The thioredoxin superfamily in oxidative protein folding

Antioxidants and Redox Signaling

Volumn 21, Issue 3, 2014, Pages 457-470

  Lu, Jun ^a   Holmgren, Arne ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN DISULFIDE ISOMERASE; THIOREDOXIN; VITAMIN K EPOXIDE REDUCTASE; THIOL DERIVATIVE;

AGING; ALZHEIMER DISEASE; ATOMIC FORCE MICROSCOPY; BACTERIAL INFECTION; CYTOPLASM; DISULFIDE BOND; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM STRESS; HUMAN; INTRACELLULAR SPACE; MAMMAL CELL; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; REVIEW; SACCHAROMYCES CEREVISIAE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY;

AGING; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; HUMANS; NEURODEGENERATIVE DISEASES; OXIDATION-REDUCTION; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; SULFHYDRYL COMPOUNDS; THIOREDOXINS;

EID: 84903784187     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5849     Document Type: Review

References (139)

1. Akhtar MW, Sunico CR, Nakamura T, and Lipton SA. Redox regulation of protein function via cysteine snitrosylation and its relevance to neurodegenerative diseases. Int J Cell Biol 2012: 463756, 2012.
2. Alanen HI, Salo KE, Pekkala M, Siekkinen HM, Pirneskoski A, and Ruddock LW. Defining the domain boundaries of the human protein disulfide isomerases. Antioxid Redox Signal 5: 367-374, 2003.
3. Alon A, Grossman I, Gat Y, Kodali VK, DiMaio F, Mehlman T, Haran G, Baker D, Thorpe C, and Fass D. The dynamic disulphide relay of quiescin sulphydryl oxidase. Nature 488: 414-418, 2012.
4. Andersen CL, Matthey-Dupraz A, Missiakas D, and Raina S. A new Escherichia coli gene, dsbG, encodes a periplasmic protein involved in disulphide bond formation, required for recycling DsbA/DsbB and DsbC redox proteins. Mol Microbiol 26: 121-132, 1997.
5. Appenzeller-Herzog C. Glutathione- and non-glutathionebased oxidant control in the endoplasmic reticulum. J Cell Sci 124: 847-855, 2011.
6. Appenzeller-Herzog C, Riemer J, Christensen B, Sorensen ES, and Ellgaard L. A novel disulphide switch mechanism in Ero1alpha balances ER oxidation in human cells. EMBO J 27: 2977-2987, 2008.
7. Appenzeller-Herzog C, Riemer J, Zito E, Chin KT, Ron D, Spiess M, and Ellgaard L. Disulphide production by Ero1alpha-PDI relay is rapid and effectively regulated. EMBO J 29: 3318-3329, 2010.
8. 7a. Å slund F, Berndt KD, and Holmgren A. Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct proteinprotein redox equilibria. J Biol Chem 272: 30780-30786, 1997.
9. Atkinson HJ and Babbitt PC. An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations. PLoS Comput Biol 5: e1000541, 2009.
10. Bader M, Muse W, Ballou DP, Gassner C, and Bardwell JC. Oxidative protein folding is driven by the electron transport system. Cell 98: 217-227, 1999.
11. Baker KM, Chakravarthi S, Langton KP, Sheppard AM, Lu H, and Bulleid NJ. Low reduction potential of Ero1alpha regulatory disulphides ensures tight control of substrate oxidation. EMBO J 27: 2988-2997, 2008.
12. Bardwell JC, McGovern K, and Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589, 1991.
13. Bessette PH,Cotto JJ,Gilbert HF, and Georgiou G. In vivo and in vitro function of the Escherichia coli periplasmic cysteine oxidoreductase DsbG. J Biol Chem274
14. Cabibbo A, Pagani M, Fabbri M, Rocchi M, Farmery MR, Bulleid NJ, and Sitia R. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem 275: 4827-4833, 2000.
15. Cao SS and Kaufman RJ. Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 17: 437-448, 2013.
16. Cao Z, Tavender TJ, Roszak AW, Cogdell RJ, and Bulleid NJ. Crystal structure of reduced and of oxidized peroxiredoxin IV enzyme reveals a stable oxidized decamer and a non-disulfide-bonded intermediate in the catalytic cycle. J Biol Chem 286: 42257-42266, 2011.
17. Chakravarthi S and Bulleid NJ. Glutathione is required to regulate the formation of native disulfide bonds within proteins entering the secretory pathway. J Biol Chem 279: 39872-39879, 2004.
18. Chambers JE, Tavender TJ, Oka OB, Warwood S, Knight D, and Bulleid NJ. The reduction potential of the active site disulfides of human protein disulfide isomerase limits oxidation of the enzyme by Ero1alpha. J Biol Chem 285: 29200-29207, 2010.
19. Cho SH, Porat A, Ye J, and Beckwith J. Redox-active cysteines of a membrane electron transporter DsbD show dual compartment accessibility. EMBO J 26: 3509-3520, 2007.
20. Cuozzo JW and Kaiser CA. Competition between glutathione and protein thiols for disulphide-bond formation. Nat Cell Biol 1: 130-135, 1999.
21. Darby NJ and Creighton TE. Characterization of the active site cysteine residues of the thioredoxin-like domains of protein disulfide isomerase. Biochemistry 34: 16770-16780, 1995.
22. Darby NJ and Creighton TE. Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry 34: 11725-11735, 1995.
23. Darby NJ, Kemmink J, and Creighton TE. Identifying and characterizing a structural domain of protein disulfide isomerase. Biochemistry 35: 10517-10528, 1996.
24. Darby NJ, Penka E, and Vincentelli R. The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. J Mol Biol 276: 239-247, 1998.
25. Dardalhon M, Kumar C, Iraqui I, Vernis L, Kienda G, Banach-Latapy A, He T, Chanet R, Faye G, Outten CE, and Huang ME. Redox-sensitive YFP sensors monitor dynamic nuclear and cytosolic glutathione redox changes. Free Radic Biol Med 52: 2254-2265, 2012.
26. Debarbieux L and Beckwith J. The reductive enzyme thioredoxin 1 acts as an oxidant when it is exported to the Escherichia coli periplasm. Proc Natl Acad Sci U S A 95: 10751-10756, 1998.
27. Dobson CM. Protein folding and misfolding. Nature 426: 884-890, 2003.
28. Eaton WA, Munoz V, Thompson PA, Henry ER, and Hofrichter J. Kinetics and dynamics of loops, alpha-helices, beta-hairpins, and fast-folding proteins. Acc Chem Res 31: 745-753, 1998.
29. Edman JC, Ellis L, Blacher RW, Roth RA, and Rutter WJ. Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 317: 267-270, 1985.
30. Ellgaard L and Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191, 2003.
31. Frand AR and Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1: 161-170, 1998.
32. Freedman RB, Hirst TR, and Tuite MF. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 19: 331-336, 1994.
33. Go YM and Jones DP. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780: 1273-1290, 2008.
34. Gordon EH, Page MD, Willis AC, and Ferguson SJ. Escherichia coli DipZ: anatomy of a transmembrane protein disulphide reductase in which three pairs of cysteine residues, one in each of three domains, contribute differentially to function. Mol Microbiol 35: 1360-1374, 2000.
35. Grauschopf U, Winther JR, Korber P, Zander T, Dallinger P, and Bardwell JC. Why is DsbA such an oxidizing disulfide catalyst. Cell 83: 947-955, 1995
36. Gross E, Kastner DB, Kaiser CA, and Fass D. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117: 601-610, 2004.
37. Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, and Fass D. 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, 2006.
38. Gross E, Sevier CS, Vala A, Kaiser CA, and Fass D. A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p. Nat Struct Biol 9: 61-67, 2002.
39. Guilhot C, Jander G, Martin NL, and Beckwith J. Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc Natl Acad Sci U S A 92: 9895-9899, 1995.
40. Haebel PW, Goldstone D, Katzen F, Beckwith J, and Metcalf P. The disulfide bond isomerase DsbC is activated by an immunoglobulin-fold thiol oxidoreductase: crystal structure of the DsbC-DsbD alpha complex. EMBO J 21: 4774-4784, 2002.
41. Hatahet F and Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 11: 2807-2850, 2009.
42. Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, and Martin JL. DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7: 215-225, 2009.
43. Holmgren A. Thioredoxin. 6. The amino acid sequence of the protein from escherichia coli B. Eur J Biochem 6: 475-484, 1968.
44. Holmgren A. Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. J Biol Chem 254: 9113-9119, 1979.
45. Holmgren A. Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254: 9627-9632, 1979.
46. Holmgren A. Enzymatic reduction-oxidation of protein disulfides by thioredoxin. Methods Enzymol 107: 295-300, 1984.
47. Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem 264: 13963-13966, 1989.
48. Holmgren A and Bjornstedt M. Thioredoxin and thioredoxin reductase. Methods Enzymol 252: 199-208, 1995.
49. Holmgren A, Soderberg BO, Eklund H, and Branden CI. Three-dimensional structure of Escherichia coli thioredoxin- S2 to 2.8A resolution. Proc Natl Acad Sci U S A 72: 2305-2309, 1975.
50. Hu J, Dong L, and Outten CE. The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix. J Biol Chem 283: 29126-29134, 2008.
51. Hwang C, Sinskey AJ, and Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502, 1992.
52. Inaba K and Ito K. Paradoxical redox properties of DsbB and DsbA in the protein disulfide-introducing reaction cascade. EMBO J 21: 2646-2654, 2002.
53. Inaba K, Masui S, Iida H, Vavassori S, Sitia R, and Suzuki M. Crystal structures of human Ero1alpha reveal the mechanisms of regulated and targeted oxidation of PDI. EMBO J 29: 3330-3343, 2010.
54. Inaba K, Murakami S, Suzuki M, Nakagawa A, Yamashita E, Okada K, and Ito K. Crystal structure of the DsbBDsbA complex reveals a mechanism of disulfide bond generation. Cell 127: 789-801, 2006.
55. Jander G, Martin NL, and Beckwith J. Two cysteines in each periplasmic domain of the membrane protein DsbB are required for its function in protein disulfide bond formation. EMBO J 13: 5121-5127, 1994.
56. Jeng MF, Campbell AP, Begley T, Holmgren A, Case DA, Wright PE, and Dyson HJ. High-resolution solution structures of oxidized and reduced Escherichia coli thioredoxin. Structure 2: 853-868, 1994.
57. Jensen KS, Hansen RE, and Winther JR. Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation. Antioxid Redox Signal 11: 1047-1058, 2009.
58. Jessop CE, Watkins RH, Simmons JJ, Tasab M, and Bulleid NJ. Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J Cell Sci 122: 4287-4295, 2009.
59. Jones DP and Go YM. Redox compartmentalization and cellular stress. Diabetes Obes Metab 12 Suppl 2: 116-125, 2010.
60. Kakihana T, Nagata K, and Sitia R. Peroxides and peroxidases in the endoplasmic reticulum: integrating redox homeostasis and oxidative folding. Antioxid Redox Signal 16: 763-771, 2012.
61. Kallis GB and Holmgren A. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine- 35 present in the reduced form of thioredoxin from Escherichia coli. J Biol Chem 255: 10261-10265, 1980.
62. Katzen F and Beckwith J. Transmembrane electron transfer by the membrane protein DsbD occurs via a disulfide bond cascade. Cell 103: 769-779, 2000.
63. Kemmink J, Darby NJ, Dijkstra K, Nilges M, and Creighton TE. Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy. Biochemistry 35: 7684-7691, 1996.
64. Kemmink J, Darby NJ, Dijkstra K, Nilges M, and Creighton TE. The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Curr Biol 7: 239-245, 1997.
65. Kemp M, Go YM, and Jones DP. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 44: 921-937, 2008.
66. Kim S, Sideris DP, Sevier CS, and Kaiser CA. Balanced Ero1 activation and inactivation establishes ER redox homeostasis. J Cell Biol 196: 713-725, 2012.
67. Klappa P, Ruddock LW, Darby NJ, and Freedman RB. The b domain provides the principal peptide-binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins. EMBO J 17: 927-935, 1998.
68. Kobayashi T, Kishigami S, Sone M, Inokuchi H, Mogi T, and Ito K. 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 U S A 94: 11857-11862, 1997.
69. Kober FX, Koelmel W, Kuper J, Drechsler J, Mais C, Hermanns HM, and Schindelin H. The crystal structure of the protein-disulfide isomerase family member ERp27 provides insights into its substrate binding capabilities. J Biol Chem 288: 2029-2039, 2013.
70. Kodali VK and Thorpe C. Oxidative protein folding and the Quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal 13: 1217-1230, 2010.
71. Kosuri P, Alegre-Cebollada J, Feng J, Kaplan A, Ingles- Prieto A, Badilla CL, Stockwell BR, Sanchez-Ruiz JM, Holmgren A, and Fernandez JM. Protein folding drives disulfide formation. Cell 151: 794-806, 2012.
72. Krause G, Lundstrom J, Barea JL, Pueyo de la Cuesta C, and Holmgren A. Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J Biol Chem 266: 9494-9500, 1991.
73. Kumar C, Igbaria A, D'Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, and Toledano MB. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 30: 2044-2056, 2011.
74. LaMantia ML and Lennarz WJ. The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell 74: 899-908, 1993.
75. Laurent TC, Moore EC, and Reichard P. Enzymatic synthesis of deoxyribonucleotides. Iv. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J Biol Chem 239: 3436-3444, 1964.
76. Li W, Schulman S, Dutton RJ, Boyd D, Beckwith J, and Rapoport TA. Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 463: 507-512, 2010.
77. Lu J and Holmgren A. Thioredoxin system in cell death progression. Antioxid Redox Signal 17: 1738-1747, 2012.
78. Lu J and Holmgren A. The thioredoxin antioxidant system. Free Radic Biol Med 8: 75-87, 2014.
79. Lundstrom-Ljung J, Birnbach U, Rupp K, Soling HD, and Holmgren A. Two resident ER-proteins, CaBP1 and CaBP2, with thioredoxin domains, are substrates for thioredoxin reductase: comparison with protein disulfide isomerase. FEBS Lett 357: 305-308, 1995.
80. Lundstrom-Ljung J and Holmgren A. Glutaredoxin accelerates glutathione-dependent folding of reduced ribonuclease A together with protein disulfide-isomerase. J Biol Chem 270: 7822-7828, 1995.
81. Lundstrom J and Holmgren A. Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin- like activity. J Biol Chem 265: 9114-9120, 1990.
82. Lundstrom J and Holmgren A. 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, 1993.
83. Lundstrom J, Krause G, and Holmgren A. 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, 1992.
84. Luthman M and Holmgren A. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry 21: 6628-6633, 1982.
85. Martin JL. Thioredoxin-a fold for all reasons. Structure 3: 245-250, 1995.
86. Martin JL, Bardwell JC, and Kuriyan J. Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468, 1993.
87. McCarthy AA, Haebel PW, Torronen A, Rybin V, Baker EN, and Metcalf P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat Struct Biol 7: 196-199, 2000.
88. Messens J, Collet JF, Van Belle K, Brosens E, Loris R, and Wyns L. The oxidase DsbA folds a protein with a nonconsecutive disulfide. J Biol Chem 282: 31302-31307, 2007.
89. Missiakas D, Georgopoulos C, and Raina S. Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo. Proc Natl Acad Sci U S A 90: 7084-7088, 1993.
90. Missiakas D, Georgopoulos C, and Raina S. The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. EMBO J 13: 2013-2020, 1994.
91. Missiakas D, Schwager F, and Raina S. Identification and characterization of a new disulfide isomerase-like protein (DsbD) in Escherichia coli. EMBO J 14: 3415-3424, 1995.
92. Molinari M and Helenius A. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402: 90-93, 1999.
93. Nakamura T and Lipton SA. Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases. Cell Death Differ 18: 1478-1486, 2011.
94. Nakamura T and Lipton SA. Emerging role of proteinprotein transnitrosylation in cell signaling pathways. Antioxid Redox Signal 18: 239-249, 2013.
95. Nelson JW and Creighton TE. Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry 33: 5974-5983, 1994.
96. Nguyen VD, Saaranen MJ, Karala AR, Lappi AK, Wang L, Raykhel IB, Alanen HI, Salo KE, Wang CC, and Ruddock LW. Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J Mol Biol 406: 503-515, 2011.
97. Ostergaard H, Tachibana C, and Winther JR. Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166: 337-345, 2004.
98. Pagani M, Fabbri M, Benedetti C, Fassio A, Pilati S, Bulleid NJ, Cabibbo A, and Sitia R. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J Biol Chem 275: 23685-23692, 2000.
99. Perez-Jimenez R, Ingles-Prieto A, Zhao ZM, Sanchez- Romero I, Alegre-Cebollada J, Kosuri P, Garcia-Manyes S, Kappock TJ, Tanokura M, Holmgren A, Sanchez-Ruiz JM, Gaucher EA, and Fernandez JM. Single-molecule paleoenzymology probes the chemistry of resurrected enzymes. Nat Struct Mol Biol 18: 592-596, 2011.
100. Perez-Jimenez R, Li J, Kosuri P, Sanchez-Romero I, Wiita AP, Rodriguez-Larrea D, Chueca A, Holmgren A, Miranda- Vizuete A, Becker K, Cho SH, Beckwith J, Gelhaye E, Jacquot JP, Gaucher EA, Sanchez-Ruiz JM, Berne BJ, and Fernandez JM. Diversity of chemical mechanisms in thioredoxin catalysis revealed by single-molecule force spectroscopy. Nat Struct Mol Biol 16: 890-896, 2009.
101. Pollard MG, Travers KJ, and Weissman JS. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell 1: 171-182, 1998.
102. Puig A and Gilbert HF. Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J Biol Chem 269: 7764-7771, 1994.
103. Puig A, Lyles MM, Noiva R, and Gilbert HF. The role of the thiol/disulfide centers and peptide binding site in the chaperone and anti-chaperone activities of protein disulfide isomerase. J Biol Chem 269: 19128-19135, 1994.
104. Rietsch A, Bessette P, Georgiou G, and Beckwith J. Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J Bacteriol 179: 6602-6608, 1997.
105. Roos G, Foloppe N, and Messens J. Understanding the pK(a) of redox cysteines: the key role of hydrogen bonding. Antioxid Redox Signal 18: 94-127, 2013.
106. Rost J and Rapoport S. Reduction-Potential of Glutathione. Nature 201: 185, 1964.
107. Rozhkova A and Glockshuber R. Thermodynamic aspects of DsbD-mediated electron transport. J Mol Biol 380: 783-788, 2008.
108. Rozhkova A, Stirnimann CU, Frei P, Grauschopf U, Brunisholz R, Grutter MG, Capitani G, and Glockshuber R. Structural basis and kinetics of inter- and intramolecular disulfide exchange in the redox catalyst DsbD. EMBO J 23: 1709-1719, 2004.
109. Rutkevich LA and Williams DB. Vitamin K epoxide reductase contributes to protein disulfide formation and redox homeostasis within the endoplasmic reticulum. Mol Biol Cell 23: 2017-2027, 2012.
110. Scherens B, Dubois E, and Messenguy F. Determination of the sequence of the yeast YCL313 gene localized on chromosome III. Homology with the protein disulfide isomerase (PDI gene product) of other organisms. Yeast 7: 185-193, 1991.
111. Schulman S, Wang B, Li W, and Rapoport TA. Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin- like redox partners. Proc Natl Acad Sci U S A 107: 15027-15032, 2010.
112. Sevier CS and Kaiser CA. Disulfide transfer between two conserved cysteine pairs imparts selectivity to protein oxidation by Ero1. Mol Biol Cell 17: 2256-2266, 2006.
113. Sevier CS, Qu H, Heldman N, Gross E, Fass D, and Kaiser CA. Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129: 333-344, 2007.
114. Shouldice SR, Heras B, Walden PM, Totsika M, Schembri MA, and Martin JL. Structure and function of DsbA, a key bacterial oxidative folding catalyst. Antioxid Redox Signal 14: 1729-1760, 2011.
115. Soute BA, Groenen-van Dooren MM, Holmgren A, LundstromJ, and VermeerC. Stimulation of the dithiol-dependent reductases in the vitamin K cycle by the thioredoxin system. Strong synergistic effects with protein disulphide- isomerase. Biochem J 281 Pt 1: 255-259, 1992.
116. Tachibana C and Stevens TH. The yeast EUG1 gene encodes an endoplasmic reticulum protein that is functionally related to protein disulfide isomerase. Mol Cell Biol 12: 4601-4611, 1992.
117. Tavender TJ, Springate JJ, and Bulleid NJ. Recycling of peroxiredoxin IV provides a novel pathway for disulphide formation in the endoplasmic reticulum. EMBO J 29: 4185-4197, 2010.
118. Tian G, Kober FX, Lewandrowski U, Sickmann A, Lennarz WJ, and Schindelin H. The catalytic activity of protein-disulfide isomerase requires a conformationally flexible molecule. J Biol Chem 283: 33630-33640, 2008.
119. Tian G, Xiang S, Noiva R, Lennarz WJ, and Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124: 61-73, 2006.
120. Tie JK and Stafford DW. Structure and function of vitamin K epoxide reductase. Vitam Horm 78: 103-130, 2008.
121. Toppo S, Vanin S, Bosello V, and Tosatto SC. Evolutionary and structural insights into the multifaceted glutathione peroxidase (Gpx) superfamily. Antioxid Redox Signal 10: 1501-1514, 2008.
122. Tu BP, Ho-Schleyer SC, Travers KJ, and Weissman JS. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290: 1571-1574, 2000.
123. Tu BP and Weissman JS. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 10: 983-994, 2002.
124. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, and Lipton SA. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441: 513-517, 2006.
125. Uys JD, Xiong Y, and Townsend DM. Nitrosative stressinduced S-glutathionylation of protein disulfide isomerase. Methods Enzymol 490: 321-332, 2011.
126. Vitu E, Kim S, Sevier CS, Lutzky O, Heldman N, Bentzur M, Unger T, Yona M, Kaiser CA, and Fass D. Oxidative activity of yeast Ero1p on protein disulfide isomerase and related oxidoreductases of the endoplasmic reticulum. J Biol Chem 285: 18155-18165, 2010.
127. Vuori K, Myllyla R, Pihlajaniemi T, and Kivirikko KI. Expression and site-directed mutagenesis of human protein disulfide isomerase in Escherichia coli. This multifunctional polypeptide has two independently acting catalytic sites for the isomerase activity. J Biol Chem 267: 7211-7214, 1992.
128. Wang C, Li W, Ren J, Fang J, Ke H, Gong W, Feng W, and Wang CC. Structural insights into the redox-regulated dynamic conformations of human protein disulfide isomerase. Antioxid Redox Signal 19: 36-45, 2013.
129. Wang X, Wang L, Wang X, Sun F, and Wang CC. Structural insights into the peroxidase activity and inactivation of human peroxiredoxin 4. Biochem J 441: 113-118, 2012.
130. Westphal V, Darby NJ, and Winther JR. Functional properties of the two redox-active sites in yeast protein disulphide isomerase in vitro and in vivo. J Mol Biol 286: 1229-1239, 1999.
131. Wiita AP, Perez-Jimenez R, Walther KA, Grater F, Berne BJ, Holmgren A, Sanchez-Ruiz JM, and Fernandez JM. Probing the chemistry of thioredoxin catalysis with force. Nature 450: 124-127, 2007.
132. Wilkinson B, Xiao R, and Gilbert HF. A structural disulfide of yeast protein-disulfide isomerase destabilizes the active site disulfide of the N-terminal thioredoxin domain. J Biol Chem 280: 11483-11487, 2005.
133. Wunderlich M and Glockshuber R. Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci 2: 717-726, 1993.
134. Xia TH, Bushweller JH, Sodano P, Billeter M, Bjornberg O, Holmgren A, and Wuthrich K. NMR structure of oxidized Escherichia coli glutaredoxin: comparison with reduced E. coli glutaredoxin and functionally related proteins. Protein Sci 1: 310-321, 1992.
135. Xiao R, Lundstrom-Ljung J, Holmgren A, and Gilbert HF. Catalysis of thiol/disulfide exchange. Glutaredoxin 1 and protein-disulfide isomerase use different mechanisms to enhance oxidase and reductase activities. J Biol Chem 280: 21099-21106, 2005.
136. Xiao R, Wilkinson B, Solovyov A, Winther JR, Holmgren A, Lundstrom-Ljung J, and Gilbert HF. The contributions of protein disulfide isomerase and its homologues to oxidative protein folding in the yeast endoplasmic reticulum. J Biol Chem 279: 49780-49786, 2004.
137. Xiong Y, Manevich Y, Tew KD, and Townsend DM. SGlutathionylation of protein disulfide isomerase regulates estrogen receptor alpha stability and function. Int J Cell Biol 2012: 273549, 2012.
138. Zito E. PRDX4, an endoplasmic reticulum-localized peroxiredoxin at the crossroads between enzymatic oxidative protein folding and nonenzymatic protein oxidation. Antioxid Redox Signal 18: 1666-1674, 2013.
139. Zito E, Melo EP, Yang Y, Wahlander A, Neubert TA, and Ron D. Oxidative protein folding by an endoplasmic reticulum- localized peroxiredoxin. Mol Cell 40: 787-797, 2010.