Oxidative protein folding in vitro: A study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase

Biochemistry

Volumn 47, Issue 46, 2008, Pages 12047-12056

  Rancy, Pumtiwitt C ^a   Thorpe, Colin ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCENTRATION (PROCESS); ENZYMES; EXPERIMENTS; FOOD ADDITIVES; HYDROGEN; HYDROGEN PEROXIDE; ISOMERS; MOLECULAR OXYGEN; OXYGEN; PROTEINS; QUENCHING;

CURRENT MODELS; DISULFIDE BONDS; DISULFIDE BRIDGES; DISULFIDE ISOMERASE; ENDOPLASMIC RETICULUM; GLUTATHIONE; HIGH CONCENTRATIONS; IN VITRO; IN VITRO EXPERIMENTS; ISOMERASE; MICROMOLAR CONCENTRATIONS; NANOMOLAR LEVELS; OXIDATIVE FOLDING; OXIDATIVE PROTEINS; QUENCHING OF THE FLUORESCENCES; REDOX BUFFERS; REFOLDING; RIBOFLAVIN BINDING PROTEINS; RIBONUCLEASE A; SULFHYDRYL;

PROTEIN FOLDING;

PROTEIN DISULFIDE ISOMERASE; RIBOFLAVIN BINDING PROTEIN; RIBONUCLEASE A; THIOL OXIDASE;

ARTICLE; DISULFIDE BOND; ENDOPLASMIC RETICULUM; HUMAN; IN VITRO STUDY; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FOLDING;

ANIMALS; CATTLE; CHICKENS; DISULFIDES; HUMANS; HYDROGEN PEROXIDE; OXIDATION-REDUCTION; OXYGEN; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; THIOREDOXINS;

AVES;

EID: 56249094492     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801604x     Document Type: Article

References (73)

1. 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 endoplamic reticulum. Mol. Cell 1, 171-182.
2. 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.
3. Hoober, K. L., Glynn, N. M., Burnside, J., Coppock, D. L., and Thorpe, C. (1999) Homology between egg white sulfhydryl oxidase and quiescin Q6 defines a new class of flavin-linked sulfhydryl oxidases. J. Biol. Chem. 274, 31759-31762.
4. Benayoun, B., Esnard-Fève, A., Castella, S., Courty, Y., and Esnard, F. (2001) Rat seminal vesicle FAD-dependent sulfhydryl oxidase: Biochemical characterization and molecular cloning of a member of the new sulfhydryl oxidase/quiescin Q6 gene family. J. Biol. Chem. 276, 13830-13837.
5. Dias-Gunasekara, S., Gubbens, J., van Lith, M., Dunne, C., Williams, J. A., Kataky, R., Scoones, D., Lapthorn, A., Bulleid, N. J., and Benham, A. M. (2005) Tissue-specific expression and dimerization of the endoplasmic reticulum oxidoreductase Ero1β. J. Biol. Chem. 280, 33066-33075.
6. Cabibbo, A., Pagani, M., Fabbri, M., Rocchi, M., Farmery, M. R., Bulleid, N. J., and Sitia, R. (2000) ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J. Biol. Chem. 275, 4827-4833.
7. Pagani, M., Fabbri, M., Benedetti, C., Fassio, A., Pilati, S., Bulleid, N. J., Cabibbo, A., and Sitia, R. (2000) Endoplasmic reticulum oxidoreductin 1-1β (ERO1-Lβ), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275, 23685-23692.
8. Papp, E., Nardai, G., Mandl, J., Banhegyi, G., and Csermely, P. (2005) FAD oxidizes the ERO1-PDI electron transfer chain: The role of membrane integrity. Biochem. Biophys. Res. Commun. 338, 938-945.
9. Hoober, K. L., Sheasley, S. S., Gilbert, H. F., and Thorpe, C. (1999) Sulfhydryl oxidase from egg white: A facile catalyst for disulfide bond formation in proteins and peptides. J. Biol. Chem. 274, 22147-22150.
10. Chakravarthi, S., Jessop, C. E., Wilier, M., Stirling, C. J., and Bulleid, N. J. (2007) Intracellular catalysis of disulphide bond formation by the human sulphydryl oxidase, QSOX1. Biochem. J. 404, 403-411.
11. Thorpe, C., and Coppock, D. L. (2007) Generating disulfides in multicellular organisms: Emerging roles for a new flavoprotein family. J. Biol. Chem. 282, 13929-13933.
12. Heckler, E. J., Rancy, P. C., Kodali, V. K., and Thorpe, C. (2008) Generating disulfides with the Quiescin-sulfhydryl oxidases. Biochim. Biophys. Acta 1783, 567-577.
13. Frand, A. R., and Kaiser, C. A. (1999) Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell 4, 469-477.
14. Kulp, M. S., Frickel, E. M., Ellgaard, L., and Weissman, J. S. (2006) Domain architecture of protein disulfide isomerase facilitates its dual role as an oxidase and an isomerase in ERO1P-mediated disulfide formation. J. Biol. Chem. 281, 876-884.
15. Benham, A. M., Cabibbo, A., Fassio, A., Bulleid, N., Sitia, R., and Braakman, I. (2000) The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lα. EMBO J. 19, 4493-4502.
16. Mezghrani, A., Fassio, A., Benham, A., Simmen, T., Braakman, I., and Sitia, R. (2001) Manipulation of oxidative protein folding and PDI redox state in mammalian cells. EMBO J. 20, 6288-6296.
17. Frand, A. R., and Kaiser, C. A. (2000) Two pairs of conserved cysteines are required for the oxidative activity of Ero1p in protein disulfide bond formation in the endoplasmic reticulum. Mol. Biol. Cell 11, 2833-2843.
18. Tu, B. P., Ho-Schleyer, S. C., Travers, K. J., and Weissman, J. S. (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290, 1571-1574.
19. Gross, E., Sevier, C. S., Heldman, N., Vitu, E., Bentzur, M., Kaiser, C. A., Thorpe, C., and Fass, D. (2006) Generating disulfides enzymatically: Reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc. Natl. Acad. Sci. U.S.A. 103, 299-304,
20. Schwaller, M., Wilkinson, B., and Gilbert, H. F. (2003) Reduction-reoxidation cycles contribute to catalysis of disulfide isomerization by protein-disulfide isomerase. J. Biol. Chem. 278, 7154-7159.
21. Gilbert, H. F. (1997) Protein disulfide isomerase and assisted protein folding. J. Biol. Chem. 272, 29399-29402.
22. Laboissiere, M. C., Sturley, S. L., and Raines, R. T. (1995) The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. J. Biol. Chem. 270, 28006-28009.
23. Darby, N. J., and Creighton, T. E. (1995) Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry 34, 11725-11735.
24. Darby, N. J., Freedman, R. B., and Creighton, T. E. (1994) Dissecting the mechanism of protein disulfide isomerase: Catalysis of disulfide bond formation in a model peptide. Biochemistry 33, 7937-7947.
25. Freedman, R. B., Klappa, P., and Ruddock, L. W. (2002) Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. EMBO Rep. 3, 136-140.
26. Coppock, D. L., and Thorpe, C. (2006) Multidomain flavin-dependent sulfhydryl oxidases. Antioxid. Redox Signaling 8, 300-311.
27. Thorpe, C., Hoober, K., Raje, S., Glynn, N., Burnside, J., Turi, G., and Coppock, D. (2002) Sulfhydryl oxidases: Emerging catalysts of protein disulfide bond formation in eukaryotes. Arch. Biochem. Biophys. 405, 1-12.
28. Hoober, K. L., and Thorpe, C. (1999) Egg white sulfhydryl oxidase: Kinetic mechanism of the catalysis of disulfide bond formation. Biochemistry 38, 3211-3217.
29. Jaje, J., Wolcott, H. N., Fadugba, O., Cripps, D., Yang, A. J., Mather, I. H., and Thorpe, C. (2007) A flavin-dependent sulfhydryl oxidase in bovine milk. Biochemistry 46, 13031-13040.
30. Heckler, E. J., Alon, A., Fass, D., and Thorpe, C. (2008) Human quiescin-sulfhydryl oxidase, QSOX1: Probing internal redox steps by mutagenesis. Biochemistry 47, 4955-4963.
31. Raje, S., and Thorpe, C. (2003) Inter-domain redox communication in fiavoenzymes of the quiescin/sulfhydryl oxidase family: Role of a thioredoxin domain in disulfide bond formation. Biochemistry 42, 4560-4568.
32. Hoober, K. L., Joneja, B., White, H. B., III, and Thorpe, C. (1996) A Sulfhydryl Oxidase from Chicken Egg White. J. Biol. Chem. 271, 30510-30516.
33. Ahmed, A. K., Schaffer, S. W., and Wetlaufer, D. B. (1975) Nonenzymic reactivation of reduced bovine pancreatic ribonuclease by air oxidation and by glutathione oxidoreduction buffers. J. Biol. Chem. 250, 8477-8482.
34. Narayan, M., Welker, E., Wedemeyer, W. J., and Scheraga, H. A. (2000) Oxidative folding of proteins. Acc. Chem. Res. 33, 805-812.
35. Raines, R. T. (1998) Ribonuclease A. Chem. Rev. 98, 1045-1065.
36. Wilkinson, B., and Gilbert, H. F. (2004) Protein disulfide isomerase. Biochim. Biophys. Acta 1699, 35-44.
37. Pattanaik, P. M., Sooryanarayana, Adiga, P. R., and Visweswariah, S. S. (1998) Refolding of native and recombinant chicken riboflavin carrier (or binding) protein: Evidence for the formation of non-native intermediates during the generation of active protein. Eur. J. Biochem. 258, 411-418.
38. McClelland, D. A., McLaughlin, S. H., Freedman, R. B., and Price, N. C. (1995) The refolding of hen egg white riboflavin-binding protein: Effect of protein disulphide isomerase on the reoxidation of the reduced protein. Biochem. J. 311 (Part 1), 133-137.
39. Becvar, J., and Palmer, G. (1982) The binding of flavin derivatives to the riboflavin-binding protein of egg white. A kinetic and thermodynamic study. J. Biol. Chem. 257, 5607-5617.
40. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31, 3784-3788.
41. Lundstrom, J., and Holmgren, A. (1990) Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. J. Biol. Chem. 265, 9114-9120.
42. Smith, A. M., Chan, J., Oksenberg, D., Urfer, R., Wexler, D. S., Ow, A., Gao, L., McAloram, A., and Huang, S. G. (2004) A high-throughput turbidometric assay for screening inhibitors of protein disulfide isomerase activity. J. Biomol. Screening 9, 614-620.
43. Crook, E. M., Mathias, A. P., and Rabin, B. R. (1960) Spectrophotometric assay of bovine pancreatic ribonuclease by the use of cytidine 2′:3′-phosphate. Biochem. J. 74, 234-238.
44. Eyer, P., Worek, F., Kiderlen, D., Sinko, G., Stuglin, A., Simeon-Rudolf, V., and Reiner, E. (2003) Molar absorption coefficients for the reduced Ellman reagent: Reassessment. Anal. Biochem. 312, 224-227.
45. Walker, K. W., Lyles, M. M., and Gilbert, H. F. (1996) Catalysis of oxidative protein folding by mutants of protein disulfide isomerase with a single active-site cysteine. Biochemistry 35, 1972-1980.
46. Schaffer, S. W., Ahmed, A. K., and Wetlaufer, D. B. (1975) Salt effects in the glutathione-facilitated reactivation of reduced bovine pancreatic ribonuclease. J. Biol. Chem. 250, 8483-8486.
47. Miller, M. S., and White, H. B., III (1986) Isolation of avian riboflavin-binding protein. Methods Enzymol. 122, 227-234.
48. Hamazume, Y., Mega, T., and Ikenaka, T. (1987) Positions of disulfide bonds in riboflavin-binding protein of hen egg white. J. Biochem. 101, 217-223.
49. Monaco, H. L. (1997) Crystal structure of chicken riboflavin-binding protein. EMBO J. 16, 1475-1483.
50. 31P NMR studies. Biochemistry 23, 569-576.
51. Mega, T., and Ikenaka, T. (1982) Methanolysis products of asparagine-linked N-acetylglucosamine and a new method for determination of N- and O-glycosidic N-acetylglucosamine in glycoproteins that contain asparagine-linked carbohydrates. Anal. Biochem. 119, 17-24.
52. Hoober, K. L., and Thorpe, C. (2002) Flavin-dependent sulfhydryl oxidases in protein disulfide bond formation. Methods Enzymol. 348, 30-34.
53. Rhodes, M. B., Bennett, N., and Feeney, R. E. (1959) The flavoprotein-apoprotein system of egg white. J. Biol. Chem. 234, 2054-2060.
54. Darby, N. J., and Creighton, T. E. (1995) Characterization of the active site cysteine residues of the thioredoxin-like domains of protein disulfide isomerase. Biochemistry 34, 16770-16780.
55. Mendes, P. (1997) Biochemistry by numbers: Simulation of biochemical pathways with Gepasi 3. Trends Biochem. Sci. 22, 361-363.
56. Tu, B. P., and Weissman, J. S. (2004) Oxidative protein folding in eukaryotes: Mechanisms and consequences. J. Cell Biol. 164, 341-346.
57. Parkkonen, T., Kivirikko, K. I., and Pihlajaniemi, T. (1988) Molecular cloning of a multifunctional chicken protein acting as the prolyl 4-hydroxylase β-subunit, protein disulphide-isomerase and a cellular thyroid-hormone- binding protein. Comparison of cDNA-deduced amino acid sequences with those in other species. Biochem. J. 256, 1005-1011.
58. Lundstrom, 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.
59. Ellgaard, L., and Ruddock, L. W. (2005) The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Rep. 6, 28-32.
60. Cheng, Z., Arscott, L. D., Ballou, D. P., and Williams, C. H., Jr. (2007) The relationship of the redox potentials of thioredoxin and thioredoxin reductase from Drosophila melanogaster to the enzymatic mechanism: Reduced thioredoxin is the reductant of glutathione in Drosophila. Biochemistry 46, 875-7885.
61. Katzen, F., and Beckwith, J. (2000) Transmembrane electron transfer by the membrane protein DsbD occurs via a disulfide bond cascade. Cell 103, 769-779.
62. Ritz, D., and Beckwith, J. (2001) Roles of thiol-redox pathways in bacteria. Annu. Rev. Microbiol. 55, 21-48.
63. Fernandes, P. A., and Ramos, M. J. (2004) Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry 10, 257-266.
64. Houk, J., and Whitesides, G. M. (1987) Structure Reactivity Relations for Thiol Disulfide Interchange. J. Am. Chem. Soc. 109, 6825-6836.
65. Bach, R. D., Dmitrenko, O., and Thorpe, C. (2008) The Mechanism of Thiolate-disulfide Interchange Reactions in Biochemistry. J. Org. Chem. 73, 12-21.
66. Lyles, M. M., and Gilbert, H. F. (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: Dependence of the rate on the composition of the redox buffer. Biochemistry 30, 613-619.
67. Lyles, M. M., and Gilbert, H. F. (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: Presteady-state kinetics and the utilization of the oxidizing equivalents of the isomerase. Biochemistry 30, 619-625.
68. White, H. B., III, and Merrill, A. H., Jr. (1988) Riboflavin-binding proteins. Annu. Rev. Nutr. 8, 279-299.
69. Freedman, R. B. (1992) in Protein Folding in the Cell in Protein Folding (Creighton, T. E., Ed.) pp 455-539, W. H. Freeman, New York.
70. Graber, C. W., Cemazar, M., Heras, B., Martin, J. L., and Craik, D. J. (2006) Protein disulfide isomerase: The structure of oxidative folding. Trends Biochem. Sci. 31, 455-464.
71. Appenzeller-Herzog, C., and Ellgaard, L. (2008) In vivo reduction-oxidation state of protein disulfide isomerase: The two active sites independently occur in the reduced and oxidized forms. Antioxid. Redox Signaling 10, 55-64.
72. Dixon, B. M., Heath, S. H., Kim, R., Suh, J. H., and Hagen, T. M. (2008) Assessment of Endoplasmic Reticulum Glutathione Redox Status Is Confounded by Extensive Ex Vivo Oxidation. Antioxid. Redox Signaling 10, 963-972.
73. Hwang, C., Sinskey, A. J., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502.