Forming disulfides in the endoplasmic reticulum

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 11, 2013, Pages 2425-2429

  Oka, Ojore B V ^a   Bulleid, Neil J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Disulfide bond; Oxidoreductase; Peroxidase; Protein disulfide isomerase (PDI); Sulfenylation; Thiol disulfide exchange

Indexed keywords

GLUTATHIONE PEROXIDASE; MENADIONE EPOXIDE; PEROXIREDOXIN 4; PROTEIN DISULFIDE ISOMERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; THIOREDOXIN;

BINDING SITE; CARBOXYLATION; CATALYSIS; CONFORMATIONAL TRANSITION; DISULFIDE BOND; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; HUMAN; ISOMERIZATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; REVIEW;

DISULFIDE BOND; OXIDOREDUCTASE; PEROXIDASE; PROTEIN DISULFIDE ISOMERASE (PDI); SULFENYLATION; THIOL-DISULFIDE EXCHANGE;

ANIMALS; DISULFIDES; ENDOPLASMIC RETICULUM; HUMANS; PROTEINS;

MAMMALIA;

EID: 84880613321     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.02.007     Document Type: Review

References (60)

1. Jansens A., van Duijn E., Braakman I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 2002, 298:2401-2403.
2. Kosuri P., Alegre-Cebollada J., Feng J., Kaplan A., Ingles-Prieto A., Badilla C.L., Stockwell B.R., Sanchez-Ruiz J.M., Holmgren A., Fernandez J.M. Protein folding drives disulfide formation. Cell 2012, 151:794-806.
3. Matagne A., Dobson C.M. The folding process of hen lysozyme: a perspective from the 'new view'. Cell. Mol. Life Sci. 1998, 54:363-371.
4. van den Berg B., Chung E.W., Robinson C.V., Mateo P.L., Dobson C.M. The oxidative refolding of hen lysozyme and its catalysis by protein disulfide isomerase. EMBO J. 1999, 18:4794-4803.
5. Hogg P.J. Disulfide bonds as switches for protein function. Trends Biochem. Sci. 2003, 28:210-214.
6. Robinson A.S., King J. Disulphide-bonded intermediate on the folding and assembly pathway of a non-disulphide bonded protein. Nat. Struct. Biol. 1997, 4:450-455.
7. Anelli T., Alessio M., Bachi A., Bergamelli L., Bertoli G., Camerini S., Mezghrani A., Ruffato E., Simmen T., Sitia R. Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J. 2003, 22:5015-5022.
8. Kadokura H., Beckwith J. Mechanisms of oxidative protein folding in the bacterial cell envelope. Antioxid. Redox Signal. 2010, 13:1231-1246.
9. Riemer J., Bulleid N., Herrmann J.M. Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 2009, 324:1284-1287.
10. Hwang C., Sinskey A.J., Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 1992, 257:1496-1502.
11. Arner E.S. Focus on mammalian thioredoxin reductases-important selenoproteins with versatile functions. Biochim. Biophys. Acta 2009, 1790:495-526.
12. Krause G., Holmgren A. Substitution of the conserved tryptophan 31 in Escherichia coli thioredoxin by site-directed mutagenesis and structure-function analysis. J. Biol. Chem. 1991, 266:4056-4066.
13. Chambers J.E., Tavender T.J., Oka O.B., Warwood S., Knight D., Bulleid N.J. The reduction potential of the active site disulfides of human protein disulfide isomerase limits oxidation of the enzyme by Ero1alpha. J. Biol. Chem. 2010, 285:29200-29207.
14. Anelli T., Sitia R. Protein quality control in the early secretory pathway. EMBO J. 2008, 27:315-327.
15. Hebert D.N., Molinari M. In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 2007, 87:1377-1408.
16. Braakman I., Bulleid N.J. Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 2011, 80:71-99.
17. Ellgaard L., Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005, 6:28-32.
18. Hatahet F., Ruddock L.W. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 2009, 11:2807-2850.
19. Krause G., Lundstrom J., Barea J.L., Pueyo de la Cuesta C., Holmgren A. Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J. Biol. Chem. 1991, 266:9494-9500.
20. Cunnea P.M., Miranda-Vizuete A., Bertoli G., Simmen T., Damdimopoulos A.E., Hermann S., Leinonen S., Huikko M.P., Gustafsson J.A., Sitia R., Spyrou G. ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress. J. Biol. Chem. 2003, 278:1059-1066.
21. Ushioda R., Hoseki J., Araki K., Jansen G., Thomas D.Y., Nagata K. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 2008, 321:569-572.
22. Jessop C.E., Tavender T.J., Watkins R.H., Chambers J.E., Bulleid N.J. Substrate specificity of the oxidoreductase ERp57 is determined primarily by its interaction with calnexin and calreticulin. J. Biol. Chem. 2009, 284:2194-2202.
23. Lyles M.M., Gilbert H.F. Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: pre-steady-state kinetics and the utilization of the oxidizing equivalents of the isomerase. Biochemistry 1991, 30:619-625.
24. Freedman R.B., Dunn A.D., Ruddock L.W. Protein folding: a missing redox link in the endoplasmic reticulum. Curr. Biol. 1998, 8:R468-R470.
25. Winter J., Klappa P., Freedman R.B., Lilie H., Rudolph R. Catalytic activity and chaperone function of human protein-disulfide isomerase are required for the efficient refolding of proinsulin. J. Biol. Chem. 2002, 277:310-317.
26. Karala A.R., Lappi A.K., Ruddock L.W. Modulation of an active-site cysteine pKa allows PDI to act as a catalyst of both disulfide bond formation and isomerization. J. Mol. Biol. 2010, 396:883-892.
27. C. Wang, W. Li, J. Ren, J. Fang, H. Ke, W. Gong, W. Feng, C.C. Wang, Structural insights into the redox-regulated dynamic conformations of human protein disulfide isomerase, Antioxid. Redox Signal. in press. (Electronic publication ahead of Print).
28. Tian G., Xiang S., Noiva R., Lennarz W.J., Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 2006, 124:61-73.
29. Denisov A.Y., Maattanen P., Dabrowski C., Kozlov G., Thomas D.Y., Gehring K. Solution structure of the bb' domains of human protein disulfide isomerase. FEBS J. 2009, 276:1440-1449.
30. Klappa P., Hawkins H.C., Freedman R.B. Interactions between protein disulphide isomerase and peptides. Eur. J. Biochem. 1997, 248:37-42.
31. Cai H., Wang C.C., Tsou C.L. Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J. Biol. Chem. 1994, 269:24550-24552.
32. Tavender T.J., Springate J.J., Bulleid N.J. Recycling of peroxiredoxin IV provides a novel pathway for disulphide formation in the endoplasmic reticulum. EMBO J. 2010, 29:4185-4197.
33. Rutkevich L.A., Williams D.B. Vitamin K epoxide reductase contributes to protein disulfide formation and redox homeostasis within the endoplasmic reticulum. Mol. Biol. Cell 2012, 23:2017-2027.
34. 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., Ruddock L.W. Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J. Mol. Biol. 2011, 406:503-515.
35. Zito E., Melo E.P., Yang Y., Wahlander A., Neubert T.A., Ron D. Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin. Mol. Cell 2010, 40:787-797.
36. Frand A.R., Kaiser C.A. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell 1998, 1:161-170.
37. Pollard M.G., Travers K.J., Weissman J.S. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1998, 1:171-182.
38. Cabibbo A., Pagani M., Fabbri M., Rocchi M., Farmery M.R., Bulleid N.J., Sitia R. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J. Biol. Chem. 2000, 275:4827-4833.
39. Pagani M., Fabbri M., Benedetti C., Fassio A., Pilati S., Bulleid N.J., Cabibbo A., Sitia R. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 2000, 275:23685-23692.
40. Tu B.P., Weissman J.S. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell 2002, 10:983-994.
41. Baker K.M., Chakravarthi S., Langton K.P., Sheppard A.M., Lu H., Bulleid N.J. Low reduction potential of Ero1alpha regulatory disulphides ensures tight control of substrate oxidation. EMBO J. 2008, 27:2988-2997.
42. Gross E., Sevier C.S., Heldman N., Vitu E., Bentzur M., Kaiser C.A., Thorpe C., Fass D. Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:299-304.
43. Inaba K., Masui S., Iida H., Vavassori S., Sitia R., Suzuki M. Crystal structures of human Ero1alpha reveal the mechanisms of regulated and targeted oxidation of PDI. EMBO J. 2010, 29:3330-3343.
44. Sevier C.S., Qu H., Heldman N., Gross E., Fass D., Kaiser C.A. Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 2007, 129:333-344.
45. Hansen H.G., Schmidt J.D., Soltoft C.L., Ramming T., Geertz-Hansen H.M., Christensen B., Sorensen E.S., Juncker A.S., Appenzeller-Herzog C., Ellgaard L. Hyperactivity of the Ero1alpha oxidase elicits endoplasmic reticulum stress but no broad antioxidant response. J. Biol. Chem. 2012, 287:39513-39523.
46. Appenzeller-Herzog C., Riemer J., Christensen B., Sorensen E.S., Ellgaard L. A novel disulphide switch mechanism in Ero1alpha balances ER oxidation in human cells. EMBO J. 2008, 27:2977-2987.
47. Kim S., Sideris D.P., Sevier C.S., Kaiser C.A. Balanced Ero1 activation and inactivation establishes ER redox homeostasis. J. Cell Biol. 2012, 196:713-725.
48. Tavender T.J., Sheppard A.M., Bulleid N.J. Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells. Biochem. J. 2008, 411:191-199.
49. Cao Z., Tavender T.J., Roszak A.W., Cogdell R.J., Bulleid N.J. 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. 2011, 286:42257-42266.
50. Zito E., Hansen H.G., Yeo G.S., Fujii J., Ron D. Endoplasmic reticulum thiol oxidase deficiency leads to ascorbic acid depletion and noncanonical scurvy in mice. Mol. Cell 2012, 48:39-51.
51. Lowther W.T., Haynes A.C. Reduction of cysteine sulfinic acid in eukaryotic, typical 2-Cys peroxiredoxins by sulfiredoxin. Antioxid. Redox Signal. 2011, 15:99-109.
52. 2 produced during disulphide formation. J. Cell Sci. 2010, 123:2672-2679.
53. E. Zito, PRDX4, an endoplasmic reticulum-localized peroxiredoxin at the crossroads between enzymatic oxidative protein folding and nonenzymatic protein oxidation, Antioxid. Redox Signal. in press. (Electronic publication ahead of Print).
54. Wei P.C., Hsieh Y.H., Su M.I., Jiang X., Hsu P.H., Lo W.T., Weng J.Y., Jeng Y.M., Wang J.M., Chen P.L., Chang Y.C., Lee K.F., Tsai M.D., Shew J.Y., Lee W.H. Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol. Cell 2012, 48:747-759.
55. Schulman S., Wang B., Li W., Rapoport T.A. Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin-like redox partners. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15027-15032.
56. Wajih N., Hutson S.M., Wallin R. Disulfide-dependent protein folding is linked to operation of the vitamin K cycle in the endoplasmic reticulum. A protein disulfide isomerase-VKORC1 redox enzyme complex appears to be responsible for vitamin K1 2,3-epoxide reduction. J. Biol. Chem. 2007, 282:2626-2635.
57. Tie J.K., Nicchitta C., von Heijne G., Stafford D.W. Membrane topology mapping of vitamin K epoxide reductase by in vitro translation/cotranslocation. J. Biol. Chem. 2005, 280:16410-16416.
58. Tie J.K., Jin D.Y., Stafford D.W. Human vitamin K epoxide reductase and its bacterial homologue have different membrane topologies and reaction mechanisms. J. Biol. Chem. 2012, 287:33945-33955.
59. Wajih N., Sane D.C., Hutson S.M., Wallin R. Engineering of a recombinant vitamin K-dependent gamma-carboxylation system with enhanced gamma-carboxyglutamic acid forming capacity: evidence for a functional CXXC redox center in the system. J. Biol. Chem. 2005, 280:10540-10547.
60. Rishavy M.A., Usubalieva A., Hallgren K.W., Berkner K.L. Novel insight into the mechanism of the vitamin K oxidoreductase (VKOR): electron relay through Cys43 and Cys51 reduces VKOR to allow vitamin K reduction and facilitation of vitamin K-dependent protein carboxylation. J. Biol. Chem. 2011, 286:7267-7278.