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Applied Microbiology and Biotechnology

, Volume 91, Issue 4, pp 957–966 | Cite as

Sulfhydryl oxidases: sources, properties, production and applications

  • Greta Faccio
  • Outi Nivala
  • Kristiina Kruus
  • Johanna Buchert
  • Markku Saloheimo
Mini-Review

Abstract

The formation of disulfide bonds in proteins and small molecules can greatly affect their functionality. Sulfhydryl oxidases (SOXs) are enzymes capable of oxidising the free sulfhydryl groups in proteins and thiol-containing small molecules by using molecular oxygen as an electron acceptor. SOXs have been isolated from the intracellular compartments of many organisms, but also secreted SOXs are known. These latter enzymes are generally active on small compounds and their physiological role is unknown, whereas the intracellular enzymes prefer proteins as substrates and are involved in protein folding. An increasing number of scientific publications and patent applications on SOXs have been published in recent years. The present mini-review provides an up-to-date summary of SOXs from various families, their production and their actual or suggested applications. The sequence features and domain organisation of the characterised SOXs are reviewed, and special attention is paid to the physicochemical features of the enzymes. A review of patents and patent applications regarding this class of enzymes is also provided.

Keywords

Application Disulfide bond Glutathione Sulfhydryl oxidase Sulphydryl oxidase Thiol oxidase 

Notes

Acknowledgements

The Finnish Cultural Foundation is acknowledged for funding the work of GF.

References

  1. Aehle W (2004) Enzymes in industry: production and applications. Wiley-VCH, GermanyGoogle Scholar
  2. Alon A, Heckler EJ, Thorpe C, Fass D (2010) QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett 584:1521–1525CrossRefGoogle Scholar
  3. Amiot C, Musard JF, Hadjiyiassemis M, Jouvenot M, Fellmann D, Risold PY, Adami P (2004) Expression of the secreted FAD-dependent sulfydryl oxidase (QSOX) in the guinea pig central nervous system. Brain Res Mol Brain Res 125:13–21CrossRefGoogle Scholar
  4. Andersen LP (1997) Method for dehairing of hides or skins by means of enzymes. European patent EP0799321A1Google Scholar
  5. Ang SK, Lu H (2009) Deciphering structural and functional roles of individual disulfide bonds of the mitochondrial sulfhydryl oxidase Erv1p. J Biol Chem 284:28754–28761CrossRefGoogle Scholar
  6. Aoyama N, Miike A, Shimizu Y, Tatano T (1985) Method for the determination of mercapto compounds and reagent for use therein. European patent EP0159870Google Scholar
  7. Banci L, Bertini I, Calderone V, Cefaro C, Ciofi-Baffoni S, Gallo A, Kallergi E, Lionaki E, Pozidis C, Tokatlidis K (2011) Molecular recognition and substrate mimicry drive the electron-transfer process between MIA40 and ALR. Proc Natl Acad Sci U S A 108:4811–4816CrossRefGoogle Scholar
  8. Bao K, Wang H (2009) Signal sequences and co-expressed chaperones for improving protein production in a host cell. United States Patent Application 20090221030A1Google Scholar
  9. Benham AM, Cabibbo A, Fassio A, Bulleid N, Sitia R, Braakman I (2000) The CXXCXXC motif determines the folding, structure and stability of human Ero1-L alpha. EMBO J 19:4493–4502CrossRefGoogle Scholar
  10. Brohawn SG, Miksa IR, Thorpe C (2003) Avian sulfhydryl oxidase is not a metalloenzyme: adventitious binding of divalent metal ions to the enzyme. Biochemistry 42:11074–11082CrossRefGoogle Scholar
  11. Chakravarthi S, Jessop CE, Willer M, Stirling CJ, Bulleid NJ (2007) Intracellular catalysis of disulfide bond formation by the human sulfhydryl oxidase, QSOX1. Biochem J 404:403–411CrossRefGoogle Scholar
  12. Chris KA, Frand AR (1999) Eukaryotic mixed disulfide bond forming proteins and related molecules and methods. International publication number WO990772Google Scholar
  13. Compagnone D, Federici G, Scarciglia L, Palleschi G (1993) Amperometric glutathione electrodes. Biosens Bioelectron 8:257–263CrossRefGoogle Scholar
  14. Coppock DL, Thorpe C (2006) Multidomain flavin-dependent sulfhydryl oxidases. Antioxid Redox Signal 8:300–311CrossRefGoogle Scholar
  15. Coppock DL, Cina-Poppe D, Gilleran S (1998) The quiescin Q6 gene (QSCN6) is a fusion of two ancient gene families: thioredoxin and ERV1. Genomics 54:460–468CrossRefGoogle Scholar
  16. Daithankar VN, Farrell SR, Thorpe C (2009) Augmenter of liver regeneration:substrate specificity of a flavin-dependent oxidoreductase from the mitochondrial intermembrane space. Biochemistry 48:4828–4837CrossRefGoogle Scholar
  17. Daithankar VN, Schaefer SA, Dong M, Bahnson BJ, Thorpe C (2010) Structure of the human sulfhydryl oxidase augmenter of liver regeneration and characterization of a human mutation causing an autosomal recessive myopathy. Biochemistry 49:6737–6745CrossRefGoogle Scholar
  18. de la Motte RS, Wagner FW (1987) Aspergillus niger sulfhydryl oxidase. Biochemistry 26:7363–7371CrossRefGoogle Scholar
  19. Degn PE, Kampp J, Chistiansen LS (2009) Improving enzymatic treatment of a proteinaceous substrate enzymatic by removal of free thiols. International publication number WO2009EP52558Google Scholar
  20. Elgawish A, Glomb M, Friedlander M, Monnier VM (1996) Involvement of hydrogen peroxide in collagen cross-linking by high glucose in vitro and in vivo. J Biol Chem 271:12964–12971CrossRefGoogle Scholar
  21. Erzhong W (2010a) Reagent (kit) for diagnosing/determining amino acid and method for determining concentration of amino acid. Patent application number CN101762486Google Scholar
  22. Erzhong W (2010b) Homocysteine diagnosis/determination reagent (kit) and homocysteine concentration determination method. Patent application number CN101762514Google Scholar
  23. Faccio G, Kruus K, Buchert J, Saloheimo M (2010) Secreted fungal sulfhydryl oxidases:sequence analysis and characterisation of a representative flavin-dependent enzyme from Aspergillus oryzae. BMC Biochemistry 11:31CrossRefGoogle Scholar
  24. Faccio G, Kruus K, Buchert J, Saloheimo M (2011) Production and characterisation of AoSOX2 from Aspergillus oryzae, a novel flavin-dependent sulfhydryl oxidase with good pH and temperature stability. Appl Microbiol Biotechnol 90:941–949CrossRefGoogle Scholar
  25. Farrell SR, Thorpe C (2005) Augmenter of liver regeneration: a flavin-dependent sulfhydryl oxidase with cytochrome c reductase activity. Biochemistry 44:1532–1541CrossRefGoogle Scholar
  26. Fass D (2008) The Erv family of sulfhydryl oxidases. Biochim Biophys Acta 1783:557–566CrossRefGoogle Scholar
  27. Feng X (2000) Enzymatic methods for dyeing with reduced vat and sulfur dyes. US patent US6,129,769Google Scholar
  28. Frand AR, Kaiser CA (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1:161–170CrossRefGoogle Scholar
  29. Frand AR, Kaiser CA (1999) Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell 4:469–477CrossRefGoogle Scholar
  30. Gerber J, Mühlenhoff U, Hofhaus G, Lill R, Lisowsky T (2001) Yeast ERV2p is the first microsomal FAD-linked sulfhydryl oxidase of the Erv1p/Alrp protein family. J Biol Chem 276:23486–23491CrossRefGoogle Scholar
  31. Gross E, Sevier CS, Vala A, Kaiser CA, Fass D (2002) A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p. Nat Struct Biol 9:61–67CrossRefGoogle Scholar
  32. Gross E, Kastner DB, Kaiser CA, Fass D (2004) Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117:601–610CrossRefGoogle Scholar
  33. Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, 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 103:299–304CrossRefGoogle Scholar
  34. Haarasilta S, Vaisanen S (1989) Method for improving flour dough. European patent EP0321811Google Scholar
  35. Haarasilta S, Purinen T, Beeisanen S, Karusuten IT (1989) Improvement of baking product in quality. European patent EP0338452Google Scholar
  36. Haarasilta S, Pillinene T, Vaisanen S, Tammersalo-Karsten I (1991) Enzyme product and method of improving the properties of dough and the quality of bread. US patent 07/341389Google Scholar
  37. Hakim M, Fass D (2009) Dimer interface migration in a viral sulfhydryl oxidase. J Mol Biol 391:758–768CrossRefGoogle Scholar
  38. Hakim M, Fass D (2010) Cytosolic disulfide bond formation in cells infected with large nucleocytoplasmic DNA viruses. Antioxid Redox Signal 13:1261–1271CrossRefGoogle Scholar
  39. Hammer FE, Scott D, Wagner FW, Lee R, de la Motte RS (1990) Microbial sulfhydryl oxidase and method. US patent US4,894,340Google Scholar
  40. Hatahet F, Nguyen VD, Salo KE, Ruddock LW (2010) Disruption of reducing pathways is not essential for efficient disulfide bond formation in the cytoplasm of E. coli. Microb Cell Fact 9:67Google Scholar
  41. Hätzelt A, Nordskog A, Leopold S, Schmiedel P, Von Rybinski W, Sundermeyer J, Döring J (2010a) Tris(heterocyclyl) metal complexes, washing and cleaning agents containing the same, and use as bleach catalysts. US patent application number US20100024133Google Scholar
  42. Hätzelt A, Nordskog A, Leopold S, Schmiedel P, Von Rybinski W, Sundermeyer J, Döring J (2010b) Biheteroaryl metal complexes as bleach catalysts. US patent application number 20100029540Google Scholar
  43. Heckler EJ, Alon A, Fass D, Thorpe C (2008) Human quiescin-sulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry 47:4955–4963CrossRefGoogle Scholar
  44. Heldman N, Vonshak O, Sevier CS, Vitu E, Mehlman T, Fass D (2010) Steps in reductive activation of the disulfide-generating enzyme Ero1p. Protein Sci 19:1863–1876CrossRefGoogle Scholar
  45. Hiniker A, Bardwell JC (2004) Disulfide relays between and within proteins: the Ero1p structure. Trends Biochem Sci 29:516–519CrossRefGoogle Scholar
  46. Hoober KL, Joneja B, White HB 3rd, Thorpe C (1996) A sulfhydryl oxidase from chicken egg white. J Biol Chem 271:30510–30516CrossRefGoogle Scholar
  47. Hoober KL, Glynn NM, Burnside J, Coppock DL, Thorpe C (1999a) Homology between egg white sulfhydryl oxidase and quiescin Q6 defines a new class of flavin-linked sulfhydryl oxidases. J Biol Chem 274:31759–31762CrossRefGoogle Scholar
  48. Hoober KL, Sheasley SL, Gilbert HF, Thorpe C (1999b) Sulfhydryl oxidase from egg white. A facile catalyst for disulfide bond formation in proteins and peptides. J Biol Chem 274:22147–22150CrossRefGoogle Scholar
  49. Hulko M, Hospach I, Nelles G, Ulmer J (2010) Sensor for thiol analytes. US patent application number 20100231899Google Scholar
  50. Inaba K, Masui S, Iida H, Vavassori S, Sitia R, Suzuki M (2010) Crystal structures of human Ero1alpha reveal the mechanisms of regulated and targeted oxidation of PDI. EMBO J 29:3330–3343CrossRefGoogle Scholar
  51. Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184CrossRefGoogle Scholar
  52. Jaje J, Wolcott HN, Fadugba O, Cripps D, Yang AJ, Mather IH, Thorpe C (2007) A flavin-dependent sulfhydryl oxidase in bovine milk. Biochemistry 46:13031–13040CrossRefGoogle Scholar
  53. Janolino VG, Swaisgood HE (1992) A comparison of sulfhydryl oxidase from bovine milk and from Aspergillus niger. Milchwissenschaft 47:143–146Google Scholar
  54. Jordan PA, Gibbins JM (2006) Extracellular disulfide exchange and the regulation of cellular function. Antioxid Redox Signal 8:312–324CrossRefGoogle Scholar
  55. Kim MD, Lee TH, OH YJ, Seo JH (2007a) Recombinant Saccharomyces cerevisiae containing protein disulfideisomerase1 coding gene and ero1 coding gene with a capacity of hirudin production, and method for production of hirudin from it. Korean patent application number KR20070041166Google Scholar
  56. Kim M, Park E, Cho J, Kim J, Cho S, Han M, Seo J (2007b) Enhanced production of antithrombotic hirudin by coexpression of Pdi1 and Ero1 in recombinant Saccharomyces cerevisiae. J Biotechnol 131:S147CrossRefGoogle Scholar
  57. Kise S, Ikuta Y, Ueno Y (1992) Second cold waving agent and method for cold waving treatment using the same. Japanase patent application number JP-Kokai 04005220Google Scholar
  58. Kodali VK, Thorpe C (2010a) Oxidative protein folding and the quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal 13:1217–1230CrossRefGoogle Scholar
  59. Kodali VK, Thorpe C (2010b) Quiescin sulfhydryl oxidase from Trypanosoma brucei: catalytic activity and mechanism of a QSOX family member with a single thioredoxin domain. Biochemistry 49:2075–2085CrossRefGoogle Scholar
  60. Koppelman SJ, van den Hout RHJ, Sleijster-Selis HE, Luijkx DMAM (2010) Modification of allergens. European patent application number EP2140880A1Google Scholar
  61. Kusakabe H, Kuninaka A, Yoshino H (1982) Purification and properties of a new enzyme, glutathione oxidase from Penicillium sp. K-6-5. Agric Biol Chem 46:2057–2067CrossRefGoogle Scholar
  62. Lange H (2001) An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2:715–720CrossRefGoogle Scholar
  63. Lee J, Hofhaus G, Lisowsky T (2000) Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett 477:62–66CrossRefGoogle Scholar
  64. Levitan A, Danon A, Lisowsky T (2004) Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279:200002–200008CrossRefGoogle Scholar
  65. Lisowsky T, Lee JE, Polimeno L, Francavilla A, Hofhaus G (2001) Mammalian augmenter of liver regeneration protein is a sulfhydryl oxidase. Dig Liver Dis 33:173–180CrossRefGoogle Scholar
  66. Mairet-Coello G, Tury A, Esnard-Feve A, Fellmann D, Risold PY, Griffond B (2004) FAD-linked sulfhydryl oxidase QSOX: topographic, cellular, and subcellular immunolocalization in adult rat central nervous system. J Comp Neurol 473:334–363CrossRefGoogle Scholar
  67. Mairet-Coello G, Tury A, Fellmann D, Risold PY, Griffond B (2005) Ontogenesis of the sulfhydryl oxidase QSOX expression in rat brain. J Comp Neurol 484:403–417CrossRefGoogle Scholar
  68. Mandels GR (1956) Properties and surface location of a sulfhydryl oxidizing enzyme in fungus spores. J Bacteriol 72:230–234Google Scholar
  69. Matsui S, Uchida HT, Taniguchi T (1985) Use of novel glutathione oxidase. Japanese patent JP60221100Google Scholar
  70. Matsui S, Uchida S, Taniguchi T (1986) Novel glutathione oxidase, its production and use. US patent 4,610,963Google Scholar
  71. Musard JF, Sallot M, Dulieu P, Fraîchard A, Ordener C, Remy-Martin JP, Jouvenot M, Adami P (2001) Identification and expression of a new sulfhydryl oxidase SOx-3 during the cell cycle and the estrus cycle in uterine cells. Biochem Biophys Res Commun 287:83–91CrossRefGoogle Scholar
  72. Neufeld HA, Green LF, Latterell FM, Weintraub RL (1958) Thioxidase, a new sulfhydryl-oxidizing enzyme from Piricularia oryzae and Polyporus versicolor. J Biol Chem 232:1093–1099Google Scholar
  73. Nguyen VD, Hatahet F, Salo KE, Enlund E, Zhang C, Ruddock LW (2011) Pre-expression of a sulfhydryl oxidase significantly increases the yields of eukaryotic disulfide bond containing proteins expressed in the cytoplasm of E. coli. Microb Cell Fact 10:1CrossRefGoogle Scholar
  74. Nicolas J, Potus J (1999) Interactions between lipoxygenase and other oxidoreductases in baking. 2nd European Symposium on Enzymes in Grain Processing 207, pp 103–120Google Scholar
  75. O’Connell T, Maurer K, Weber T, Prüser I (2010) Compositions comprising perhydrolases and alkylene glycol diacetates. European patent application number EP2171048Google Scholar
  76. Ogino H, Uchiho T, Yokoo J, Kobayashi R, Ichise R, Ishikawa H (2001) Role of intermolecular disulfide bonds of the organic solvent-stable PST-01 protease in its organic solvent stability. Appl Environ Microbiol 67:942–947CrossRefGoogle Scholar
  77. Olsen HS (2002) Method for the separation of flour. US patent 6,451,553Google Scholar
  78. Ostrowski MC, Kistler WS (1980) Properties of a flavoprotein sulfhydryl oxidase from rat seminal vesicle secretion. Biochemistry 19:2639–2645CrossRefGoogle Scholar
  79. Ostrowski MC, Kistler WS, Williams-Ashman HG (1979) A flavoprotein responsible for the intense sulfhydryl oxidase activity of rat seminal vesicle secretion. Biochem Biophys Res Commun 87:171–176CrossRefGoogle Scholar
  80. Pocsi I, Prade RA, Penninckx MJ (2004) Glutathione, altruistic metabolite in fungi. Adv Microb Physiol 49:1–76CrossRefGoogle Scholar
  81. Popper L (2009) Method for manufacturing a laminated dough comprising sulfhydryl oxidase enzyme. European patent EP2103220Google Scholar
  82. Quan S, Schneider I, Pan J, Von Hacht A, Bardwell JC (2007) The CXXC motif is more than a redox rheostat. J Biol Chem 282:28823–28833CrossRefGoogle Scholar
  83. Raje S, 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 42:4560–4568CrossRefGoogle Scholar
  84. Rancy PC, Thorpe C (2008) Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase. Biochemistry 47:12047–12056CrossRefGoogle Scholar
  85. Ribotta PD, Leon AE, Anon MC (2003) Effects of yeast freezing in frozen dough. Cereal Chem 80:454–458CrossRefGoogle Scholar
  86. Riemer J, Bulleid N, Herrmann JM (2009) Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324:1284–1287CrossRefGoogle Scholar
  87. Rodriguez I, Redrejo-Rodriguez M, Rodriguez JM, Alejo A, Salas J, Salas ML (2006) African swine fever virus pB119L protein is a flavin adenine dinucleotide-linked sulfhydryl oxidase. J Virol 80:3157–3166CrossRefGoogle Scholar
  88. Rony HR, Schieff GJ, Cohen DM, Rennagel WR (1958) Sulfhydryl oxidase activity in skin homogenates. J Invest Dermatol 30:43–50Google Scholar
  89. Ruddock L (2010) Method for producing natively folded proteins in a prokaryotic host. WIPO patent application WO/2010/139858Google Scholar
  90. Schmid N, Bolliger C, Smith LJ, van Gunsteren WF (2008) Disulfide bond shuffling in bovine alpha-lactalbumin: MD simulation confirms experiment. Biochemistry 47:12104–12107CrossRefGoogle Scholar
  91. Senkevich TG, Weisberg AS, Moss B (2000) Vaccinia virus E10R protein is associated with the membranes of intracellular mature virions and has a role in morphogenesis. Virology 278:244–252CrossRefGoogle Scholar
  92. Sevier CS, Kaiser CA (2002) Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol 3:836–847CrossRefGoogle Scholar
  93. Sevier CS, Cuozzo JW, Vala A, Aslund F, Kaiser CA (2001) A flavoprotein oxidase defines a new endoplasmic reticulum pathway for biosynthetic disulphide bond formation. Nat Cell Biol 3:874–882CrossRefGoogle Scholar
  94. Sevier CS, Qu H, Heldman N, Gross E, Fass D, Kaiser CA (2007) Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129:333–344CrossRefGoogle Scholar
  95. Shewry P (1997) Disulphide bonds in wheat gluten proteins. J Cereal Sci 25:207–227CrossRefGoogle Scholar
  96. Shewry PR, Halford NG, Belton PS, Tatham AS (2002) The structure and properties of gluten: an elastic protein from wheat grain. Philos Trans R Soc Lond B Biol Sci 357:133–142CrossRefGoogle Scholar
  97. Silaneskenny FJ, Degenhardt A (2010) Increased stability of flavor compounds. US patent application number 20100015276Google Scholar
  98. Souppe J (1997) A novel enzyme combination. European patent EP0705538A1Google Scholar
  99. Starnes RL, Katkocin DM, Miller CA, Strobel Jr. RJ (1986) Microbial sulfhydryl oxidase. US patent 06/738764Google Scholar
  100. Swaisgood HE (1977) Process of removing the cooked flavour from milk. US patent US 4,053,644Google Scholar
  101. Swaisgood HE (1980) Sulphydryl oxidase: properties and applications. Enzyme Microb Technol 2:265–272CrossRefGoogle Scholar
  102. Swaisgood HE, Janolino VG, Skudder PJ (1987) Continuous treatment of ultrahigh-temperature sterilized milk using immobilized sulfhydryl oxidase. In: Mosbach K (ed) Methods in enzymology, vol 136. Academic Press Inc., New York, pp 423–431Google Scholar
  103. Tanaka N, Sato K (1999) Dough modifier for baked product and production of baked product by using same. Japanese patent JP11056219Google Scholar
  104. Tavender TJ, Bulleid NJ (2010) Molecular mechanisms regulating oxidative activity of the Ero1 family in the endoplasmic reticulum. Antioxid Redox Signal 13:1177–1187CrossRefGoogle Scholar
  105. Thorpe C, Jaje J (2009) Isolation of quiescin-sulfhydryl oxidase from milk. US patent application number 20090042269Google Scholar
  106. Thorpe C, Hoober KL, Raje S, Glynn NM, Burnside J, Turi GK, Coppock DL (2002) Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch Biochem Biophys 405:1–12CrossRefGoogle Scholar
  107. Timur S, Odaci D, Dincer A, Zihnioglu F, Telefoncu A (2008) Biosensing approach for glutathione detection using glutathione reductase and sulfhydryl oxidase bienzymatic system. Talanta 74:1492–1497CrossRefGoogle Scholar
  108. Vaisanen S, Haarasilta S, Scott D (1996) Compositions and method for improving flour dough. US patent 5,547,690Google Scholar
  109. Veggiani G, de Marco A (2011) Improved quantitative and qualitative production of single-domain intrabodies mediated by the co-expression of Erv1p sulfhydryl oxidase. Protein Expr Purif (in press)Google Scholar
  110. Vignaud C, Kaid N, Rakotozafy L, Davidou S, Nicolas J (2002) Partial purification and characterization of sulfhydryl oxidase from Aspergillus niger. J Food Sci 67:2016–2022CrossRefGoogle Scholar
  111. Vitu E, Bentzur M, Lisowsky T, Kaiser CA, Fass D (2006) Gain of function in an ERV/ALR sulfhydryl oxidase by molecular engineering of the shuttle disulfide. J Mol Biol 362:89–101CrossRefGoogle Scholar
  112. Vitu E, Kim S, Sevier CS, Lutzky O, Heldman N, Bentzur M, Unger T, Yona M, Kaiser CA, Fass D (2010) Oxidative activity of yeast Ero1p on protein disulfide isomerase and related oxidoreductases of the endoplasmic reticulum. J Biol Chem 285:18155–18165CrossRefGoogle Scholar
  113. Wang W, Winther JR, Thorpe C (2007) Erv2p: characterization of the redox behavior of a yeast sulfhydryl oxidase. Biochemistry 46:3246–3254CrossRefGoogle Scholar
  114. Wang C, Wesener SR, Zhang H, Cheng YQ (2009) An FAD-dependent pyridine nucleotide-disulfide oxidoreductase is involved in disulfide bond formation in FK228 anticancer depsipeptide. Chem Biol 16:585–593CrossRefGoogle Scholar
  115. Wu CK, Dailey TA, Dailey HA, Wang BC, Rose JP (2003) The crystal structure of augmenter of liver regeneration: a mammalian FAD-dependent sulfhydryl oxidase. Protein Sci 12:1109–1118CrossRefGoogle Scholar
  116. Yamada H, Suga Y, Takamori K (1989) Reaction mechanism catalyzed by skin sulfhydryl oxidase. Nippon Hifuka Gakkai Zasshi 99:499–502Google Scholar
  117. Zanata SM, Luvizon AC, Batista DF, Ikegami CM, Pedrosa FO, Souza EM, Chaves DF, Caron LF, Pelizzari JV, Laurindo FR, Nakao LS (2005) High levels of active quiescin Q6 sulfhydryl oxidase (QSOX) are selectively present in fetal serum. Redox Rep 10:319–323CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Greta Faccio
    • 1
  • Outi Nivala
    • 1
  • Kristiina Kruus
    • 1
  • Johanna Buchert
    • 1
  • Markku Saloheimo
    • 1
  1. 1.VTT Technical Research Centre of FinlandEspooFinland

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