Small-molecule diselenides catalyze oxidative protein folding in vivo

ACS Chemical Biology

Volumn 5, Issue 2, 2010, Pages 177-182

  Beld, Joris ^a,b   Woycechowsky, Kenneth J ^a,c   Hilvert, Donald ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL STRAIN; CATALYSIS; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ESCHERICHIA COLI; IN VIVO STUDY; NONHUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING;

CATALYSIS; CYSTEINE; CYSTINE; DISULFIDES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ORGANOSELENIUM COMPOUNDS; OXIDATION-REDUCTION; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; SULFHYDRYL COMPOUNDS;

PROKARYOTA;

EID: 77449091017     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb9002688     Document Type: Article

References (35)

1. Berndt, C., Lillig, C. H., and Holmgren, A. (2008) Thioredoxins and glutaredoxins as facilitators of protein folding, Biochim. Biophys. Acta 1783, 641-650.
2. Dailey, F. E., and Berg, H. C. (1993) Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 90, 1043-1047.
3. Dumoulin, A., Grauschopf, U., Bischoff, M., Thöny-Meyer, L., and Berger-Bächi, B. (2005) Staphylococcus aureus DsbA is a membrane-bound lipoprotein with thiol-disulfide oxidoreductase activity, Arch. Microbiol. 184, 117-128.
4. 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.
5. Woycechowsky, K. J., Wittrup, K. D., and Raines, R. T. (1999) A small-molecule catalyst of protein folding in vitro and in vivo, Chem. Biol. 6, 871-879.
6. Winter, J., Lilie, H., and Rudolph, R. (2002) Recombinant expression and in vitro folding of proinsulin are stimulated by the synthetic dithiol Vectrase-P, FEMS Microbiol. Lett. 213, 225-230.
7. Wunderlich, M., and Glockshuber, R. (1993) In vivo control of redox potential during protein folding catalyzed by bacterial protein disulfide-isomerase (DsbA), J. Biol. Chem. 268, 24547-24550.
8. 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.
9. Walker, K. W., and Gilbert, H. F. (1994) Effect of redox environment on the in vitro and in vivo folding of RTEM-1 β-lactamase and Escherichia coli alkaline phosphatase, J. Biol. Chem. 269, 28487-28493.
10. Beld, J., Woycechowsky, K. J., and Hilvert, D. (2007) Selenoglutathione: Efficient oxidative protein folding by a diselenide, Biochemistry 46, 5382-5390.
11. Beld, J., Woycechowsky, K. J., and Hilvert, D. (2008) Catalysis of oxidative protein folding by smallmolecule diselenides, Biochemistry 47, 6985-6987.
12. 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.
13. Grauschopf, U., Winther, J. R., Korber, P., Zander, T., Dallinger, P., and Bardwell, J. C. A. (1995) Why is DsbA such an oxidizing disulfide catalyst? Cell 83, 947-955.
14. Jonda, S., Huber-Wunderlich, M., Glockshuber, R., and Mössner, E. (1999) 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 J. 18, 3271-3281.
15. 2-thioredoxin, Biochemistry 33, 3404-3412.
16. 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. U.S.A. 93, 13048-13053.
17. Berg, H. C. (2003) The rotary motor of bacterial flagella, Annu. Rev. Biochem. 72, 19-54.
18. Hizukuri, Y., Kojima, S., Yakushi, T., Kawagishi, I., and Homma, M. (2008) Systematic Cys mutagenesis of FlgI, the flagellar P-ring component of, Escherichia coli, Microbiology 154, 810-817.
19. Elliott, K. A. C. (1930) On the catalysis of the oxidation of cysteine and thioglycollic acid by iron and copper, Biochem. J. 24, 310-326.
20. Hiniker, A., Collet, J.-F., and Bardwell, J. C. A. (2005) Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC, J. Biol. Chem. 280, 33785-33791.
21. 2+ on the oxidative folding of synthetic maurotoxin in vitro, J. Biomol. Struct. Dyn. 26, 75-81.
22. Tsen, C. C., and Tappel, A. L. (1958) Catalytic oxidation of glutathione and other sulfhydryl compounds by selenite, J. Biol. Chem. 233, 1230-1232.
23. Lundström, J., Krause, G., and Holmgren, A. (1992) A Pro to His mutation in active site of thioredoxin increases its disulfide-isomerase activity 10-fold. New refolding systems for reduced or randomly oxidized ribonuclease, J. Biol. Chem. 267, 9047-9052.
24. Ito, K., and Inaba, K. (2008) The disulfide bond formation (Dsb) system, Curr. Opin. Struct. Biol. 18, 450-458.
25. Maskos, K., Huber-Wunderlich, M., and Glockshuber, R. (2003) DsbA and DsbC-catalyzed oxidative folding of proteins with complex disulfide bridge patterns in vitro and in vivo, J. Mol. Biol. 325, 495-513.
26. Bessette, P. H., Åslund, F., Beckwith, J., and Georgiou, G. (1999) Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm, Proc. Natl. Acad. Sci. U.S.A. 96, 13703-13708.
27. Rosa, R. M., Roesler, R., Braga, A. L., Saffi, J., and Henriques, J. A. P. (2007) Pharmacology and toxicology of diphenyl diselenide in several biological models, Braz. J. Med. Biol. Res. 40, 1287-1304.
28. Ganther, H. E. (1999) Selenium metabolism, selenoproteins and mechanisms of cancer prevention: Complexities with thioredoxin reductase, Carcinogenesis 20, 1657-1666.
29. 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: Influence of electrostatic interactions on stability and redox properties, J. Biol. Chem. 272, 21692-21699.
30. Bader, M. W., Hiniker, A., Regeimbal, J., Goldstone, D., Haebel, P. W., Riemer, J., Metcalf, P., and Bardwell, J. C. A. (2001) Turning a disulfide isomerase into an oxidase: DsbC mutants that imitate DsbA, EMBO J. 20, 1555-1562.
31. Thannhauser, T. W., Konishi, Y., and Scheraga, H. A. (1984) Sensitive quantitative analysis of disulfide bonds in polypeptides and proteins, Anal. Biochem. 138, 181-188.
32. Vidal-Aroca, F., Giannattasio, M., Brunelli, E., Vezzoli, A., Plevani, P., Muzi-Falconi, M., and Bertoni, G. (2006) One-step high-throughput assay for quantitative detection of β-galactosidase activity in intact Gram-negative bacteria, yeast and mammalian cells, BioTechniques 40, 433-440.
33. Brickman, E., and Beckwith, J. (1975) Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and φ80 transducing phages, J. Mol. Biol. 96, 307-316.
34. Reed, L. J., Gunsalus, I. C., Schnakenberg, G. H. F., Soper, Q. F., Boaz, H. E., Kern, S. F., and Parke, T. V. (1953) Isolation, characterization and structure of α-lipoic acid, J. Am. Chem. Soc. 75, 1267-1270.
35. Stary, F. E., Jindal, S. L., and Murray, R. W. (1975) Oxidation of -lipoic acid, J. Org. Chem. 40, 58-62.