Going through the Barrier: Coupled disulfide exchange reactions promote efficient catalysis in quiescin sulfhydryl oxidase

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 5274-5284

  Israel, Benjamin A ^a   Kodali, Vamsi K ^a   Thorpe, Colin ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COVALENT BONDS; ENZYMES;

DISULFIDE BONDS; DISULFIDE EXCHANGE; MECHANISTIC STUDIES; REACTION COORDINATES; REDOX CENTERS; SULFHYDRYL OXIDASE; THERMODYNAMIC BARRIERS;

SULFUR COMPOUNDS;

FLAVINE NUCLEOTIDE; QUIESCIN SULFHYDRYL OXIDASE; THIOL OXIDASE; THIOREDOXIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; CONTROLLED STUDY; CYTOPLASM; DISULFIDE BOND; ENZYME MECHANISM; HUMAN; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; SULFIDE OXIDIZER; THERMODYNAMICS; TRYPANOSOMA BRUCEI;

DISULFIDE; ENZYME MECHANISMS; OXIDASE; OXIDATION-REDUCTION; PROTEIN FOLDING; QSOX; QUIESCIN SULFHYDRYL OXIDASE; REDOX; SULFHYDRYL;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANAEROBIOSIS; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; DITHIOTHREITOL; FLAVIN-ADENINE DINUCLEOTIDE; KINETICS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SPECTROPHOTOMETRY; THERMODYNAMICS; THIOREDOXINS;

EID: 84894442245     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.536219     Document Type: Article

References (74)

1. 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
2. Rancy, P. C., and Thorpe, C. (2008) Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase. Biochemistry 47, 12047-12056
3. Codding, J. A., Israel, B. A., and Thorpe, C. (2012) Protein substrate discrimination in the quiescin sulfhydryl oxidase (QSOX) family. Biochemistry 51, 4226-4235
4. 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
5. Pagani, M., Fabbri, M., Benedetti, C., Fassio, A., Pilati, S., Bulleid, N. J., Cabibbo, A., and Sitia, R. (2000) Endoplasmic reticulum oxidoreductin 1-l (ERO1-L), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275, 23685-23692
6. Araki, K., and Inaba, K. (2012) Structure, mechanism, and evolution of Ero1 family enzymes. Antioxid. Redox Signal. 16, 790-799
7. Zito, E., Melo, E. P., Yang, Y., Wahlander, A., Neubert, T. A., and Ron, D. (2010) Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin. Mol. Cell 40, 787-797
8. Tavender, T. J., Springate, J. J., and Bulleid, N. J. (2010) Recycling of peroxiredoxin IV provides a novel pathway for disulphide formation in the endoplasmic reticulum. EMBO J. 29, 4185-4197
9. Sato, Y., Kojima, R., Okumura, M., Hagiwara, M., Masui, S., Maegawa, K., Saiki, M., Horibe, T., Suzuki, M., and Inaba, K. (2013) Synergistic cooperation of PDI family members in peroxiredoxin 4-driven oxidative protein folding. Sci. Rep. 3, 2456
10. Nguyen, V. D., Saaranen, M. J., Karala, A. R., Lappi, A. K., Wang, L., Raykhel, I. B., Alanen, H. I., Salo, K. E., Wang, C. C., and Ruddock, L. W. (2011) Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J. Mol. Biol. 406, 503-515
11. Schulman, S., Wang, B., Li, W., and Rapoport, T. A. (2010) Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin-like redox partners. Proc. Natl. Acad. Sci. U.S.A. 107, 15027-15032
12. 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
13. 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
14. Thorpe, C., Hoober, K. L., Raje, S., Glynn, N. M., Burnside, J., Turi, G. K., and Coppock, D. L. (2002) Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch. Biochem. Biophys. 405, 1-12
15. Coppock, D. L., and Thorpe, C. (2006) Multidomain flavin-dependent sulfhydryl oxidases. Antioxid. Redox Signal. 8, 300-311
16. Kodali, V. K., and Thorpe, C. (2010) Oxidative protein folding and the quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid. Redox Signal. 13, 1217-1230
17. Sevier, C. (2012) Erv2 and quiescin sulfhydryl oxidases: Erv-domain enzymes associated with the secretory pathway. Antioxid. Redox Signal. 16, 800-808
18. Hoober, K. L., Sheasley, S. L., 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
19. Limor-Waisberg, K., Ben-Dor, S., and Fass, D. (2013) Diversification of quiescin sulfhydryl oxidase in a preserved framework for redox relay. BMC Evol. Biol. 13, 70
20. Ouyang, X., DeWeese, T. L., Nelson, W. G., and Abate-Shen, C. (2005) Loss-of-function of Nkx3.1 promotes increased oxidative damage in prostate carcinogenesis. Cancer Res. 65, 6773-6779
21. Song, H., Zhang, B., Watson, M. A., Humphrey, P. A., Lim, H., and Milbrandt, J. (2009) Loss of Nkx3.1 leads to the activation of discrete downstream target genes during prostate tumorigenesis. Oncogene 28, 3307-3319
22. Katchman, B. A., Antwi, K., Hostetter, G., Demeure, M. J., Watanabe, A., Decker, G. A., Miller, L. J., Von Hoff, D. D., and Lake, D. F. (2011) Quiescin sulfhydryl oxidase 1 promotes invasion of pancreatic tumor cells mediated by matrix metalloproteinases. Mol. Cancer Res. 9, 1621-1631
23. Soloviev, M., Esteves, M. P., Amiri, F., Crompton, M. R., and Rider, C. C. (2013) Elevated transcription of the gene QSOX1 encoding quiescin Q6 sulfhydryl oxidase 1 in breast cancer. PLoS One 8, e57327
24. Katchman, B. A., Ocal, I. T., Cunliffe, H. E., Chang, Y.-H., Hostetter, G., Watanabe, A., Lobello, J., and Lake, D. F. (2013) Expression of quiescin sulfhydryl oxidase 1 is associated with a highly invasive phenotype and correlates with a poor prognosis in Luminal B breast cancer. Breast Cancer Res. 15, R28
25. Mebazaa, A., Vanpoucke, G., Thomas, G., Verleysen, K., Cohen-Solal, A., Vanderheyden, M., Bartunek, J., Mueller, C., Launay, J. M., Van Landuyt, N., D'Hondt, F., Verschuere, E., Vanhaute, C., Tuytten, R., Vanneste, L., De Cremer, K., Wuyts, J., Davies, H., Moerman, P., Logeart, D., Collet, C., Lortat-Jacob, B., Tavares, M., Laroy, W., Januzzi, J. L., Samuel, J. L., and Kas, K. (2012) Unbiased plasma proteomics for novel diagnostic biomarkers in cardiovascular disease: identification of quiescin Q6 as a candidate biomarker of acutely decompensated heart failure. Eur. Heart J. 33, 2317-2324
26. Antwi, K., Hostetter, G., Demeure, M. J., Katchman, B. A., Decker, G. A., Ruiz, Y., Sielaff, T. D., Koep, L. J., and Lake, D. F. (2009) Analysis of the plasma peptidome from pancreas cancer patients connects a peptide in plasma to overexpression of the parent protein in tumors. J. Proteome Res. 8, 4722-4731
27. Ilani, T., Alon, A., Grossman, I., Horowitz, B., Kartvelishvily, E., Cohen, S. R., and Fass, D. (2013)Asecreted disulfide catalyst controls extracellular matrix composition and function. Science 341, 74-76
28. Kodali, V. K., and Thorpe, C. (2010) Quiescin sulfhydryl oxidase from Trypanosoma brucei: catalytic activity and mechanism of a QSOX family member with a single thioredoxin domain. Biochemistry 49, 2075-2085
29. Alon, A., Grossman, I., Gat, Y., Kodali, V. K., DiMaio, F., Mehlman, T., Haran, G., Baker, D., Thorpe, C., and Fass, D. (2012) The dynamic disulphide relay of quiescin sulphydryl oxidase. Nature 488, 414-418
30. Hoober, K. L., and Thorpe, C. (1999) Egg white sulfhydryl oxidase: kinetic mechanism of the catalysis of disulfide bond formation. Biochemistry 38, 3211-3217
31. Raje, S., and Thorpe, C. (2003) Inter-domain redox communication in flavoenzymes of the quiescin/sulfhydryl oxidase family: role of a thioredoxin domain in disulfide bond formation. Biochemistry 42, 4560-4568
32. Heckler, E. J., Alon, A., Fass, D., and Thorpe, C. (2008) Human quiescinsulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry 47, 4955-4963
33. Gorelick, R. J., and Thorpe, C. (1986) Electron-transferring flavoprotein from pig kidney: flavin analogue studies. Biochemistry 25, 7092-7098
34. Williams, C. H., Jr., Arscott, L. D., Matthews, R. G., Thorpe, C., and Wilkinson, K. D. (1979) Methodology employed for anaerobic spectrophotometric titrations and for computer-assisted data analysis. Methods Enzymol. 62, 185-198
35. Williams, C. H., Jr. (1992) in Chemistry and Biochemistry of Flavoenzymes (Müller, F., ed) pp. 121-211, CRC Press, Boca Raton, FL
36. Lees, W. J., and Whitesides, G. M. (1993) Equilibrium constants for thioldisulfide interchange reactions-a coherent, corrected set. J. Org. Chem. 58, 642-647
37. Alon, A., Heckler, E. J., Thorpe, C., and Fass, D. (2010) QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett. 584, 1521-1525
38. 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 Signal. 10, 55-64
39. Jessop, C. E., and Bulleid, N. J. (2004) Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 279, 55341-55347
40. Hagiwara, T., Inaba, H., Yoshida, S., Nagaizumi, K., Arai, M., Hanabusa, H., and Fukutake, K. (1996) A novel mutation Gly16723Arg in type 2A and a homozygous mutation in type 2B von Willebrand disease. Thromb. Haemost. 76, 253-257
41. Huber-Wunderlich, M., and Glockshuber, R. (1998) A single dipeptide sequence modulates the redox properties of a whole enzyme family. Fold. Des. 3, 161-171
42. Zapun, A., Bardwell, J. C., 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
43. Chambers, J. E., Tavender, T. J., Oka, O. B., Warwood, S., Knight, D., and Bulleid, N. J. (2010) The reduction potential of the active site disulfides of human protein disulfide isomerase limits oxidation of the enzyme by Ero1. J. Biol. Chem. 285, 29200-29207
44. Hatahet, F., and Ruddock, L. W. (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 11, 2807-2850
45. Lundström, J., and Holmgren, A. (1993) Determination of the reductionoxidation potential of the thioredoxin-like domains of protein disulfideisomerase from the equilibrium with glutathione and thioredoxin. Biochemistry 32, 6649-6655
46. Farrell, S. R., and Thorpe, C. (2005) Augmenter of liver regeneration: a flavin dependent sulfhydryl oxidase with cytochrome C reductase activity. Biochemistry 44, 1532-1541
47. Wang, W., Winther, J. R., and Thorpe, C. (2007) Erv2p: characterization of the redox behavior of a yeast sulfhydryl oxidase. Biochemistry 46, 3246-3254
48. Walsh, C., Fisher, J., Spencer, R., Graham, D. W., Ashton, W. T., Brown, J. E., Brown, R. D., and Rogers, E. F. (1978) Chemical and enzymatic properties of riboflavin analogues. Biochemistry 17, 1942-1951
49. Stankovich, M. T., and Massey, V. (1976) Determination of the redox potential of deazariboflavin by equilibration with flavins. Biochim. Biophys. Acta 452, 335-344
50. Thorpe, C., and Williams, C. H., Jr. (1976) Differential reactivity of the two active site cysteine residues generated on reduction of pig heart lipoamide dehydrogenase. J. Biol. Chem. 251, 3553-3557
51. Daithankar, V. N., Farrell, S. R., and Thorpe, C. (2009) Augmenter of liver regeneration: substrate specificity of a flavin-dependent oxidoreductase from the mitochondrial intermembrane space. Biochemistry 48, 4828-4837
52. Brohawn, S. G., Miksa, I. R., and Thorpe, C. (2003) Avian sulfhydryl oxidase is not a metalloenzyme: adventitious binding of divalent metal ions to the enzyme. Biochemistry 42, 11074-11082
53. Hoober, K. L., Joneja, B., White, H. B., 3rd, and Thorpe, C. (1996) A sulfhydryl oxidase from chicken egg white. J. Biol. Chem. 271, 30510-30516
54. 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
55. Chivers, P. T., Prehoda, K. E., and Raines, R. T. (1997) The CXXC motif: a rheostat in the active site. Biochemistry 36, 4061-4066
56. 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
57. Quan, S., Schneider, I., Pan, J., Von Hacht, A., and Bardwell, J. C. (2007) The CXXC motif is more than a redox rheostat. J. Biol. Chem. 282, 28823-28833
58. Lewin, A., Crow, A., Hodson, C. T., Hederstedt, L., and Le Brun, N. E. (2008) Effects of substitutions in the CXXC active-site motif of the extracytoplasmic thioredoxin ResA. Biochem. J. 414, 81-91
59. Wunderlich, M., and Glockshuber, R. (1993) Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci. 2, 717-726
60. Aslund, 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
61. Inaba, K., and Ito, K. (2002) Paradoxical redox properties of DsbB and DsbA in the protein disulfide-introducing reaction cascade. EMBO J. 21, 2646-2654
62. Siedler, F., Rudolph-Böhner, S., Doi, M., Musiol, H. J., and Moroder, L. (1993) Redox potentials of active-site bis(cysteinyl) fragments of thiolprotein oxidoreductases. Biochemistry 32, 7488-7495
63. Gilbert, H. F. (1995) Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol. 251, 8-28
64. Rudolf, J., Pringle, M. A., and Bulleid, N. J. (2013) Proteolytic processing of QSOX1A ensures efficient secretion of a potent disulfide catalyst. Biochem. J. 454, 181-190
65. Kadokura, H., Katzen, F., and Beckwith, J. (2003) Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72, 111-135
66. Inaba, K., and Ito, K. (2008) Structure and mechanisms of the DsbB-DsbA disulfide bond generation machine. Biochim. Biophys. Acta 1783, 520-529
67. Nakamoto, H., and Bardwell, J. C. (2004) Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim. Biophys. Acta 1694, 111-119
68. Tapley, T. L., Eichner, T., Gleiter, S., Ballou, D. P., and Bardwell, J. C. (2007) Kinetic characterization of the disulfide bond-forming enzyme DsbB. J. Biol. Chem. 282, 10263-10271
69. Inaba, K., Takahashi, Y. H., Ito, K., and Hayashi, S. (2006) Critical role of a thiolate-quinone charge transfer complex and its adduct form in de novo disulfide bond generation by DsbB. Proc. Natl. Acad. Sci. U.S.A. 103, 287-292
70. Dmitrenko, O., and Thorpe, C. (2008) A computational analysis of the interaction between flavin and thiol(ate) groups. Implications for flavoenzyme catalysis. J. Sulfur Chem. 29, 415-421
71. Inaba, K., Murakami, S., Suzuki, M., Nakagawa, A., Yamashita, E., Okada, K., and Ito, K. (2006) Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 127, 789-801
72. Inaba, K., Murakami, S., Nakagawa, A., Iida, H., Kinjo, M., Ito, K., and Suzuki, M. (2009) Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. EMBO J. 28, 779-791
73. Wood, P. M. (1988) The potential diagram for oxygen at pH7. Biochem. J. 253, 287-289
74. Regeimbal, J., and Bardwell, J. C. (2002) DsbB catalyzes disulfide bond formation de novo. J. Biol. Chem. 277, 32706-32713