Complementation of DsbA deficiency with secreted thioredoxin variants reveals the crucial role of an efficient dithiol oxidant for catalyzed protein folding in the bacterial periplasm

EMBO Journal

Volumn 18, Issue 12, 1999, Pages 3271-3281

  Jonda, Silke ^a   Huber Wunderlich, Martina ^a,b   Glockshuber, Rudi ^a   Mössner, Ekkehard ^a  

^a ETH ZURICH   (Switzerland)

^b BAYER PHARMA AG   (Germany)

Author keywords

Disulfide bond formation; Disulfide oxidoreductases; DsbA; Redox potential; Thioredoxin

Indexed keywords

OXIDOREDUCTASE; THIOREDOXIN;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME DEFICIENCY; ESCHERICHIA COLI; GENETIC COMPLEMENTATION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECRETION;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CATALYSIS; CATALYTIC DOMAIN; DISULFIDES; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; HALF-LIFE; HIRUDINS; HUMANS; MUTATION; OXIDANTS; OXIDATION-REDUCTION; PEPTIDES; PERIPLASM; PROTEIN DISULFIDE-ISOMERASE; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS; RECOMBINANT FUSION PROTEINS; THIOREDOXIN; TOLUENE;

EID: 0033564233     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.12.3271     Document Type: Article

References (64)

1. Ajouz, B., Berrier, C., Garrigues, A., Besnard, M. and Ghazi, A. (1998) Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J. Biol. Chem., 273, 26670-26674.
2. Akiyama, Y., Kamitani, S., Kusukawa, N. and Ito, K. (1992) In vitro catalysis of oxidative folding of disulfide-bonded proteins by the Escherichia coli dsbA (ppfA) gene product. J. Biol. Chem., 267, 22440-22445.
3. Andersen, J.F., Sanders, D.A., Gasdaska, J.R., Weichsel, A., Powis, G. and Montfort, W.R. (1997) Human thioredoxin homodimers: regulation by pH, role of aspartate 60, and crystal structure of the aspartate 60→asparagine mutant. Biochemistry, 36, 13979-13988.
4. Åslund, F., Berndt, K.D. and Holmgren, A. (1997) Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem., 272, 30780-30786.
5. Bachmann, B.J. (1972) Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev., 36, 525-557.
6. Bader, M., Muse, W., Zander, T.P. and Bardwell, J.C.A. (1998) Reconstitution of a protein disulfide catalytic system. J. Biol. Chem., 273, 10302-10307.
7. 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.
8. Bardwell, J.C.A., Lee, J., 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.
9. Chivers, P.T., Laboissiere, M.C.A. and Raines, R.T. (1996) The CXXC motif: imperatives for the formation of native disulfide bonds in the cell. EMBO J., 15, 2659-2667.
10. Dailey, F.E. and Berg, H.C. (1993) Mutants in disulfide bond fnrmation that disrupt flagellar assembly in Escherichia coli. Proc. Natl Acad. Sci. USA, 90, 1043-1047.
11. Darby, N.J. and Creighton, T.E. (1995a) Characterization of the active site cysteine residues of the thioredoxin-like domains of protein disulfide isomerase. Biochemistry, 34, 16770-16780.
12. Darby, N.J. and Creighton, T.E. (1995b) Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry, 34, 11725-11735.
13. Darby, N.J., Raina, S. and Creighton, T.E. (1998) Contributions of substrate binding to the catalytic activity of DsbC. Binchemistry, 37, 783-791.
14. Debarbieux, L. and Beckwith, J. (1998) The reductive enzyme thioredoxin 1 acts as an oxidant when it is exported to the Escherichia coli periplasm. Proc. Natl Acad. Sci. USA, 95, 10751-10756.
15. Derman, A.I., Prinz, W.A., Belin, D. and Beckwith, J. (1993) Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science, 262, 1744-1747.
16. 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.
17. Frand, A.R. and Kaiser, C.A. (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell, 1, 161-170.
18. Freedman, R.B., Hawkins, H.C. and McLaughlin, S.H. (1995) Protein disulfide-isomerase. Methods Enzymol., 251, 397-406.
19. Froshauer, S., Green, G.N., Boyd, D., McGovern, K. and Beckwith, J. (1988) Genetic analysis of the membrane insertion and topology of MalF, a cytoplasmic membrane protein of Escherichia coli. J. Mol. Biol., 200, 501-511.
20. Gilbert, H.F. (1990) Molecular and cellular aspects of thiol - disulfide exchange. Adv. Enzymol., 63, 69-172.
21. Gilbert, H.F. (1995) Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol, 251, 8-28.
22. Grauschopf, U., Winther, J.R., Korber, P., Zander, T.P., Dallinger, P. and Bardwell, J.C.A. (1995) Why is DsbA such an oxidizing disulfide catalyst? Cell, 83, 947-955.
23. Guddat, L.W., Bardwell, J.C.A. and Martin, J.L. (1998) Crystal structures of reduced and oxidized DsbA: investigation of domain motion and thiolate stabilization. Structure, 6, 757-767.
24. Guilhot, C., Jander, G., Martin, N.L. and Beckwith, J. (1995) Evidence that the pathway of disulfide bond forlation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc. Natl Acad. Sci. USA, 92, 9895-9899.
25. Hennecke, J., Sebbel, P. and Glockshuber, R. (1999) Random circular permutation of DsbA reveals segments that are essential for protein folding and stability. J. Mol. Biol., 286, 1197-1215.
26. Holmgren, A. and Björnstedt, B. (1995) Thioredoxins and Glutaredoxins. Methods Enzymol., 252, 199-209.
27. Holst, B., Tachibana, C. and Winther, J.R. (1997) Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum. J. Cell Biol., 138, 1229-1238.
28. Huber-Wunderlich, M. and Glockshuber, R. (1998) A single dipeptide sequence modulates the redox properties of a whole enzyme family. Folding and Design, 3, 161-171.
29. Humphreys, D.P., Weir, N., Mountain, A. and Lund, P.A. (1995) Human protein disulfide isomerase functionally complements a dsbA mutation and enhances the yield of pectate lyase C in Escherichia coli. J. Biol. Chem., 270, 28210-28215.
30. Hwang, C., Sinskey, A.J. and Lodish, H.F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science, 247, 1496-1502.
31. Jacobi, A., Huber-Wunderlich, M., Hennecke, J. and Glockshuber, R. (1997) Elimination of all charged residues in the vicinity of the active-site helix of the disulfide oxidoreductase DsbA. J. Biol. Chem., 272, 21692-21699.
32. Katti, S.K., LeMaster, D.M. and Eklund, H. (1990) Crystal structure of thioredoxin from Escherichia coli at 1.68 Å resolution. J. Mol. Biol., 212, 167-184.
33. 15N NMR spectroscopy. Biochemistry, 35, 7684-7691.
34. Kemmink, J., Darby, N.J., Dijkstra, K., Nilges, M. and Creighton, T.E. (1997) The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Curr. Biol., 7, 239-245.
35. Kishigami, S. and Ito, K. (1996) Roles of cysteine residues of DsbB in its activity to reoxidize DsbA, the protein disulphide bond catalyst of Escherichia coli. Genes to Cells, 1, 201-208.
36. Kishigami, S., Kanaya, E., Kikuchi, M. and Ito, K. (1995a) DsbA-DsbB interaction through their active site cysteines. Evidence from an odd cysteine mutant of DsbA. J. Biol. Chem., 270, 17072-17074.
37. Kishigami, S., Akiyama, Y. and Ito, K. (1995b) Redox states of DsbA in the periplasm of Escherichia coli. FEBS Lett., 364, 55-58.
38. 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.
39. Kortemme, T., Darby, N.J., and Creighton, T.E. (1996) Electrostatic interactions in the active site of the N-terminal thioredoxin-like domain of protein disulfide isomerase. Biochemistry, 35, 14503-14511.
40. Krause, G., Lundström, J., Barea, J.L., Pueyo de la Cuesta, C. and Holmgren, A. (1991) Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J. Biol. Chem., 266, 9494-9500.
41. Laboissiere, M.C., Chivers, P.T. and Raines, R.T. (1995) Production of rat protein disulfide isomerase in Saccharomyces cerevisiae. Protein Expr. Purif., 6, 700-706.
42. Lin, T.-Y. and Kim, P.S. (1989) Urea dependence of thiol-disulfide equilibria in thioredoxin: confirmation of the linkage relationship and a sensitive assay for structure. Biochemistry, 28, 5282-5287.
43. Lundström, J. and Holmgren, A. (1993) Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase from the equilibrium with glutathione and thioredoxin. Biochemistry, 32, 6649-6655.
44. Lunn, C.A. and Pigiet, V.P. (1982) Localization of thioredoxin from Escherichia coli in an osmotically sensitive compartment. J. Biol. Chem., 257, 11424-11430.
45. Martin, J.L. (1995) Thioredoxin - a fold for all reasons. Structure, 3, 245-250.
46. 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.
47. Mössner, E., Huber-Wunderlich, M. and Glockshuber, R. (1998) Thioredoxin variants mimicking the active sites of other thiol/disulfide oxidoreductases. Protein Sci., 7, 1233-1244.
48. Ostermeier, M., De Sutter, K. and Georgiou, G. (1996) Eukaryotic protein disulfide isomerase complements Escherichia coli dsbA mutants and increases the yield of a heterologous secreted protein with disulfide bonds. J. Biol. Chem., 271, 10616-10622.
49. Pigiet, V.P. and Schuster, B.J. (1986) Thioredoxin-catalyzed refolding of disulfide-containing proteins. Proc. Natl Acad. Sci. USA, 83, 7643-7647.
50. Pollard, M.G., Travers, K.J. and Weissman, J.S. (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell, 1, 171-182.
51. Raina, S. and Missiakas, D. (1997) Making and breaking disulfide bonds. Annu. Rev. Microbiol., 51, 179-202.
52. Rietsch, A. and Beckwith, J. (1998) The genetics of disulfide bond metabolism. Annu. Rev. Genet., 32, 163-184.
53. 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.
54. 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.
55. Rodríguez-Peña, J.M., Alvarez, I., Ibáñez, M. and Rotger, R. (1997) Homologous regions of the Salmonella enteritidis virulence plasmid and the chromosome of Salmonella typhi encode thiol:disulphide oxidoreductases belonging to the DsbA thioredoxin family. Microbiology, 143, 1405-1413.
56. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. van Straaten, M., Missiakas, D., Raina, S. and Darby, N. (1998) The functional properties of DsbG, a thiol-disulfide oxidoreductase from the periplasm of Escherichia coli. FEBS Lett., 428, 255-258.
58. Wunderlich, M. and Glockshuber, R. (1993a) Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci., 2, 717-726.
59. Wunderlich, M. and Glockshuber, R. (1993b) In vivo control of redox potential during protein folding catalyzed by bacterial protein disulfide-isomerase (DsbA). J. Biol. Chem., 268, 24547-24550.
60. Wunderlich, M., Otto, A., Seckler, R. and Glockshuber, R. (1993) Bacterial protein disulfide isomerase: efficient catalysis of oxidative protein folding at acidic pH. Biochemistry, 32, 12251-12256.
61. Wunderlich, M., Otto, A., Maskos, K., Mücke, M., Seckler, R. and Glockshuber, R. (1995) Efficient catalysis of disulfide formation during protein folding with a single active-site cysteine. J. Mol. Biol., 247, 28-33.
62. Zapun, A. and Creighton, T.E. (1994) Effects of DsbA on the disulfide folding of bovine pancreatic trypsin inhibitor and alpha-lactalbumin. Biochemistry, 33, 5202-5211.
63. Zapun, A., Bardwell, J.C.A. and Creighton, T.E. (1993) The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo. Biochemistry, 32, 5083-5092.
64. Zapun, A., Missiakas, D., Raina, S. and Creighton, T.E. (1995) Structural and functional characterization of DsbC, a protein involved in disulfide bond formation in Escherichia coli. Biochemistry, 34, 5075-5089.