Six conserved cysteines of the membrane protein DsbD are required for the transfer of electrons from the cytoplasm to the periplasm of Escherichia coli

EMBO Journal

Volumn 18, Issue 21, 1999, Pages 5963-5971

  Stewart, Eric J ^a,b   Katzen, Federico ^a   Beckwith, Jon ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

Cytochrome; Disulfide bond; Electron transport; Isomerization; Membrane topology

Indexed keywords

CYSTEINE; CYTOCHROME C; MEMBRANE PROTEIN;

ARTICLE; CYTOPLASM; DISULFIDE BOND; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; REDUCTION;

ALKALINE PHOSPHATASE; AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CYSTEINE; DISULFIDES; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; PERIPLASM; PROTEIN BIOSYNTHESIS; PROTEIN DISULFIDE-ISOMERASE; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0033230589     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.21.5963     Document Type: Article

References (39)

1. Andersen, C.L., Matthey-Dupraz, A., Missiakas, D. and Raina, S. (1997) A new Escherichia coli gene, dsbG, encodes a periplasmic protein involved in disulphide bond formation, required for recycling DsbA/DsbB and DsbC redox proteins. Mol. Microbiol., 26, 121-132.
2. Bader, M., Muse, W., Zander, T. and Bardwell, J. (1998) Reconstitution of a protein disulfide catalytic system. J. Biol. Chem., 273, 10302-10307.
3. Bader, M., Muse, W., Ballou, D.P., Gassner, C. and Bardwell, J.C.A. (1999) Oxidative protein folding is driven by the electron transport system. Cell, 98, 217-227.
4. Bardwell, J.C.A., McGovern, K. and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell, 67, 581-589.
5. Bardwell, J.C.A., Lee, J.-O., Jander, G., Martin, N., Belin, D. and Beckwith, J. (1993) A pathway for disulfide bond formation in vivo. Proc. Natl Acad. Sci. USA, 90, 1038-1042.
6. Bessette, P.H., Cotto, J.J., Gilbert, H.F. and Georgiou, G. (1999) In vivo and in vitro function of the Escherichia coli periplasmic cysteine oxidoreductase DsbG. J. Biol. Chem., 274, 7784-7792.
7. Boyd, D., Manoil, C. and Beckwith, J. (1987) Determinants of membrane protein topology. Proc. Natl Acad. Sci. USA, 84, 8525-8529.
8. Boyd, D., Traxler, B. and Beckwith, J. (1993) Analysis of the topology of a membrane protein by using a minimum number of alkaline phosphatase fusions. J. Bacteriol., 175, 553-556.
9. Crooke, H. and Cole, J. (1995) The biogenesis of c-type cytochromes in Escherichia coli requires a membrane-bound protein, DipZ, with a protein disulphide isomerase-like domain. Mol. Microbiol., 15, 1139-1150.
10. Dailey, F.E. and Berg, H.C. (1993) Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc. Natl Acad. Sci. USA, 90, 1043-1047.
11. Darby, N.J., Raina, S. and Creighton, T.E. (1998) Contributions of substrate binding to the catalytic activity of DsbC. Biochemistry, 37, 783-791.
12. De Lorenzo, F., Goldberger, R.F., Steers, E.J., Givol, D. and Anfinsen, B. (1966) Purification and properties of an enzyme from beef liver which catalyzes sulfhydryl-disulfide interchange in proteins. J. Biol. Chem., 241, 1562-1567.
13. Fabianek, R.A., Hennecke, H. and Thöny-Meyer, L. (1998) The active-site cysteines of the periplasmic thioredoxin-like protein CcmG of Escherichia coli are important but not essential for cytochrome c maturation in vivo. J. Bacteriol., 180, 1947-1950.
14. Fabianek, R.A., Hofer, T. and Thöny-Meyer, L. (1999) Characterization of the Escherichia coli CcmH protein reveals new insights into the redox pathway required for cytochrome c maturation. Arch. Microbiol., 171, 92-100.
15. Fong, S.T., Camakaris, J. and Lee, B.T. (1995) Molecular genetics of a chromosomal locus involved in copper tolerance in Escherichia coli K-12. Mol. Microbiol., 15, 1127-1137.
16. Frishman, D. (1996). DSBC protein: A new member of the thioredoxin fold-containing family. Biochem. Biophys. Res. Commun., 219, 686-689.
17. Guilhot, C., Jander, G., Martin, N.L. and Beckwith, J. (1995) Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc. Natl Acad. Sci. USA, 92, 9895-9899.
18. Guzman, L.-M., Belin, D., Carson, M.J. and Beckwith, J. (1995) Tight regulation, modulation and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol., 177, 4121-4130.
19. Jander, G., Martin, N.L. and Beckwith, J. (1994) Two cysteines in each periplasmic domain of the membrane protein DsbB are required for its function in protein disulfide bond formation. EMBO J., 13, 5121-5128.
20. Jeng, M.F., Holmgren, A. and Dyson, H.J. (1995) Proton sharing between cysteine thiols in Escherichia coli thioredoxin: implications for the mechanism of protein disulfide reduction. Biochemistry, 34, 10101-10105.
21. Joly, J.C. and Swartz, J.R. (1997) In vitro and in vivo redox states of the Escherichia coli periplasmic oxidoreductases DsbA and DsbC. Biochemistry, 36, 10067-10072.
22. Kishigami, S. and Ito, K. (1996) Roles of cysteine residues of DsbB in its activity to recognize DsbA, the protein disulfide catalyst of Escherichia coli. Genes Cells, 1, 201-208.
23. Kishigami, S., Kanaya, E., Kikuchi, M. and Ito, K. (1995) DsbA-DsbB interaction through their active-site cysteines. Evidence from an odd cysteine mutant of DsbA. J. Biol. Chem., 270, 17072-17074.
24. Kobayashi, T. and Ito, K. (1999) Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J., 18, 1192-1198.
25. Kobayashi, T., Kishigami, S., Sone, M., Inokuchi, H., Mogi, T. and Ito, K. (1997) Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc. Natl Acad. Sci. USA, 94, 11857-11862.
26. Link, A.J., Phillips, D. and Church, G.M. (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol., 179, 6228-6237.
27. Manoil, C. and Beckwith, J. (1986) A genetic approach to analyzing membrane protein topology. Science, 233, 1403-1408.
28. Martin, J.L., Bardwell, J.C.A. and Kuriyan, J. (1993) Crystal structure of DsbA protein required for disulphide bond formation in vivo. Nature, 365, 464-468.
29. Missiakas, D., Georgopoulos, C. and Raina, S. (1994) The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. EMBO J., 13, 2013-2020.
30. Missiakas, D., Schwager, F. and Raina, S. (1995) Identification and characterization of a new disulfide isomerase-like protein (DsbD) in Escherichia coli. EMBO J., 14, 3415-3424.
31. Rietsch, A. and Beckwith, J. (1998) The genetics of disulfide bond metabolism. Annu. Rev. Genet., 32, 163-184.
32. Rietsch, A., Belin, D., Martin, N. and Beckwith, J. (1996) An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl Acad. Sci. USA, 93, 13048-13053.
33. Rietsch, A., Bessette, P., Georgiou, G. and Beckwith, J. (1997) Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J. Bacteriol., 179, 6602-6608.
34. Sambongi, Y. and Ferguson, S.J. (1994) Specific thiol compounds complement deficiency in c-type cytochrome biogenesis in Escherichia coli carrying a mutation in a membrane-bound disulphide isomerase-like protein. FEBS Lett., 353, 235-238.
35. San Millan, J.L., Boyd, D., Dalbey, R., Wickner, W. and Beckwith, J. (1989) Use of phoA fusions to study the topology of the Escherichia coli inner membrane protein leader peptidase. J. Bacteriol., 171, 5536-5541.
36. Schulz, H., Hennecke, H. and Thöny-Meyer, L. (1998) Prototype of a heme chaperone essential for cytochrome c maturation. Science, 281, 1197-1200.
37. Shevchik, V.E., Condemine, G. and Robert-Baudouy, J. (1994) Characterization of DsbC, a periplasmic protein of Erwinia chrysanthemi and Escherichia coli with disulfide isomerase activity. EMBO J., 13, 2007-2012.
38. Thomas, P.E., Ryan, D. and Levin, W. (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem., 75, 168-176.
39. Zeng, H., Snavely, I., Zamorano, P. and Javor, G.T. (1998) Low ubiquinone content in Escherichia coli causes thiol hypersensitivity. J. Bacteriol., 180, 3681-3685.