack R.L. Stanley N.R. Bogsch E.G. Robinson C. Berks B.C. Palmer T. J. Biol. Chem. 2000; 275: 16717-16722Abstract Full Text Full Text PDF PubMed Scopus (223) Google I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google in a of and Cell anaerobic for at in a Turner R.J. Shaw G. J. J.H. J. Biol. Chem. 2000; 275: Full Text Full Text PDF PubMed Scopus (58) Google Scholar), with and the cell was in a of and The cell was at a cell at for to and protein the cell was at for to the cytoplasmic and membrane The membrane and in a of A by of a The membrane at for to the and membrane by in a of A. at and an of fraction was DmsD was the of (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar) and was used within a of A method Biochem. Scopus Google Scholar) was used to the protein of fraction and was used to the by Western blot an the to DmsD in all DmsD was the of the not DmsD was not in the various strains in the studies of DmsD was of the of the and membrane of DmsD was The of DmsD in the various was Western blot analysis the a of in a The an and with The of DmsD in the cytoplasmic and membrane was as the of DmsD in cell fraction was by the of to the DmsD This was used to the of DmsD in the and the of DmsD in fraction the The fraction of may be a membrane fraction or a cytoplasmic fraction. The of DmsD to the membrane to the cytoplasmic was by the of DmsD in and that to as in of of and mutant E. coli with in at in in a of the with a of at while the two not four for an to Cell and the of DmsD the for the anaerobic of E. coli E. coli lipid of E. coli lipid The lipid was with in of A. The was at with and The was to by of the a Cell at for the of A was to the which at and used within of Studies Using Size studies the of F. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google Scholar). DmsD was with various ratios of and in for at The an containing of with of to The was with a of two of with a also with and The was as a of and the of DmsD and the also and used for molecular DmsD to by at for the was a Proteins in fraction by the of of The at for at for and The was in of and of and by The of the DmsD was by Western as in Studies of E. coli and E. coli with with of and with a of various isopropyl and of the was to the at containing of The for and for This was four for at at The and proteins as in the The membrane in of and in the of the membrane with an of was membrane and by and the of DmsD in the various was Western blot analysis the of and with of and and as DmsD with the E. coli under to the of DmsD in E. coli with and the Western blot analysis of revealed of DmsD in all strains and by Western of the and cell not DmsD was not in targeting within the cell not be to Western blot the that under anaerobic conditions, DmsD is associated with the E. coli inner membrane fraction and is not found in the cytoplasmic fraction washing of the with not in of DmsD the membrane DmsD was not in the fraction not This was in and E. coli strains and of DmsD in to the DmsD was found in the cytoplasmic and membrane of a ΔtatABCDE with The of of protein into of the was the Western blot are not of the of DmsD in a fraction of E. coli. In to the DmsD in the cytoplasmic to the membrane of E. coli a the Western blot data was of DmsD in the ΔtatABCDE revealed that of DmsD was in the cytoplasmic fraction with that associated with the membrane fraction in the a not in of the DmsD the of the which subunits important for the interaction of DmsD with the Tat the of DmsD in was in E. coli, DmsD was in the membrane of strains with tatA, tatD, tatE, or gene In contrast, the and and to the for the and the of DmsD was in the while was associated with the inner membrane In all a not the DmsD the membrane of DmsD in a dmsABC or not the targeting of DmsD to the inner membrane was upon the of a mutant was In this DmsD was in the membrane fraction and the membrane an of the of the effect of an aerobic the targeting of DmsD, and E. coli strains with under aerobic conditions. In to the for E. coli in anaerobic DmsD was primarily in the DmsD was also found in the cytoplasmic fraction of a The of with effect the of DmsD within the with found associated with the membrane. DmsD with E. coli the interaction of DmsD with the membrane was protein or lipid DmsD was with E. coli The of the was as a not at while a and of DmsD at was of interaction DmsD and E. coli lipid upon the of DmsD with a of This was by two at and to E. coli lipid and Western blot analysis of the that DmsD was not in the of not The for all ratios of DmsD to not of the of DmsD with the E. coli type of interaction is DmsD and the E. coli inner the E. coli and with various DmsD the membrane in the of all used in the of was significant of DmsD in the fraction to the The an not the with which DmsD was associated with the E. coli with of DmsD tightly associated with the membrane at of with in the the of in an of DmsD in the However, in the of was the of DmsD the membrane An not In this various E. coli for the of DmsD, with the of the of DmsD within E. coli. This was by Western blot analysis an the Under anaerobic conditions DmsD is found the E. coli inner membrane of and dmsABC mutant In contrast, the of DmsD was found in the cytoplasmic fraction of a mutant under the conditions. This interaction is by the or absence of in the was to the nature of the interaction of DmsD with the E. coli inner membrane under anaerobic conditions. data and membrane washing studies that DmsD is interacting with an integral membrane investigation revealed that the interaction of DmsD with the E. coli cytoplasmic membrane is upon the TatB and TatC subunits. The in this that DmsD is associated with the E. coli inner membrane under anaerobic conditions. the TatA, or TatE subunits to the as DmsD is associated with the inner membrane. is not required for protein translocation the Tat pathway (9Wexler M. Sargent F. Jack R.L. Stanley N.R. Bogsch E.G. Robinson C. Berks B.C. Palmer T. J. Biol. Chem. 2000; 275: 16717-16722Abstract Full Text Full Text PDF PubMed Scopus (223) Google Scholar), it is not that DmsD in and the targeting of DmsD is not by the absence of the TatA or TatE subunits. The with the and strains are in with which that the TatA and TatE homologues have overlapping functions in the Tat pathway (4Sargent F. Bogsch E.G. Stanley N.R. Wexler M. Robinson C. Berks B.C. Palmer T. EMBO J. 1998; 17: 3640-3650Crossref PubMed Scopus (444) Google Scholar, 5Weiner J.H. Bilous P.T. Shaw G.M. Lubitz S.P. Frost L. Thomas G.H. Cole J.A. Turner R.J. Cell. 1998; 93: 93-101Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar). DmsD was also associated with the E. coli inner membrane in a mutant This suggests that the targeting of DmsD to the E. coli inner membrane is not by with the DmsA The absence of the Tat complex has a effect the of DmsD within E. coli. a fraction of DmsD is still to the inner the absence of the translocase to the interaction of DmsD with the membrane. This was in the and in which DmsD was found primarily in the cytoplasmic that DmsD interacts with the TatB and TatC subunits of the translocase complex. A in to the interaction of DmsD with the Tat complex. However, the absence of subunits not to in a of DmsD in the cytoplasmic fraction. This suggests that subunits are important for the interaction of DmsD with the Tat complex. are in with work, which has that the TatB and TatC subunits in and form a functional and structural (10Sargent F. Stanley N.R. Berks B.C. Palmer T. J. Biol. Chem. 1999; 274: 36073-36082Abstract Full Text Full Text PDF PubMed Scopus (249) Google Scholar, 14Bolhuis A. Mathers J.E. Thomas J.D. Barrett C.M. Robinson C. J. Biol. Chem. 2001; 276: 20213-20219Abstract Full Text Full Text PDF PubMed Scopus (222) Google Scholar, 17Jack R.L. Sargent F. Berks B.C. Sawers G. Palmer T. J. Bacteriol. 2001; 183: 1801-1804Crossref PubMed Scopus (115) Google Scholar). Recent studies have also shown that a TatBC complex containing TatA protein is capable of binding a Tat signal while a complex composed predominantly of TatA with of TatB was of this interaction Leeuw E. Granjon T. Porcelli I. Alami M. Carr S.B. Muller M. Sargent F. Palmer T. Berks B.C. J. Mol. Biol. 2002; 322: 1135-1146Crossref PubMed Scopus (91) Google Scholar). the interaction of DmsD, a twin-arginine protein, with the TatB and TatC subunits is with which suggests that the TatBC proteins form a receptor complex capable of the twin-arginine signal sequence of proteins (18Palmer T. Berks B.C. Microbiology. 2003; 149: 547-556Crossref PubMed Scopus (81) Google Scholar, K. Mori H. J. Cell Biol. 2001; 154: 719-729Crossref PubMed Scopus (244) Google Scholar). The and membrane washing for the interaction of DmsD with a protein component of the E. coli inner membrane. In a related study, F. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google Scholar) and used to a membrane-associated signal recognition binds to the inner membrane of E. coli. is involved in the targeting of to the E. coli inner membrane an interaction with S. de G. G. B. J. EMBO J. 1998; 17: PubMed Scopus Google Scholar, T. EMBO J. PubMed Scopus Google Scholar). or not DmsD interacts with the E. coli inner membrane lipid The by Western blot analysis the of DmsD, that DmsD is not interacting with the lipid component of the suggesting that the interaction is protein washing of the anaerobic with various that a as is to the interaction of DmsD with the membrane. This suggests that DmsD is interacting tightly with an integral membrane protein or studies J. A. L. T. L. J. M. H. H. J. and R. J. in have shown that DmsD to in the of which is with the which a significant of DmsD was the E. coli inner membrane. it that DmsD is required for the of interaction with the membrane. important this is that the physiological conditions have a significant effect the of DmsD in E. coli, as by the distinct for E. coli DmsD binds the twin-arginine signal sequences of dimethylsulfoxide and reductase (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar), two enzymes that are under anaerobic conditions J.H. Microbiology. 1996; PubMed Scopus Google Scholar, J.H. PubMed Scopus Google Scholar, Microbiol. PubMed Scopus Google Scholar). it that the interaction of DmsD with the membrane be upon an anaerobic DmsD is associated with the membrane in anaerobic analysis of the sequence suggests that DmsD is not a membrane J. The in this that under anaerobic conditions, DmsD is to the membrane-bound Tat complex in E. coli and is interacting tightly with the TatBC signal sequence receptor complex. It was also shown that this interaction is of the DmsA and is upon the physiological conditions of the this the that DmsD might as a targeting (22Oresnik I.J. Ladner C.L. Turner R.J. Mol. Microbiol. 2001; 40: 323-331Crossref PubMed Scopus (145) Google Scholar), in the interaction of DmsA with the Tat An for the be to the by which this F. Sargent of and J. of for E. coli mutant G. for the and T. L. for with protein and of

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